Oceanography and Marine Biology Voulme 27

OCEANOGRAPHY AND MARINE BIOLOGY
AN ANNUAL REVIEW
Volume 27
OCEANOGRAPHY AND MARINE

BIOLOGY
AN ANNUAL REVIEW
Volume 27
HAROLD BARNES, Founder Editor

MARGARET BARNES, Editor
The Dunstaffnage Marine Research Laboratory
Oban, Argyll, Scotland
Assistant Editors
A.D.Ansell
R.N.Gibson
T.H.Pearson
ABERDEEN UNIVERSITY PRESS
FIRST PUBLISHED IN 1989

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Aberdeen University Press 1989
British Library Cataloguing in Publication Data
Oceanography and marine biology: an annual
review.Vol. 27
1. OceanographySerials
2. Marine biologySerials
551.46005
ISBN 0-203-01629 -7 Master e-book ISBN
ISBN 0-203-19 130-7 (Adobe eReader Format)

ISBN 0-08-036397-0 (Print Edition)
ISSN 0075-3218
PREFACE
The demand for this series of Annual Reviews continues unabated. Many people are still willing to
contribute and we are grateful to them. It is always a pleasure to acknowledge the willingness with which
they accede to our editorial requests. The success of the series depends on their co-operation; without it our
task would be impossible. We thank them all and also the publishers for maintaining the regular appearance
of these Annual Reviews.
In the first 27 volumes of the series titles of references have not been included. The reason was the space
they would occupy which it was thought could be better spent on text. Present demand, however, indicates
that a change is necessary. From Volume 28 onwards it is hoped to include full titles in reference lists.
CONTENTS
page
PREFACE
iv
A Comparison of Marine Photosynthesis with Terrestrial Photosynthesis: a Biochemical

Perspective
GRAHAM J.KELLY
The Ecology and Behaviour of Ascidian Larvae

IB SVANE AND CRAIG M.YOUNG
28
Egg Production in Cirripedes

MARGARET BARNES
62
Biology of Marine Herbivorous Fishes

MICHAEL H.HORN
134
The Benguela Ecosystem. Part VI. Seabirds

A.BERRUTIN.J.ADAMS AND S.JACKSON
222
Review of Research Relevant to the Conservation of Shallow Tropical Marine Ecosystems

B.G.HATCHER, R.E.JOHANNES AND A.I.ROBERTSON
284
AUTHOR INDEX
353
SYSTEMATIC INDEX
386
SUBJECT INDEX
398
Oceanogr. Mar. Biol. Annu. Rev., 1989, 27,

Margaret Barnes, Ed.
Aberdeen University Press
A COMPARISON OF MARINE PHOTOSYNTHESIS WITH

TERRESTRIAL PHOTOSYNTHESIS: A BIOCHEMICAL
PERSPECTIVE
GRAHAME J.KELLY*
CSIRO Marine Laboratories, G. P. O. Box 1538, Hobart, Tasmania 7001, Australia
ABSTRACT The maximum photosynthetic rate of marine microalgaeboth cultures and natural
populationsis often estimated as being two to four times higher than that of leaves of terrestrial
plants, although the average estimate is one to two times. In an attempt to ascertain whether the
higher estimates are biochemically feasible, the photosynthetic biochemistry of the two groups
of plants is compared. A survey of the literature on the physiology and biochemistry of marine
algae shows that: (1) their chlorophyll a content (dry weight basis) is similar to that of leaves of
terrestrial plants, (2) the in vitro values obtained for photosynthetic electron transport and ribulosel,5-bisphosphate carboxylase activity have all been low, (3) carboxylation of
phosphoenolpyruvate can account for no more than 10% of net carbon fixation, (4)
photorespiration, which would have little influence on estimates of primary productivity, is
possibly prevented by active uptake of inorganic carbon, (5) photoinhibition is either avoided or
protections against it exist, and (6) the extent of dark respiration during photosynthesis is not
known.
Information in the literature indicates that the actual in situ (light-limited) photosynthesis of
marine microalgae is 7% of its potential (at light saturation). Assuming that phytoplankton
biomass (chlorophyll) has been correctly estimated, and that the biochemistry of marine algal
photosynthesis is similar to that of terrestrial plants, then the current estimate of in situ marine
photosynthesis is concluded to be biochemically reasonable.
INTRODUCTION
This review is an attempt to put into some order the rambling thoughts of a peas-and-barley biochemist whose
head was suddenly immersed in the ocean. Peas-and-barley biochemists are accustomed to expecting
maximum rates of photosynthesis (Pmax: photosynthesis at saturating light and carbon dioxide and ambient
temperature) of between 200 and 400 moles CO2 fixedmg chlorophyll1h1. These rates are equivalent to
GRAHAME J.KELLY
assimilation numbers (i.e. photosynthesis expressed as mg carbon fixed.mg chl. a1h1) of between 2.4 and
4.8. I was therefore rather surprised to find that estimates of the Pmax of marine phytoplankton commonly
yielded assimilation numbers between 5 and 10 (and sometimes approaching 20), and that investigators of
marine photosynthesis often fear that assimilation numbers much below 5 may represent under-estimates of
the true values. This difference between the marine and terrestrial sectors is illustrated by the contrast
between the following two quotations: Maximum rates of photosynthesis [by land plant leaves] depend on
species and growth conditions; they can surpass 300 mol CO2 reduced.mg chlorophyll1h1 (i.e.
assimilation number of 3.6) (Heber, Neimanis & Dietz, 1988); Often cited as evidence of low growth rates
has been the fact that assimilation ratios reported from open-ocean stations have almost always been <5 g
carbon.g chlorophyll a1h1 (Laws, DiTullio & Redalje, 1987).
The core of this review analyses this apparently superior photosynthetic performance of marine
phytoplankton over terrestrial plants. Particular attention is given to the known and unknown biochemical
aspects of photosynthesis in these two groups of plants, and to the interplay between this biochemistry and
the plants respective environments. I conclude that, while all but the highest of the claimed rates of Pmax
by marine phytoplankton are biochemically feasible, the concern that current measurements of primary
productivity in the ocean may be misleadingly low is not necessarily valid, because higher estimates of
Pmax would be inconsistent with the known biochemistry of photosynthesis.
CURRENT ESTIMATES OF TERRESTRIAL AND MARINE PHOTOSYNTHESIS
ACTUAL PHOTOSYNTHESIS
Actual (i.e. in situ marine algal photosynthesis is generally agreed to average about 60g carbon fixedm2yr
1 (Ryther, 1969; Whittaker & Likens, 1975; Malone, 1980; Dring, 1982, p. 91; Boynton et al., 1983).
Production in the nutrient-poor tropical oceans is usually below this average, while it is above the average in
the nutrient-rich cooler waters of the northern and southern oceans, and off the west coasts of Africa and the
Americas (Bunt, 1975). Production is relatively high in shallow coastal regions where both macroalgae
(seaweeds) and microalgae (phytoplanktonic and benthic) occur, but because these areas are comparatively
small, they contribute only 23% of the total marine photosynthesis. The open ocean phytoplankton
contributes the remaining 77% (Table I); this review, therefore places most emphasis on marine microalgal
photosynthesis.
Terrestrial photosynthesis, similarly expressed on an area basis, is about five-fold greater than ocean
photosynthesis. Assuming dry matter to be 45% carbon (Walker, 1979), the mean net primary productivity
on land is estimated to be 350 g carbonm2yr1 (Whittaker & Likens, 1975). When photosynthesis is
expressed on a chlorophyll basis, a contrasting picture, however, emerges. Photosynthesis expressed in the
form of assimilation numbers (i.e., mg carbon fixedmg chl. a1h1) gives 0.053 for terrestrial and 0.31 for
marine photosynthesis. For the open-ocean phytoplankton, the value is 0.43. (These calculations are based
on the values in Table I, and assume dry matter to be 45% carbon, and one year to have 4380 hours of
daylight). Thus, based upon chlorophyll, marine photosynthesis is six times greater
TABLE I
* Present address: Department of Biology, Queensland University of Technology, G.P.O. Box 2434, Brisbane,
Queensland, 4001 Australia.
PHOTOSYNTHESIS: A BIOCHEMICAL PERSPECTIVE
Global net productivity of terrestrial and marine plants (from Whittaker & Likens, 1975)
Production 109 tonnes dry
matteryr1 (P)
Chlorophyll 107 tonnes

(Chl)
Biomass 109 tonnes dry

matter
Community Total
Total
Total
Marine
Open ocean 42
13
Coastala
118
Terrestrial
24
7
69
1.0
0.8
23
4
3
93
1.0
2.9
1840
0.06
0.16
99.8
PChl1 103
4.2
1.6
0.51
Continental shelves, estuaries, seaweed beds, reefs.
than terrestrial photosynthesis, although the chlorophyll a contents of both groups of plants, expressed as a
percentage of dry weight, are apparently about the same (see p. 17).
POTENTIAL PHOTOSYNTHESIS
The above actual assimilation numbers are in fact much lower than potential photosynthesis values. Many
investigations have been made with phytoplankton, and from a sample of these (Table II), a mean potential
assimilation number of 6.4 is obtained. Most values in this Table were measured with high irradiances. The
assimilation number of 0.43 for actual open ocean productivity is only 7% of this potential value because
(1) the phytoplankton grow at depths where irradiance is not saturating for photosynthesis, (2) irradiance is
low early in the morning and late in the afternoon, and (3) respiratory losses occur, probably mainly at
night. Unlike land plants, which must cope with periodic water shortage and a less-than-saturating supply of
CO2, there seems to be no other major hindrance to phytoplankton photosynthesis (Table III).
As emphasised earlier, the measured potential rates of photosynthesis (Pmax) by phytoplankton
(Table II) are, however, often well above maximum values measured for terrestrial plants. The mean
assimilation number for 49 C3 land plants under saturating irradiance (but in air, and therefore below
saturation with respect to CO2) was 1.8 (Bjrkman, 1981). From a comparable survey (Boardman, 1977)
mean Pmax values of 2.0 for sun species, and 0.39 for shade species can be calculated. In a more recent
study of 10 C4 plants, the mean Pmax was 2.2 (Usuda, Ku & Edwards, 1984; the terms C3 and C4 are
explained on p. 28). Bean, pea, spinach, tomato, and wheat leaves, saturated with both light and CO2, gave
values between 3.6 and 4.9 (Dietz, Neimanis & Heber, 1984; Dietz, 1986; Stitt, 1986; Chow & Anderson,
1987a; Kobza & Edwards, 1987; Terashima & Evans, 1988). Biochemical experiments on photosynthetic
electron transport suggest that an assimilation number in excess of 4.3 (as recorded for sunflower) is
unlikely with terrestrial
TABLE II
A selection of assimilation assimilation numbers in the laboratory and in the field. Some assimilation numbers have
been calculated from values of other parameters provided by the authors
Alga or locality
Assimilation numbers mg Cmg chl a

1h1
Reference
Various oceanic waters

Skeletonema sp.
Peruvian coast
Skeletonema costatum
18
4.8
0.47.4
5.1
Steemann Nielsen & Hansen, 1961

Cassie, 1963
Strickland et al., 1969
Jrgensen, 1970
GRAHAME J.KELLY
Alga or locality

1h1
Reference
Various oceanic waters
4.9
Nannochloris atomis
Glenodinium sp.
N. Pacific gyre
Three diatoms
Two dinoflagellates
Gulf of Maine
One diatom and one chlorophyte
Ten species
Ceratium longipes
Pyrocystis noctiluca
Near Hawaii
Narragansett Bay
Bedford Basin
Near Hawaii
4.5
1.1
8.8
0.20.5
3.0
118
2.85.3
1.65.8
2.210.4
2.9
514.5
1.75.8
1.6
11.218.9
Tropical Atlantic
Near Hawaii
Synechococcus spp.
Vineyard Sound
Thalassiosira fluviatilis
Phaeodactylum tricornutum
Chlorella sp.
Br. Columbian coast
South of Tasmania
8.5
10.3
16.0
1020
16
11.5
7.5
119
2.6
Celtic Sea
Tropical Pacific
Firth of Forth
Antarctic
N.W.Atlantic
Hudson Bay
Antarctic
Great Barrier Reef
Synechococcus
N.Pacific gyre
16
7.5
3.5
38
0.27.4
19
0.84.4
314
612
9.5
3.3
Gulf of Fos
0.514
Eppley, 1972 (average of 17 values,

mostly from other investigators)
Yentsch, 1974
Burris, 1977
Venrick, Beers & Heinbokel, 1977
Kremer & Berks, 1978
Przelin & Alberte, 1978
Glover & Morris, 1979
Falkowski & Owens, 1980
Glover, 1980
Taguchi, 1981
Rivkin et al., 1982
Bienfang & Takahashi, 1983
Furnas, 1983
Smith et al., 1983
Williams, Heinemann, Marra & Purdie,
1983
Gieskes & Kraay, 1984
Laws et al., 1984
Barlow & Alberte, 1985
Glibert, Dennett & Goldman, 1985
Hobson, Morris & Guest, 1985
Holdsworth, 1985
Thinh & Griffiths, 1985
Forbes, Denman & Mackas, 1986
Furuya, Hasumoto, Nakai & Nemoto,
1986
Joint & Pomroy, 1986
King, 1986
Mills & Wilkinson, 1986
Palmisano et al., 1986
Przelin et al., 1986
Rochet, Legendre & Demers, 1986
Sakshaug & Holm-Hansen, 1986
Furnas & Mitchell, 1987
Kana & Glibert, 1987a
Laws et al., 1987
Mortain-Bertrand, Descolas-Gros &
Jupin, 1987
Plante-Cuny & Bodoy, 1987
Alga or locality

1h1
Reference
McMurdo Sound
Brittany Coast
Prorocentrum mariae-lebouriae
Gulf of Maine
Mediterranean Sea
0.18.1
3.4
0.55.8
5
5.1
Rivkin & Putt, 1987

Videau, 1987
Coats & Harding, 1988
Legendre et al., 1988
Lohrenz et al., 1988
plants (Delaney & Walker, 1978). Marine phytoplankton, however, have been credited with assimilation
numbers two or three times this value (see Table II).
Such high assimilation numbers could be the consequence of either (1) errors in the estimate of either
photosynthetic CO2 fixation rate or chlorophyll content, or (2) a photosynthetic biochemistry that has the
capacity for a several-fold greater rate of CO2 fixation than that in the leaves of land plants. These
possibilities are discussed in this review. Attention is being given to these points, not so much because the
values appear high (although in most cases not inconceivably high), but because concern has been expressed
in the oceanographic literature that the 14C technique may have often led to photosynthesisand hence the
primary productivity of the oligotrophic open oceanbeing under-estimated (Sheldon & Sutcliffe, 1978;
Shulenberger & Reid, 1981; Dring, 1982, p. 89; Jenkins, 1982; Gieskes & Kraay, 1984; Joiris, 1985;
Cullen, Zhu & Pierson, 1986).
TABLE III
Comparison of oceanic photosynthesis with terrestrial photosynthesis
Land
Ocean
White light
Up to full sunlight (1700 Em2s1) but many leaves
shaded
Photosynthetic cells support many non-photosynthetic
cells and skeletal material
Often water-restricted
Often nutrient-restricted
Limited by supply of inorganic carbon (CO2)
Blue-green light
Lower intensity (10 to several hundred Em2s1
Little to support
Never water-restricted
Adequate nutrients?a
Probably not limited (sea water at pH 82 contains 2 mM )
The relationship between phytoplankton growth and nutrient supply is largely beyond the scope of this review.
Suffice to mention that certain nutrients (particularly nitrogen, phosphorus, and iron) are often at very low
levels in the oligotrophic open ocean, such that any long-term expansion of the phytoplankton population as
a whole is prevented, while grazing of phytoplankton and subsequent nutrient regeneration by heterotrophs
are tightly coupled, so that the growth of individual phytoplankton cells is seldom nutrientlimited (deficiency
symptoms have seldom been observed in natural populations) (Goldman, McCarthy & Peavey, 1979; Rivkin
et al., 1982; Goldman, 1986; Balch, Garside & Renger, 1987; Martin & Fitzwater, 1988). In coastal and highlatitude regions of the oceans, physical mixing and advection, as well as regeneration, become, however,
major processes for supplying nutrients, contributing to greater and seasonally more variable primary
productivity in these regions (Lorenzen, 1976; Kirk, 1983, p. 277).
GRAHAME J.KELLY
THE 14C TECHNIQUE

The most popular method for estimating phytoplankton CO2 fixation used at present was introduced by
Steemann Nielsen (1952) some 35 years ago. The procedure is described in detail by Strickland & Parsons
(1972), but in essence, 14C-labelled bicarbonate is added to a sample of sea water containing its natural
population of phytoplankton. Photosynthesis is allowed to proceed for several hours, after which the sample
is filtered, washed (to remove unfixed ), and the remaining radioactivity is measured. Assimilation numbers
are calculated from this measurement and an estimate of chlorophyll.
In general, the procedure has yielded acceptably high assimilation numbers for Pmax (Table II).
Nevertheless, there is a widely held suspicion that it gives greatly under-estimated values (Round, 1981, p.
259; Gieskes & Kraay, 1984) because it does not allow for the presence of toxic metal ions on bottle walls,
the depletion of nutrients, the rupture of cells on filters, respiration, and grazing by microzooplankton. It is,
however, unlikely that the underestimates would be large given that the assimilation numbers obtained are of
the same order of magnitude as the accepted Pmax of land plants.
Instead, the likelihood of over-estimation needs to be considered. This could result from either
erroneously high values of 14C incorporation or erroneously low values for chlorophyll (chlorophyll is
discussed below). Admittedly it is, at present, difficult to see how either of these possibilities could arise
frequently.
Evidence for some over-estimation of net CO2 fixation has been provided from 14C experiments with
cultures; it has been attributed to respiration of carbohydrate reserves not labelled with 14C during the
experiments (Li & Goldman, 1981; Richardson, Samuelsson & Hllgren, 1984). In what is known of the
carbon metabolism of photosynthetic cells, there is, however, no major pathway whereby a separate pool of
carbohydrate reserves are respired during photosynthesis. Alternatively, in the field, over-estimates might
result from non-photosynthetic fixation of Bacteria (including, presumably, marine bacteria) contain
enzymes that catalyse the carboxylation of phosphoenolpyruvate (PEP) (Gieskes & Kraay, 1984) and/or
pyruvate, and phytoplankton are also able to carboxylate PEP. These carboxylations are not connected to
photosynthesis in bacteria, and cannot contribute more than 10% of the net photosynthetic carbon fixation in
phytoplankton (see Fig 4, p. 30)or in any other photosynthetic cell for that matter, because the only
carboxylase connected to a series of reactions that permits plant growth is ribulose-l,5-bisphosphate
carboxylase (RuBP carboxylase, see p. 26). PEP carboxylation may, however, occur temporarily at high
rates, using PEP generated from carbohydrate reserves accumulated during active photosynthesis at some
other time or place.
In attempts to correct for PEP carboxylations, researchers usually include control incubations in the dark.
These have often given positive values (so-called dark fixation), not infrequently equal to 50% or more of
the values obtained with incubations in the light (Yentsch, 1974). This dark fixation may, however, not all
continue in the light; for example, the phytoplankton may carboxylate more PEP in the dark than in the
light. Attempts to control this unknown factor by replacing dark controls with light-plus-photosyntheticpoison controls (Legendre, Demers, Yentsch & Yentsch, 1983) are of questionable value, because poisoned
photosynthesis can lead to metabolic perturbations that re-establish dark metabolism.
CHLOROPHYLL
ESTIMATION OF CHLOROPHYLL
Assimilation numbers could just as easily be wrong because of chlorophyll estimates as carbon-fixation
estimates. This possibility will not be exhaustively discussed here, but four points may be mentioned. First,
chlorophyll in small picoplanktonic algae may have escaped detection in the past because the pores of filters
were too large to retain these cells. Secondly, acetone does not extract any chlorophyll from intact cells of
some algae (e.g. Pelagococcus: Vesk & Jeffrey, 1987); thus the proportion of tough cells such as these
actually broken by preliminary homogenisation or sonication should be considered. Methanol will extract
chlorophyll from these cells (Holm-Hansen & Riemann, 1978; Wood, 1985), but the subsequent estimation
is less exact because methanol causes allomerisation of chlorophyll. Thirdly, the accuracy of chlorophyll
estimations from in vivo fluorescence is still being debated (Harris, 1978; Leftley, Bonin & Maestrini, 1983;
Falkowski & Kiefer, 1985; Keller, 1987). Finally, some microalgae are reported to have chloroplasts so fragile
that enzymic degradation of chlorophyll a occurs during preparation of the sample for estimation. Jeffrey &
Hallegraeff (1987) found that degradation to chlorophyllide a occurred to a significant extent in 27 of 93
examined species. The chlorophyllide a would, however, be estimated as chlorophyll a in
spectrophotometric and fluorimetric procedures (but not using HPLC), so prob ably did not contribute to
under-estimates in the past. Suzuki & Fujita (1986), however, reported that degradation to phaeophorbide a
occurred in the diatom Skeletonema costatum; if this is a widespread occurrence, then it is likely that
chlorophyll a would have been under-estimated by spectrophotometry and fluorimetry.
CELLULAR CHLOROPHYLL a CONTENT
Another reason for phytoplankton having relatively higher assimilation numbers than terrestrial plants
might be because phytoplankton cells contain relatively less chlorophyll a. This would be possible if a
greater share of the light-harvesting task in marine algal cells were taken over by pigments other than
chlorophyll a, such as chlorophylls b and c, carotenoids, and biliproteins (Hiller & Goodchild, 1981;
Przelin, 1981; Siefermann-Harms, 1987). This would result in high assimilation numbers (i.e. CO2 fixed
per unit of chlorophyll a). Most available information argues, however, against this explanation. First, the
limiting step that determines photosynthetic capacity (at light-saturation) is believed to be a reaction of
photosynthetic electron transport or of CO2 fixation rather than light-harvesting (see p. 20). Thus, the
contents of accessory pigments would be irrelevant to the light-saturated rate of photosynthesis.
Secondly, even under light-limited conditions where the photosynthetic rate is determined by lightharvesting, high values for carbon fixed per unit of chlorophyll a are unlikely to result from low chlorophyll
a contents, because reported values for the latter are similar to those of the leaves of terrestrial plants. The
mean chlorophyll a content of the leaves of 49 C3 land plants calculated from values given by Bjrkman
(1981), is about 0.9% of dry weight. Similarly, values of 0.8% and 1.3% are obtained from values given by
Boardman (1977) for five sun species and five shade species, respectively (assuming dry weight to be onesixth of fresh weight). From data on marine microalgae, I estimate the values also to be about 1 % of dry
weight (Table IV). In addition, 1 % is the global estimate for the open ocean, from 3g dry matter (biomass)
m2 and 0.03g chl.m2 (Whittaker & Likens, 1975). Thus,
TABLE IV
GRAHAME J.KELLY
Chlorophyll a content of marine phytoplankton

Alga(e)
Chlorophyll a % dry weight
Reference
Six species
Two dinoflagellates
Dunaliella and Skeletonema
11 diatoms and 8 dinoflagellates
Five field samples
Two psychrophilic diatoms
15 species
11 species
Two Thalassiosira species
Pelagococcus subviridis
Prorocentrum mariae-lebouriae
3.0a
Jrgensen, 1970
Vesk & Jeffrey, 1977
Przelin & Alberte, 1978
Falkowski, 1981
Hitchcock, 1982
Kirk, 1983, p. 181
Van Baalen, 1985
Geider, 1987
Moal et al., 1987
Sakshaug et al., 1987
Vesk & Jeffrey, 1987
Coats & Harding, 1988
0.403.7a
0.8a
13
0.6a
0.9b
0.472.2
1.2b,c
1.5a,b
2.9a,b
1.5a
1.12.9a
Calculated from cell volume, and assuming dry weight to be one sixth of fresh weight.
Mean value.
c Calculated from carbon: chlorophyll a ratios corrected to growth at 50 Em2s1, and taking dry matter to be 45%
carbon.
b
most available measurements do not indicate any significant difference between the chlorophyll a contents
of land plants and marine plants.
Nevertheless, some scattered information does suggest that certain microalgae may contain relatively
little chlorophyll a. Cells that are nutrient-depleted, and thus growing slowly, have low chlorophyll a
contents, as evidenced by carbon: chlorophyll a ratios in excess of 100 (Eppley, 1972). Nevertheless, due to
their slow growth these cells would not be expected to have high assimilation numbers. The low
chlorophyll contents may represent a physiological response of the cells to avoid harvesting more light
energy than can be used for growth, thus avoiding photoinhibition (see p. 34). The low contents are unlikely
to be due to a lack of nitrogen for incorporation into additional chlorophyll molecules, because the nitrogen
demand for chlorophyll is quite loweven in healthy cells it is only about 2% of the nitrogen demand for
protein.
Cyanobacteria, in which phycobilipigments perform much of the light-harvesting, and most of the
chlorophyll a is restricted to photosystem I (Mimuro & Fujita, 1977; Hiller & Goodchild, 1981), might also
be thought to have relatively low chlorophyll a levels. But this is not necessarily so: in white-light grown
Anacystis nidulans (a freshwater species) it was 0.68% of dry weight (Evans & Alien, 1973), and from
studies of marine Synechococcus (Barlow & Alberte, 1985; Kana & Glibert, 1987b; Przelin, Glover &
Campbell, 1987) chlorophyll contents of between 0.3 and 3.3% of dry weight are obtained on the basis of
dry matter being 45% carbon, dry weight being one-sixth of fresh weight, and cells being spheres of 1.0 m
diameter. Thus, it is difficult to propose that marine cyanobacteria have notably less chlorophyll a than do
eukaryotic photosynthetic cells. This conclusion is relevant because cyanobacteria, together with small
eukaryotes, comprise the picoplankton that make up a significant portion of the biomass of autotrophic
cells in deep regions of the tropical oceans (Platt, Subba Rao & Irwin, 1983; Glover, Keller & Guillard,
1986; Iturriaga & Mitchell, 1986). In an extensive review of algal picoplankton, Stockner & Antia (1986)
tabulated eight marine assimilation numbers, the approximate mean of which was 2.3, which is lower than
the mean (6.4) of the values in Table II.
A final point is that the chlorophyll content of a sea-water sample may not be taken as an indicator of the
photo synthetic capacity of the microalgae in that water. Work with terrestrial plants has shown that lightsaturated photosynthesis in air is only poorly correlated with the chlorophyll content of leaves, but is highly
correlated with the leafs content of ribulose-1,5-bisphosphate (RuBP) carboxylase, which is the enzyme
responsible for at least 90% of the photosynthetic CO2 assimilation (Bjrkman, 1981; Usuda, Ku &
Edwards, 1984; Makino, Mae & Ohira, 1984; Evans, 1986). A similar conclusion was recently made for the
marine alga Dunaliella tertiolecta (Sukenik, Bennett & Falkowski, 1987).
CELL GROWTH RATES
The values for open-ocean phytoplankton listed in Table I, show annual production to be 42-times the
standing stock. This implies that the mean turnover time of the phytoplankton carbon pool in surface water
is days, from which it can be inferred that the growth rate of cells varies between low values (growth
effectively ceased) to values typical of rapidly growing cells (e.g. 1day1). In cells with a carbon content of
45% of the dry weight and a chlorophyll content of 1% (i.e. carbon: chlorophyll a ratio of 45), a growth rate
of 1day1 corresponds to a photosynthetic rate of 45 mg carbon fixedmg chl. a1day1, or assimilation
number (for 12 h of daylight) of 3.8 (see also Eppley, 1972; Falkowski, 1981). This is 60% of the mean of
the values in Table II, and close to the maximum values observed in land plants. Very high growth rates,
such as the 3 h generation time estimated by Sheldon & Sutcliffe (1978), would give assimilation numbers
greater than those usually observed for land plants. Do such values represent the upper limits for Pmax? It
would seem so: the maximum growth rate of Chlorella fully charged with reducing equivalents and
energy was reported as a doubling time of 3 h (Pirt, 1986).
Other data are consistent with doubling times being considerably greater than 3 h. Eppley (1972)
reviewed the growth rates for 160 laboratory cultures of both freshwater and marine microalgae grown at
temperatures up to 33C largely in continuous light, and all were below 4.4day1. This maximum
corresponds to a doubling time of 5.5 h, and to an assimilation number of 8.4 if carbon and chlorophyll a
contents were as above, and lighting was continuous. Geider (1987) concludes from theoretical
considerations that a growth rate of 2.6day1 at 20C is the maximum attainable, but requires a carbon:
chlorophyll a ratio of 27, in which case the chlorophyll a content would approach 1.7% of dry weight (once
again assuming dry matter to be 45% carbon) and the corresponding maximum assimilation number would
be 5.7, which is close to the mean of the values in Table II. Langdon (1987) found that the photosynthetic
efficiencies of several species were very similar, at about 0.02 g carbong chl. a1h1. This value predicts
that a potential assimilation number of 6.4 (i.e. the mean of the values in Table II) will occur if light
saturation of photosynthesis is reached at 320 Most species would be almost or completely light-saturated at
this irradiance.
TEMPERATURE
As most values of marine and terrestrial photosynthesis have been obtained from measurements at ambient
temperatures, temperature is not discussed in detail in this review. The reader is referred to Eppley (1972)
for an account of the effect of temperature on phytoplankton production, including observations of
temperature coefficient (Q10) values close to 2.0. This author briefly referred to the Blehrdek equation,
and it may be worth noting that the response of photosynthesis to change in temperature possibly follows
the Blehrdek equation (McMeekin et al., 1987) more closely than the Arrhenius equation. Re-analysis of
data presented by Fu & Gibbs (1987) on the effect of temperature on photosynthesis by spinach, pea, and
10
GRAHAME J.KELLY
Chlorella indicates that, in each case, the observed responses obey the Blehrdek equation, with an
exponent of 1, quite closely (D.A.Ratkowsky, pers. comm.). Tmin values of between +1C and 2C were
obtained. This parameter Tmin specifies a lower temperature where growth (or, in this case, photosynthesis)
theoretically becomes zero due exclusively to the lowering of temperature. (In practice, other factors such
as freezing may stop growth before Tmin is reached). In a study of the response of phytoplankton
photosynthesis to temperature, Li (1985) found that the Blehrdek equation, with an exponent of 2, fitted
the data quite well. Tmin values between 14.4C and 23.4C were obtained, the lower values being for
phytoplankton from colder waters. Optimum temperatures varied from 11.8C (for samples collected from
1.1C water) to 27.3C (for samples from 27.5C water).
BIOCHEMICAL DETERMINANTS OF Pmax
A comparison of the reported photosynthetic capacities of leaves of terrestrial plants and marine
phytoplankton raises the question of which biochemical step determines the Pmax. Boardman (1977) noted
that photosynthetic capacity will be influenced by one or more of the dark steps of photosynthesis, such
as the rate of diffusion of CO2 from the cell wall to the chloroplast, the rate of photosynthetic electron
transport, and the carboxylation reaction, but is expected to be independent of the efficiency of light
absorption and the primary photochemistry. Leaves of plants grown under high light intensities are capable
of higher rates of light-saturated photosynthesis (measured with air-levels of CO2) than are leaves of plants
grown under low light intensities; this applies whether the rates are expressed on a chlorophyll basis or a
leaf area basis, since chlorophyll per unit leaf area varies little between the two groups of plants. The
increased photosynthesis by the high-light plants correlates with increased activities of RuBP carboxylase
and photosynthetic electron transport, and increased amounts in the leaf of the electron transport component
cytochrome f (Boardman, 1977; Bjrkman, 1981; Chow & Anderson, 1987a; Evans, 1987). Thus, in leaves
of terrestrial plants, Pmax appears to be primarily determined by the contents of electron transport chains
and RuBP carboxylase molecules (von Caemmerer & Farquhar, 1981; Dietz, Neimanis & Heber, 1984;
Heber, Neimanis & Dietz, 1988).
A comparable study of a marine microalga (Dunaliella tertiolecta), grown at five irradiances between 80
and 1900 has been reported recently by Sukenik et al. (1987). They also obtained evidence that the cells
content of RuBP carboxylase determined its Pmax, except at very high light intensities where the capacity
for photosynthetic electron transport would determine its Pmax. The response of the microalga to low or
high light was, however, rather different to that of plant leaves: neither the cells content of RuBP
carboxylase nor the photosynthetic capacity per cell changed, but the chlorophyll a content in the low-light
cells was about six times greater than in the high-light cells; their Pmax was consequently one-sixth that of
highlight cells. The cytochrome fcontent of Dunaliella cells also increased fourfold in response to low light
(rather than decreasing, as happens in plant leaves). Another electron transport component, plastoquinone
(which is implicated in the rate-limiting reaction of photosynthetic electron transport: Harris, 1978;
Richardson, Beardall & Raven, 1983), also increased in low-light grown Dunaliella. In pea leaves (Chow &
Anderson, 1987b) and in the freshwater microalga Scenedesmus obliquus (Fleischhacker & Senger, 1978),
the levels of both cytochrome f and plastoquinone were, however, lower in low-light grown plants than in
high-light grown. The responses of Dunaliella also differed from those reported for diatoms. Some diatoms
(but not all) contain similar amounts of chlorophyll a, whether grown at low or high light intensities (see
Kirk, 1983, p. 305); and with respect to RuBP carboxylase, the activity per cell in Phaeodactylum
tricornutum increased over sixfold between about 10 and 200 (Beardall & Morris, 1976). Thus it appears
11
Fig 1.A stoichiometric representation of the generation of NADPH and ATP during non-cyclic photosynthetic
electron transport in the pigment-containing membranes of chloroplasts.
that, while photosynthetic capacity is determined by the capacities for photosynthetic transport and RuBP
carboxylation, the mechanism(s) by which this is achieved may not be the same in all species.
As the efficiency of light absorption is not expected to influence photosynthetic capacity, the variations in
chlorophyll a content that are normally observed should not directly influence this parameter. These
changes in chlorophyll a level will, however, influence Pmax, because Pmax is an expression of
photosynthetic capacity per unit of chlorophyll a. The independence of photosynthetic capacityand the
dependence on Pmaxon chlorophyll a level needs to be kept in mind when chlorophyll a levels vary
considerably. Variation appears to be more common in phytoplankton than in leaves of terrestrial plants,
but the tendency in phytoplankton appears to be in the direction of high chlorophyll levels in low-light
adapted cells. There is no strong indication that the opposite trend (low chlorophyll levels in highlight
adapted cells) extends to the point where chlorophyll levels are markedly lower (and thus Pmax values are
markedly higher) than for the leaves of sun plants on land.
PHOTOSYNTHETIC ELECTRON TRANSPORT AND LIGHT-HARVESTING
POTENTIAL OF PHYTOPLANKTON
PHOTOSYNTHETIC ELECTRON TRANSPORT
Theoretically, it should be possible to demonstrate that chloroplast membranes isolated from marine algae
are able to evolve oxygen during photosynthetic electron transport at a rate comparable with an assimilation
number of 6.4 (Table II). This is because the photo-assimilation of one molecule of CO2 utilises 2 NADPH,
and 2 NADPH are produced by the photosynthetic electron transport that releases one molecule of O2, as
shown in Figure 1. The oxidation of two molecules of water by a poorly understood (Avron, 1981), Mndependent system (black boxs represents oxidation state) releases one molecule of oxygen, four
protons (into the thylakoid lumen) and four electrons. Each electron is moved through the electron transport
chain, receiving as it goes two boosts of light energy (from captured photons) to move it from the reaction
centre chlorophylls P-680 and P-700 to (respectively) the relatively electronegative components Qox (a
special plastoquinone) and the Fe3+ of bound iron-sulphur centres. Thus, the complete transit of the four
electrons requires eight photons. During this electron transport, four more protons are translocated from the
stroma to the thylakoid lumen by the plastoquinone (PQ) oxidation/reduction cycle. The total of eight
accumulated protons subsequently moves out through a coupling factor that uses the energy in this proton
gradient to synthesise 2.67 ATP. Four of the protons return to the plastoquinone cycle, while the other four
(conceivably those released from the water-splitting step) rejoin, in effect, their four electrons when the
latter arrive at NADP+, to form NADPH. This NADPH may then be used in CO2 fixation (see Fig.3, p. 28).
As mentioned above, the processes are balanced so that, during carbohydrate synthesis, one CO2 is fixed for
each O2 evolved and each eight photons captured: (a) , (b) as shown in Figure 3, exactly are used during the
conversion of one CO2 to carbohydrate.
Excellent representations of the dynamics of photosynthetic electron transport have recently been
presented by Gounaris, Barber & Harwood (1986) and Murphy (1986). These authors describe how
plastoquinone and (probably over shorter distances) plastocyanin, may diffuse along thylakoid membranes,
moving reducing equivalents between three intrinsic supermolecular complexes: (1) photosystem II with
12
GRAHAME J.KELLY
associated light-harvesting pigment-proteins and proteins involved in water-splitting, (2) cytochromes b6

and f and iron-sulphur protein, and (3) photosystem I with associated light-harvesting pigment-proteins and
proteins involved in ferredoxin reduction.
The light-harvesting pigment-proteins of plant leaves, green algae and phycobiliprotein-containing algae
have been rather well characterised (Hiller & Goodchild, 1981; Gounaris et al., 1986; Murphy, 1986), and
descriptions of the comparable pigment-proteins from diatoms and other algae containing chlorophyll c are
now becoming available (Brown, 1988; Hiller, Larkum & Wrench, 1988; and references therein). In contrast,
studies of the function of chloroplast membranes from these algae are few, and the highest measured rates
of O2 evolution are equivalent to an assimilation number of only 1.4 (Popovic, Colbow, Vidaver & Bruce,
1983; Samuelsson & Prezlin, 1985; Sandmann, 1985), well below the average of 6.4 obtained for the Pmax
of intact phytoplankton cells (Table II). If Pmax is indeed limited by the rate of photosynthetic electron
transport (specifically, by the rate of re-oxidation of reduced plastoquinone: Harris 1978; Richardson et al.,
1983) then, in order to support the high rates of photosynthesis reported for phytoplankton, evidence must
be found of higher rates of O2 evolution by algal photosynthetic membranes.
LIGHT-HARVESTING POTENTIAL
A second aspect of the conversion of light energy to chemical energy is to consider, from first principles,
how it is possible that open-ocean phytoplankton, which contain only 4% of the worlds chlorophyll, are
capable of carrying out 24% of the production (Table I) using the low irradiances available to them at the
depths where most live.
The average chlorophyll content of the open ocean is around 30 mgm2 (Whittaker & Likens, 1975).
From calculations based on Falkowski (1981), it is estimated that the cells containing this 30 mg
chlorophyll could process mg chlorophyll a (molecular weight 894) contains molecules, and therefore
would be incorporated into 1016 oxygen-evolving units (OEUs), each involving 2000 molecules
chlorophyll (plus other machinery; the OEU is the ratio of the chlorophyll molecules to the evolved O2
molecules under saturating flashes of light; it is not necessarily a structural entity). The OEUs process
eight photons per turnover (Fig 1). With turnover time of s (mean of the three fastest marine microalgal
values in Fig 1 of Falkowski, 1981), 1016 OEUs would process photonss1, or (because 1 E contains [i.e.
1 mole] of photons). A value higher than would be obtained if faster turnover times and/ or smaller units were
entered into the calculation, but Falkowski (1981) and Sukenik, Bennett & Falkowski (1987) present
minimum values of about 2.4 ms and 3.5 ms, respectively, for turnover time, and a minimum of 2000 for
OEU size. Higher values were obtained for cells grown under low light intensities, which suggests the
calculated capacity of would be realistic for field populations of phytoplankton. This capacity of is
equivalent to only 2% of the photosynthetically active radiation that arrives at the sea surface during full
sunshine (i.e. : Harris 1978; Richardson et al., 1983), but of course it is equivalent to a higher percentage of
the lower irradiances available at the depths where most phytoplankton occur (see Lorenzen, 1976; Kirk,
1983, pp. 237 and 242).
Nevertheless, this light-harvesting capacity of is ample to provide the assimilatory power to perform the
estimated in situ photosynthesis of 69 g carbonm1.yr1 (from Table I, and ocean area of ). Because 69 g
carbon is 5.75 moles, and because the photo-assimilation of each mole of carbon requires at least 8 moles
photons (i.e. 8 E), then a total of 46 Eyr1 must be captured, or Admittedly, this is a theoretical minimum,
based on a quantum yield of 1/8 (1 CO2 fixed per 8 photons used). It is equivalent to 9% of the potential
light capture of . This calculation is, in effect, the photochemical equivalent of the earlier calculation that
13
gave the actual assimilation number for open ocean productivity (from Table I) as 7% of the mean potential
value (from Table II).
Both this calculation and the earlier one, however, represent theoretical extremes. They are based on a
quantum yield of 1/8, whereas actual quantum yields seldom exceed 1/10 (Myers, 1980; Priscu, 1984;
Dubinsky, Falkowski & Wyman, 1986; but see Osborne & Geider, 1987). This raises the light requirement
to Furthermore, to compensate for dark respiratory losses, and to accommodate the extra photochemical
energy needed to assimilate nitrogen (including the substantial energy investment of 16 photons to reduce ),
produce lipids, and power energy-dependent membrane transporters, a value of (say) would be more
realistic.
Thus, the cells under the average m2 of ocean actually use about one-seventh of the light energy they are
capable of using This relatively low value presumably reflects imperfect light capture because of such
factors as uneven packaging of chlorophyll within cells, reaction centres being temporarily closed when
photons arrive, optical properties of cell walls and, of course, the cells sometimes being at depths where
available irradiance is low.
If these estimates are correct, the capacity of algae to convert light energy into biomass restricts ocean
photosynthesis to a ceiling of not more than seven times the assimilation number of 0.43 (the estimate
calculated from Table I), and this ceiling would only be reached if all the phytoplankton were saturated with
light every day for 12 h. The assimilation number would then increase to 3.0 which, perhaps not
incidentally, is close to the maximum considered possible for land plants (Delaney & Walker, 1978). Thus,
it must be concluded that if ocean photosynthesis is greater than estimated at present, it must be a
consequence of one or more of the following: (1) the phytoplankton being more saturated with light than
previously believed, (2) the oceans phytoplankton biomass being under-estimated, (3) photochemical
reactions being unexpectedly efficient.
EFFICIENCY OF CONVERSION OF RADIANT ENERGY TO BIOMASS
The use of 46 Einsteins of light to fix 69 g carbon does not mean that all the energy of this light is converted
to chemical energy. The maximum conversion theoretically possible is 34% with 680 nm light. This value is
obtained from the following. The eneregy content of a Thus, the energy in 46 Einsteins of light The energy
released by burning an amount of glucose containing 69 g carbon (i.e. 0.96 mole) is, however, only 34% of
this, i.e.
When light of shorter wavelengthsand therefore consisting of higher-energy photonsis harvested (as
is common in the marine environment where accessory pigments such as fucoxanthin and peridinin collect
blue-green light), the theoretical maximum efficiency of conversion is lower, because the extra energy
content of the blue-green photons, as compared with 680 nm photons, is lost as radiation-less (thermal) deexcitation before any conversion of light energy to chemical energy begins (Walker, 1979). In addition, the
conversion efficiency is further reduced if the more realistic quantum yield of 1 CO2 fixed per. 10 photons
is adopted. Thus, with this quantum yield and 500 nm light, the maximum possible conversion reduces to
19%. In practice, actual energy conversion is well below the theoretical maximum because only a fraction
of the available photons are captured and used (see Kirk, 1983, p. 237). For naturally occurring
phytoplankton, one of the higher measurements of photosynthesis4 g carbon fixedm2day1 was
obtained off the Coast of Peru (Strickland, Eppley & Rojas de Mendiola, 1969). If these algae were from a
depth where average irradiance was 300 then the efficiency of energy conversion would have been 6%. By
contrast, a coastal pond culture of Phaeodactylum tricornutum converted 13% of the photosynthetically
active radiant energy incident on the pond surface (Thomas et al., 1984). On a global scale, only about 0.
14
GRAHAME J.KELLY
Fig 2.Tenfold elevation of the intracellular CO2 concentration in marine algae by movement of 2 mM from outside at
pH 8.2 to inside at pH 7.2.
12% of the energy in photosynthetically active radiation reaching the ocean surface is, however, assimilated
in phytoplankton production (based on a fixation rate of 69 g carbon fixedm2yr1, and an average
irradiance each 12-h day of see Fig. 7, p. 38). Lieth (1973) gives an even lower estimate of 0.07%. These values
appear small. The radiant energy available at the depths where phytoplankton grow is, however, much
lower than at the surface, and if all cells are, on average, at the 5% light level (i.e. ) then the efficiency of
conversion of the light energy actually available is a more respectable 2.4%. This value agrees closely with
that recently obtained in the field by Kishino, Okami, Takahashi & Ichimura (1986). Using sophisticated
instrumentation, these authors determined that the efficiency was 5% at the 1.5% light level.
INORGANIC CARBON UPTAKE

Inorganic carbon exists in water as CO2, H2CO3, and (Raven, 1970; Kremer 1981a). Water in equilibrium with
the atmosphere contains dissolved CO2 at a concentration of 10 M. This concentration is little influenced
by either pH or salinity. Thus, the oceans contain But CO2 dissolved in water is in equilibrium with H2CO3
and according to: From this equation, it is clear that the concentration of HCO3 will vary with pH. In salt
water, H2CO3 is half-dissociated at pH 5.93 (Raven, 1970), at which pH the concentrations of CO2 and will
both be 10 M; as pH increases, the concentration of increases. Consequently, the ocean, which is at a
slightly alkaline pH of 8.2, contains at close to 2mM, 200 times the concentration of CO2.
The species of inorganic carbon used for photosynthesis is CO2, which is the substrate for RuBP
carboxylase. A low level of CO2 in the environment can limit photosynthesis (the growth of wellilluminated C3 plants on land is CO2-limited). In water, the problem becomes greater, because the rate of
diffusion of CO2 in water is less by a factor of 105 than that in air (Raven 1970).
It may not be surprising, then, that current evidence points to as the species of inorganic carbon taken up
by marine microalgae (Colman & Gehl, 1983; Aizawa, Tsuzuki & Miyachi, 1986; Burns & Beardall, 1987;
Dixon & Merrett, 1988) and seaweeds (Beer & Eshel, 1983; Brechignac & Andre, 1984; Bidwell &
McLachlan, 1985; Cook, Lanaras & Colman, 1986). Experiments with Dunaliella, Synechococcus, and
Ulva indicate that the uptake is not via simple diffusion into the cell, but rather that a carrier (presumably a
protein) actively pumps into the cell, using energy (probably ATP) generated during photosynthesis. In
some instances, accumulation of inorganic carbon in the cell to concentrations several- to many-fold that of
the surrounding medium was detected (Zenvirth & Kaplan, 1981 ; Badger & Andrews, 1982; Colman,
1984). The taken up by cells must be protonated to form H2CO3, and this must then be dehydrated to CO2
for use by RuBP carboxylase. The slow dehydration step is catalysed by carbonic anhydrase, a common
enzyme in photosynthetic cells, including marine microalgae (Aizawa & Miyachi, 1984; Lucas & Berry,
1985; Burns & Beardall, 1987; Dixon & Merrett, 1988).
If the pH of the cytoplasm of phytoplankton cells is close to that of leaf cells (about 7.2) then the
instantaneous effect of moving 2 mM into the cytoplasm at this pH would be to increase the intracellular
CO2 concentration to over 100 M (Fig 2), or even higher if active uptake raises the intracellular
concentration about 2 mM. This would have a profound influence on the likelihood of photorespiration
occurring in marine phytoplankton (see p. 31).
15
Fig 3.The Calvin cycle of CO2 fixation. Lower: the cycle drawn to show net conversion of 3 CO2 to a 3-carbon sugar
(triose-P) ; note that the three CO2-accepting molecules (3 RuBP) are fully regenerated by the cycle. Upper: details of
the reactions in which CO2 is fixed, and the products (two glycerate-3-P) converted to two triose-P in reactions that use
ATP and i.e. it is in these two reactions that most of the solar energy captured by the photochemistry (Fig 1) is
incorporated into carbohydrate.
CARBOXYLATION
RuBP CARBOXYLATION
At least half a dozen enzymes can fix CO2 into organic compounds, but only one of these is connected to a
series of reactions that permits the net fixation of CO2, and therefore plant growth (Walker, 1974; Kelly,
Latzko & Gibbs, 1976). This enzyme is RuBP carboxylase and the sequence of reactions (popularly termed
the Calvin cycle) permits plant growth because it is able to reduce CO2 to carbohydrate while at the same
time regenerating the original amount of the CO2-acceptor (RuBP). For example, in Figure 3 the net
reduction of three CO2 to one triose-sugar occurs concomitantly with the re-synthesis of the three RuBP
(ready, as it were, to fix three more CO2). The activity of RuBP carboxylase in phytoplankton must
therefore be comparable with observed photosynthesis rates, i.e. able to accommodate the measured
assimilation number (average 6.4 in Table II). Relative to land plants, few measurements of the carboxylase
activity have been made; the average of those available is equivalent to an assimilation number of only 2.0
(Table V). In contrast, numbers averaging 7.6 are reported for the activities in the leaves of land plants
(Lilley & Walker, 1975; Delaney & Walker, 1978; Yokota & Canvin, 1985; Kobza & Edwards, 1987;
Ramachandra Reddy & Das, 1987; Terashima & Evans, 1988) which are not claimed to have such high
photosynthetic rates as are claimed for phytoplankton. Higher activities will need to be demonstrated,
especially given the conclusion of Sukenik, Bennett & Falkowski (1987) that Pmax can be limited by
carbon fixation rather than electron transport.
Several reports present values for RuBP carboxylase activity in units that cannot be converted to
assimilation numbers. Glover & Morris (1979) compared the activity per cell with maximum photosynthesis
rates in seven cultured microalgae; the average activity was only 34% of the average photosynthetic rate
(Table V). Other workers have presented activity in unwieldy units that the reader must translate, e.g. Smith
& Platt (1985) use untransformed units, d.p.m. L1 hr1.
Taken together, these results imply that either photosynthesis rates have been over-estimated, or RuBP
carboxylase activities have been under-estimated. Given that the extraction of active enzymes from algae,
particularly diatoms and dinoflagellates, is not easy (Everest, Hipkin & Syrett, 1986), and neither is the
assay of RuBP carboxylase, the second possibility seems to be the more likely, although some contribution
from the other is not ruled out.
PEP CARBOXYLATION
Most scientists do not, however, favour either of the above explanations. Rather, they suggest that the
deficit in measured RuBP carboxylase activity may be made up by the carboxylation of
phosphoenolpyruvate (PEP). Two enzymes can carboxylate PEP: PEP carboxylase e.g., in dinoflagellates,
and PEP carboxykinase e.g., in diatoms and macrophytic brown algae (Akagawa, Ikawa & Nisizawa, 1972;
Holdsworth & Bruck, 1977; Kerby & Evans, 1983; Descolas-Gros & Fontugne, 1985). The finding that
marine algae have a significant potential for PEP carboxylation (Karekar & Joshi, 1973; Beardall, Mukerji,
16
GRAHAME J.KELLY
Glover & Morris, 1976) originally resulted in suggestions that their photosynthetic mechanisms were akin
to those of terrestrial C4 plants and CAM plants (see below), which use PEP carboxylation extensively for
cap
TABLE V
Laboratory and field measurements of RuBP carboxylase activity and photosynthesis
Assimilation number
Alga or locality
Carboxylase mg
carbon.mg
Photo-synthesis chl a Carboxylase/

1h1
Photosynthesis %
Reference
Phaeodactylum
tricornutum
Boothbay Harbor
Phaeodactylum
tricornutum
Gulf of Maine
3.0
5.9
51
4.0
1.1
?
0.56
>100
0.4a
8a
Seven cultures
34a
Amphidinium
carterae
1.1
Pyrocystis noctiluca
Bedford Basin
Dunaliella tertiolecta
Skeletonema
costatum
Synechococcus spp.
in eddy surface waters
1.2
?
5.4
0.5
4.0
1.6
6.8
3.3
30
14
79
15
1.0a
1.0a
100
Beardall & Morris,

1976
Beardall et al., 1976
Holdsworth &
Colbeck, 1976
Glover & Morris,
1979
Glover & Morris,
1979
Appleby, Colbeck,
Holdsworth &
Wadman, 1980
Rivkin et al., 1982
Smith et al., 1983
Sukenik et al., 1987
Mortain-Bertrand et
al., 1987
Przelin et al., 1987
Approximate mean values.
turing CO2, but this idea lost popularity when it was found that algal photosynthetic rates correlated with
RuBP carboxylase activity, but not with PEP carboxylase activity (Mukerji, Glover & Morris, 1978; Glover
& Morris, 1979; Smith, Platt & Harrison, 1983).
Terrestrial C4 plants and CAM plants utilize PEP carboxylase to capture CO2 in, respectively, the C4
pathway and crassulacean acid metabolism (CAM); hence the terms C4 plants and CAM plants. These
mechanisms are not alternatives to the Calvin cycle because, by themselves, they would not permit plant
growth. In any event, it is quite unlikely that any unicellular marine alga could be classed as a C4 plant or
CAM plant, because the former requires co-operation between two types of cells in the one plant, while the
latter is an adaptation for survival in arid environments. Consequently, marine algae are almost certainly
C3 plants. The origin of the terms C3 and C4 have, however, caused some confusion. C3 refers to the
fact that a three-carbon compound (glycerate-3-P, see Fig 3) is the first product of CO2 fixation, whereas C4
denotes that a four-carbon compound (oxaloacetate, see Fig 4) is initially observed. As phytoplankton
synthesise more protein and less carbohydrates than do multicellular plants, much triose-P produced by the
Calvin cycle must move via PEP to produce the carbon skeletons needed for amino-acid biosynthesis. A
good portion of this PEP is carboxylated with CO2 to produce oxaloacetate (which is, itself, a carbon
17
Fig 4.The Calvin cycle as the producer of PEP for PEP carboxylation. The maximum long-term ratio of PEP
carboxylation: RuBP carboxylation during growth is 1:3. If two thirds of the triose-P (representing the product of CO2
fixation) is used for the synthesis of carbohydrates, lipids, and amino acids not derived from oxaloacetate (as is usual),
then the ratio reduces to 1:9. Consequently, attempts to credit PEP carboxylation with more than 10% of the total
photosynthetic carbon fixation are fundamentally in error.
skeleton, and is a precursor of several others). Although this gives a C4 flavour to algal CO2 fixation, the
principal purpose of oxaloacetate synthesis in marine algae (amino-acid synthesis) is entirely unrelated to that
of C4 and CAM plants (a CO2-capturing mechanism).
Nevertheless, the concept that PEP carboxylation may make up for a perceived insufficiency of RuBP
carboxylation has persisted, and has supported a considerable amount of theoretical discussion (Morris,
1980; Priscu & Goldman, 1983; Smith et al., 1983). But, as emphasised by Figure 4, the concept itself is
wrong. In growing photosynthetic cells, three CO2 must be fixed by RuBP carboxylase in order to generate
a PEP before a CO2 can be fixed by PEP carboxylase or PEP carboxykinase. This is because there is no
known biochemical pathway whereby the product of PEP carboxylation (oxaloacetate) can be metabolised
so that three of its four carbons are used to regenerate CO2-acceptor (PEP) while the other is kept in the
reduced form and used for plant growth (Kelly et al., 1976). Consequently, since one net PEP carboxylation
requires three prior RuBP carboxylations, the maximum contribution of PEP carboxylation to total
photosynthetic CO2 fixation is 25%. This theoretical limit reduces to about 10% in practice because not all
amino-acid skeletons can be derived from oxaloacetate, and because protein is only one of the major products
of cell growth; others, for example sugars, polysaccharides and lipids, cannot be synthesised from
oxaloacetate without the loss of the CO2 that was fixed during PEP carboxylation. The practical value of
about 10% for the contribution of PEP carboxylation is in good agreement with experimental values of 6.7
to 12.7% recently obtained for two diatoms (Mortain-Bertrand, Descolas-Gros & Jupin, 1988).
Finally, there may be stages in the growth cycle of an alga where PEP carboxylation equals or exceeds
RuBP carboxylation. Microalgal cultures in the stationary phase appear to have this attribute (Mukerji et al.,
1978; Glover & Morris, 1979), but these cells are obtaining PEP from a carbohydrate reserve (e.g. mannitol
in brown algae) previously synthesised entirely through RuBP carboxylation (Kremer, 1981b).
PHOTORESPIRATION AND MARINE ALGAE
DOES PHOTORESPIRATION OCCUR IN MARINE ALGAE?
Photosynthetic cells of terrestrial C3 plants exhibit a major light-dependent set of reactions that results in O2
uptake, CO2 release, and the consumption of energy (Fig 5). Due to its light dependence and gas exchanges,
it has been called photorespiration, but it is otherwise not at all like dark (mitochondrial) respiration.
Photorespiration occurs when O2 replaces CO2 in the RuBP carboxylase (now called carboxylase/
oxygenase) reaction, leading to the formation of one glycerate-3-P, plus a smaller (2-carbon) compound
called glycolate (not two glycerate-3-P, as in Fig 3). A series of six reactions then converts two glycolate
molecules to one glycerate-3-P and one CO2 (Fig 5). If all molecules of RuBP were oxygenated, plant
growth would cease. The combination of the enzymes relative affinities for CO2 and O2 and the relative
concentrations of these two gases in air results, however, in a situation somewhat akin to Figure 5b where
carboxylation exceeds oxygenation sufficiently for plant growth to proceed.
The real function of photorespiration is not yet known. It may act as a release valve to dissipate
photosynthetically generated energy, as in Figure 5a, when the CO2 supply is restricted (e.g. during periods
18
GRAHAME J.KELLY
Fig 5.Photorespiration. a, at the CO2 compensation point, where the amount of CO2 lost by photorespiration is exactly
balanced by the amount fixed in the Calvin cycle; at this state, where the ratio of RuBP carboxylated: oxygenated is 1:2,
9 ATP and 6 NAD(P)H are wasted, while plant growth is zero. b, the situation with terrestrial C3 plants in normal air,
where carboxylation to oxygenation is approximately 1:0.7, and growth (represented by the synthesis of a molecule of
sucrose from 12 CO2) in the presence of photorespiration is possible.
of water stress when stomates close), thereby preventing over-reduction of the photochemical apparatus
and subsequent photoinhibition (see below; Osmond, 1981; but see Powles, Comic & Louason, 1984).
Nevertheless, it still proceeds in C3 plants when stomates are open, reducing productivity by 30 to 50%. In
C4 plants photorespiration is, however, inhibited because the C4 pathway concentrates CO2 in the vicinity of
RuBP carboxylase, and because O2 and CO2 are straightforward competitors for entry onto the enzymes
active site, the increased CO2 concentration overwhelms the oxygenase reaction so that it is effectively
eliminated.
A different mechanism appears to produce a similar consequence in marine algae. As mentioned on p.
26, the effects of pH and/or the active uptake of inorganic carbon lead to intracellular CO2 concentrations of
100 M or more in marine algae. Consequently, the CO2:O2 ratio would be expected to increase such that,
in these cells too, the oxygenase reaction would be overwhelmed.
This does not mean that marine algae may not be capable of photo-respiration. They can synthesise
glycolate (Lloyd, Canvin & Culver, 1977; Glover & Morris, 1981; Fogg, 1983) and they possess enzymes
for converting it to glycerate (Paul & Volcani, 1976). But despite claims that photorespiration may occur
(Burris, 1977; Morris & Glover, 1981), the likelihood of it occurring under natural conditions is small
(Lloyd et al., 1977; Birmingham, Coleman & Colman, 1982; Burns & Beardall, 1987), and most recent
work showing that O2 has little or no effect on the rates of photosynthesis by marine algae argues against it
(Colman & Gehl, 1983; Colman, 1984; Bidwell & McLachlan, 1985; Beer & Israel, 1986; Cook & Colman
1987; Johnston & Raven, 1987). A study of coccoid marine cyanobacteria by Glover & Morris (1981)
indicated that these marine photosynthetic cells have a greater potential for photorespiration than have
eukaryotic marine algae, but even in this case the magnitude of photorespiration in the presence of 2 mM
was near zero.
One further consideration, however, counteracts these arguments. Build-up of CO2 in cells (due to effects
of pH and/or active uptake) will lead to increased photosynthesis and, consequently, increased O2 evolution.
This may produce locally high concentrations of O2 in chloroplasts, favouring RuBP oxygenase activity and
photorespiration. Evidence for such an event in three freshwater green microalgae provided with inorganic
carbon (CO2 plus HCO3) at concentrations up to 0.6 mM has recently been obtained (Yokota & Kitaoka,
1987). Similar experiments with marine microalgae growing in 2 mM inorganic carbon are required.
PHOTORESPIRATION AND PRODUCTIVITY ESTIMATES
If photorespiration in phytoplankton does occur, it would not affect productivity estimations based on
measurements of O2 evolution (using the Winkler technique), as suspected by some workers (see Round,
1981, p. 259). Reference to Figure 5a shows that a zero change in CO2 (one CO2 taken up, and one
released) correlates with a zero change in O2: three O2 are used two during oxidation of two RuBP, and
net of one during oxidation of two glycolatewhile three O2 are liberated from water (see Fig. 1, p. 22)
during the photosynthetic electron transport that generates the required reducing power (five NADPH and
one NADH; Fig 5a). The amount of O2 used during glycolate oxidation is the same whether the glycolate is
oxidised by an oxidase, as shown in Figure 5, or by a mitochondrial dehydrogenase linked to respiratory O2
19
consumption; both types of oxidation have been detected in algae. With photorespiration proportionately
less than photosynthesis, as when net CO2 fixation proceeds (Fig 5b), the net O2 evolution will equal the net
CO2 assimilation, as if this CO2 fixation were occurring in the absence of photorespiration.
Photorespiration would affect productivity estimations using the 14C-technique, but not dramatically. It is
most probable that total CO2 fixation minus photorespiratory CO2 evolution would be estimated, because
photorespiratory and photosynthetic metabolisms share common intermediates and are obligatorily
interconnected (Fig 5), so that 14C entering the Calvin cycle will also enter photorespiration after a short
delay. In a sense, the result would be the same as for O2 measurements, i.e. (net) CO2 fixation would be
measured as if it were occurring in the absence of photorespiration.
PHOTOINHIBITION
If photorespiration is absent, the question arises as to how phytoplankton dispose of excess
photosynthetically generated energy. Failure to dispose of this excess energy is thought to be one cause of
photoinhibition, whereby over-reduction of electron transport components causes a chain of events that results
in damage to one or more of the components that make up the reaction centre of photosystem II
(Allakhverdiev, etlkov, Klimov & etlik, 1987; Demeter, Neale & Melis, 1987; Lidholm, Gustafsson &
quist, 1987; Kirilovsky, Vernotte, Astier & tienne, 1988; Ohad, Koike, Shochat & Inoue, 1988). The
damage can become so extensive as to be irreversible, and cell death follows. Other possible mechanisms for
protecting against photoinhibition implicate (1) carotenoids; (2) use of energy to reduce O2 to the
superoxide anion (Mehler reaction) which, however, must subsequently be dealt with; (3) spillover of
energy from photosystem II to photosystem I; (4) cyclic electron flow around photosystem II; and (5)
reduction in the level of light-harvesting pigments (Samuelsson et al., 1985; Ben-Amotz, Gressel & Avron,
1987; Demmig, Winter, Krger & Czygan, 1987; Geider, 1987; Siefermann-Harms, 1987; Falkowski,
Kolber & Fujita, 1988). In addition, as Harris (1978) has argued, phytoplankton populations may normally
largely avoid photoinhibition, either passively (vertical mixing; sinking), or actively (motile microalgae may
swim away form excessive light). Support for this viewpoint has come from Vincent, Neale & Richerson
(1984), who describe an extensive (but still reversible) photoinhibition of phytoplankton each morning in
the high-altitude Lake Titicaca (Peru-Bolivia) when the phytoplankton became temporarily trapped under
extreme irradiance by a near-surface thermocline.
On the other hand, algae that are continually exposed to high light intensities are apparently more resistant
to photoinhibition. Seaweeds, Synechococcus, Thalassiosira pseudonana, and a population of benthic
microalgae dominated by Euglena obtusa and Pleurosigma angulatum all showed no evidence of
photoinhibition under almost full sea-surface irradiance (Penniman & Mathieson, 1985; Mills & Wilkinson,
1986; Przelin, Putt & Glover, 1986; Kana & Glibert, 1987a; Sakshaug, Demers & Yentsch, 1987). Thus,
there appears to be a broad spectrum of tolerance to photoinhibition in algae. At least some of this variation
may be an adaptation, in that photosynthetic cells exposed daily to high irradiance contain less lightharvesting pigments per electron-transport chain (compared with shade-adapted cells), and are thus less
likely to overload their light processing machinery (Osmond, 1981).
To a certain degree, microalgae may avoid photoinhibition by using excess photochemical energy rather
than allowing it to accumulate to the point where all reaction centres become occupied. Such utilisation
could involve the assimilation of more CO2 than is required for growth. This may help to explain why
stressed (e.g. nitrogen-deficient) cells of some species excrete large quantities of carbohydrates, as
polysaccharides or glycolate, during photosynthesis (Jensen, 1984; Vieira & Myklestad, 1986; Al-Hasan &
20
GRAHAME J.KELLY
Fogg, 1987); these excretions would be the end-product of energy harvested in a process not linked to cell
growth (see also Dring, 1982, p. 75). Exudation of low molecular weight organic compounds by nonstressed cells is, however, believed by Bjrnsen (1988) to be a consequence of passive diffusion through the
cell membrane.
Not only high intensities of photosynthetically active radiation, but also the much lower intensities of UVB light (290320 nm) normally encountered in the solar spectrum cause photoinhibition of algae that occur
high in water columns (Harris, 1978; Richardson, Beardall & Raven, 1983, Dhler, 1984; Jokiel & York,
1984; Vincent et al., 1984, Wood, 1987). The mechanism of this inhibition is not known. Likely
explanations are that the nucleic acids or components of the photosynthetic electron transport chain are
damaged. The photosynthetic cells of leaves of terrestrial plants are protected from UV-B-induced
photoinhibition by flavonoid compounds in the non-photosynthetic cells of the leaf epidermis (Caldwell,
1981).
DARK (MITOCHONDRIAL) RESPIRATION
DOES MITOCHONDRIAL RESPIRATION PROCEED DURING
PHOTOSYNTHESIS?
In productivity experiments using the question arises whether gross photosynthesis (total CO2 fixation
itself) or net photosynthesis (total CO2 fixation minus CO2 loss through respiration and/or photorespiration)
is measured. Investigations of this question have reached differing conclusions: that it measures gross
photosynthesis (Dring & Jewson, 1982), net photosynthesis (Smith & Platt, 1984), or some value in
between, depending on the growth rate (Harris & Piccinin, 1983).
This problem will not be solved until the extents of mitochondrial respiration (in the dark and in the light)
and photorespiration are known. There are, however, some indications. First, as outlined above,
photorespiration may not occur in phytoplankton living in natural conditions, and even if it did, it would not
be likely to affect productivity measurements. Thus, only dark (mitochondrial) respiration need be
considered. It is not known whether the dark (mitochondrial) respiration of photosynthetic cells is
suppressed during photosynthesis, and if so, to what extent (Kelly, 1983). In one sense, respiration may be
unnecessary in that its prime purpose (complete oxidation of carbohydrate to CO2 in order to generate
energy) would seem inappropriate in a cell harvesting light energy and reducing CO2 to carbohydrate. A
portion of the Krebs cycle (tricarboxylic acid cycle) would, however, need to proceed at a low rate in order
to generate -ketoglutarate, which is the precursor of four amino acids and of chlorophyll. This could
proceed as shown in Figure 6, in which a net evolution of one CO2 per -ketoglutarate synthesised would
occur. But note that, for the growth of cells containing 50% protein and 1% chlorophyll (dry weight basis),
the required rate of this partial Krebs cycle would lead to a CO2 evolution equivalent to only 2% of the
photosynthetic CO2 fixation.
Despite this requirement for some Krebs cycle activity for growth, a concomitant respiratory O2 uptake
would not necessarily occur because the reducing power (NADH) generated during -ketoglutarate
synthesis could be delivered to the cytosol and used there, as shown in Figure 6. The respiratory electron
transport chain would then remain inactive.
Some recent experiments with the freshwater green microalgae Chlamydomonas reinhardtii and
Selenastrum minutum suggest, however, that both the Krebs cycle and respiratory electron transport
function during photosynthesis in these algae (Peltier & Thibault, 1985; Husic & Tolbert, 1987; Weger,
Birch, Elrifi & Turpin, 1988), but the extent to which this is so in other algae is not known, and once again
21
Fig 6.Limited operation of the mitochondrial Krebs cycle during photosynthesis in order to generate -ketoglutarate.
Two molecules of glycerate-3-P (from photosynthetic CO2 fixation) are converted to one -ketoglutarate and one CO2,
and two NAD+ are reduced in the process. A metabolic shuttle may dispose of this reducing power in the cytosol (as
shown) or respiratory electron transport may oxidise it, with consumption of one O2.
the question of function arises. With respect to the function, Husic & Tolbert (1987) have alluded to the
alternative (cyanide-resistant) pathway of respiratory electron transport in plant mitochondria. This pathway
is not coupled to ATP synthesis and is therefore a means of burning off excess carbohydrate (Lambers,
1982), an intriguing possibility in view of the suggestion that marine algae may not be able to dispose of
excess energy by photorespiring as land plants do. The alternative pathway, however, generates superoxide
anions and peroxide, thus mechanisms for the removal of these toxic substances would need to accompany
any alternative pathway activity.
All of these considerations have been subsequently disturbed by an experiment, elegant in its simplicity,
in which an inhibitor of mitochondrial electron transport was shown to inhibit photosynthesis by barley leaf
protoplasts, but to have no effect on the photosynthesis of chloroplasts isolated from these protoplasts
(Krmer, Stitt & Heldt, 1988). It was concluded that mitochondrial electron transport is required during
photosynthesis to generate ATP for cytosolic metabolism, and that the ultimate electron donor is
photosynthetically-generated NADPH shuttled from chloroplasts to mitochondria, more or less by a
reversal (and extension) of the malateoxaloacetate shuttle shown in Figure 6. The advantage of this system
is that it is energetically efficient (3.8 ATP per 4 photons, compared with 1.3 ATP per 4 photons when the
ATP is generated during either cyclic or pseudocyclic electron transport in chloroplasts). It could therefore
be useful to phytoplankton cells growing in a low light environment, especially because these cells require
cytosolic ATP for protein synthesis (an ATP supply rate of about 7% of the rate of CO2 fixation is needed
only for the activation and attachment of amino acids to growing polypeptide chains), and to pump
inorganic carbon into cells (possibly an even more ATP-demanding process; Yokota et al., 1987).
Note that this system of producing ATP by oxidising NADPH of chloroplast origin involves
mitochondrial electron transport only; Krebs cycle activity would not be required. Thus, respiratory oxygen
uptake would occur, but respiratory CO2 evolution would not (other than that noted above for ketoglutarate synthesis). Phytoplankton appear to possess ample respiratory electron transport activity
(Kenner & Ahmed, 1975).
MITOCHONDRIAL RESPIRATION AND PRODUCTIVITY ESTIMATES
Of course, the extent of mitochondrial respiration during the night also needs to be evaluated for
productivity estimates. Most data indicate that the rate at which marine algae respire in darkness is
equivalent to about 10% of the light-saturated rate of photosynthesis (Harris, 1978; Falkowski & Owens,
1980; Taguchi, 1981; Richardson et al., 1983; Geider, Osborne & Raven, 1985; Smith & Geider, 1985;
Gerard, 1986). Assuming respiration occurs both day and night, then at maximum growth rates the net
photosynthesis would equal 80% of gross photosynthesis. This percentage may, however, be higher if
respiration is partially or completely inhibited during photosynthesis, as discussed above, and there is other
evidence for this (Burris, 1980; Scherer, Strzl & Bger, 1984). There is also evidence that any respiratory
CO2 released in illuminated cells is quickly re-assimilated by photosynthesis before it can leave the cell
(Scherer et al., 1984). This possibility, which was denied by Bidwell (1977), was proposed in the 1950s for
Dunaliella euchlora (Ryther, 1956).
22
GRAHAME J.KELLY
Fig 7.Efficiencies in marine production. Mean daytime surface irradiance of is equal to (Richardson et al., 1983), and
thus to and to Average photosynthesis (Table I) of 69 g carbonm2yr1 is converted to its energy equivalent as
described on p. 25. Average fish production is calculated by dividing total production at the end of food chains ( tonnes
fresh weight [Ryther, 1969], equivalent to approximately tonnes carbon) by total ocean area and then converting to
energy units as for the phytoplankton.
Although respiration appears to use only a small fraction of carbohydrate produced under light saturation,
it may become more significant to the balance of carbon metabolism under light limitation. Phytoplankton
commonly occur at depths where irradiance is low, so respiration could be important in assessing net
photosynthesis in the ocean, but to what extent is not clear; it has been estimated that 40% of gross
photosynthesis in the ocean is lost in dark respiration (see Burris, 1980) but some species, when
growing slowly in dim light, appear able to adjust their respiration to a correspondingly low level
(Falkowski & Owens, 1980; Geider, 1987; Langdon, 1987). Of course, if irradiance falls so low that
photosynthesis and respiration are equal, then growth will cease. At this point, the irradiance is termed the
light compensation point. Experiments indicate this point to range between low values near for diatoms
grown in low light, to high values of over for dinoflagellates (Falkowski & Owens, 1980; Rivkin, Seliger,
Swift & Biggley, 1982; Hobson & Guest, 1983; Geider & Osborne, 1986; Langdon, 1987).
CONCLUDING COMMENT
The efficiency with which solar energy is used to convert inorganic precursors into fish in the ocean is 0.
00014%, based on an average sea-surface irradiance of and an annual total fish production of tonnes carbon
(Fig. 7). Taking the value for marine algal photosynthesis to be 69 g carbon fixedm2yr1 (Table I, see p.
13), then the global efficiencies for the two sections of this conversion (i.e. sunlight to algae, and algae to
fish) are a little above 0.1 % each. For sunlight to algae, the value varies regionally from 0.02 to 5%; the
overall mean is relatively low (0.12%) because much light energy is atenuated by the overlying water
column before it reaches the algae (Kirk, 1983, p. 244), resulting in marine photosynthesis being, on
average, markedly light-limited. For algae to fish, the low value is a consequence of having about three
links, on average, in the marine food chain from the microscopic phytoplankton to the fish at the end of the
food chains (Ryther, 1969).
In time, the value for marine algal production, and thus the efficiency values shown in Figure 7, may be
revised. From the biochemical viewpoint, revisions may be needed when the extents of respiration and
photorespiration in marine phytoplankton are better understood. As emphasised in this review, upward
revisions cannot, however, be confidently based on high estimates of Pmax values for marine
photosynthetic cells unless it is demonstrated that these cells have a photosynthetic machinery with a
significantly greater capacity for CO2 fixation than that of the photosynthetic cells of terrestrial plants.
ACKNOWLEDGEMENTS
I am grateful for many helpful discussions with S.W.Jeffrey who introduced me to the marvellous minute
plants of the ocean, and with J.S.Parslow, who taught me much about their growth.
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THE ECOLOGY AND BEHAVIOUR OF ASCIDIAN

LARVAE*
IB SVANE
Kristineberg Marine Biological Station, Kristineberg 2130, S-450 34 Fiskebckstil,
Sweden
and
CRAIG M.YOUNG
Harbor Branch Oceanographie Institution, 5600 Old Dixie Highway, Fort Pierce, Florida
34946, USA
ABSTRACT Recent studies of ascidian larval biology reveal a diversity of structure and behaviour
not previously recognised. The introduction of direct methods for observing ascidian larvae in
situ has provided important insights on larval behaviour, mortality, and dispersal not possible with
the microscopic larvae of most other marine invertebrates. In the context of these recent advances,
this review considers the ecology of pelagic phases (egg, embryo, and larva) of the ascidian life
cycle and relates aspects of reproduction and larval biology to the recruitment, abundance, and
distribution of adult populations.
INTRODUCTION
The ascidian larva functions in site selection and dispersal while transporting adult rudiments between
generations (Berrill, 1955, 1957; Millar, 1971; Cloney, 1987). Interest in the ecology of ascidian larvae has
recently been stimulated by the introduction of new ideas and methods, most notably in situ observations of
living larvae. The resulting advances justify a reconsideration of ascidian larval ecology. From an
ecological standpoint, all pelagic phases of the ascidian life cycle (which may include eggs, embryos and
larvae) influence adult populations. Thus, our definition of larval ecology is broad; it includes reproductive
processes leading to the production of gametes and larvae, as well as post-settlement consequences of larval
processes.
The literature on larval evolution as it relates to ascidian and chordate phylogeny is large, and will not be
considered in the present paper. Reviews on ascidian biology dealing with aspects of reproduction and larval
ecology have been published by Millar (1971), Berrill (1975), and Cloney (1987), and detailed reviews on
* Harbor Branch Contribution No. 678.
THE ECOLOGY AND BEHAVIOUR OF ASCIDIAN LARVAE
29
Fig 1.Generalised life cycles of typical solitary ascidians (top) and compound ascidians (bottom). The diagrams
incorporate characteristics of many species; not all aspects (e.g., fusion of colonies) are present in the life cycle of any given
species.
ascidian metamorphosis have been presented by Cloney (1978, 1982). More recently, ascidian
metamorphosis and larval locomotion have been treated as parts of general comprehensive reviews by
Burke (1983) and Chia, Buckland-Nicks & Young (1984), respectively. It is our goal to bring together a
scattered literature that comprises ascidian larval ecology. While emphasising ecological aspects of larval
release, development, dispersal, behaviour, and settlement in relation to the distribution and abundance of
adult populations, we also deal with reproductive, morphological, and developmental problems that help to
elucidate aspects of ascidian larval ecology.
REPRODUCTION, FERTILISATION, AND LARVAL ANATOMY
MODES OF REPRODUCTION
Ascidians may be either oviparous (typical of most solitary ascidians), ovoviviparous (typical of most
compound ascidians), or viviparous (Fig 1). True viviparity in which nutrients are exchanged between
parent and embryo across a placenta-like structure is known to occur in only a single species, Hypsistozoa
fasmeriana (Brewin, 1959). Much of the earlier literature, including the classic works of Berrill (e.g. 1929,
1935, 1950) uses the term in reference to ovoviviparous species that retain embryos to hatching, but without
apparent transfer of nutrients after ovulation. In oviparous forms, fertilisation and all subsequent
developmental stages occur externally.
Ascidian embryology and developmental biology have been the subjects of numerous important studies
which have been reviewed by Cloney (1987) and Berrill (1975), and provided the theme for a recent
symposium (Lambert, 1982). Conklins (1905) study is still the classic description of cell lineage, although
there has been a late resurgence of cell lineage studies using modern fluorescent markers and immunological
techniques (Whittaker, 1987). The most common developmental pattern (urodele development) terminates
in the production of a swimming tadpole larva. Many molgulids and a few species in the family Styelidae
(Pelonia corrugata and Polycarpa tinctor) undergo direct development, bypassing the larval stage completely
(reviewed by Berrill, 1931; Millar, 1971; Young et al., 1988). In ascidians, such direct development is
known as anural development (Fig 2).
As in many other kinds of animals, larval size is correlated with the degree of parental protection.
Compound ascidians releasing fully developed larvae generally produce relatively few large larvae, whereas
the eggs released by oviparous solitary ascidians are relatively more numerous and result in the production
of much smaller, less differentiated tadpoles.
In many invertebrates, there appears to be a correlation between adult size and brooding (Menge, 1975;
Strathmann & Strathmann, 1982); within a given taxon, species with smaller individuals are more likely to
brood than those with larger individuals. If we define an individual as a single zooid, not a colony, the
relationship also seems to hold in ascidians. Accordingly, most colonial ascidians, having small zooids,
brood relatively large complex larvae which develop from large eggs. Among solitary ascidians, brooders
tend to have small bodies and produce relatively large eggs and larvae, whereas oviparous species often
Order of authorship is alphabetical.
30
Fig 2.Generalised life cycle of a molgulid ascidian with anural development.
have relatively larger bodies and produce small eggs. Exceptions to this pattern are found in Boltenia
echinata (Berrill, 1948b; Svane, 1983) and Corella inflata (Child, 1927; Lambert, Lambert & Abbott,
1981), both of which brood small eggs and produce small, simple tadpole larvae. At least one solitary
ascidian, Polycarpa pomaria, is observed in the laboratory to brood facultatively. It is normally oviparous
and produces small eggs, but developing larvae have not been found in the atrial cavity in nature (Berrill,
1950).
One explanation for the relationship between brooding and zooid size is that cost of reproduction
prohibits formation of numerous eggs in small individuals (Vance, 1973; Chia, 1974; Menge, 1976; Heath,
1977; Strathmann & Strathmann, 1982). This explanation, however, begs the question of why very large
colonies of genetically identical zooids invest their resources for sexual reproduction in few large tadpoles
rather than numerous small ones. Strathmann, Strathmann & Emson (1984) have suggested that selffertilisation can lead to brooding in echinoderms. The same argument could be applied to ascidians if we
knew the extent of self-fertilisation.
Botryllus schlosseri, which brood their embryos in the atrial cavity, can be either semelparous or
iteroparous (R.Grosberg, pers. comm.). When fully developed larvae are removed surgically from the atrial
cavities of a semelparous colony, the brood is replaced, suggesting that reproduction is not constrained by
energy limitations. When a brood is replaced with inert glass beads, the colony dies shortly thereafter, just
as in a typical semelparous colony (R.Grosberg, pers. comm.). Based on these findings, Grosberg has
suggested that large broods prevent water flow through the atrium, killing the parent colony before a second
brood is formed.
FERTILISATION
Sperm morphology and the physiology of ascidian fertilisation have been reviewed by Lambert (1982).
Ascidian sperm are among the simplest in the animal kingdom in that they lack a midpiece. The excentric
mitochondrion lies next to the nucleus in the head region. Paradoxically, this simple sperm must penetrate a
complex egg covering consisting of two layers of somatic cells and a chorion. Ascidian eggs have an
effective block to polyspermy that appears to involve the egg membrane rather than the accessory cells or
chorion (Lambert & Lambert, 1981). Moreover, many species demonstrate complete or partial blocks to
self-fertilisation (Morgan, 1938, 1942). Stolidobranchs tend to have a better block to self-fertility than
phlebobranchs (Cloney, 1987). Many ascidiids and corellids are completely self-fertile. Several species in
the genus Ascidia demonstrate a partial block to self-fertility when first spawned, but this block wears off
during the first few hours, ultimately permitting virtually 100% self-fertilisation (Scofield, Schlumpberger,
West & Weismann, 1982 for A. ceratodes; Young, unpubl. data on A. callosa and A. mentula).
Although self-sterility clearly implies the absence of self-fertilisation in nature, the converse (absence of
a block to self-fertility) does not necessarily indicate that eggs are routinely self-fertilised in the field.
Indeed, the extent to which self-fertilisation occurs in nature is unknown. Ovulation and subsequent
development have been observed in isolated zooids of Ecteinascidia turbinata, suggesting that selffertilisation is likely (Lambert, 1982). Some species release sperm seconds to minutes before eggs are
spawned, providing an opportunity for sperm to disperse and mix with that of other individuals before
fertilisation (Lambert & Brandt, 1967; Lambert et al., 1981). Recent electrophoretic evidence for two selffertile species, Chelyosoma production and Corella inflata, indicates that populations are not inbred; both
populations have high levels of heterozygosity (S.Cohen, pers. comm.). Although the observed
31
Fig 3.Representative tadpole larvae of compound ascidians, including Diplosoma macdonaldi (A), Botryllus planus
(B), Distaplia occidentalis (C), Ecteinascidia turbinata (D) and Eudistoma capsulatum (E). Only the styelid Botryllus
has a modified sensory vesicle. BB: branchial basket. BS: oral siphon. AS: atrial siphon. Other labels as in Fig 4.
Fig 4.Representative tadpole larvae of solitary ascidians. Boltenia villosa (A), Corella inflata (B), and Halocynthia
igaboja (C) have both a statocyte and an ocellus in the sensory vesicle. Styela coriacea (D) has a compound sensory
organ known as a photolith, whereas Molgula occidentalis (E) has a statocyte but no ocellus. N: notochord; O: ocellus;
S: statocyte; P: adhesive papilla ; PL: photolith; A: ampulla; TF: tail fin; F: tail tunic.
heterozygosity is not given, all alleles of Ciona intestinalis reported by Schmidtke, Weiler, Kunz & Engel
(1977) were highly polymorphic. Lyerla & Lyerla (1978), however, found that the colonial species
Clavelina picta and C. oblonga were monomorphic and may experience high levels of inbreeding. Whether
this is due to obligate self-fertilisation or almost total asexual reproduction, or a combination of both, is
unknown (Lyerla & Lyerla, 1978).
Ascidian sperm demonstrate chemotactic attraction to eggs under laboratory conditions (Miller, 1975,
1982). Although there is some species specificity in these interactions, many stolidobranchs demonstrate
low levels of specificity (Miller, 1982).
LARVAL ANATOMY
Ever since the chordate nature of the ascidian tadpole larva was recognised by Kowalevsky (1866),
phylogenetic questions have motivated detailed studies of tadpole structure and development. Because
details of tadpole morphology have been reviewed in depth several times during the past two decades
(Millar, 1971; Berrill, 1975; Katz, 1983; Cloney, 1978, 1987), we shall deal only with structures that
control larval habitat selection and swimming behaviour that are directly relevant to the ecology of larvae
themselves. Those portions of the larva that have been called the adult action system (developing and
fully developed adult structures present in the larva) will not be reviewed here.
The overall sizes of ascidian larvae range up to 4.5 mm, with the largest being found among colonial
ascidians in the order Aplousobranchiata: Hypsistozoa fasmeriana (Brewin, 1959), Polycitor circes (Millar,
1963), and Eudistoma digitatum (Millar, 1964). The largest tadpoles are also among the most complex, as
they contain well-developed rudiments of adult structures (Fig 3). By contrast, the simple larvae typically
produced by oviparous species are generally about 1 mm long (see Fig 4). Cloney (1978) has calculated that
the large complex larva of Hypsistozoa fasmeriana is approximately 3500 times greater in volume than
Molgula occidentalis which has a simple tadpole larva.
The typical tadpole of a solitary ascidian consists of a trunk (also called the body or head in the
earlier literature), which is 150250 m long and 100125 m wide, and a tail about 750 m in length,
though this may vary. A detailed review of larval morphology in a simple tadpole is given for ciona
intestinalis by Katz (1983). Katz, following earlier workers (Grave, 1944; Scott, 1946) classified the larval
tissues into two categories. The six organ systems that comprise the larval action system are the tunic,
epidermis, notochord, tail musculature, adhesive organs and nervous system. Four additional organ systems
carried by the larva will ultimately become organs of the adult stage, but without immediate ecological
relevance during the larval period (Grave, 1944; Scott, 1946). The simple type of larva is found in the
phlebobranchiate familes Cionidae, Ascidiidae, Corellidae, and Diazonidae, but also has been retained in
the phylogenetically more derived stolidobranchiate families Pyuridae, Styelidae, and Molgulidae. In
colonial ascidians (Aplousobranchiata and the stolidobranchiate subfamily Botryllinae), a more elaborate
larva is found wherein oral papillae occur in great variety, and numerous adult structures, non-functional in
32
the larvae, may be present (Barnes, 1971; Millar, 1971; Cloney, 1977). Larvae of some colonial ascidians may
even have a functional heart (Cloney, 1982). Although the general complement of sensory and locomotory
structures is similar in the larvae of solitary and compound ascidians, many of the subtle differences could
have ecological or behavioural significance.
The surface of an ascidian larva is covered with a secreted, non-cellular tunic layer. This transparent
tunic, also called the test or cuticle, is elaborated into two fins which, in tadpoles of solitary ascidians, are
situated dorsally and ventrally on the trunk and tail. The fins are formed by extra-embryonic test cells
present between the egg chorion and the embryo (Cloney & Cavey, 1982; Robinson, Kusten & Cloney,
1986). At hatching, the test cells often persist on the outside of the tunic fin for a period of time (Grave,
1921; Cloney & Cavey, 1982; Katz, 1983), although it is not known whether their persistence into the posthatching stage has any ecological significance. In any case, the test cells generally fall off before
metamorphosis. Tadpole larvae of most solitary ascidians are laterally flattened for their entire length. In
addition to the large dorsal and ventral fins, other smaller fins may be arranged in various positions on the
lateral sides of the tail (Katz, 1983). Some colonial ascidians, but not all (see Grave & Woodbridge, 1924),
have tails which are rotated through 90 degrees by a quarter twist at the base of the tail (Damas, 1904;
Grave, 1921; Grave & McCosh, 1924). Berrill (1950) hypothesised that the twist results from limited space
for development in the chorion. Although this appears to be an adequate proximate explanation, there has
been no speculation as to why chorion size should be constrained in larger embryos. Perhaps it is limited in
small zooids by the space available for brooding. If this is the case, one might expect larger chorionic
spaces (and perhaps untwisted tails) in the embryos of atrial brooders than oviducal brooders. One
consequence of the twisted tail is a more erratic, spiral swimming pattern.
All ascidian larvae move by flexing muscles in the tail. These muscles are arranged in three longitudinal
bands situated laterally (or, in the case of compound ascidians with twisted tails, dorsally and ventrally) and
bounding the notochord. The notochord consists of about 40 squamous, matrix-filled cells surrounded by a
fibrous sheath (Cloney, 1964; Mancuso & Dolcemascolo, 1977). The tail is innervated not only by the
neuromuscular junctions that stimulate the muscle blocks (reviewed by Katz, 1983), but also by axons
connected to pairs of ciliary sensory cells lying along the midline of the tail epidermis (Torrence & Cloney,
1982). It is not known whether these are proprioceptors that signal tail posture or if the receptors provide the
larva with sensory input concerning some aspect of the outside environment. Most tadpoles respond quickly
to tactile stimulation of the tail tunic (R.A.Cloney, pers. comm.).
The anterior end of the trunk is equipped with three adhesive papillae. Cloney (1978) has identified at
least nine different types of papillae, which he has classified into three major groups: non-everting
glandular papillae, everting glandular papillae, and non-glandular papillae. The papilla structure may play a
role in determining how well larvae select substrata. For example, some tadpoles with simple coniform
papillae secrete adhesive even before contacting the substratum (Cloney, 1978). Although one might expect
that this would reduce their capability for habitat selection, several species with this sort of papillae are
known to discriminate among substrata at settlement (Young & Braithwaite, 1980a; Young, 1982). Also
counter-intuitive is the observation that some tadpoles which can expose their adhesive abruptly by everting
the papillae (reviewed by Cloney, 1978) seem to be quite indiscriminate with respect to attachment surface.
The larvae of Botryllus schlosseri and Symplegma viride have a sucker-like holdfast mechanism, under
nervous control, which reportedly allows the larva to attach and release its hold several times before
selecting a final site for metamorphosis (Grave, 1934). At the opposite extreme, larvae of some urodele
molgulids (e.g., Molgula citrina, M. manhattensis, M. occidentalis) either lack papillae (Cloney, 1978) or
have tiny oral papillae that do not function in attachment. In these species, either the entire larval body
becomes adhesive (Kingsley, 1882; Grave, 1944) or attachment is by means of a large primary ampulla near
33
the anterior end. The larvae of M. occidentalis, which fall into this latter category, are capable of
discriminating among substratum types (Young, in press), presumably by delaying the release of ampullar
adhesive until after encountering an appropriate habitat. It is not surprising, therefore, that Torrence &
Cloney (1983, 1988) have reported sensory neurons in the anterior epidermis of this species. Attachment in
some anural species occurs shortly after the egg contacts sea water (Young et al., 1988). Follicle cells
surrounding the egg chorion of M. pacifica undergo a holocrine secretion of adhesive shortly after spawning.
The embryo develops to hatching on the first substratum contacted by the egg, after which the juvenile
moves away a short distance (Young et al., 1988).
The adhesive papillae of most tadpoles are probably sensory as well as adhesive in function. Torrence &
Cloney (1983,1988) have demonstrated the presence of sensory neurons in the oral papillae of Diplosoma
macdonaldi and many other ascidians in several families. Similar neurons, as well as an associated papillar
ganglion, have been reported at the light microscope level for the larvae of Botryllus schlosseri (Grave,
1934; Grave & Riley, 1935). Although the ultrastructural studies provide few cues as to the functions of the
papillar receptors, behavioural evidence suggests that they may function both as mechanoreceptors and
chemoreceptors (Cloney, 1978; Young & Braithwaite, 1980a; Young, 1982; Davis, 1987; Torrence &
Cloney, 1988).
The cerebral vesicle of an ascidian larva generally contains at least two sensory structures that control
swimming behaviour and orientation: a multicellular ocellus for the reception of light, and a statocyte
containing a statolith for the reception of gravity (Fig 4). A third type of possible sensory structure has been
found in both phlebobranchs and stolidobranchs (Dilly, 1969; Eakin & Kuda, 1971; Reverberi, 1979;
Svane, 1982). This structure is located in the dorso-posterior wall of the cerebral vesicle, imbedded in the
tissue lateral to the cerebral vesicle, or confined to an auxiliary vesicle which communicates with the
cerebral vesicle at the level of the statocyte (Svane, 1982; Vorontosova & Malakhov, 1984; Svane & Young,
unpubl.). The cells carry 2 m globular ciliary structures and resemble coronet cells (although more simple)
typical for the saccus vasculosus found in elasmobranchs and many ganoid and teleost fishes. The globular
cilia possess a modified (9+0) arrangement with tubules that open into the lumen of the cerebral vesicle
(Eakin & Kuda, 1971). These structures have been variously interpreted as a second ocellus (Dilly, 1969;
Torrence & Cloney, 1988) or hydrostatic pressure receptors (Eakin & Kuda, 1971). The only species of
tadpole larva that has, however, been tested for a pressure sensitivity demonstrated no such response (Crisp
& Ghobashy, 1971). Alternatively, if the ascidian coronet cells are homologous to those of fishes, they
could have a secretory function as suggested by Lanzing & Lennep (1971) and Emanuelsson &
Mecklenburg (1974) or they could function as a receptor for low molecular weight materials (Jansen &
Flight, 1969). The actual function or functions, however, remain unknown.
The morphology and ultrastructure of the ocellus and statocyte have been studied in detail (e.g. Dilly,
1961, 1962, 1964; Barnes, 1971; Eakin & Kuda, 1971; Katz, 1983; Vorontosova & Malakhov, 1984).
Structural details of these organs vary substantially among species, and these differences have often been
assumed to produce behavioural differences (Berrill, 1975). A typical ocellus, as exemplified by Ciona
intestinalis, consists of three lens cells, a number of neurosensory retinal cells and a unicellular pigmented
cup (Dilly, 1964; Eakin & Kuda, 1971; Turon, 1988). Similar ocelli are found in colonial aplousobranchs
(Grave, 1921; Barnes, 1971, 1974). The larvae of most styelids have either simplified ocelli or compound
sensory structures that incorporate elements of both the ocellus and the statocyte into a single structure. For
example, in larvae of Styela partita, the ocellus is reduced to a small melanic granule surrounded by a thin
layer of optically clear material (Grave, 1944; Whittaker, 1966), whereas colonial styelids such as Botryllus
have the statocyte and ocellus combined into a photolith (Garstang & Garstang, 1928; Grave, 1934;
Berrill, 1949; Torrence & Cloney, 1988). Larvae of the solitary styelid Cnemidocarpa finmarkiensis are
34
reported to possess both an ocellus and a photolith (Vorontosova & Malakhov, 1984). The styelid genera
Dendrodoa and Polycarpa (Millar, 1971), as well as the pyurid Herdmania momus (Svane & Young, unpubl.),
and most urodele molgulids (Grave, 1926; Berrill, 1931) have statocytes, but no pigmented ocellus. The
behavioural and ecological implications of these structural variations remain largely undocumented.
TIMING AND SYNCHRONY OF REPRODUCTION
SEASONAL PATTERNS OF REPRODUCTION
Successful reproduction in cross-fertilising organisms depends on synchrony among members of the
population. Although a few species, including both tropical (Goodbody, 1961, 1963) and temperature
(Lambert, 1968; Berrill, 1957; Svane & Lundlv, 1981) ones, reproduce throughout the year, most ascidians
reproduce in one or two discrete peaks during the annual cycle (reviewed by Millar, 1971; Berrill, 1975).
Sexual and asexual portions of the reproductive cycle occur simultaneously in some compound ascidians
and alternate in regular cycles in others (Millar, 1971). Previous workers have assumed that because
reproductive cycles are correlated with temperature, temperature is the causative factor that entrains the
cycles. Other factors that covary with temperature on an annual basis, including day length, phytoplankton
concentrations, lunar periods, and tide levels, have not, however, been investigated. The important work of
Pearse and his colleagues (Pearse & Eernisse, 1982; Pearse & Beauchamp, 1986; Pearse & Walker, 1986;
and others) on the role of light in entraining circannual reproductive cycles in echinoderms should inspire
similar studies in ascidians, particularly because many solitary ascidians are easily reared in laboratory seawater systems.
DIEL PATTERNS OF LARVAL RELEASE AND SPAWNING
In colonial ascidians, fully developed larvae may be incubated in the oviduct, in the atrial chamber of a
zooid, in a specialised brood pouch (e.g. Distaplia spp.), or in the common cloacal chambers of the colony.
Larval release may involve expulsion of the larva from an existing opening or directly through the tunic of
the colony. The timing of larval release is controlled by light in every species that has been experimentally
investigated (Table I). In general, spawning occurs in response to light following a period of dark
adaptation. The duration of light exposure required, which has been called the dormant period (Huus, 1939)
or the latency period (Lambert, Lambert & Abbott, 1981), varies somewhat among species. Olson (1983)
tabulated the latency period for nine species of compound ascidians. We have expanded his table to include
many additional species, including solitary ascidians and several colonial species not reported in the
primary literature (Table I). Of 27 species for which observations or data are available, 16 release larvae in
the early morning or within a short time after exposure to light in the laboratory. Five species release larvae
all day (one of which continues to produce larvae throughout the night; Grave, 1936), five release between
the late morning and early afternoon hours, and one releases in the afternoon (Table I). With a single
exception, Podoclavella moluccensis (A.Davis, pers. comm.), the species releasing larvae at midday are
didemnids which contain symbiotic algae, and which transfer the symbionts between generations during the
larval stage (Duyl, Bak & Sybesma, 1981; Olson, 1983).
The actual mechanism of larval release remains poorly understood for most colonial ascidians.
Metandrocarpa taylori has been observed to eject larvae forcefully by means of a general contraction of
body wall musculature (Abbott, 1955). Euherdmania claviformis and Pycnoclavella stanleyi move larvae
through the atrium by a series of contractions in the thoracic region according to Trason (1957, 1963).
35
Larvae of Eudistoma ritteri have been observed to swim actively from the atrial chamber of the adult zooid
(Levine, 1962). We do not, however, know whether release is under control of the adult nervous system or
if, alternatively, larvae leave spontaneously following stimulation of their photoreceptors. In Distaplia
occidentalis, adult control
TABLE I
Spawning or larval release in relation to light-dark cycles
Species
Polyclinidae
Aplidium (Amaroucium)
constallatum
A. stellatum
A. antillense
Polycitoridae
Distaplia occidentalis
D. corolla
Polycitor mutabilis
Cystodytes lobatus
Eudistoma hepaticum
E. olivaceum
E. capsulatum
Clavelina oblonga
Didemnidae
Diplosoma listerianum
D. similis
Didemnum molle
Leptoclinum mitsukurii
Trididemnum solidum
Lissoclinum voeltzkowi
L. patella
Perophoridae
Perophora viridis
Ecteinascidia turbinata
Cionidae
Ciona intestinalis
Corellidae
Corella
paralellogramma
C. willmeriana
Average spawning latency Spawning time Settlement time References

20 min
morning
morning
Scott, 1954; Mast, 1921
23 h
morning
morning
morning
morning
Gotelli, 1987
Bingham, pers. comm.
15 min
morning
morning
late morning
continuous
all day
morning
morning
morning
all day
midday
continuous
all day
morning
morning
morning
all day
Watanabe & Lambert,

1973
Oka, 1943
Lambert, 1979
morning
midday
11001400
morning
midday
midday
11001800
morning
midday
midday
morning
midday
midday
afternoon
Crisp & Ghobashy, 1971

Olson, 1983
Olson, 1983
Yamaguchi, 1975
Duyl et al., 1981
Olson, 1983
Olson & McPherson, 1987
morning
morning
morning
morning
Grave & McCosh, 1924

Young, unpubl.
34 h
min
03 h
27 min
morning
morning
Lambert & Brandt,

1967; Conklin, 1905 ;
Whittingham, 1967
1117 min
morning
morning
Huus, 1939, 1941
15.1 min (sperm)
morning
Lambert et al., 1981
36
C. inflata
Chelyosoma
productum
Styelidae
Styela partita
S. plicata (Japan)
S. plicata (Calif.)
Botryllus schlosseri
12.6 min (sperm)
20.8 min (eggs)

Lambert et al., 1981
18.9 min (eggs)
Young & Braithwaite,
1980a
morning
morning
1112 h
afternoon
1012 h
evening
afternoon
all day
all day
morning
morning
morning
morning
B. planus
Botrylloides mutabilis
B. nigrum
Metandrocarpa taylori
15 min
morning
morning
morning
morning
Polyandrocarpa tincta
P. misakiensis
morning
afternoon (16.30)
morning
11.5h
24 h
continuous
Symplegma viride
Pyuridae
Halocynthia roretzi
1112pm
twice a day (2 types)
Molgulidae
Molgula manhattensis
M. citrina
M. pacifica
few min
Conklin, 1905; Rose,

1939
Yamaguchi, 1975
West & Lambert, 1976
Grave, 1934; Grave &
Woodbridge, 1924
Yamaguchi, 1975
Morgan, 1977
Watanabe & Lambert,
1973
Grave, 1936
Hashimoto &
Watanabe, 1982
Grave, 1936
Hirai & Tsubata, 1956
Watanabe & Tokioka,

1972
morning
all day
night
Berrill, 1931;
Whittingham, 1967;
Conklin, 1905
Grave, 1926
Young et al., 1988
seems unlikely, since the brood pouches (which originate from the adult oviducts; Berrill, 1948a) often
occur in the tunic as isolated entities following the regression of the zooids (Watanabe & Lambert, 1973).
Reese (1967) and Woollacott (1979) have shown that isolated sperm ducts of Ciona intestinalis can be
induced to spawn by exposure to light. Whether Distaplia brood pouches release larvae by a similar
mechanism is not known. Because larvae of D. occidentalis are not active at the moment of release, larval
activity seems, however, an unlikely explanation in this species (Watanabe & Lambert, 1973).
The physiology of larval release has been investigated in greatest detail for two temperate species, D.
occidentalis and Metandrocarpa taylori (Watanabe & Lambert, 1973). Under natural illumination, larvae
were released about 1 h after sunrise, but with higher intensities of artificial illumination, the average
latency period was reduced to 15 min. Because colonies could be stimulated to release larvae at any time of
the day (following adequate dark adaptation), it was concluded that endogenous rhythms play no role in
larval release. The rate of larval release was correlated positively with the length of the dark adaptation
period. Colonies kept in continuous darkness released relatively fewer larvae than colonies maintained in
37
continuous light. Larval release rate has also been correlated with temperature in Podoclavella moluccensis
(Davis, in press).
Among solitary ascidians, many phlebobranchs have large gonoducts in which masses of eggs and sperm
are stored before spawning, whereas most stolidobranchs have no such storage gonoducts. In the latter
group, eggs and sperm are released directly from the gonads. Ciona intestinalis has been reported to spawn
in approximately three-day cycles in which gametes are shed into the gonoduct for several successive days,
then spawned when the oviduct is full (Yamaguchi, 1975).
Although few case studies are available, the mechanisms of spawning in solitary ascidians are understood
better than the mechanisms of larval release in colonial ascidians. C. intestinalis, which spawns shortly after
exposure to light, has been investigated most intensively (Lambert & Brandt, 1967; Whittingham, 1967).
Because the photoreceptor that mediates spawning is located at the distal tip of the spermoduct (Reese,
1967), and the spermoduct possesses an extensive network of microtubules (Woollacott, 1979) the
spermoduct acts as an independent effector system. The isolated spermoduct can be stimulated to spawn in
the same manner as the intact animal (Reese, 1967; Woollacott, 1979). The action spectrum for spawning
peaks at wavelengths that implicate cytochrome c as the photoreceptor pigment (Lambert & Brandt, 1967).
Other solitary ascidians that spawn in the early morning include several phlebobranchs in the family
Corellidae (Huus, 1939; Lambert et al., 1981), as well as the molgulid Molgula manhattensis. It may be
significant that every one of these, irrespective of taxonomic affinity, has transparent or transluscent tunic.
The reverse side of this correlation also holds; every solitary stolidobranch species with opaque tunic that
has been examined spawns many house after the onset of light stimulation (as in Styela plicata; Yamaguchi,
1975; West & Lambert, 1976 and Halocynthia roretzi; Hirai & Tsubata, 1956). Only one solitary ascidian,
Molgula pacifica, has been reported to spawn in the dark (Young et al., 1988). As gametes of the latter
species are entirely self-fertile, its reproductive pattern may not require diel synchrony among individuals in
a population. Likewise, Grave (1926) observed no pattern of release in response to light in Molgula citrina.
Yamaguchi (1975) reports that Styela plicata and Ciona intestinalis both spawn after dark in Japan. Both of
these species spawn, however, earlier in the day in other parts of the world.
The ecological significance of morning larval release by most ovoviviparous ascidians has not been
investigated. Thorson (1964) speculated that early morning release allows the larvae maximal time to
distinguish between light and dark substrata at settlement. Most compound ascidian larvae swim for no
more than a few hours; presumably they select habitats long before the sun has set. With only a few
exceptions, all reported data on ascidian spawning times come from laboratory settings in which the adults
were exposed to relatively high light intensities. Watanabe & Lambert (1973) have shown with at least one
species that the latency period is a function of the cumulative quanta of energy with which the ascidian is
illuminated. Thus, spawning can be delayed by illuminating with lower light intensities. Although diel
changes in underwater light regimes have not been related quantitatively to any of the species with
morning release, it seems possible that release could actually occur long after sunrise. Water turbidity,
depth, cloud cover, season, and other factors influencing underwater irradiance should all play a role in
determining when compound ascidians release larvae. Larval release has been observed in situ by divers for
several tropical didemnids, all of which support extracellular algal symbionts of the genus Prochloron or
Synechocystis (Duyl et al., 1981; Olson, 1983; Olson & McPherson, 1987) and all of which release larvae at
midday. The algae are transferred between generations by the larvae (Kott, 1981; Lafargue & Duclaux,
1979; Olson, 1980). When a larva is released into the common cloacal cavity, algae residing in the cavity
become entangled in filaments of the rastrum, a specialised structure located at the postero-dorsal end of the
larval trunk (Kott, 1981). Olson (1983) has provided evidence that juveniles, which lack adult pigmentation,
require lower light levels than adult colonies can tolerate, but also must select habitats where there is
38
adequate light for photosynthesis of the symbionts. He argues that selection of such habitats is best done when
conditions for ultraviolet irradiation are harshest, in the middle of the day. Didemnum molle and other
didemnids with short (about 15 min) larval lives accomplish this by releasing brooded larvae between late
morning and early afternoon (Duyl et al., 1981; Olson, 1983).
Because light is an important settlement cue for the tadpole larvae of many solitary ascidians (Young,
1982; Young & Chia, 1984; Svane, 1987), one might expect that spawning of these oviparous species would
be timed so that larvae would attain metamorphic competency during daylight hours (Thorson, 1964). Data
are insufficient to support strong conclusions in this regard, but it is interesting to note that most solitary
ascidians that reportedly spawn in the morning hatch after about 24 h, but that Styela plicata which has a 12h latency period for spawning (West & Lambert, 1976), develops in half that time (Yamaguchi, 1975). Thus,
many solitary ascidians attain metamorphic competency at about the same time of day, but accomplish it by
different means. This observation suggests that spawning times and developmental periods could have
evolved jointly to increase opportunities for habitat selection. Additional work is needed on the interactions
linking these various factors.
THE PELAGIC PERIOD

DISPERSAL POTENTIAL AND DURATION OF THE PLANKTONIC PERIOD
The potential for ascidian dispersal in the larval stage is correlated with the kind of development they
exhibit. Direct developers, viviparous, and ovoviviparous species generally spend no more than a few hours
in the plankton (Berrill, 1935), whereas oviparous species may sometimes prolong larval life for as much as
a week and still undergo successful metamorphosis (Svane, 1984; Young; unpubl. data on Ascidia callosa).
In one respect this correlation between the length of larval life and developmental period is unexpected. The
large larvae of compound ascidians, being orders of magnitude greater in volume than those of solitary
ascidians, presumably have energy stores sufficient to support a longer larval life. Variability in the total
length of pelagic life can originate from processes and adaptations occurring in any of the pre-settlement
stages (egg, embryo, or larva).
In oviparous ascidians, a portion of the dispersal period is passed in the egg and embryonic stages.
Although these life-history stages cannot swim; they demonstrate several possible adaptations that may
affect dispersal (Fig 5). At a given sea-water density and viscosity, the sinking rate of a sphere at low
Reynolds number is determined by the balance between its density and its drag, the latter being a function
of cross-sectional area. If an organism can increase its drag without a proportional increase in density, it
will sink more slowly (Vogel, 1981; Chia, Buckland-Nicks & Young, 1984). Ascidians seem to have
accomplished this in three different ways. First, many ascidian eggs undergo an osmotic expansion of the
perivitelline space shortly after contacting sea water (Berrill, 1929, 1975). Secondly, additional diameter is
conferred by the follicle cells, which are heavily vacuolated (hence, light) cells, extraembryonic in origin,
that cover the outside of the chorion. Finally, the follicle cells of a few phlebobrachs (Ascidiella aspersa,
Corella inflata, C. willmeriana, C. parallelogramma) are lighter than sea water and cause the eggs to float.
Lambert & Lambert (1978) have demonstrated that the follicle cells of C. inflata float because their
vacuoles contain ammonia, which is lighter than sea water. In the latter species, however, egg flotation
facilitates brooding rather than dispersal (Child, 1927; Young, 1988).
The duration of the embryonic (i.e. pre-hatching) period in ascidians is partly a function of egg-size and
water temperature (Figs 6 and 7), so temperate and cold-water species with oviparous development
39
Fig 5.Ascidian egg adaptations. Ova of Styela montereyensis (A and B), an ascidian with typical extraembryonic cell
layers. Newly spawned eggs (C) and 16-celled embryos (D) of Halocynthia aurantium. Note that the chorion swells
after spawning, increasing the effective surface area and drag of the egg without a commensurate increase in mass. Eggs
of Corella inflata (E) showing floating, ammonia-filled follicle cells that facilitate brooding. Eggs of Molgula pacifica
(F) attached to the substratum by a sticky adhesive coat secreted by follicle cells. FC: follicle cells; CH: chorion; TC:
test cell; OV: ova; EM: embryo; AC: adhesive coat.
Fig 6.Relationship between temperature and duration of embryonic development (to completion of tadpole). Species:
Ascidia atra, A.curvata, A.mentula, A.prunum, A.mammillata, Ascidiella aspersa. Redrawn from Berrill (1935).
Fig 7.Relationship between egg-size and duration of embryonic development (up to completion of tadpole) at 16C.
Species: Molgula, Styela, Ascidia, Ciona, Diazona, Corella, Boltenia, Polycarpa, Tethyum, Syplegma, Dendrodoa,
Distomus, Stolonica. Redrawn from Berrill (1935).
probably spend more time in the plankton than similar species in the tropics. As an example, Styela gibbsii
takes 30 h to hatch as a competent larva at 10C in Washington (Cloney, 1987), whereas the congeneric S.
plicata spends only 12 h in the embryonic stage at temperatures between 18 and 26C (Yamaguchi, 1975).
The same relationship applies within single species that occur over wide geographic ranges or in areas
where temperatures fluctuate over a wide range. For example, the time from fertilisation to hatching in
Ascidiella aspersa may be as short as 15 hours at 23C or as long as 39 hours at 8C (Knaben, 1952).
Within a species, there may be substantial variability in the duration of the free-swimming period (Grave,
1920, 1928; Grave & McCosh, 1924; Grave & Woodbridge, 1924; Levine, 1962; Olson & McPherson,
1987, and many others). At least three major monographs (Berrill, 1935; Grave, 1935; Grave & Nicoll,
1939), attempted to explain this variability over a half century ago; nevertheless, many of the variables
influencing length of larval life remain undetermined. Habitat selection may play a major role in
determining the length of larval life. Some species with specific habitat requirements delay metamorphosis
in the absence of suitable cues (Young, 1982); others settle faster in the presence of conspecifics (or extracts
of conspecifics; Grave, 1935; Svane, Havenhand & Jrgensen, 1987) or under particular light conditions
(Crisp & Ghobashy, 1971) than they otherwise might. Larval life may be shortened or prolonged artificially
by a wide array of chemical reagents, hormones, and other artificial treatments (Grave, 1935; Grave &
Nicoll, 1939; Lynch, 1961), but it is doubtful if these have any ecological relevance.
In some oviparous species, only a fraction of larvae delay settlement for a prolonged period (e.g., up to 10
days in Ascidia mentula and 6 days in Ciona intestinalis; Svane, 1984, and unpubl.). The remainder settle much
earlier. Indeed, settling curves for many species plotted from the literature demonstrate a marked negative
skew (long tails on the upper end of the curve) (Millar, 1971). Grave & Nicoll (1939) observed that larval
longevity of Ascidia nigra decreased as the breeding season advanced but did not discover the factor
controlling this phenomenon. Although they hypothesised the existence of an hormonal aging factor that
controlled the onset of metamorphosis, the fact that many larvae settled shortly after hatching indicated that
such a factor was not necessary (Grave & Nicoll, 1939). Larvae of some colonial ascidians are incapable of
settlement immediately upon release, whereas others (e.g., Didemnum molle; Olson, 1985) apparently have
no pre-competent period. Within a given species, there is some variation in the time to settlement. For example,
Olson (1985) reported that some larvae of D. molle settled immediately, whereas others swam for as long as
20 min. It is not known whether the latter individuals were competent to settle upon release.
It seems likely that ascidians demonstrate the same inverse relationship between larval survival and time
spent in the plankton as other invertebrates (Thorson, 1950; Menge, 1972; Vance, 1973; Chia, 1974; Emlet,
McEdward & Strathmann, 1987), although this question has not been specifically addressed for ascidians.
Ascidians in general may have short larval life because there is greater advantage to survival than dispersal.
40
Certainly the advantages of dispersal to benthic invertebrates have been difficult to demonstrate (see
Jackson & Strathmann, 1981; Palmer & Strathmann, 1981; Svane, 1984).
Because the larvae of many compound ascidians are large enough to observe underwater, dispersal of
several such species has been studied in situ. Olson (1985) followed numerous larvae of D. molle at Lizard
Island on the Great Barrier Reef. Direction and speed of dispersal were related directly to current speed.
Although the larvae swam during the dispersal phase, their swimming appeared virtually ineffectual
because of the dominant influence of currents. Most recruitment occurred on the upstream edges of patch
reefs downstream from source populations. Active swimming against the current was only observed close to
the bottom or in the lee of coral heads, where the current moved very slowly (Olson, 1985). This
observation suggests that swimming may function primarily in site selection rather than dispersal. Young
(1985), noted that the larvae of Ecteinascidia turbinata spent a large portion of their pelagic period drifting
passively without any spontaneous movements whatsoever, but Davis & Butler (in press) have found that
larvae of Podoclavella moluccensis swim almost continuously, with only brief resting periods. In both
species, dispersal distance seemed, however, to correlate with current speed. Observations made by Olson &
McPherson (1987) confirm that dispersal depends mainly on currents, not swimming.
There is evidence that larval swimming time is severely over-estimated by experiments conducted in
closed containers of sea water. Olson (1985) found that swimming times of larvae released naturally on the
reef ranged from 40 to 370 s, whereas larvae captured and retained underwater in closed Plexiglass boxes
had settlement times distributed around a mean of 15 min, even when a dark surface was present in the box.
Likewise, Duyl et al. (1981) noted that although some beaker-reared larvae of Trididemnum solidum settled
in about 15 min, others delayed settlement as long as 3 h. More field observations are needed before we
completely understand the nature and extent of the laboratory bias.
In quiet harbours, dispersal of ovoviviparous ascidians may be very short indeed. Grosberg & Quinn
(1986) investigated recruitment of Botryllus schlosseri on a 1-m square settling panel in the Eel Pond at
Woods Hole, Massachusetts. A genetically characterised adult having a rare allele in the population was
placed in the middle of the panel, and positions of recruits having the same allele were plotted. Settlement
was found to be a function of distance from the adult colony, with most individuals settling within a few
centimetres. Berrill (1955) has attributed aggregation in the brooding styelid Dendrodoa grossularia to
similar short distance dispersal. Lambert (1968) also noted consistently high local recruitment near parents
in Corella inflata, a solitary corellid that retains larvae until they are competent to settle.
Although maximum dispersal potential can be estimated by knowing something about the combined
lengths of the pre-competent and competent periods (Jackson & Strathmann, 1981) and the speeds of currents
larvae are likely to encounter, such estimates may not be representative of the actual dispersal distances
achieved by the larvae. Dispersal can be shortened by mortality, early settlement, or entrapment in areas
with little or no current. Olson & McPherson (1987) have provided a convincing in situ demonstration of
this point for the larvae of Lissoclinum patella on the Great Barrier Reef. Based on in vitro field
measurements of the length of larval life, it was predicted that a larva should be able to disperse several
hundred metres over a period of about two hours. In observing free-swimming larvae in the field, it was,
however, discovered that the majority were consumed by predatory fishes and cnidarians, and the remainder
settled less than 10 m from the parent colonies (Olson & McPherson, 1987). Thus, the potential dispersal
was approximately an order of magnitude greater than the realised dispersal.
Many colonial marine animals, including bryozoans, sponges, and some cnidarians demonstrate very
short dispersal distances as a result of brooding (reviewed by Jackson, 1986). Philopatry (as short dispersal
distance is sometimes called) may result in greater temporal stability of local populations than is found in
41
species with longer dispersal (Chernoff, 1985). Other ecological and evolutionary consequences of
philopatry have been discussed by Shields (1982) and Jackson (1986).
DYNAMICS OF LOCOMOTION
From the standpoint of anatomy and ultrastructure, the tail is the best understood portion of a tadpole
(reviewed by Katz, 1983). It is, therefore, surprising that there have been no careful studies of the
mechanics of larval swimming in ascidians. In general terms, tadpoles move by alternating contractions and
relaxations of the lateral muscle blocks that run alongside the tail. The elastic notochord antagonises the
contractions of muscle blocks, translating the longitudinal forces into lateral (or sometimes dorso-ventral)
flexions of the tail. Tadpole larvae, because they are small in size, function at low Reynolds numbers where
inertial forces are overshadowed by the effects of viscosity. Consequently, tadpoles only move when their
tails beat; there is virtually no glide stroke. The trunk of a tadpole does not remain stationary as the head of
a fish does. Instead, it moves from side to side, with a displacement from the midline that may be either
equal to or slightly less than the amplitude of the tail flexions. Cloney (1959) has noted that a swimming
larva of Boltenia villosa flexes around two stationary nodes in the tail region, one just behind the trunk and
the other about one-third of the way forward from the end of the tail fin. That portion of the tail between the
nodes moves with about the same amplitude as the tip of the fin and the anteriormost portion of the trunk. In
addition, larvae of many colonial ascidians have a 90-degree twist in the tail, causing the tail to beat dorsally
and ventrally rather than laterally.
Grave (1920) was apparently the first to note that larvae of ascidians spin on their longitudinal axis while
swimming. He was not able to ascertain experimentally the cause of this spin, but proposed several possible
mechanisms. In Aplidium constellation, Grave (1920) attributed the spin to an interaction among three
mechanisms: a horizontal tail fin, lateral asymmetry in the trunk, and oblique alignment of the myofibrils in
the muscle blocks of the tail (Grave, 1920). Both the horizontal tail fin and the lateral trunk asymmetry
apparently resulted from development of the tail within the narrow confines of a small chorionic space. The
manner in which the tail folds against the trunk during development molds the trunk tunic into a sort of
short spiral (Grave, 1920, 1921). Because of this corkscrew shape, the tadpoles of Aplidium constellatum
rotate even as they sink passively through the water column (Grave, 1920). In Botryllus schlosseri (which
has a vertical tail fin; Grave & Woodbridge, 1924) and Perophora viridis (horizontal fin; Grave & McCosh,
1924), clockwise rotation during swimming was attributed in part to asymmetrical insertion of the tail at the
posterior end of the trunk (Grave & McCosh, 1924; Grave & Woodbridge, 1924) and in part to the axial
torsion imparted to the tail movements by a spiral arrangement of myofibrils. Now that methods are
available for analysis of movements and flow effects at low Reynolds numbers (Vogel, 1981), the time is
right for a re-analysis of locomotory methods in ascidian tadpoles.
Ascidian tadpoles move faster than invertebrate larvae which employ ciliary locomotion, but slower than
some crustacean larvae (reviewed by Chia et al., 1984). Berrill (1931) demonstrated a positive correlation
between swimming speed and larval size. Swimming speeds of tadpoles, as measured in the laboratory,
range from 0.22.5 cm/s (Berrill, 1931; Chia et al., 1984; Olson, 1985).
LARVAL ORIENTATION WITH RESPECT TO PHYSICAL CUES
The sensory structures in the tadpole cerebral vesicle (ocelli, statocysts or modifications thereof) mediate both
kinetic and tactic (sensu Fraenkel & Gunn, 1940) responses. Although some workers (e.g., Millar, 1971)
have referred to ascidian phototaxis as a phototropism, the term is incorrect. Tropisms (orientation of new
42
growth with respect to a physical scalar or vector) may occur in adult ascidians, but not in ascidian larvae.
Photokinesis, which involves a change in activity level resulting from a light stimulus, is common in
ascidian tadpoles, and there is also evidence for directional responses to the physical vectors of light and
gravity. Such directional responses are correctly termed phototaxis and geotaxis, respectively.
Following Thorsons (1964) review in which generalised behaviours of invertebrate photoresponse were
suggested, reviews on ascidian biology have adopted the generalisation that larvae are photopositive at
release or hatching, then become progressively more photonegative before settlement (Millar, 1971; Berrill,
1975). While this paradigm seems to fit a few species, careful examination of the available data on ascidian
phototaxis reveals so much variability within and among species that broad generalisations seem
unwarranted. Even different broods of larvae from the same individual or population often show statistical
differences in the proportions of larvae demonstrating particular behaviours. In this section, we will review
the nature of this behavioural variability and discuss the ecological ramifications thereof.
The light wavelengths and intensities that ascidian larvae can detect have been considered by Mast
(1921), Grave (1935) and Young (1982). Mast (1921), found that the larvae of Aplidium constellation were
unable to detect very low (30 m.c.) absolute intensities of white light, but demonstrated a shadow response
when higher intensities were reduced abruptly by even 10 m.c. of energy. Tadpoles also responded to red
light, though the spectral distribution of this light was not reported (Mast, 1921). The wavelength and intensity
thresholds for the shadow response were studied by Young (1982) for 12 species of solitary ascidians. All
species were able to sense light intensities as low as and tadpoles of one species, Ascidia callosa, responded
at the lowest intensity tested, (Young, 1982). Using a monochromator to produce 10 nm band-width beams
of light, it was shown that all 12 species were most sensitive to wavelengths in the blue and green regions of
the spectrum. The upper visual threshold was between 575 and 650 nm (red-orange light), and none of the
tadpoles tested responded to light below 425 nm (Young, 1982). Grave (1935) reported that the larvae of
several colonial ascidians responded equally to all wavelengths in the human visible spectrum, although he
did not report the bandpass data on the filters used for making these observations.
Photokinesis
In ascidian tadpoles, two kinds of photokinetic responses have been documented. In the first, tadpoles
accumulate in regions of low light intensity just before settlement. Crisp & Ghobashy (1971) have
demonstrated the kinetic nature of this phenomenon by studying the settlement distribution of Diplosoma
listerianum in a chamber illuminated by horizontal light passing through a graded neutral density filter.
Because the light source was diffuse and at right angles to the chamber, the authors interpreted the
responses as a photokinesis. Larvae did not show any preference for a particular region of the light gradient
while swimming, but accumulated at an intensity of 300 500 lux at settlement (Crisp & Ghobashy, 1971).
Dim light was preferred over complete darkness.
The second manifestation of photokinesis, commonly called the shadow response, seems to be present in
virtually all tadpoles with functional ocelli (Young & Chia, 1985) and at least one species, Molgula
occidentalis, which lacks an ocellus (Torrence & Cloney, 1988). The only exception reported in the
literature is Metandrocarpa taylori (Abbott, 1955). In the laboratory, ascidian larvae resting on the bottom
of the culture vessel or drifting passively in the water column are stimulated to swim by an abrupt reduction
in light intensity. This response was discovered independently by Mast (1921) and Grave (1920) in Aplidium
constellatum. Mast (1921) also reported that swimming tadpoles respond to shadows by changing the
position of the tail, a process which he used to explain phototactic orientation. Sudden increases in light
43
intensity do not elicit kinetic responses in resting ascidian tadpoles, though they may elicit changes in tail
position in active ones (Mast, 1921).
Only a few hypotheses have been advanced to explain the function of the shadow response. Crisp &
Ghobashy (1971) and Grave (1935) noted that ascidian larvae settle sooner when stimulated to swim by
frequent shadows than when held under constant illumination, but Young & Chia (1985) found this same
relationship with only one of eight solitary ascidian species tested. For a species that needs shaded areas for
survival (Olson, 1983; Young & Chia, 1984), it would seem reasonable that a tadpole should quickly
undergo metamorphosis in a region with many shadows. Woodbridge (1924) extended this idea to explain
how Botryllus schlosseri tadpoles locate seagrass blades, which is their normal habitat. She noted that larvae
drifting passively in the water column would be stimulated to swim when passing through the shadow cast
by a blade of seagrass. Larvae so stimulated swam upward 64% of the time and often contacted a seagrass
blade.
Because overhangs, rock crevices, and other shaded habitats tend to be excellent habitats for many
ascidians (Millar, 1971; Berrill, 1975; Olson, 1983; Young & Chia, 1984; and others), one might suppose
that the almost universally occurring shadow response could function in habitat location for many species of
ascidians. This was tested experimentally in the laboratory for eight species by Young & Chia (1985).
Tadpoles were offered choices between shaded overhangs and unshaded habitats under conditions of
constant and fluctuating illumination. It was expected that larvae in the latter treatments would be
stimulated to swim more often than larvae in the former, and would thereby be more likely to locate the
optimal habitats. Only one species, Styela gibbsii, located the downward-facing surface significantly more
often in fluctuating light than in constant light. None of the species located shaded habitats more often as a
result of the shadow response. It was concluded that the shadow response does not facilitate selection of an
optimal light regime at settlement (Young & Chia, 1985).
Geotaxis and phototaxis
A generalised description of ontogenetic changes in ascidian orientation behaviour has persisted in the
literature for nearly 60 years. Millar (1971) has summarised the stereotyped behaviour as follows: The
ascidian larva has a characteristic pattern of behaviour consisting of an initial period when it swims upward
(positive phototropism and negative geotropism) followed by a period when it swims or sinks downwards.
The initial phase serves to distribute larvae, and it is in the second phase that the critical reaction is elicited
in response to a decrease in light. The larva then swims towards dark areas, which in nature tend to be the
vertical or lower surfaces of rocks etc. This idea of ontogenetic change in orientation behaviour holds best
for the compound ascidians that have been investigated; solitary ascidians seem to exhibit much more
variability in their behaviour (Table II, Young & Braithwaite, 1980a; Young, 1982; Svane, 1987). Most data
reporting the phototactic behaviour in ascidian larvae are casual observations made during studies of
settlement and metamorphosis (Thorson, 1964). Many authors have, however, noted that all tadpoles do not
behave the same way. There is often marked variability in behaviour among tadpoles of the same age and
parentage, and also among individuals of different parentage within a given species. Thus, phototaxis in
ascidians is best considered not as a stereotyped behaviour, but as a phenomenon with a statistical
distribution.
Ontogenetic changes in phototaxis and geotaxis have been documented convincingly in several
ovoviviparous colonial ascidians which have a comparatively short planktonic life (Table II). The most
detailed study, that of Crisp & Ghobashy (1971), indicates that Diplosoma listerianum conforms nicely to
the classical generalisation. Larvae of this species remain strongly geonegative and slightly photopositive
44
throughout the swimming period then switch to the opposite responses just before settlement (Crisp &
Ghobashy, 1971). Swimming behaviour is modified by suboptimal temperatures and strong light, but is not
influenced by hydrostatic pressures as high as two atmospheres (Crisp & Ghobashy, 1971). Botryllus
schlosseri, like Diplosoma listerianum, remains weakly photopositive throughout most of its larval life
(Grave & Woodbridge, 1924). Approximately two thirds of the larvae of Perophora viridis retain their
positive phototaxis for their entire larval period; the remaining one third reportedly become photonegative
towards the end of larval life (Grave & McCosh, 1924). In Aplidium constellatum, the photopositive period
lasts for only a few seconds and the larvae spend most of their free-swimming period alternating periods of
rest and activity in less illuminated regions (Grave, 1920).
Several workers have made observations on behavioural changes of colonial ascidians in the field. Duyl,
Bak & Sybesma (1981), Olson (1983, 1985) and Olson & McPherson (1987) all noted initial upwardswimming periods following release of didemnids on coral reefs. In Lissoclinum patella, the larvae moved
upward for only about one minute (over a distance of about a metre) before they began swimming
downward. In situ settlement experiments in a sealed chamber with a window at one end, however,
indicated that larvae settle near the light (Olson & McPherson, 1987). Young (1986) made continuous in
situ observations of behavioural changes in Ecteinascidia turbinata larvae of different ages. Contrary to the
work with other compound ascidians, he found no evidence for an initial upward swimming period. Newly
released larvae drifted passively more often than they swam. Throughout larval life, there were no
significant differences in the amounts of time spent swimming upward and swimming downward.
Swimming behaviour was extremely vari
TABLE II
Summary of ascidian tadpole photoresponses investigated to date. C: compound, S: solitary, X: response present, 0:
response absent, +: responcses positive, : respo onse negative, V: response variable, ?: not reported
Shadow Phototaxis
Family
Species
C/S response early late
Polyclinidae
pellucidum
Aplidium
(Amaroucium)
C
A. constellatum
Didemnidae
Trididemnum solidum
Polycitoridae
Cionidae
Diplosoma
listerianum
C
Distaplia sp.
Ciona intestinalis
Grave, 1920; Mast,

1921
Grave, 1936; Mast,
1921
V
?
C
S
+
?
?
0
+
Duyl et al., 1981

0
Perophoridae
Perophora viridis
Corellidae
C. willmeriana
Chelyosoma
productum
Corella inflata
S
S
S
X
X
X
0
0
Young, 1982
Young &
Braithwaite, 1980a
Reference
Crisp & Ghobashy,

1971
Berrill, 1948a
Berrill, 1947; Castle,
1896; Dilly, 1964;
Dybern, 1963
Grave & McCosh,
1924
Young, 1982
45
Shadow Phototaxis
Family
Species
C/S response early late
Reference
Ascidiidae
Ascidia nigra
Goodbody, 1963;
Grave, 1936
A. callosa
A. paratropa
A. mentula
Styelidae
S
S
S
Dendrodoa
grossularia
C
X
X
X
S
0
0
Young, 1982
Young, 1982
Svane, 1987
0
Symplegma viride
Polyandrocarpa
tincta
P. gravel
Styela montereyensis
C
C
X
X
+
+
_
_
Grave &
Woodbridge, 1924;
Woodbridge, 1924
Grave, 1936
Grave, 1936
C
S
X
X
+
0
_
V
S. coriacea
S. gibbsii
S. partita
Cnemidocarpa
finmarkiensis
Metandrocarpa
taylori
Pyuridae
Boltenia villosa
Halocynthia igaboja
Molgulidae
S
S
S
S
X
X
X
X
0
0
0
0
_
_
_
Grave, 1936
Young &
Braithwaite, 1980b
Young, 1982
Young, 1982
Grave, 1941, 1944
Young, 1982
Abbott, 1955
Pyura haustor
S
S
Molgula citrina
S
X
X
S
X
0
0
0
0
_
V
0
Young, 1982
Young, 1982
0
Botryllus schlosseri
Berrill, 1950
Young, 1982
Grave, 1926
able among individual tadpoles, and the ontogenetic changes in swimming behaviours predicted by the
standard paradigm (Thorson, 1964; Millar, 1971; Berrill, 1975) did not occur (Young, 1986).
In solitary ascidians, behavioural responses to light and gravity are extremely variable. Two species,
Ascidia nigra (Grave, 1935; Goodbody, 1963) and Ciona intestinalis (Berrill, 1947; Millar, 1953; Dybern,
1963), have been reported to pass through photopositive and photonegative phases, but this conclusion is
based on casual observations and field distributions (Dybern, 1963) rather than careful behavioural
experiments. Svane (1987, and unpubl.) has demonstrated experimentally that both C. intestinalis and
Ascidia mentula remain photonegative during their entire free-swimming period. Styela partita is negatively
geotactic under all light conditions, and demonstrates negative phototaxis early in larval life (Grave, 1941,
1944). Late-stage larvae cease swimming and sink passively to the bottom (Grave, 1941, 1944). Although
Grave (1944) attributed this behaviour to a reduced ocellus in styelid larvae, similar behaviour is
demonstrated by Ascidia mentula, a species with a complete 3-lens ocellus (Svane, 1987). The larva of
Molgula citrina, which lacks an ocellus, displays short bouts of negative geotaxis followed by random
swimming and periods of rest (Grave, 1926). No response to light was observed (Grave, 1926).
46
Fig 8.Phototactic orientation mechanism of Aplidium constellation, as explained by Mast (1921). The mechanism
relies on the orientation of the pigment cup, which allows light to strike the retinal cells only from the anterior or right
sides.
The larval ocellus of Ciona savignyi differentiates after hatching, and the larvae are reported to pass
through at least four different behavioural phases that correspond to the ocellar changes (Kajiwara &
Yoshida, 1985). Newly hatched larvae are strongly geonegative but do not respond to light. Within 30 min
of hatching, larvae in culture vessels swarm at the surface in dense aggregations (Kajiwara & Yoshida,
1985). Larvae begin to exhibit the shadow response 1.5 h after hatching, and the response becomes stronger
as larval life proceeds. Finally, larvae developed a strong negative phototaxis after 3.5 h according to
Kajiwara & Yoshida (1985).
In the San Juan Islands of Washington, photoresponses of 12 species of solitary ascidians have been
studied (Young & Braithwaite, 1980a,b; Young, 1982). None of the species showed predictable positive
phototaxis at hatching, although most demonstrated an intermittent negative geotaxis early in larval life.
Photoresponses at settlement were extremely variable in some species (e.g., Chelyosoma productum, Styela
montereyensis), while other species (e.g., Pyura haustor, Corella willmeriana, Cnemidocarpa finmarkiensis)
chose shaded substrata more often than expected by chance. The settlement distributions indicative of
geotactic responses (choices of upward-facing and downward-facing surfaces) were similarly variable
within and among species (Young, 1982). The species differences in phototaxis and geotaxis correlated well
with the distributions of adults in the field.
Taken together, the data on taxes in solitary ascidians suggest that photoresponse is variable among
species and that broad generalisations cannot be made. There is more consistency among the short-lived
larvae of colonial ascidians, but even the latter differ in many important details.
Mast (1921) is the only worker to have considered in detail the mechanism of phototactic orientation in
ascidian tadpoles. Many invertebrate larvae that respond to directional light stimuli (e.g., crustacean zoeae,
polychaete setigers) have two distantly positioned photoreceptors. The mechanism of orientation seems to
involve moving back and forth until an equal amount of energy enters each eye. Using simple but elegant
observational techniques with larvae of Aplidium constellatum, Mast postulated a credible mechanism by
which tadpole larvae orientate with a single photoreceptor (Fig. 8). The pigment cup in the ocellus of A.
constellatum is directed anterolaterally on the right side (which Mast termed the ocular side) of the trunk.
Thus, the retinal cells are stimulated only by light directed from the front or from the ocular side; light
directed from the rear of the animal or from the left side does not stimulate the ocellus. In a tadpole larva
moving perpendicular to a beam of light, the ocellus is alternately illuminated and shaded by the trunk as
the animal spins on its own longitudinal axis. Each time the ocellus is shaded, it stimulates the tail to bend
slightly and briefly (while still vibrating) toward the ocular side. This causes the animal to turn slightly
away from the light. With another half rotation, the retinal cells receive full illumination, causing the tail to
bend toward the abocular side and producing the same effect as before. After this process has been repeated
during several revolutions, the animal becomes situated such that its pigment cup shades the retinal cells
continuously. In this position, no tail bending occurs, and the direction of movement is away from the light
in a straight line. Photopositive animals orientate exactly the same way, except that they bend their tails
toward the abocular side when the ocellus is shaded and toward the ocular side when it is abruptly
illuminated (Mast, 1921). Both the shadow response and the phototactic response described by Mast (1921)
depend on reflexes stimulated by abrupt changes in light intensity. There are, however, several subtle
differences in addition to the net behavioural effect. First, the shadow response occurs only when an animal
is at rest, whereas the phototactic stimulation occurs only in actively swimming animals. Secondly, the
47
shadow response occurs only when light intensity is decreased. An abrupt increase in intensity has no effect
on resting tadpole larvae. Swimming animals, on the other hand, respond both to increases and decreases in
illumination. Finally, the shadow response stimulates vibration of the tail, whereas phototaxis stimulates a
bending of the tail while the latter continues to vibrate (Mast, 1921).
Masts (1921) hypothesis on the mechanism of phototactic orientation is supported by the work of
Kajiwara & Yoshida (1985) on Ciona savignyi. In this species, the pigment of the ocellus is diffuse and
irregular in shape at hatching. It passes through a series of changes and increases in pigment density for the
first 3.5 h of larval life until it finally takes on the characteristic cup shape. Behavioural changes correspond
remarkably well to the changes in ocellus morphology. The shadow response begins when the ocellus
becomes packed with dense pigmented tubules, 1.5 h after hatching, but directed swimming (negative
phototaxis) does not occur until the pigment cup is completely formed (Kajiwara & Yoshida, 1985).
LARVAL MORTALITY
As with most invertebrate larvae, relatively little is known about the sources of mortality occurring during
the pelagic phase. Most work to date has been on predators. Encounters between predatory fishes and three
different species of larvae have been observed in the field (Olson, 1983; Olson & McPherson, 1987; Davis
& Butler, in press). 87% of 133 larvae of Lissoclinum patella followed in the field were consumed by
predatory fishes, zoanthids, or corals (Olson & McPherson, 1987). The major predators were territorial
pomacentrids. Although the fish were equally abundant at all depths between 5 and 25 m, a higher
percentage of tadpoles were consumed at shallow depths than at greater depths. Olson & McPherson (1987)
attributed this difference to the fact that tadpoles passed pomacentrid territories repeatedly in shallow water
as they were buffeted by the surge. One species of fish with a small mouth, Pomacentrus lepidogenys
rejected larvae that they ingested. However, the egested larvae were always damaged too badly to continue
swimming (Olson & McPherson, 1987). Predation rates on Podoclavella moluccensis in Southern Australia
were much lower; of 270 larvae followed in the field, only two were mouthed by fishes, and both lived to settle
successfully (Davis, unpubl.). Similarly, larvae of the didemnid, Didemnum molle were always rejected by
fishes and always survived the attacks (Olson, 1983). Unidentified ascidian tadpoles have been taken in the
guts of the pinfish Lagodon rhomboides in the Gulf of Mexico (J.Luzcovich, pers. comm.). This same fish
species and several others accept tadpoles of many species of compound ascidians in laboratory aquaria
(B.Bingham, unpubl.).
Larval defences against predators (reviewed by Young & Chia, 1987) may be structural, behavioural, or
chemical. The prevalence of both structural (Young, 1985) and chemical (Stoecker, 1978, 1980) defences in
adult ascidians suggests that such mechanisms might also be present in larvae. However, besides anecdotal
evidence (e.g., rejection of larvae by fishes in the field; Olson, 1983; Davis & Butler, in press), there is only
one example of an ascidian larval defence in the literature: distastefulness in larvae of Ecteinascidia
turbinata. The bright orange tadpole larvae of this perophorid ascidian are mouthed then rejected by several
species of fish, including Lagodon rhomboides (Young & Bingham, 1987). By homogenising the larvae and
embedding the homogenate in agar pellets, it was shown that the tadpoles are rendered unpalatable not by a
structural defence but by a potent chemical substance (Young & Bingham, 1987). Fish that had experienced
the taste of Ecteinascidia turbinata larvae learned quickly to avoid them as food, suggesting the possibility
of aposematic (or warning) coloration. This hypotheses was tested by creating artifical mimics of
palatable ascidian tadpoles (Clavelina oblonga) using orange stain. Fish that had not tasted unpalatable
orange tadpoles of Ecteinascidia turbinata consumed the mimics readily, but experienced fish avoided all
orange tadpoles regardless of species (Young & Bingham, 1987). The chemistry of the defence mechanism
48
remains unknown, but Bingham (pers. comm.) has now found several other ascidians in which orange
coloration is correlated with unpalatability to fishes.
Several sessile benthic predators are known to prey on ascidian larvae. The temperate octocoral
Alcyonium siderium and the sea anemone Metridium senile, both of which are common on subtidal rocks in
New England, often contain large numbers of ascidian tadpoles in their guts (Sebens & Koehl, 1984). It has
been proposed that these cnidarians reduce competitive interactions with adult compound ascidians
(Aplidium stellatum) by consuming the competitors larvae (Sebens & Koehl, 1984). Davis & Butler (in
press) observed ingestion of larval Podoclavella moluccensis by the hard coral Culicia tenella in the field.
Corals also captured a small percentage of Lissoclinum patella larvae on the Great Barrier Reef (Olson &
McPherson, 1987).
Adult ascidians sometimes consume their own eggs and larvae or the offspring of other species of
ascidians (Young, 1988). It has been shown that the tendency toward larval cannibalism is greater in species
that occur as solitary individuals in the field than among species that live in aggregations and settle
gregariously as larvae (Young, 1988). Rejection of conspecific eggs relative to those of other species has
also been observed for Ciona intestinalis (Havenhand, pers. comm.). Species that reject their own tadpoles
do so by means of the crossed reflex (Hecht, 1918), in which objects stimulating the oral tentacles or the
inside of the incurrent siphon epithelium elicit closure of the excurrent siphon followed by a strong
contraction of the body wall musculature (Young, 1988). Species with larger siphon diameters tend to reject
eggs and larvae less often than species with small siphon diameters. Young (1988) has proposed that an
efficient rejection mechanism might be an important prerequisite for gregarious settlement responses in
ascidians.
There are undoubtedly numerous sources of mortality other than predators that eliminate larvae or
embryos during their planktonic period (Thorson, 1950, 1966). However, very few such factors have been
investigated for ascidians. Goodbody & Fisher (1974) reared the embryos of Ascidia nigra in sea water
collected from three different habitats and demonstrated higher hatching success in water from the open
ocean than in water from two inshore habitats. Survival differences were attributed to pH and salinity
(Goodbody & Fisher, 1974). Many larvae are probably lost by drifting away from appropriate settlement
sites. However, the extent of this loss has not been estimated.
SETTLEMENT
The transition between pelagic and benthic existence involves two processes, settlement and
metamorphosis. In ascidians, settlement may be defined as the process of locating and affixing to the
juvenile habitat. It generally, though not always, precedes metamorphosis. Metamorphosis is defined as the
sequence of morphological events that transform the larva into a sessile, feeding juvenile (Cloney, 1982).
These processes may include (but are not limited to) attachment, resorption of the tail, rotation of the trunk,
emigration of blood cells from the hemocoel to the tunic, extension of epidermal ampullae, retraction of the
sensory vesicle, and destruction of larval structures (Cloney, 1982). A larva capable of undergoing these
metamorphic changes successfully is termed competent (Jackson & Strathmann, 1981).
The processes by which ascidian tadpoles select habitats may involve numerous characteristic behaviours
including phototaxis, thigmotaxis, chemotaxis, kin recognition, and gregariousness. Behaviour only
becomes important, however, given the appropriate ecological opportunities (Moore, 1975). Thus, inherent
behavioural patterns must interact with the distribution of available habitats, with pre-settlement mortality,
and with factors modifying larval distribution in the plankton to produce the pattern of settlement.
49
Settlement distributions are modified in turn by post-settlement mortality and migration (the latter in
didemnids and some molgulids) to produce the distributional patterns of the juveniles and adults.
Because microscopic juveniles are generally difficult to monitor in the field, there are few data on the
settlement distributions of invertebrate larvae in general. Just as the number of recruits (where recruit is
defined as an individual large enough to observe in the field) is not necessarily representative of the number
of settlers because of mortality occurring between the two stages (Keough & Downes, 1982; Connell, 1985;
Butler, 1986; Davis, 1987), so the distribution of recruits does not always reflect the settlement
distribution. Nevertheless, the positive information contained in recruitment or distributional data should
not be ignored; often, the only sites where we know with certainty that settlement occurred are those
occupied by juveniles or adults. Colonial ascidians are often large enough to observe from the very moment
of settlement, so the problem of distinguishing recruits from settlers is less acute in some members of the
Ascidiacea than in many other invertebrate groups.
Most behavioural studies have considered responses to single factors in isolation, whereas tadpoles are
confronted in the field with interactive, complex suites of potential settlement cues. Whether settlement
cues are ranked consistently or change in relative importance under different environmental conditions is not
known. Some larvae, including those of soft-sediment molgulids, have been described as non-discriminating
at settlement. Such are presumed to settle randomly within whatever regions competent larvae arrive. In the
literature, three major spatial patterns have been attributed to larval behaviour: (1) small-scale singlespecies aggregations that result from gregarious settlement behaviour, (2) epibiosis and multiple-species
aggregations, and (3) occurrence in shaded or cryptic habitats, generally attributed to negative phototaxis.
LARVAL RESPONSES TO CONSPECIFICS
Many solitary ascidians form clumps (Fig 9). Dense aggregations may occur on virtually any scale, only the
smallest of which are likely to be influenced by settlement choices of the larvae (Butman, 1987).
Aggregation is common on soft bottoms where other ascidians may be among the only available hard
substrata for settlement (Young, 1985), but also occurs on rock surfaces where ascidian tunic is much less
common than other available substrata (Young, 1982). Members of the genus Pyura, particularly in the
southern hemisphere, commonly form dense beds in the lower intertidal zone. These include P. praeputialis
in New South Wales, Australia (Dakin, Bennett & Pope, 1948; Underwood & Fairweather, 1986), P.
chilensis and P. stolonifera in Chile (Gutierrez & Lay, 1965; Paine & Suchanek, 1983), P. pachydermatina
in New Zealand (Batham, 1956), P. stolonifera in South Africa (Stephenson, 1942; Day, 1974) and P.
haustor in Washington, USA (Young, 1982). Subtidal styelids and pyurids that aggregate include
Bolteniopsis prenenti (Monniot, 1965), Microcosmus vulgaris (Monniot, 1965), Styela gibbsii (Young,
1985), Dendrodoagrossularia (Berrill, 1955) and Pyura haustor (Young, 1982, 1985). Molgula occidentalis
form aggregations on virtually all scales from fourths of metres up to tens of metres on the relatively flat
terrain of intertidal sandbars (Young, in press). Molgulids occurring in small-scale aggregations on hard
substratum include M. complanata (Schmidt, 1982a, b), M.manhattensis (Monniot, 1965), M. occulata
(Monniot, 1965) and the anural M. pacifica (Young et al., 1988). Subtidal aggregations have been reported
in numerous phlebobranchs including Chelyosoma productum (Young & Braithwaite, 1980a), Corella
inflata (Lambert, 1968), and Ascidia mentula (Havenhand & Svane, in press). Aggregations of some species
tend to have unimodal size distributions, suggesting that they are formed by the nearly simultaneous settlement
of larvae on a common substratum, whereas aggregations of other species are polymodal, consisting of
numerous small individuals attached to the tunic of larger ones. These patterns suggest two different kinds
50
Fig 9.Small-scale aggregations of ascidians. A: subtidal clump of Ciona intestinalis in Gullmarsfjorden, Sweden, B:
intertidal aggregation of Dendrodoa grossularia, probably formed by philopatric dispersal. Note two large adults (A)
surrounded by numerous younger recruits (R). C: aggregation of Pyura haustor, a species with strongly gregarious
larvae at 20 m depth in the San Juan Islands, Washington, USA. D: adult and juvenile Ascidia mentula in
Gullmarsfjorden, Sweden. This species settles gregariously. E: social ascidian Clavelina picta at 15 m depth in the
Bahamas. Apparent aggregations are formed by asexual budding, not larval processes. F: high-density clump of Styela
montereyensis on an intertidal piling in Neah Bay, Washington. Larvae of this species are not gregarious (Young,
1988).
of behaviour, both of which have been documented in ascidians: aggregation among siblings or other
individuals of the same age, and selection of adult conspecifics as a settlement site.
Chemical cues associated with adults and juveniles stimulate metamorphosis and settlement in many
ascidian species. Grave (1935) and Grave & Nicoll (1939) discovered that larvae of Ascidia nigra and
Polyandrocarpa sp. were induced to settle sooner in adult or larval tissue extracts than in plain sea water.
The same phenomenon has now been shown to occur in Ascidia mentula, Ascidiella scabra, (Svane,
Havenhand & Jrgensen, 1987), and Pyura haustor (Young, unpubl. data). In all of these species, the time
to settlement is related to the concentration of the adult extracts to which larvae are exposed. Significantly,
extracts of tunic, the tissue larvae are most likely to contact, are more potent inducers than visceral extracts
(Svane et al., 1987). Ascidiella scabra can be stimulated to undergo metamorphosis while still enclosed in
their egg envelope (Svane et al., 1987), suggesting that larvae are competent to settle immediately after
hatching. Although Grave & Nicoll (1939) reported a species specific effect (tissue extracts of
Polyandrocarpa do not stimulate metamorphosis in Ascidia nigra), Svane et al. (1987) found little evidence
for specificity between the two closely related ascidiids, Ascidiella scabra and Ascidia mentula. Larvae of
Pyura haustor can be stimulated to undergo metamorphosis by exposure to sea water that has passed
through the branchial sac and atrium of conspecific adults (Young, 1978). All of these phenomena are known
only from the laboratory. Although their ecological significance remains unproven, the observations suggest
not only that adult-associated cues could be important inducers of metamorphosis, but also that larvae may
be able to detect water-borne (as opposed to surface-bound) cues.
Larvae of several ascidians respond to newly settled juveniles. In dense cultures of Chelyosoma
productum, larvae settle in a distinctly non-random manner (Young & Braithwaite, 1980a) and select areas
with established juveniles much more often than regions colonised only by algae and bacteria (Young &
Braithwaite, 1980a). Duyl, Bak & Sybesma (1981) showed that larvae of Trididemnum solidum settle
sooner when even a single juvenile is present in a beaker than when no established juvenile is present. In
related studies with Ascidia nigra, it was shown that curves of settlement versus time have steeper slopes
when large numbers of larvae are present in the vials (Grave & Nicoll, 1939). Grosberg (1981) compared
settlement density of Botryllus schlosseri among plates with varying densities of established juvenile
colonies present. Although juveniles were avoided by many species of invertebrates, the presence of
juveniles had no apparent effect on the settlement rates of conspecifics or any other species of ascidian.
These data are supported by Schmidt (1982b) showing random spatial distributions among B. schlosseri
settlers in Britain. Schmidt (1982b) also recorded the distribution of two other species of ascidians,
Diplosoma listerianum, and Molgula complanata, on Perspex panels after submergence for four weeks; M.
complanata was found to be aggregatively distributed while Diplosoma listerianum were distributed
randomly. Schmidt (1982a,b) concluded that the observed distribution pattern resulted from tadpole choices
or the absence thereof. In D. listerianum this conclusion was supported by nearest neighbour distances in
laboratory settlement experiments, but the evidence for larval behaviour as a determinant of juvenile spatial
pattern in Molgula complanata is equivocal, since post-settlement processes operating during the four week
51
submergence period were not addressed. Havenhand & Svane (in press) demonstrated that distributions of
newly settled Ascidia mentula in Petri dishes were significantly different from random at densities higher
than 5 per cm2, but not at lower densities.
The second pattern of single-species aggregation, characterised by a polymodal age distribution within a
given clump, implies that larvae attach directly to the surfaces of established adults. Because the same
pattern can, however, result from differential mortality in which survival is greater in that portion of the
population settled on adults, careful settlement experiments are required before behavioural preferences are
implicated as the cause. Such choice experiments have been run with several species. Larvae of Pyura
haustor, a species that forms aggregations in the rocky intertidal zone, and in both soft and hard subtidal
habitats, demonstrate a strong preference for the tunic of adult conspecifics as a settlement site (Young,
1982). Other substrata, including rocks, mollusc shell, and the tunic from various other ascidians are
selected much less often than P. haustor tunic. Experiments in which the grooves and crevices of adult tunic
are removed by a clean cut indicate that the attraction is not to structural or textural features, but rather to
some chemical aspect of the adult. The possible selective advantage of this behaviour has been investigated
by allowing larvae to settle on living adults and on rocks in the laboratory, then outplanting the juveniles to
intertidal habitats where the adults naturally occur (Young, 1983). Over a two-week period, survival on
adults was significantly higher than survival on adjacent rocks. Young (1984) attributed this difference to
higher moisture and lower temperatures in the ascidian clumps during periods of tidal exposure.
Havenhand & Svane (in press) have investigated gregarious settlement of Ascidia mentula, a species that
consistently aggregates in the fjords of western Sweden. Over an 11-year period, recruitment of juveniles at
several subtidal sites was correlated with adult density. In the laboratory, three pieces of evidence were
indicative of gregarious settlement responses: aggregation of juveniles, acceleration of metamorphosis in
response to adult tunic extracts, and apparent attraction to adult tunic. In the latter experiments, larval
distribution was examined after 10 min of incubation in a submerged tube with an adult affixed to one end.
There were consistently more larvae at the adult end than the opposite end. Although this experiment is
indicative of gregarious larval behaviour, it does not demonstrate whether distant chemotaxis is involved or
if larvae simply remain in the vicinity of an adult following random encounter.
Adults and juveniles of Molgula occidentalis cover themselves completely with sand by means of fine
tunic filaments all over the body. Larvae offered a choice of sand collected from the environment, sand
removed from adults, or adult tunic selected the adult sand significantly more often than the other substrata
(Young, in press). This ability to select a habitat may seem surprising in that these molgulid larvae have
very reduced oral papillae (Cloney, 1978), but sensory neurons have been located in the anterior epidermis
of the apapillate larva (Torrence & Cloney, 1988) (Fig 10).
Young (1988) tested eight ascidian species for gregarious settlement by offering natural rocks and adult
tunic to larvae as alternative substratum choices. Besides those species already discussed (Pyura haustor,
Chelyosoma productum), only one, Styela gibbsii, was gregarious in laboratory experiments. Four other
species that sometimes attach to adults under field conditions (Styela montereyensis, Boltenia villosa,
Ascidia callosa, and Halocynthia igabojd) did not demonstrate strong preferences for adult tunic in the
laboratory. The remaining five species tested did not select adult tunic as a preferred substratum. This
pattern was expected, as none of them are found attached to conspecifics in the field (Young, 1988). Young
52
Fig 10.Attachment process of the apapillate larvae of Molgula occidentalis (A). Newly metamorphosed juvenile (B)
showing sticky primary ampulla which provides initial attachment to the substratum. Juvenile several days old (C)
attached to adjacent sand grains with secondary ampullae. Sediment-covered adults (D) on an intertidal sandflat.
(1985) provided field evidence that aggregation in Styela gibbsii reduces predation by the subtidal asteroid
Evasterias troschelii by limiting the predators access to a region of soft tunic on the posterior end.
SETTLEMENT RESPONSES TO OTHER ORGANISMS
On both hard and soft bottoms, many species of solitary ascidians occur in multiple species aggregations
where individuals are attached directly to individuals of other species. Monniot (1965) described the
ecological relationships in such aggregations, termed blocs de Microcosmus in which large individuals of
Microcosmus vulgaris provide attachment surfaces for many species of ascidians and other invertebrates. In
Washington, aggregations dredged from deep, muddy bottoms often include as many as eight different
species of solitary ascidians. Boltenia villosa and Styela gibbsii live attached to the tunic of Halocynthia
igaboja and Pyura haustor, where they obtain protection from the predatory gastropod Fusitriton
oregonensis (Young, 1985, 1986). In laboratory experiments, it has been demonstrated that larvae of both
these epizooitic species prefer the tunic of the host species over the tunics of other species, as well as
common inorganic substrata from their environment including rock and shell (Young, 1982). Moreover, the
larvae of both Boltenia villosa and Styela gibbsii delay metamorphosis in the absence of suitable substratum
(Young, 1982).
Davis (1987) documented the settlement choices of larvae of Podoclavella moluccensis by following,
larvae underwater and noting the outcome (settlement or rejection) of their first encounter with a substratum.
Besides wooden pier pilings, most of the available substrata were sponges of several species. When a
substratum was acceptable, a larva beat its tail vigorously for 35 min after attachment. Attached larvae
were capable of rejecting a substratum by detaching with a short flick of the tail. Larvae generally rejected
sponges, particularly those of the genera Dendrocia and Mycale. During the first month after settlement,
survival was significantly higher on bare space and on the preferred sponges than on those sponges most
often rejected by the larvae, suggesting that the settlement choices had an adaptive component (Davis,
1987). Moreover, larval choices were good predictors of the relative proportions of recruits appearing on the
various available substrata in the system.
SETTLEMENT RESPONSES TO PHYSICAL CUES
Ascidians often occur in cryptic habitats such as cracks, crevices, and the dark undersides of rocks or
overhangs. It has often been assumed that these habitats are located by negtive photo taxis (Dybern, 1963;
Thorson, 1964; Crisp & Ghobashy, 1971; Millar, 1971; Berrill, 1975). The same pattern could, however,
result from other behaviours including the shadow response (Woodbridge, 1924; Young & Chia, 1984),
rugophilia, and negative geotaxis. Many selective pressures operate more intensely in open than cryptic
sites, particularly during the juvenile stage. These include predation (Keough & Downes, 1986), silt (Young
& Chia, 1984; Svane, 1987), competition with diatoms or filamentous algae (Goodbody, 1963; Young &
Chia, 1984), grazing by herbivorous snails (Young & Chia, 1984) and ultraviolet light (Olson, 1983). Thus,
both behaviour and selective mortality must be considered as important determinants of a cryptophilic
distribution. Indeed, photonegative behaviour probably evolved in response to the predictable differences in
mortality between open and shaded habitats.
53
By integrating field recruitment studies with laboratory experiments on larval behaviour, Dybern (1963)
demonstrated that negative phototaxis in the larval stage can explain the crytophilic distribution of Ciona
intestinalis in Gullmarsfjorden, Sweden. Although he did not consider the possibility that post-settlement
mortality on upward-facing surfaces could enhance the distributional pattern, Dyberns (1963) observation
that deep-water (low light) populations often occur on such surfaces supports his hypothesis that larval
behaviour sets the pattern of distribution.
On subtidal limestone outcroppings in the Gulf of Mexico, the compound ascidian Aplidium stellatum
recruits primarily on vertical surfaces, which are much less common than horizontal ones (Gotelli, 1987).
Laboratory experiments with the larvae demonstrated that vertical surfaces were chosen over horizontal
ones in a consistent 2:1 ratio regardless of the relative proportions of the two kinds of surfaces. The nature of
the behaviour producing this pattern has not been investigated.
While following larvae of Didemnum molle underwater on the Great Barrier Reef, Olson (1983) observed
that nearly all individuals settled on the undersurfaces of coral rubble and that recruits on horizontal
settlement panels occur mostly on the undersides, within a few centimetres from the edge. In vitro
experiments demonstrated, in agreement with the field observations, that larvae select shaded over unshaded
surfaces. The advantage of photonegative settlement behaviour becomes apparent in the juvenile stage.
Individuals reared in exposed reef habitats died within four days of settlement, possibly of exposure to
ultraviolet light (Olson, 1983). The behaviour of D. molle larvae contrasts markedly with that of Lissoclinum
patella, another didemnid containing symbiotic Prochloron algae (Olson & McPherson, 1987). Larvae of the
latter species settled exclusively near the light end of a 1-m long light gradient. Olson & McPherson (1987)
used this photopositive settlement behaviour to explain the low density of adult colonies at depths greater than
25 m. Alternative hypotheses (e.g., low survival of symbionts due to lower light levels) were, however, not
tested.
A comparative study of larval settlement behaviour in 12 species of ascidians in the Puget Sound region
of Washington, USA, showed that some species were strongly photonegative at settlement, whereas others
did not discriminate between illuminated and shaded substrata (Young, 1982). In most cases, larval
behaviour was a good predictor of adult distribution in rocky subtidal habitats. Photonegative larval
behaviour has also been implicated as a determinant of distribution in Diplosoma listerianum (Crisp &
Ghobashy, 1971) and Botryllus schlosseri (Woodbridge, 1924; Dybern, 1963). Young & Svane (unpubl.)
compared larval behaviour and field distribution of two solitary ascidians in Florida, one (Microcosmus
exasperatus) of which lacks a pigmented ocellus, and one (Ascidia nigra) of which discriminates between
light and dark regions at settlement. Recruitment of the two species on half-shaded Plexiglas plates in the
field followed the laboratory predictions; Microcosmus exasperatus settled randomly, whereas Ascidia
nigra demonstrated a preference for the dark portions of the plates (Young & Svane, unpubl.).
ROLE OF REPRODUCTIVE AND LARVAL PROCESSES IN RECRUITMENT
In recent years, population biologists working in the marine environment have placed an increasing
emphasis on processes that control the abundance (or supply) of new recruits (Underwood & Denley,
1984; Connell, 1985; Roughgarden, Iwasa & Baxter, 1985). In ascidians, as in other benthic marine
invertebrates with open populations, both temporal patterns of abundance (i.e. population dynamics) and
spatial patterns of distribution are influenced by developmental mode, mortality occurring during the larval
stage, advection and diffusion of larvae, and larval behaviour, as well as the distribution, fecundity and
mortality of adult populations. We have already discussed many of these factors as isolated topics. In this
54
section, we will consider the relative contributions of these factors in producing spatial and temporal
patterns of ascidian recruitment.
For our purposes, recruitment may be defined as appearance of a new generation of ascidians in a benthic
population. The definition is operational rather than absolute, since different sampling protocols cause
recruits to be first documented at different ages after settlement (Keough & Downes, 1982; Connell, 1985).
Thus, a settler is the product of larval processes alone, but a recruit is the composite product of larval
processes and events occurring during that portion of the post-settlement stage before the animal is first
noticed by the ecologists.
It is axiomatic that recruitment varies from place to place and from time to time. One might expect that
recruitment events would be tied closely to reproductive seasonality (reviewed by Millar, 1971), but local
patterns of mortality can result in no recruitment even when many larvae are produced.
In a discrete population, it should be possible to estimate pre-recruitment mortality by comparing
fecundity and recruitment. If recruitment were determined entirely by larval production, then one would
expect a perfect correlation between patterns of fecundity and patterns of recruitment (Gotelli, 1987); lower
levels of correlation should reflect variability in pre-recruitment losses. Most benthic invertebrates have,
however, open populations where immigration and emigration are difficult or impossible to assess
(Roughgarden et al., 1985). Quantitative comparisons of fecundity and recruitment become meaningful only
where populations are closed or discrete, where dispersal time is very short, or where larval losses can be
measured by direct obervations. Fortunately, some ascidian populations meet these criteria. Davis & Butler
(in press) have presented evidence that the ascidian Podoclavella moluccensis has closed populations in the
gulfs of South Australia. Using underwater observation of larvae, Davis (1988) estimated the number of
individuals surviving to each major life history stage. Of 6430 larvae produced per m2, only 6.1 % settled.
This estimate of larval mortality is about the same order of magnitude as estimates for other benthic
invertebrates, including bivalves with much longer-lived larvae (reviewed by Strathmann, 1985; Young &
Chia, 1987). About 63% of the settlers survived the first month to become recruits and 14% of recruits
survived to become reproductive adults. Thus, only 0.56% of all larvae survived to sexual maturity (Davis,
1987). Gotelli (1987) studied a shallow subtidal population of Aplidium stellatum on a discrete limestone
outcropping. Just over 50% of the temporal variation in recruitment could be explained by variation in the
number of zooids brooding larvae in the previous month (Gotelli, 1987). The rest of the variability in
recruitment was attributed to unstudied and variable losses in the larval and juvenile stages.
Life table and survivorship curves have been calculated for many ascidians (Goodbody, 1962, 1963;
Lambert, 1968; Goodbody & Gibson, 1974; Nomaguchi, 1974; Svane & Lundlv, 1981; Svane, 1983, 1987;
Young & Chia, 1984; Young, 1985; Keough & Downes, 1986; Davis, 1987), but almost none of these
consider mortality (wastage, in the terminology of Thorson, 1950, 1966) in the plankton, and only a few
have characterised mortality immediately after settlement. The compound ascidian Podoclavella
moluccensis is the only species for which mortality in all life history stages has been estimated (Davis, 1988).
Olson & McPherson (1987) have estimated larval mortality of one additional species by direct observation,
and several workers have studied the contribution of early post-settlement mortality. One method of
documenting the mortality occurring during these early (and often microscopic) benthic stages is to
transplant laboratory-settled juveniles on artificial substrata to the field habitats of interest. This method has
been used for eight species of solitary ascidians in Washington (Young & Chia, 1984), for Ascidia mentula
in Sweden (Svane, 1987), for Ascidia nigra in the Caribbean (Goodbody, 1963), and for Ciona intestinalis
in Japan (Nomaguchi, 1974; Yamaguchi, 1975). High resolution monitoring of larger juveniles in the field
has yielded similar data for several compound ascidians (Olson, 1983; Keough & Downes, 1986; Davis,
1987). Most of these studies indicated high habitat specific early mortality. All of those studies in which
55
Fig 11.Cluster dendrogram of correlation coefficients of recruitment over a 12-year period for Ascidia mentula at
three stations each at two depth levels in Gullmarsfjorden on the Swedish west coast. Redrawn from Svane (1984).
mortality was measured in different seasons or in different years showed high temporal variation. The causes
of this temporal variation in survival have not been explored adequately in any system.
Because temperature is correlated with the timing of reproduction in many ascidian species (Millar,
1971), populations of the same species living under different temperature regimes might be expected to
either recruit at different times or demonstrate differences in the duration of the reproductive period. This is
reflected in the size-frequency distributions of Scandinavian populations of Ciona intestinalis. Shallowwater populations which experience relatively high summer temperatures consist of only a single generation
at a time, whereas deeper populations living where temperatures are relatively low and stable may have up
to three generations represented in the age structure, because of multiple recruitment events (Dybern, 1963;
Millar, 1971; Svane, 1983). Synchronous recruitment of Podoclavella moluccensis has been noted by Davis
& Butler (in press) at several sites in South Australia. However, Keough (1983) compared recruitment of
Ciona intestinalis, Botrylloides leachii, Didemnum sp. and other sessile animals at two sites in Southern
Australia separated by a distance of approximately 100 km and found no synchrony between sites. Svane
(1983, 1984, 1988) found good synchrony in recruitment of Ascidia mentula, Ciona intestinalis, and
Ascidiella sp. between sites separated by distances of 110 km and 9 km in Sweden.
When comparing 12 years of recruitment patterns from stations in Gullmarsfjorden and in the archipelago
off the Swedish west coast, Svane (1984) showed that recruitment correlated significantly between stations
in the inner fjord and that portion of the central fjord greater than 20 m deep, while the station in the
exposed archipelago correlated significantly with the shallow (15 m) station in the central portion of the
fjord (Fig 11). This pattern was explained by the hydrographic properties of the area which may cause
entrapment of eggs and larvae for long periods of time. Although temperature or other factors may help to
explain the absence of recruitment synchrony between widely separated sites, many other factors (e.g.,
larval mortality; aggregation, local physical factors) are likely to be important; as always, correlation is
fraught with the danger of misinterpretation!
The solitary ascidians on subtidal rock walls of the Swedish west coast (Svane & Lundlv, 1981, 1982;
Svane, 1983) have been monitored more intensively than those at any other site. Over a 12-year period,
repeated sampling revealed major differences in the longevity and recruitment dynamics of four major
species, Ciona intestinalis, Boltenia echinata, Ascidia mentula, and Pyura tessellata. The most common
annual species in the system, Ciona intestinalis, fluctuated widely from year to year (Svane, 1983), whereas
the longest-lived species, Pyura tessellata, had a constant population size over the entire study (Svane &
Lundlv, 1982; Svane, 1983). Those species with the most stable populations also had low fecundity and
recruitment.
Solitary ascidians with relatively short (less than two years) generation time such as Corella inflata
(Lambert, 1968), Ascidia nigra (Goodbody, 1962), and Ciona intestinalis (Dybern, 1963; Gulliksen, 1972;
Svane, 1983) often demonstrate large local variations in population size from year to year. Current
paradigms would predict that such species should be excellent colonisers, having high fecundities and fast
growth to reproductive maturity (Jackson, 1977). These species are weedy; by producing many gametes,
they are likely to have larvae present whenever an ecological opportunity (e.g. in the form of a new
substratum) becomes available for settlement. Many short-lived species are poor competitors for space
(Goodbody, 1965; Lambert, 1968) or are readily preyed upon due to their thin, gelatinous tunic (Lambert,
1968; Gulliksen & Skjaeveland, 1973; Young, 1986). Lambert (1968) has suggested that the brooding
mechanism of Corella inflata is a method for producing multiple generations at a good site before individuals
56
begin to lose ground to superior competitors such as compound ascidians (but see Young, 1988, for an
alternative hypothesis).
Annual, or short lived, ascidians are commonly found in fouling communities occurring on submerged
hard substrata such as experimental panels (e.g. Sutherland, 1974; Field, 1982; Kay & Butler, 1983; Todd &
Turner, 1986, and many others). Recruitment onto these hard substrata is highly unpredictable and the
communities themselves are highly unstable both temporally and spatially (Dayton, 1984). Longer lived
ascidians may, however, stabilise these communities for a period of time (Sutherland, 1981). Recruitment
onto fouling panels and subsequent community development is influenced strongly by substratum size,
quality, and the orientation of the panels (e.g., Keough, 1983; Todd & Turner, 1986). The developing
communities are rarely comparable to those found on natural hard substrata since different organising forces
operate (Svane, 1988). Kay & Keough (1981) found that relatively small isolated patches (the pen shell
Pinna bicolor) were colonised mainly by larval recruitment while cleared patches on pilings nearby were
colonised by the vegetative extension of adjacent sponges and colonial ascidians. Submerged artificial hard
substrata may therefore be regarded as larval filters in which the effective pore size is determined by the
physical properties of the material and by the surrounding environment, on both small and large scales.
Fecundity is related inversely to tunic dry weight (Svane, 1983). Thus, species with low fecundity (e.g.
Pyura tessellata) compensate by increasing longevity (more than 11 years) with a tough, protective adult
tunic. Although these species seem to recruit rarely because of their low fecundity, their populations are
often more stable than populations of species with higher recruitment potential that risk more of their
available energy by sending larvae into the plankton.
EPILOGUE
Over the past half century, studies of ascidian tadpole larvae have progressed along many fronts. In recent
years, ultrastructural studies have shed light on attachment, locomotory, and behavioural mechanisms, and
behavioural studies indicate functions for known structures. Studies of long-term recruitment dynamics
integrated with laboratory studies of larvae show how various life-history stages integrate to produce
temporal and spatial patterns of variation which are of interest to the ecologist. Ascidians have proved ideal
for general studies of larvae for many reasons, among which are short larval life, lecithotrophy (larvae need
not be fed in culture), diversity of behaviours and structures, and ease of obtaining material for experiments.
The large size of some colonial ascidian larvae allows us to follow, observe, and manipulate larvae in their
natural environment. Logistic problems prohibit the use of such direct methods in most other invertebrate
groups. Although in the past five years a rapid development in the use of in situ techniques has been seen,
there remains a variety of important and unresolved questions in ascidian larval ecology specifically and
invertebrate larval ecology in general that could be addressed using ascidian tadpole larvae.
ACKNOWLEDGEMENTS
We wish to thank our colleagues for valuable comments and criticism. We are particularly indebted to Brian
Bingham, Lane Cameron, Andy Davis, Jon Havenhand, and Randy Olson for providing assistance and
valuable information. One of us (I.Svane) is grateful to Dr T.Brattegrd and the Marine Biological Station,
University of Bergen, for providing excellent working facilities during the preparation of this work. The
study was supported by the Swedish Natural Science Research Council, contract no. B-BU 8526300 to
I.Svane and in part by National Science Foundation grant no. OCE-8400406 to C.M.Young. The project
was conceived and completed during reciprocal transatlantic visits supported by our respective institutions.
57
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EGG PRODUCTION IN CIRRIPEDES

MARGARET BARNES
The Scottish Marine Biological Association, The Dunstaffnage Marine Research
Laboratory, Oban, Argyll, PA34 4AD, Scotland
ABSTRACT gE g production in three orders, Acrothoracica, Rhizoce phala, and Thoracica has
been dealt with in this review. The Acrothoracica are burrowing forms, the Rhizocephala are
parasitic, and the Thoracica the true barnacles. uM ch of the information on egg production
concerns the Thoracica. There are, however, scattered references to egg production in the other
two orders.
Cirripedes may be hermaphroditic or have separate sexes in which case dwarf males are needed
for fertilisation. In some cases hermaphrodites have complemental or apertural males. Transfer
of spermatozoa, ac tivated by secretions of the oviducal gland, penetrate the oviducal sac and
fertilisation results. gE gs a re developed outside the body but within the mantle cavity of the adult.
The relative virtues of self- and cross-fertilisation have been discussed.
Animals producing lecithotrophic nauplii usually have broods of fewer than usual eggs of a
larger siz e than normal. The rhiz ocephalans are an exception; their eggs are small and numerous.
Acrothoracicans also have lecithotrophic nauplii but the eggs are bigger and fewer than in the
rhizoce phalans. Some lepadomorphs have lecithotrophic larvae and within the balanomorphs the
teT racl
ita species produce some anomalies; three species are lecithotrophic and the rest, as far as
is known, are planktotrophic.
At high latitudes and low temperature the fertilisation of eggs and release of nauplii has to be
carefully controlled with probably only one brood a year. At lower latitudes, where temperature
is higher and environmental conditions remain favourable longer, many broods can be produced
in quick succe ssion.
INTRODUCTION
As members of the Crustacea, cirripedes have an exclusively sessile habit either as free-living filter-feeders
or as highly specialised parasites. They may be estuarine or marine and are found at all depths of the ocean
in a wide variety of habitats. The sub-class Cirripedia (a member of the Maxillopoda, see e.g. Newman,
63
Zullo & Withers, 1969) was traditionally regarded to comprise the orders Apoda, Ascothoracica, Thoracica,
Acrothoracica, and Rhizocephala. The Apoda, represented by the parasite Protolepas bivincta, was removed
from the Cirripedia after Bocquet-Vdrine (1972a, 1979) showed that the parasite was an epicaridean. The
Ascothoracica encompasses primitive crustaceans living as parasites of echinoderms and coelenterates and
are generally found in deep water. They are suctorial rather than cirral feeding, the nauplii lack frontal horns
(Zullo, 1979) and all stages are capable of feeding; this is not true of the other orders. The sperm
morphology differs from that of the remainder of the cirripedes (Grygier, 1982, 1983a). There has also been
some discussion about the position of the gonopores and whether carapace pores could be homologous to
frontal horn glands (Grygier, 1983b). Hallberg, Elofsson & Grygier (1985) have now found that the
ascothoracid larva described by Grygier (1983c) does indeed have functional compound eyes suggesting a
close relationship to the Cirripedia. There is still, however, only a limited amount of material available for
such comparisons. In view of the controversy that has been apparent for some time about the position of the
Ascothoracicathe most recent account being that of Grygier (1987)it seems reasonable at present to
keep it separate from the Cirripedia but as a sub-class of the Maxillopoda (Newman, 1982). This account of
egg production in cirripedes will, therefore, only be concerned with the orders Thoracica, Acrothoracica,
and Rhizocephala.
The Acrothoracica represent burrowing forms, the Rhizocephala parasitic forms without appendages or
digestive tract, and the Thoracica the true barnacles. Most of the information regarding egg production
concerns the last of these three orders. There are, however, numerous references, many of them anecdotal,
to egg production in the other orders and an attempt will be made to summarise these. Systematics and
nomenclature are not the concern of this article and it is, therefore, the intention to use the names given by
the various workers in their published papers.
GENERAL
Cirripedes may be either hermaphroditic or have separate sexes (Darwin, 1851, 1873; Batham, 1945a;
Henry & McLaughlin, 1965, 1967; McLaughlin & Henry, 1972; Gomez, 1974; Foster, 1978, 1983;
Newman, 1980; Dayton, Newman & Oliver, 1982; Crisp, 1983; Hui & Moyse, 1984). When the sexes are
separate the males are referred to as dwarf males. In some cases hermaphrodites may also have one or more
males attached in which case they are called complemental males. Crisp (1983) introduced the term
apertural males for individuals he found settled on the operculum of Chelonobia patula. Similar males have
been found in Chirona tennis (Zevina & Poliakova, 1986). These apertural males are capable of feeding and
appear to be potential hermaphrodites in which development has been arrested.
The determination of sex in cyprids of barnacles carrying dwarf or complemental males has received some
attention over the years as can be seen from the work of the following authors: Khnert (1934), Callan
(1941), Veillet (1956, 1961), Yanagimachi (1961a), Gomez, Faulkner, Newman & Ireland (1973), Gomez
(1974, 1975), Heg (1984), and Walker (1985, 1987).
Complemental and dwarf males are greatly reduced and consist of little more than the reproductive
structures; their comparative anatomy has been reviewed recently by Klepal (1987). They may be attached
in or about the external aperture of a normal hermaphrodite or female. At maturity spermatozoa are
introduced into the visceral tissue or mantle cavity (body chamber) of the mature hermaphrodite or female.
The transfer of spermatozoa may be by an injection of cells from the male in the Rhizocerphala (see e.g.
Ichikawa & Yanagimachi, 1958; Reischman, 1959) or via a penis in the Acrothoracica and Thoracica (first
seen by R. Bishop and recorded by Bate, 1869). In some cases the penis is capable of great extension in
length for this purpose. Because semen is introduced into a functional female near the oviducal opening but
64
MARGARET BARNES
not into the female genital tract exception may be taken to the use of the word copulation; it has, however,
been widely used although some people prefer the term pseudo-copulation.
In the Acrothoracica and Thoracica oviducts running from the ovaries enter the mantle cavity at the base
of the first cirri. Movement of ova from the ovaries via the oviducts is stimulated by semen covering the
exit of the oviducts in the mantle cavity. Spermatozoa, if not already motile, are activated by secretions from
the oviducal gland and the oviducal sac containing the ova is penetrated (Walley, 1965; Barnes, Barnes &
Klepal, 1977; Klepal & Barnes, 1977; Klepal, Barnes & Barnes, 1977; Walker, 1977a, 1980). Fertilisation
takes place at this time and in all cirripedes the eggs develop external to the body but within the mantle
cavity of the adult. In what follows the term egg will be used for the fertilised ovum plus its nutritive and
protective tissues and from which, in the case of cirripedes, one of the planktonic stages emerges. The
embryo will be regarded as the young organism in its stages of development within the egg.
Within the eggs of cirripedes the embryos develop, eventually hatch and the young leave the mantle
cavity. At this time it may be as a Stage I nauplius or, in some cases, as a cyprid. There are several nauplius
stages (up to six) followed by a cyprid stage which eventually settles and becomes the adult animal. In some
Rhizocephala the cyprid stage is followed by a kentrogon stage (which produces the reproductive adult) or a
trichogon stage (Heg, 1987).
FERTILISATION
Cross-fertilisation is obligatory in most cirripedes although several instances of self-fertilisation are known.
Self-fertilisation may occur in some species when individuals are isolated by distances greater than the
length of the extended penis (see e.g. Barnes & Crisp, 1956; Barnes & Barnes, 1958). In such cases
parthenogenesis or activation by water-borne spermatozoa must be shown to be absent. The former could be
eliminated by detailed cytological investigations. This has never been done but because male and female
gonads are ripe simultaneously and cross-fertilisation is normal in the same species, parthenogenesis is
unlikely. Fertilisation by water-borne spermatozoa also appears improbable (Barnes & Crisp, 1956). First,
there is no decrease in the incidence of egg masses in isolated animals with increasing distance of isolation.
Secondly, seminal fluid is rarely seen to be emitted except as a result of the stimulus of copulation and then
takes place within the mantle cavity when the semen at first coagulates on contact with sea water. Thirdly,
oviposition itself normally only occurs in association with the copulatory stimulus. Self-fertilisation,
therefore, remains the only possible mechanism.
The percentage of a population whose egg masses have reached a given stage of development is always
greater in contiguous compared with isolated individuals, indicating that in the latter oviposition may be
delayed. This delay is almost certainly dependent on the absence of the appropriate stimulus to oviposition
associated with copulation. Eventually the threshold value of this stimulus must be reached and perhaps
under these conditions movements of the penis within the mantle cavity are sufficient to initiate discharge
of semen and to induce oviposition. Although many apparently viable nauplii may be obtained from the ripe
egg masses contained in isolated, and presumably self-fertilised, individuals there are often many
unsegmented and abnormal eggs. This suggests that self-fertilised eggs are less viable. The fact that the
number of normal, viable nauplii from an animal of a given size is less when it is growing isolated than
when it is in a position to be cross-fertilised also suggests that the latter is a more effective form of reproduction
(Barnes & Crisp, 1956).
Instances of self-fertilisation have been found in Verruca stroemia (Barnes & Crisp, 1956), Balanus
amphitrite (Patel & Crisp, 1961), B. amphitrite communis (Pillay & Nair, 1972), B. balanus (Barnes &
Barnes, 1954; Crisp, 1954), B. eburneus (Cheung & Nigrelli, 1969; Landau, 1976), B. improvisus
65
(E.Furman, pers. comm.), B. perforatus (Barnes & Crisp, 1956), B. trigonus (Werner, 1967), Octolasmis
warwickii (Harker, 1975), and possibly in Platylepas ophiophilus (Zann, 1975) although this is not yet
confirmed. There is evidence that several species of Chthamalus can self-fertilise (Barnes & Crisp, 1956;
Barnes & Barnes, 1958; Tenerelli, 1958; Klepal & Barnes, 1975). In this genus many of the species extend
to high intertidal levels and the capacity to resort ultimately to self-fertilisation may have a survival value.
The population density at such levels may not always be sufficient to ensure proximity of individuals for
mutual copulation. The advantages of hermaphrodites which normally cross-fertilise being able, in some
circumstances, to self-fertilise have been discussed by Tomlinson (1966), Ghiselin (1969), and Sastry (1983).
Ghiselin (1984) has discussed the use of dwarf or complemental males which can be regarded as a form of
self-fertilisation when they originate from the adult to which they eventually become attached. In many
instances it is assumed that this is not the case.
REPRODUCTIVE GONADS
The processes of spermatogenesis and oogenesis are outwith the scope of this review albeit spermatozoa
and ova are necessary for egg production and deserve a mention. The most detailed experimental work on
these processes has been done on members of the Thoracica. Early workers were aware that the
spermatozoa of some cirripedes were finely filiform and capable of movement at some time in their life. In
more recent times modern methods of study including scanning and electron microscopy have been used to
extend our knowledge of cirripede spermatozoa and spermatogenesis. Rigo (1941) worked on Balanus
amphitrite communis; Bocquet-Vdrine & Pochon-Masson (1969) on B. perforatus; Munn & Barnes
(1970a,b) and Barnes, Klepal & Munn (1971) on B. amphitrite amphitrite, B. balanoides, B. balanus, B.
crenatus, B. eburneus, and B. perforatus, also Chthamalus stellatus, Verruca stroemia, and Elminius
modestus; and Honma & Nakajima (1973) on Balanus eburneus. The relative inactivity of the spermatozoa
of B. balanoides was commented on by several of these authors and also by Walley, White & Brander
(1971) and Walker (1977b) who found that fluid from the oviducal gland stimulated activation at the time
of oviposition. Turquier & Pochon-Masson (1969) worked on the spermatozoa of the acrothoracid
Trypetesa (=Alcippe) nassarioides. References to the early work can be found in many of these recent
papers.
Gonad production involves biochemical synthesis with the formation of nucleic acids for spermatozoa
and the mobilization of lipid and protein for ova. Food reserves may or may not be stored by the adult
animal prior to gonad development. In boreo-arctic barnacles such as Balanus balanoides and B. balanus
assimilation and storage of reserves begins in March to April at the time of the diatom increase (Barnes,
Barnes & Finlayson, 1963). Gonad production in these species is relatively slow, beginning in early May
and lasting until October in B. balanoides and early February in B. balanus. Final maturation takes place
immediately before fertilisation (Barnes, Barnes & Klepal, 1977) in late October to November in the former
species and February in the latter. The precise time of fertilisation varies by a few weeks depending on
latitude. After oviposition and fertilisation these animals are devoid of spermatozoa and ova until feeding
begins again. After fertilisation the penis of B. balanoides is shed in one or two moults (Klepal, Barnes &
Barnes, 1975) and is gradually replaced, the length rapidly increasing from August to reach a maximum in
October immediately prior to copulation (Barnes & Stone, 1972).
In warm-water genera such as Chthamalus there are several cycles of gonad production in a year allowing
for several broods of eggs (Crisp & Patel, 1969) in contrast to the one annual brood in boreo-arctic species.
In general the behaviour of C. stellatus seems to be markedly independent of environmental conditions as
far as food is concerned (Barnes, 1972). In some species the male gonads may remain active throughout the
66
MARGARET BARNES
year and ovaries may or may not carry mature ova or ova available for final maturation as soon as
environmental conditions are favourable. In Balanus improvisus Blom (1965) reports large amounts of
spermatozoa in winter but practically no oocytes they begin to increase when sea-water temperature rises
in April. In B. rostratus, however, oocytes are produced throughout the year according to Korn (1985) while
male gonads only regenerate from June onwards and the animals fertilise in late September to October. A
large number of oocytes degenerate before fertilisation; resorption of oocytes can also be seen in figures given
for B. amphitrite and B. eburneus by Fyhn & Costlow (1975). Other species, although not breeding
continuously, retain mature germinal cells throughout the year, reproduction being initiated as soon as
conditions allow it. This appears to be so in B. perforatus and B. eburneus near Tarante, Italy (Lepore,
Sciscioli & Gherardi, 1979) and in B. algicola in South Africa (Sandison, 1954).
RHIZOCEPHALA
The Rhizocephala are parasites of crustaceans, particularly decapods. The adult has a modified form and
bears no resemblance to other cirripedes; the affinities are only shown by the larval stages and the
spermatozoa. An up-to-date account of rhizocephalans has been given by Heg & Ltzen (1985). There are
usually four nauplius stages, with the characteristic frontal horns but no alimentary canal, followed by a cyprid
(Codreanu, 1959; Heg, 1982). In some cases the hatching embryo is a nauplius and sometimes a cyprid.
The more primitive rhizocephalans are ectoparasitic and the adult (reproductive) body develops in situ at the
site of attachment of the cyprid to the host; there is no kentrogon stage. Such is the case in Duplorbis
(Smith, 1906), Chthamalophilus delagei (Bocquet-Vdrine, 1961), and Boschmaella balani (BocquetVdrine, 1968).
The majority of rhizocephalans, however, develop from a kentrogon formed from the settled cyprid. The
kentrogon penetrates the host and develops endoparasitically for several months, depending on the species.
An adult reproductive body eventually emerges and becomes the externa while the internal nutritive
structure (the interna) remains within the hosts body. This process has been known since the time of
Delage (1884) but has recently been studied in detail by Heg (1985a) for Lernaeodiscus porcellanae. The
complete life history of this species has been determined by Ritchie & Heg (1981) and Heg & Ritchie
(1985).
The externa has a visceral mass, containing the ovaries, and is surrounded by a mantle. This is separated
ventrolaterally from the visceral mass by a mantle cavity which develops as the externa matures. There is
usually one mantle aperture at an extremity of the externa. Sylon, the sole genus of the Sylonidae, differs
from most other rhizocephalans in having two mantle apertures (Ltzen, 1981). In most rhizocephalans the
aperture is open soon after the emergence of the externa but in some it may only open very late in the
development of the externa or even when the embryos are ready for release. Such is the case in Clistosaccus
paguri (Heg, 1982, 1985b). In Thompsonia there is no mantle aperture (Reinhard & Stewart, 1956).
Development of the externae depends on exposure to male cyprids. If virgin externae are kept in isolation
and out of contact of male cyprids, they neither moult nor begin production of ova. In Lernaeodiscus
porcellanae they can remain in this state almost indefinitely (Ritchie & Heg, 1981). In Sacculina carcini
virgin externae quickly die and drop off the host if no contact with male cyprids is made. Ltzen (1981)
has, however, reported ovulation in two full-grown Sylon hippolytes in which implantation of male cells had
failed; the ova, however, did not develop.
Rhizocephalans are now known to have separate sexes (see e.g. Reinhard, 1942a; Ichikawa &.
Yanagimachi, 1958, 1960; Yanagimachi, 1961a,b; Yanagimachi & Fujimaki, 1967) although originally
(Delage, 1884; Smith, 1906) they were thought to be hermaphroditic. Bocquet-Vdrine (1961) described the
67
Chthamalophilidae as self-fertilising hermaphrodites and she later (Bocquet-Vdrine, 1972b) expressed

doubts about the function of male cyprids in Sacculina carcini. This has, however, now been settled by the
work of Heg (1984, 1987). He found that there are small (female) and large (male) cyprids in S. carcini.
The female cyprids settle on the host and the males on the externae; this is in agreement with other
rhizocephalans. Two sizes of cyprids were recognised by Veillet (1943a, 1945) in Triangulus galatheae and
their separate roles were clarified by Yanagimachi (1961a,b) during experiments with Peltogasterella
gracilis. A size difference (greater in some cases than others) between male and female cyprids is now
established in the Peltogastridae and the Lernaeodiscidae (Ritchie & Heg, 1981), the Sylonidae and the
Clistosaccidae (Ltzen, 1981; Heg, 1982), as well as in the Sacculinidae (Heg, 1984).
Invasion by cells from male cyprids is necessary for further development of externae (see above). This
invasion is generally thought to be through .the mantle aperture into one or two male cell receptacles, the
testes (Ichikawa & Yanagimachi, 1960; Heg, 1985b; Heg & Ritchie, 1985). Heg (1987) found a
trichogon stage produced by male cyprids and has described what happens between settlement of the cyprid
on an externa and the arrival of male cells in the receptacle of Sacculina carcini. A trichogon stage is
present in the Sacculinidae, the Lernaeodiscidae and possibly in the Peltogastridae. A few genera lack
receptacles, e.g. Mycetomorpha, Thompsonia, and Sylon. In those species that lack a mantle opening, or it
only opens after spermatogenesis, the male cells must be injected through the integument and mantle of the
virgin externa. Ichikawa & Yanagimachi (1958, 1960) do not regard the male testis in Sylonidae as a
testis in the true sense of the word but rather that there is a female organ serving to hold a mass of male
cells from the transformed male cyprid. There is no special receptacle for these cells and where they are
found varies according to the genus. Spermatogenesis may, therefore, take place in the mantle cavity as in
Duplorbis (Smith, 1906), in the colleteric gland in Sylon (Veillet, 1962; Ltzen, 1981) or in the mantle of
Mycetomorpha (Reinhard & Evans, 1951) and Thompsonia (Yanagimachi & Fujimaki, 1967).
In the Peltogasteridae (Reinhard, 1942a; Ichikawa & Yanagimachi, 1958), Sacculinidae (Ichikawa &
Yanagimachi, 1960), and Lernaeodiscidae (Ritchie & Heg, 1981) spermatogenesis begins in the male cell
receptacles and they become the only source of spermatozoa. This process begins in Clistosaccus paguri,
which only has one receptacle, when ova within the ovary reach about 60 m diameter. When the ova are
about 100 m spermatogonia differentiate and when 165 m the receptacle is filled with spermatozoa.
Ovulation and release of spermatozoa into the mantle cavity are simultaneous and in this species the mantle
aperture opens at the same time (Heg, 1982). A similar synchrony is recorded for other species although
the mantle aperture may be already open (Ltzen, 1981; Ritchie & Heg, 1981). Ova pass through the
atrium of the colleteric gland and are fertilised in the mantle cavity. After ovulation the externa exhibits
peristaltic movements which serve to mix spermatozoa and ova together and to ventilate the mantle cavity.
Although the mantle aperture is technically open it remains compressed during embryogenesis. During
ovulation in Peltogaster paguri the aperture is tightly closed (Reinhard, 1942b). In Lernaeodiscus
porcellanae ventilation may also be assisted by the grooming action of the castrated host which treats the
externae as its own brood. When this is prevented the externae soon become fouled. In particular, the grooming
assists during the moult which occurs after the release of each batch of nauplii (or cyprids). The nauplii are
also released into the current generated by the host during grooming; this aids dispersion of the cirripede
young (Ritchie & Heg, 1981). When embryogenesis is complete the embryos hatch and are expelled from
the mantle cavity through the mantle aperture; Reischman (1959) has described this for Peltogasterella.
Information on the sizes of ova and eggs produced by rhizocephalans is scattered throughout the literature
from as early as Delage (1884) to the present day. Even Leuckart (1859) stated of Sacculina inflata
ovarian eggs were usually smaller than those of the egg-tubes but gave no sizes. Descriptions of the
rhizocephalans collected during the Siboga Expedition (Van Kampen & Boschma, 1925; Boschma, 1931)
68
MARGARET BARNES
mention the presence of eggs in the mantle cavity of many species but only give sizes in a few cases. These
are given in Table I; sometimes sizes have been estimated from scaled drawings. Other records from the
literature are also shown in Table I. Sometimes the size of nauplius stage I is given if no information about
the egg is
TABLE I
Rhizocephala: summary of relevant literature on breeding seasons, sizes and numbers of young, cyp=cyprid ; St I=stage
I nauplius ; +=or more ; *=embryo released as cyprid from mantle cavity of adult, if known
Species
Place
Breeding
season
Incubation
time, days
Sizes (LB), Number of

m
eggs per
brood
Number of
broods per
year
References
Chthamalo
philus
delagei*
Clistosaccu
s paguri*
cyp 6070
Sweden
About 30
ova 165
cyp 18490
1 or 1+ per
life
Drepanorch
is neglecta
All year,
summer
peak
BocquetVdrine,
1961
Heg, 1982,
1985b
cyp 140
Drepanorch
is villosa
Heterosacc
us
ruginosus
Lernaeodis
cus
cornutus
Lernaeodis
cus
galatheae
Siboga,
Exped.
egg 100
egg
135108
St I 200
egg 94
Krger,
1940
Veillet,
1943a,b
Lernaeodis
cus
porcellanae
small cyp
130
large cyp
180
egg
160126
Krger,
1940
All year
10 to 14
100+ to 20
000
About
every 15
days
Mller,
1862
Ritchie &
Heg, 1981
Peltogaster
paguri
egg
200120
small cyp
227202
large cyp
255232
30 to 40
St I 210 to
280
9800 to
28000
BocquetVdrine,
1961
Boschma,
1931
George,
1959
McMumch,
1917;
NilssonCantell,
1921;
Reinhard,
1942b, 1946
Species
Place
Breeding
season
Incubation
time, days
Sizes (LB), Number of

m
eggs per
brood
Number of
broods per
year
References
Peltogaster
sulcatus
St I 250
Peltogaster
ella gracilis
Hokkaido,
Japan
Bering Sea
St I L=B
NilssonCantell,
1921
Reischman,
1959
Small ova
140 to 150
Large ova
158 to 160
Small egg
140 to 150
Large egg
160 to 170
Small St I
220 to 245
Large St I
255 to 275
Yanagimach
i, 1961a
Peltogastere
lla socialis
St I 207 to
247
Japan
N.W.
Pacific,
Alaska,
Bering Sea
About 14
Peltogastere
lla
subterminali
s
Sacculina
carcini
N.W.
Pacific,
Alaska
California
Millport,
Scotland
St I (190 to
216) (126
to 148)
Shirase &
Yanagimac
hi, 1957
R.Mersey,
England
Plymouth,
England
Roscoff,
France
MarMay
Max Aug
Dec
Min Jan
Mar
Day, 1935
MarOct
Orton, 1936
JuneAug
28 to 35
2+
Delage,
1884
France
ova 8060
egg
180150
egg
120100
Isefjord,
Denmark
JulyOct
12 to 18
100 000 to
300 000
BocquetVdrine,
1964
Ltzen,
1984
Reinhard,
1944
Reinhard,
1944
Foxon,
1940;
Heath, 1971
69
70
MARGARET BARNES
egg 7054
Sacculina
micracantha
Sacculina
papposa
Sacculina
rotundata
Madras,
India
Sacculina
setosa
Sacculina
sulcata
Sacculina
sp.
Siboga
Exped.
Siboga
Exped.
Siboga
Exped.
St I
165120
Krger,
1940
Hoek, 1909
egg 134
egg 100
egg 100
St I
215135
egg 100
George,
1949
egg 110
JulyJan
(75 ova in 2
mm adult)
Black Sea
Sylon
challengir*
Sylon
hippolytes*
Sylon
schneideri
Thompsonia
cubensis
egg
182129
egg
170125
St I
190135
ova 60
Hoek, 1888
1 per life
ova 8060
20 000 to
200 000
Ltzen,
1981
Hoek, 1888
Cuba
ova 9580
egg 85+
Thompsonia
sp.*
Thompsonia
sp.*
Great
Barrier Reef
egg 34
cyp 200
Triangulus
galatheae
Bocquetia
rosea
S California
St I
257100
cyp 88.91.
89
Septodiscus
flabellum
Septosaccus
cuenoti
Siboga
Exped.
Siboga
Exped.
Mutsu Bay,
Japan
Boschma,
1931
Boschma,
1931
Boschma,
1931
Boschma,
1931
Boschma,
1931
Elston,
Wilkinson
& Burge,
1985;
Krger,
1940
Codreanu,
1959
Reinhard &
Stewart,
1956
Potts, 1915
BocquetVdrine,
1961
Veillet, 1945
Pawlik,
1987
71
available. The difference in size between the mature egg and nauplius stage I is very little. Egg size may
also increase during embryogenesis and in many cases the stage of development is not recorded.
Veillets (1943a, 1945) suggestion that the sex of a cyprid is determined at the egg stage was confirmed
by Yanagimachi (1961a,b) who went further and said it was determined in the ovary. Yanagimachi (1960) also
considered the chromosome numbers of large and small eggs. Ritchie & Heg (1981) confirmed the earlier
work on Peltogaster paguri and Sacculina senta (Ichikawa & Yanagimachi, 1960) and Peltogasterella
gracilis (Yanagimachi, 1961b) that two sizes of eggs may be produced but added that Lernaeodiscus
porcellanae does not always produce broods of one sex. They found that the sex of the broods varied with
season and that during the transition broods of mixed sex could be produced. Broods were predominantly
female in summer and male in winterthese males being necessary for virgin externae that would emerge
in the following spring. In Sacculina carcini (Heg, 1984) some broods contain only one sex while others may
be mixed. Heg suggests that this may reflect the nutritional state of the externa which may itself be
determined by the condition of the host. It may also be that in summer broods are laid in quick succession
thus tending to deplete the nutritional reserves of the externa. Walker (1985, 1987) has examined nauplii
from broods of S. carcini taken at different times of the year; he also found a progressive change from male
to female cyprids from spring to summer reverting to males again from autumn to winter.
The sizes of externae are difficult to measure because of their shape and because they may be distended
when carrying eggs in the mantle cavitythe amount of distension depending on the stage of development
of the embryos (Reinhard, 1942b). The size of the externa at maturity may vary according to species or the
number of externae per host. According to Boschma (1931) Peltogasterella socialis externae 57 mm long
have eggs in the mantle cavity whereas Sacculina carcini externae do not carry eggs until they are between
10 and 12 mm long (Foxon, 1940; Heath, 1971). In Sylon hippolytes size at maturity may be 10.4, 8.4 or 7.2
mm long depending on whether the host is carrying 1, 2 or 4 externae (Ltzen, 1981). In Peltogaster paguri
(Reinhard, 1942b) externae of 6 mm length may be mature on small hosts; on larger hosts they are not
mature until 9 mm long.
Season of maturity can also vary depending on temperature or even the life cycle of the host (Foxon,
1940). Some species have peak periods of reproduction during the summer and a rest period in the winter,
such as Sacculina carcini in Denmark (Ltzen, 1984), although further south the reproductive period of this
species may be longer (Delage, 1884; Day, 1935; Orton, 1936; Foxon, 1940; Heath, 1971; Walker, 1987).
Some species may be continuously reproductive, such as Lernaeodiscus porcellanae (Ritchie & Heg, 1981),
with incubation time depending on temperature and the time of year. In some species the externa may
produce only one brood and then die and fall off the host, such as in Sylon hippolytes (Ltzen, 1981).
Results are not expressed in the same way in the literature (see Table I) which often makes comparisons
difficult.
Day (1935) suggested that reproduction in Sacculina carcini is synchronised with that of its host so that
food reserves normally used by the host can be appropriated by the parasite. While this is possible it is
known (Heath & Barnes, 1970) that the ovaries of the host, Carcinus maenas, show their greatest increase
in size in the summer and yet nauplii and cyprids of Sacculina carcini are most abundant in winter
(Pyefinch, 1948). It is suggested, therefore, that it is the developing interna, rather than the externa, which
requires optimal conditions for growth. Furthermore, as rhizocephalan nauplii are lecithotrophic their
release at a time when there is little plankton in the winter, far from being disadvantageous, may be an
advantage in reduced losses due to predation (Heath, 1971).
The number of eggs found in the mantle cavity after each ovulation depends on the size of the externa
and some authors are careful to give this. The most comprehensive account is that of Ltzen (1981; see
Table II) for Sylon hippolytes. Numbers of eggs found in other species are given in Table I. It is of interest
72
MARGARET BARNES
that Peltogaster paguri of externa size 12 mm produces 28 000 eggs per brood which, allowing say 6
broods per summer (Reinhard, 1942b) would be 168 000 eggs per year (life?). From Table II it can be seen
that Sylon hippolytes of the same size externa produces 120 000152 700 eggs in its one brood per life. The
former species releases the embryo as a nauplius and the latter as a cyprid. It has been said that species
releasing as cyprids may not produce as many offspring as those releasing as nauplii (Heg, 1982). This is
hardly borne out by this result. A better comparison may be with Lernaeodiscus porcellanae which releases
as a nauplius and may produce several hundred to 20 000 eggs per brood (Ritchie & Heg, 1981). In
summer this can be every 1014 days but will obviously be less frequent at lower winter temperatures. If
one assumes a brood say every month on the average (it breeds continuously according to Ritchie & Heg,
1981) then it will produce up to 240 000 eggs per year which is more than in Sylon hippolytes and may be
an under-estimate. At two more broods per year the number would increase to 280 000; in this case there
are many more nauplii produced than cyprids.
The merits of releasing young as nauplii or cyprids is discussed by Heg (1982). Dispersion of the
species is ensured by nauplii which remain swimming in the water for several days. Reduction of the
planktonic stages, and consequently of the length of planktonic life, reduces the risk of predation and
increases the chance of survival. In species such as Clistosaccus paguri,
TABLE II
Number of eggs in six externae of Sylon hippolytes calculated from serial sections (Ltzen, 1981)
Size of externae (mm)
Approximate
Length
Width
Height
number eggs
5.9
7.6
8.1
10.0
14.0
15.2
3.4
5.2
6.1
8.3
10.0
9.6
4.1
4.8
4.9
7.0
5.0
9.0
18 900
75 500
105 900
120 000
152 700
203 300
producing only one or very few broods during the lifetime of an externa, the lack of dispersion and greater
chance of survival ensures that the cyprids remain in the vicinity of the hermit crab (host) population.
ACROTHORACICA
Cirripedes of the order Acrothoracica are burrowing and non-parasitic. They have a soft mantle without
calcareous plates and are dioecious with dwarf males. The order is predominantly found in warm-temperate
regions and generally in shallow (30 m) water (Ross & Newman, 1969; Zullo, 1979). Newman & Ross
(1971) have, however, reported a species, Australophialus tomlinsoni, from depths of 300600 m south of
the Antarctic Convergence and two truly deep-water species have been found: Weltneria hessleri at 1000 m
depth off Bermuda (Newman, 1971) and W. exargilla in the Bay of Biscay at a depth of 1500 m (Newman,
1974).
The females live in self-excavated burrows usually in limestone, coral skeletons or mollusc shells. W.
exargilla is different in that it burrows into soft clayey siliceous substrata which are fairly low in calcium
carbonate. The tiny males are generally found near the aperture of the females in a pocket of the mantle
tissue near the area of the ovary. In some species the males are, however, found attached to the wall of the
73
burrow. The acrothoracids so far described are small usually being only a few millimetres long (see
Table III). The females are about ten times longer than the males. The burrows of these soft bodied
barnacles provide them with the protection necessary because of the absence of a calcareous shell. The
burrow is largely formed by abrasion caused by chitinous teeth on the mantle surface of the female although
a cyprid larva settling on a suitable substratum has no mantle teeth suggesting that the initial penetration
may be by chemical dissolution (Tomlinson, 1969). Indeed Turquier (1968) mentioned the use of carbonic
anhydrase in burrowing by Trypetesa nassarioides and Tomlinson (1973) found papillae on the external
surface of the mantle. In view of Turquiers work Tomlinson suggested that these papillae might be
secreting carbonic anhydrase or other alkaline phosphatase and that teeth, developed later, act only after
enzymatic softening of the substratum. A chemical action combined with abrasion was also mentioned by
Kamens (1981).
The attachment area of the female is a major structural element within the burrow and allows movement
of the mantle. As the mantle is cemented to the burrow wall at this point it cannot moult in this area and remains
of exuxiae build up forming a horny disk (see Grygier & Newman, 1985, for a discussion about this disk).
Dwarf males may be attached to the margins of this disk embedded in the mantle of the female, e.g. in
Alcippe lampas (=Trypetesa lampas) (Berndt, 1903), Lithoglyptes indiens and Trypetesa lateralis
(Tomlinson, 1969), and Cryptophialus melampygos (Batham & Tomlinson, 1965). In some cases the males
may be attached to the burrow walls, e.g. in Berndtia purpurea (Utinomi, 1950). There are also cases where
males have been found attached to either the mantle of the female or the burrow wall, such as in Kochlorine
floridana (Wells & Tomlinson, 1966), Berndtia nodosa (Tomlinson, 1967), and Cryptophialus
coronophorus (Smyth, 1986). Utinomi (1964) failed to find any males in his study of Tryptesa habei; they
TABLE III
Acrothoracica: comparison of size of adult female and size and number of young, cyp=cyprid;? stage doubtful
Species
Trypetesidae
Trypetesa lateralis
Cryptophialidae
Australophialus
pecorus
Cryptophialus
melampygos
2.5
2.6
2.7
Cryptophialus
minutus
Lithoglyptidae
Berndtia purpurea
2.2
2.4
2.5
Size of young (LB), Size of female (LB), Number of young per

m
mm
brood
References
1.21.3 also 2.0
egg 250180
cyp 500200
180
Tomlinson, 1953,
1955
largest 1.280.82
egg 220 to 270

cyp 350 to 370
egg 260210
1 to 8
Turquier, 1985a
14
Batham &
Tomlinson, 1965
19 to 60
Darwin, 1854
14
Utinomi, 1961
1.9 to 2.1
cyp 530230
largest 2.54
1.7
cyp 470260
33
44
31
egg 254
cyp 229 to 406
egg 320
65
21
85
74
MARGARET BARNES
Species
2.6
2.6
2.7
Lithoglyptes
tectoscrobis
Weltneria exargilla
Size of young (LB), Size of female (LB), Number of young per

m
mm
brood
5.7(1.7 to 1.0)
(6.2 to 11.4) (1.5 to
3.9)
64
57
32
egg 180130
St? 510370
1200 estimated by
volume
About 150
References
Grygier & Newman,

1985
Newman, 1974
may have been lost during the preparation of the material for examination.
The size of the adult male is less than that of the cyprid from which it develops. The adult male lacks
feeding appendages and the maturation process is at the expense of larval food reserves. Mature males
consist mainly of reproductive material and its maturation must be synchronised in some way with that of
the female if fertilisation is to be effective. Khnert (1934) raised larvae of Alcippe lampas (=Trypetesa
lampas) in separate vessels and found that males would differentiate without the presence of females but
would not become fully mature. Tomlinson (1969) suggests that part of the maturation of the male may be
under the chemical influence of the female. The partial burial of the male in the females mantle tissue near
the ovary may be significant in this respect.
The dwarf males in acrothoracids usually have a penis although it has not been seen in some species and
is even reported as absent in others. In some species of Lithoglyptes the presence or absence has not been
resolved but according to Tomlinson (1969) it is usually present. He was, however, not sure of it in L.
hirsutus (Turquier, 1963). Newman (1971) did not find a penis in Weltneria hessleri; this may have been
due to the immaturity of the males examined as Tomlinson (1969) suspected in Cryptophialus
heterodontus. In Kochlorine ulula and Cryptophialus rossi a penis could not be positively identified by
Tomlinson (1973), but he did find a penis sheath in the latter species. In C. epacrus a penis was found. In
Kochlorine floridana the penis matures late in life (Wells & Tomlinson, 1966) whereas in K. bocqueti
Turquier (1977) found none. In Trypetesa lateralis (Turquier, 1967c) the male is greatly reduced and there
is no penis sheath. There is only a short penis in T. nassarioides (Turquier, 1967c, 1971) and Utinomi (1964)
records its presence as doubtful in T. habei but a penis sheath is present. The sheath is formed from the
mantle of the male (Smyth, 1986). The spermatozoa of T. lateralis can be activated by sea water, the length
of time depending on the salinity of the water (Tomlinson, 1969). Turquier & Pochon-Masson (1969) made
an ultrastructural study of spermiogenesis in T. nassarioides and showed it to be normal for cirripedes;
dwarf males have a true fertilising role. The method of insemination needs further study as details of
copulation and fertilisation have not been described in detail for any acrothoracid (Tomlinson, 1960, 1969;
but see also Turquier, 1977). By whatever method involved the mature ova and sperm come into contact
and fertilised egg masses are found in the mantle cavity of the females.
During its life a female may be served by a few or many males. In Kochlorine floridana Wells &
Tomlinson (1966) found up to five relatively short-lived dwarf males per female. In Australophialus
turbonis there may be about 12 per female; up to 17 have been seen (Tomlinson, 1969). In Cryptophialus zulloi
Tomlinson (1973) found remains of at least 27 males in the area of the attachment disk of the female.
According to Turquier (1972a) the dwarf males of Trypetesa, in spite of their short life, are able to fertilise
several egg masses. When their testes are empty they may be replaced by other males. In Cryptophialus
melampygos old spent males are replaced during the life of the female (Batham & Tomlinson, 1965).
75
The ovaries lie on the dorsal side of the female under the thickened layer of the disk and the oviducts
each end in an atrium which opens into the mantle cavity. Ovaries and oviducts have been described in
Alcippe lampas by Berndt (1903) and in Berndtia purpurea by Utinomi (1950, 1960). The fertilised ova
(eggs) remain in the mantle cavity of the female as two separate egg lamellae until hatching takes place
(Tomlinson, 1969). Embryonic development takes place within the egg case. As early as 1849 Hancock
reported seeing eggs in the mantle cavity of Alcippe lampas and watched the hatching of swimming nauplii.
Whether the embryos eventually hatch as nauplii or cyprid larvae varies in different genera. In the
Crytophialidae where hatching has been described it is usually as a cyprid. Although in Australophialus
turbonis (Tomlinson, 1969) whether the nauplius is free-swimming or retained to the cyprid stage is not
known; in A. pecorus the larvae is liberated as a cyprid (Turquier, 1985a). In the Lithoglyptidae species of
the genus Weltneria are released as cyprids (Tomlinson, 1969: W. spinosa, W. reticulata; Turquier, 1985a:
W. zibrowii; Newman, 1974: W. exargilla). Balanodytes taiwanus (Tomlinson, 1969) also hatches as a
cyprid. In species of the genera Berndtia and Lithoglyptes so far described the embryos, however, hatch as
nauplii (Tomlinson, 1969: L. indicuns, L. mitis, L. scamborachis; Utinomi, 1950, 1960: Berndtia purpurea).
In the Trypetesidae some members of the same genus may hatch as nauplii (Berndt, 1903; Genthe, 1905;
Khnert, 1934: Alcippe (=Trypetesa) lampas; Turquier, 1976b: Trypetesa nassarioides) whereas T. lateralis
hatches as a cyprid (Tomlinson, 1955).
Whether hatched as nauplii, which develop through four stages (Visscher, 1938, says six in Alcippe
lampas but this has never been confirmed by other workers) or cyprids the larvae are expelled from the
female by contractions of the mantle cavity as seen by Genthe (1905) in Alcippe (=Trypetesa) lampas. The
cyprids may be free swimming or have reduced swimming appendages as, for example in Cryptophialus
melampygos (Batham & Tomlinson, 1965). In this species the cyprids can only crawl and so are splashed
about in the sea water and as a result dispersion is reduced and dense infestations can occur (Tomlinson,
1969). Newman & Tomlinson (1974) have discussed the dispersion of species which lack pelagic larvae and
have non-swimming or only weakly swimming cyprids.
According to Turquier (1972a) the sex in Trypetesa species is determined before the cyprid settles
although there is no sexual dimorphism in the cyprids. A biometrical study of the larvae of T. nassarioides
(Turquier, 1972b) indicated a seasonal variation in size but these variations have no relation to sex. White
(1970) found No obvious chromosomal mechanism of sex determination in T. lampas. In T. lateralis a
female cyprid settles on a suitable substratum and attaches itself by its antennules. It proceeds to burrow
into the substratum. The cyprid carapace is shed and the young barnacle quickly passes beneath the surface
of the substratum. Developing male cyprids lose their carapace and become progressively smaller
decreasing from to as low as (Tomlinson, 1955).
There are only a few records of the number of ova produced or eggs incubated in the mantle cavities of
female acrothoracids. Those available are summarised in Table IV. As can been seen the number of eggs
varies from 18 in Australophialus pecorus (Turquier, 1985a) to 1200 estimated volumetrically by Grygier
& Newman (1985) in Lithoglyptes tectoscrobis. It is not known how accurate this number is but it is far
above other maximum counts of 150 or 180 in Weltneria exargilla (Newman, 1974) or Trypetesa lateralis
(Tomlinson, 1955).
TABLE IV
76
MARGARET BARNES
Acrothoracica: summary of relevant literature on breeding seasons, sizes and numbers of young, cyp=cyprid; St I=stage
I nauplius; +=or more; *=embryo released as cyprid from mantle cavity of adult, if known
Species
Place
Breeding
season
Incubation
time, days
Sizes (LB),
m
Number of
References
eggs per brood
Japan
egg 240
numerous
Utinomi, 1964
egg 340250
St I 450
Trypetesa
(=Alcippe)
lampas
Trypetesa
lampas
Heligoland,
North Sea
MaySept
St I 550450
Roscoff,
France
9 to 10
Florida, USA
Trypetesa
lateralis*
Trypetesa
nassarioides
June+?
California
NovJan and
June
FebOct
Max Apr Aug
Australophial
us pecorus*
Mediterranean
Sea, N. Africa
Cryptophialus
coronophorus
Cryptophialus
lanceolatus*
Guam
egg 380280
St I 400
cyp 600
egg 250180
cyp 500200
egg 280210
St I 340
cyp 450170
egg 220 to
270
cyp 350 to
370
cyp 300 to
310
cyp 500200
Berndt, 1903;
Khnert,
1934; Krger,
1940
NilssonCantell, 1921,
1978
Turquier,
1967a
Trypetesidae
Trypetesa
habei
Alcippe
lampas
Roscoff,
France
6 to 12
Spivey, 1979
180
Turquier,
1967a,b,c
Tomlinson,
1953, 1955
Cryptophialid
ae
1 to 8
Turquier,
1985a
Smyth, 1986
Tomlinson,
1969
14 to 44
Batham &
Tomlinson,
1965
19 to 60
Darwin, 1854
Newman &
Ross, 1971
1485
ova 220160 cyp 470260

egg 320
cyp 450170
Utinomi, 1950,
1960, 1961
Turquier, 1977
Cryptophialus
melampygos
Otago, New
Zealand
Cryptophialus
minutus*
Cryptophialus
tomlinsoni*
Lithoglyptidae
Berndtia
purpurea
Kochlorine
bocqueti
Kochlorine
floridana
Chile
Jan+?
Antarctica
Japan
AugSept
Madagascar
egg 260210
St I? 320200
cyp 500200
to 560260
egg 254
cyp 230 to 406
cyp 500200
cyp 550190
Wells &
Tomlinson,
1966
Kochlorine
hamata
Lithoglyptes
mitis
Lithoglyptes
scamborachis
cyp 420225
Lithoglyptes
tectoscrobis
Weltneria
exargilla
Weltneria
reticulata*
Weltneria
spinosa*
Weltneria
zibrowii
Tongo
cyp (338 to
538) (153 to
184)
egg 180130
Bay of Biscay
July+
Mediterranean
Sea, Algeria,
North Africa
einige
Dutzend
77
Noll, 1875
Tomlinson,
1969
Tomlinson,
1969
St? 510370
1200 estimated
by volume
about 150
Grygier &
Newman, 1985
Newman, 1974
cyp 545245
cyp 870365
cyp 800360
Tomlinson,
1969
Tomlinson,
1969
Turquier, 1985b
Comparison between size of female and number of eggs in brood incubated are given in Table III
together with the size of the egg, nauplius and/or cyprid, whichever measurement is given in the original
reference. Lithoglyptes tectoscrobis appears to have one of the smallest eggs which may be one of the
reasons for their greater number compared with Weltneria exargilla. Both these genera belong to the same
family Lithoglyptidae, and the females of the species are within the same size range (Table III). Berndtia pur
purea also belongs to the Lithoglyptidae but the female is somewhat smaller (Table III) and contains 1485
eggs depending on size of parent (Utinomi, 1961). The size of the hatched nauplius is similar to that of
Alcippe lampas (Khnert, 1934) and, as a matter of interest, is about twice as big as the corresponding stage
of e.g. Balanus crenatus ( Herz, 1933) and B. amphitrite albicostatus Ishida ( & Yasugi 1937). The
Cryptophialidae have much smaller females and fewer eggs (160) which are larger than those of
Lithoglyptes tectoscrobis. The only species of the Trypetesidae, in which the number of eggs is given, is
very small, similar to Australophialus pecorus but has a slightly smaller egg and a much larger brood.
Because of the general uncertainty of the data it is difficult to come to any definite conclusions about size of
female and the size and number of eggs produced.
Development of any batch of eggs is synchronous (Turquier, 1985a) and the time from fertilisation to
hatching ranges from 612 days depending on temperature in Trypetesa nassarioides and T. lampas
(Turquier, 1967a,b,c). Cyprids leave the mantle cavity before a new batch of ova are fertilised in
Cryptophialus melampygos (Batham & Tomlinson, 1965). In this species a female of 1.2 mm length may get
an immature male but will not be ovigerous until 1.61.8 mm long. Three out of four females more than 1.7
mm long had eggs or larvae in the mantle cavity at all times of the year; the majority of breeding females
were 1.92.1 mm long.
Information on the breeding seasons of the various species is also fragmentary (Table IV). C.
melampygos breeds throughout the year at Otago, New Zealand, according to Batham & Tomlinson (1965)
so that, although the broods are relatively small, the total number of nauplii produced per year could be
several hundred. The C. minutus found to contain 1960 eggs by Darwin (1854) had been collected in early
January in Chile. Trypetesa nassarioides and T. lampas from the Roscoff region of France breed from
78
MARGARET BARNES
February to October with a maximum from April to August (Turquier, 1967a,b). T. lampas at Heligoland
was sexually mature and fertilised from May to August (Khnert, 1934). Cyprids may be found as early as
June, in great numbers in August, and none in February (Nilsson-Cantell, 1978). At Woods Hole, Visscher
(1938) found larvae of T. lampas in June but they were rare in July and August. In Florida, T. lampas
contains late embryos and first stage nauplii in June (Spivey, 1979) suggesting perhaps a similar breeding
season to that of the same species in Europe. The greatest larval settlement of T. lateralis in California was
in November to January with a minor peak in June (Tomlinson, 1953). Allowing for the time of
development of the larvae this would mean the peak of the breeding season was in August to September.
Turquier (1972b) gives the most detailed account of the reproductive cycle of T. nassarioides in the Baie
de Morlaix, France. He sampled the population for 16 months from May to August of the following year.
Young females settling early in the year reached a length of 3 mm by August and 5 mm by the end of the
summer. Maturity was reached three to four months after settling so their reproductive activity was short in
the first year. Growth was reduced or even suspended during the winter but survival was good. In animals
settling late in the first year, and perhaps becoming only 1 mm long by December, there was considerable
mortality. Reproductive activity started again in February and throughout the season the females continued
to produce broods of 200350 larvae each time until the end of summer when about 7 8 mm long. Their
lifespan appears to be about 18 months.
The start of reproductive activity in February coincides, off the Atlantic coast of France, with minimum
sea-water temperature and continues as the sea-water temperature rises to a maximum in August and begins
to decrease again. The effect of temperature on reproduction seems less dramatic than in the Thoracica. The
effect of light may also be less important than in the Thoracica as the cirripedes are buried in the interior of
the host shells or substratum where the level of light will be low. The larvae are lecithotrophic and while
food may be necessary for the adults for vitellogenesis, it is not essential for the larvae to be liberated when
food is available in the sea water. The release of a brood seems to depend on an internal mechanism. It is
possible to find females with mature males in which vitellogenesis has apparently been achieved and which
are breeding but remain incapable of releasing the brood (Turquier, 1972b).
THORACICA
The largest and most diverse order of the Cirripedia is the Thoracica which contains three living suborders,
the Lepadomorpha, Verrucomorpha, and Balanomorpha. The first of these has the greatest bathymetrie range
from intertidal to at least 5000 m (Nilsson-Cantell, 1950). It contains the stalked barnacles belonging to the
living superfamilies Ibloidea, Heteralepadoidea, Lepadoidea, and Scalpelloidea (Newman, 1987). The
Verrucomorpha are also widely distributed both geographically and bathymetricallyup to 4630 m
according to Nilsson-Cantell (1950). The living genus Verruca is asymmetrical and sessile. The
classification of the Balanomorpha has been repeatedly revised over the years since Darwins (1854)
monograph, a recent attempt being that of Newman & Ross (1976, 1977), who give three superfamilies:
Chthamaloidea, Coronuloidea, and Balanoidea. Following Newman (1987), however, there are five living
superfamilies, Chionelasmatoidea, Pachylasmatoidea, Chthamaloidea, Coronuloidea, and Balanoidea. The
sessile acorn barnacles belong to the Balanomorpha.
LEPADOMORPHA
The Lepadomorpha contains barnacles having a capitulum and a peduncle. The capitulum is often protected
by calcareous plates but in some cases these may be vestigial or even absent. The prosoma is contained within
79
the capitulum; the peduncle may or may not have calcareous scales. It contains the testes in males and the
ovaries in females and hermaphrodites.
Ibloidea
Species of Ibla are tiny pedunculate barnacles with weakly calcified plates often seeking protection in
crevices or shells of other animals including cirripedes. They may be intertidal or in shallow water
sometimes attached to Pollicipes species or associated with Tetraclita species (Achituv & Klepal, 1981).
Five species are now recognized and of these two are hermaphrodites with complemental malesIbla
quadrivalvis and I. pygmaea (=I. segmentata)and the other three are females with dwarf malesI.
cumingi (=I. sibogae), I. idiotica, and I. atlantica (Klepal, 1985). Egg sizes (Table V ) in all species are
relatively large compared with those of cirripedes in general and because the animals are small the number
of eggs per brood is also small. Only a limited number of large eggs can be accommodated in the mantle
cavity of the parent. According to Broch (1922) ovigerous I. pygmaea may have about 16 large eggs at a
time in the mantle cavity whereas I. quadrivalvis may have 100 to 300 (Anderson, 1965). Batham (1945a)
found 20 ova in the ovary of a female I. idiotica that was 3 mm long. The number of eggs in I.cumingi
depends on the size of parent, about 400 being the average (Klepal, 1985) which agrees with Hoeks (1907)
number of 480 in I. sibogae (=I. cumingi). The highest number recorded for this species is 1225 by Gaonkar
& Karande (1980). In I. quadrivalvis the released nauplius stages are free-swimming but in I. idiotica the
swimming habit is eliminated and development to the cyprid stage takes place within the mantle cavity of
the parent. In both cases the larvae are lecithotrophic.
In Bombay waters I. cumingi 5 mm long or over contain ovarian tissue at all times of the year but the
main breeding season is in mid-February to April and from August into November (Gaonkar & Karande,
1980). During the monsoon months when water quality, especially salinity, is changing there is apparently
no fertilisation. In the Philippines, Resell (1967) found that females 11.5 to 15 mm long were ovigerous. I.
quadrivalvis breeds throughout the year except for May and June (late autumn and early winter) in
Australian waters with peaks of release of young in September and February to March (Wisely & Blick,
1964). This is confirmed by Anderson (1965) who gives 16 17 days at 23C from fertilisation to release. He
says that although only 100 300 larvae are produced by brood, throughout the season an adult may release
about 10 000 young.
Heteralepadoidea
This is a superfamily containing small pedunculates without calcareous plates or scales and about which
there is not much information on reproduction. Heterolepas cornuta from the eastern Pacific was found to
contain eggs but because of lack of data in earlier reports on this species Ross (1975) was not able to detect
any seasonal variation in the reproductive cycle. He did not give any numbers or size of eggs except to say
that the size was comparable with that given by Stubbings (1965). The sizes that could be found in the literature
for Heterolepas, Paralepas and Anelasma species are included in Table VI.
TABLE V
80
MARGARET BARNES
Ibloidea: summary of available literature on breeding seasons and size and number of young per brood. St I=stage I
nauplius
Species
Place
Breeding season Size of young

(LB), m
Number of young References

per brood
Ibla sibogae
Indonesia
480
Hoek, 1907
Ibla cumingi
India
Molo Strait
MarMay not
during
monsoons; ova
all year
St I 300
Hoek, 1907
Gulf of Elat
ripe ova 11085

up to 500300
Ibla idiotica
Otago, New
Zealand
Ibla pygmaea
Australia
egg 340
St I 360
400
depending on
parent size
20
Karande, 1974a;
Karande &
Thomas, 1976;
Gaonkar &
Karande, 1980
Klepal, 1985
20
Batham, 1945a
Anderson, 1965
about 16
Broch, 1922
egg 320
egg 400275
100300
Krger, 1940
Anderson, 1965;
Wisely & Blick,
1964
Ibla quadrivalvis
3812S: 14940
E
Australia
AugMay
large female
egg 210160
small female
egg 140160
egg 180130
max 1225
TABLE VI
Heteralepadoidea: size of young and places found, cyp=cyprid; St I=stage I nauplius
Species
Place
Size of young (LB), m
References
Anelasma squalicola
From sharks in North Sea

Heteralepas cornuta
Heteralepas minuta
Heteralepas smilius
Paralepas minuta
Paralepas scyllarusi
egg 400280
egg 558
Senegal?
Gulf of Guinea
Chinese waters
Senegal
Kyusyu
St I 660220
Krger, 1940
Darwin, 1851
egg 190111
cyp 1120560
egg 270120
egg 199107
egg 233
Hoek, 1909
Stubbings, 1965
Stubbings, 1961
Ren, 1983
Stubbings, 1965
Utinomi, 1967
Lepadoidea
The Lepadoidea are all hermaphrodites, without complemental males and are oceanic in occurrence. They
are often attached to floating objects and may be widely dispersed from the initial populations. Lepas
species are mainly known from their appearance on material found by chance either drifting in the sea or
washed up on the shore.
81
A full account of the development of Lepas fascicularis from egg to adult has been given by WillemesSuhm (1876) who said that the cyprid was probably short-lived as only a few were found even where there
were many hundreds or thousands of nauplii. It may be, however, that there is great mortality or predation
of late stage nauplii. The size of eggs and larvae given by Willemes-Suhm compare favourably with those
of later workers but the number of eggs is lower; this does, however, depend on the size of the parent
animal. Bigelow (1896) gave an account of the early development of L. fascicularis and of Lepas sp.
(Bigelow, 1902) but did not give any sizes.
Information on the number and sizes of eggs and/or nauplius stages so far available on Lepas sp. is
summarised in Table VII. There is virtually nothing known about L. anaserifera and L. hilli except that
immature ova have been seen in the former (Darwin, 1851) and in the latter 29 out of 57 adults of 16.519
mm capitulum length after 60 days attached to a ship plying between Dakar and Barbados contained egg
lamellae (Evans, 1958). L. anatifera var. testudinata on buoys in New Zealand waters may contain hatching
eggs 45 weeks after settlement at capitulum lengths ranging from 2327 mm (Skerman, 1958a). For
L.australis it is only known that in New Zealand coastal waters nauplii are found 68 weeks after settlement
of the parents, these having reached a capitulum length of 21 mm (Skerman, 1958a). In this species the
cyprid is 20002250 long (Darwin, 1851; Nilsson-Cantell, 1930a) compared with 1250 m for L. pectinata
(Stebbing & Fowler, 1904) and 1300 m for L. fascicularis (Willemes-Suhm, 1876). The ova, eggs, and
stage I nauplius all seem to be smaller in L. anatifera than in L. fascicularis (see Table VII). These sizes
may depend somewhat on the temperature at which development takes place (Patel, 1959). The number of
developing eggs in these two species is given as 1400 to many thousands or even tens of thousands in L.
anatifera (Hoek, 1884; Witschi, 1935; Zann & Harker, 1978) and in L. fascicularis the figure of 4000 is
given by Burmeister (1843) as quoted by Willemes-Suhm (1876) or up to 300 000 found by Thorner &
Ankel (1966) in a single animal of 27 mm capitulum length found in the tropics. This figure is much higher
than any others quoted. Krger (1927) quotes Burmeister (spelling it Burmester) (1843) as finding 40 000
eggs in L. anatifera whereas Willemes-Suhm (1876) said the species was L. fascicularis and the number
4000. It has not been possible to trace the original 1843 reference in order to settle this discrepancy.
Willemes-Suhm (1876) also suggests that the Pacific and Atlantic forms of L. fascicularis may be
different.
In the laboratory Patel (1959) found that L. anatifera produced ripe eggs (presumably eggs containing
larvae ready to hatch) of 290 m long136 m wide at 1920C and 266122 m at 2425C. At this
temperature breeding was continuous with embryonic development taking about two weeks. He found,
however, that penis activity was inhibited below 19C and because such a temperature is rarely reached in
the North Sea the failure to reproduce in northern European waters is probably based on a failure to
copulate. Patel (1959) did suggest that copulation in L. fascicularis might be possible at a lower temperature
than in L. anatifera. Broch (1924, 1927), however, reports that L. fascicularis, like all lepadids cannot
reproduce effectively in northern waters. Thorner (1967) says that the adults can exist in the North Sea but
that reproduction is not possible except under the most optimal conditions. In the North Sea mature animals
with ova in the peduncle and eggs in the mantle cavity are found on floating objects but developing stages
are never found (Broch, 1924; Thorner & Ankel, 1966; Thorner, 1967) and there is a lack of larval stages in
North Sea plankton. The species has a high rate of reproduction in warmer water. Larvae are found in the
Mediterranean (Groom, 1894, quoted by Nilsson-Cantell, 1978, for L. anatifera) and off the southwest of
Great Britain (Bainbridge & Roskell, 1966, for L. fascicularis). Support for this is also given by Plankton
Recorder samples taken in the North Atlantic. The 16C isotherm reaches 49N in July and 51N in August
but falls back below 50N in September. Larval stages of Lepas are only found during July and are limited
to regions where the mean monthly sea-surface temperature is above 16C.
82
MARGARET BARNES
In New Zealand waters L. anatifera var. testudinata breeds at 1720C (Skerman, 1958a). Zann &
Harker (1978) found L. anatifera containing egg masses in February off north Queensland, Australia.
Breeding L. hilli were in temperatures of 2426C en route from Dakar to Barbados (Evans, 1958). In the
Bass Strait L. anserifera produced ova at temperatures normally about 1720C (Darwin, 1851).
Other genera of the Lepadoidea about which there is some information on egg production are included in
Table VIII. In all the species listed the eggs are relatively small and given as numerous. This is in
agreement with the Lepas species (Table VII) and is in contrast to the Scalpellum species (Table IX) which
produce larger and fewer eggs. Lepas anatifera (Patel, 1959) and Octolasmis aymonini geryonophila
(Coln-Urban et al., 1979) have been shown not to be capable of self-fertilisation under laboratory
conditions. Rasmussen (1980) examined several hundred Conchoderma auritum taken from fishing vessels
off Namibia between May and October. 72% of animals with a scutum length greater than 7 mm contained
eggs. It is not clear in how
TABLE VII
Lepas species: notes on breeding seasons, size and number of young, cyp=cyprid ; St I, St II=stage I and II nauplius,
respectively
Species
Notes
Sizes of young (LB), Number of young per

m
brood
References
L. anatifera
Hoek, 1884, 1909
egg (166 to 189)

(113 to 120)
St I 250
ova 140100
egg 240
St I 250
40 000
Nauplii found in
Mediterranean Sea in
Feb, Mar, May, Oct.
In British waters in
Sept
In culture
In Mediterranean
reproduces in May
From beacons in New
Zealand waters
mature after about 40
days
L. anserifera
may be 1000s or 10,

000s
Krger, 1922, 1927,

1940
Nilsson-Cantell, 1978
egg (266 to 290)

(122 to 136)
depending on
temperature
Patel, 1959
many 1000s
Witschi, 1935
Le Reste, 1965
Skerman, 1958a
Adult 12.5 mm
capitulum, 783 20.5
mm, 22 840
Zann & Harker, 1978
Reproduces mid Apr

to June in
Mediterranean; 6
days between broods
St I 308158
Le Reste, 1965
L. australis
South Shetland Is.,

cyp 2550
Antarctica
From beacons in New
Zealand waters
mature after about 50
days
cyp 15002500
L. fascicularis
egg 260117
Pacific between
St I 350
Japan and Hawaii in

June-July; off S.W.
Great Britain in Sept
St II 220
N.Pacific between
180 and 156W
many with lamellae
ova 260
300 000 in adult with
St I 1300700
capitulum 27 mm
North Sea plankton
St I 350
ova 260
St I 350
cyp max 1300700
L. hilli
50% animals had egg
lamellae after 60 days
L. pectinata
North Sea plankton
St I 260
egg 170113
St I 260
Reproduces in
Mediterranean in Jan,
Mar, Apr, May, Oct.
Off S.W. Great
Britain in Sept
cyp 1250
83
Nilsson-Cantell,
1930a
Skerman, 1958a
Darwin, 1851
Krger, 1940
Bainbridge &
Roskell, 1966
Thorner & Ankel,
1966
Hoek, 1909
Willemes-Suhm,
1876
Evans, 1958
Krger, 1940
Hoek, 1909
Stebbing & Fowler,

1904
TABLE VIII
Lepadoidea other than Lepas species: summary of breeding time, size and number of young per brood, cyp=cyprid; St
I=stage I nauplius
Species
Notes
Alepas intermedia
Collected Dec 536

egg 220
S: 13252E
Collected Feb 719 egg 300130
5S: 1 1649E
Tasmania in Jan
egg 190110
Arabian Gulf en route St I 278173
to N.Europe
egg 186132
Alepas morula
Alepas pacifica
Conchoderma
attrition
Conchoderma
virgatum
Sizes of young (LB), Number of young per References

m
brood
numerous
Hoek, 1907
numerous
Hoek, 1907
large egg masses
Tubb, 1946
Dalley, 1984
numerous
Hoek, 1884, 1909
84
MARGARET BARNES
Species
Notes
Sizes of young (LB), Number of young per References

m
brood
Dichelaspis darwini
St I 290
Mediterranean, 3
larvae Jan
Krger, 1940
Le Reste, 1965
ova 100
St I 213
egg 230
egg 227115
Coker, 1901
Pilsbry, 1907
Krger, 1940
Dichelaspis mlleri
Megalasma minus
Megalasma
(Megalasma) minus
Microlepas diademae
Octolasmis aymonini
geryonophila
Octolasmis grayii
Octolasmis lowei
Octolasmis mlleri
Beaufort, North
Carolina, USA
gravid late May to
mid July
Octolasmis warwickii
North Queensland,
Australia gravid
between April and
Oct
Poecilasma
carinatum
Poecilasma obliquum
Trilasmis
(Poecilasma) obliqua
Sumba, April
Gulf of Mexico,
cultured, reproduces
July to Sept
Sumatra
egg (260 to 280)100 numerous

St I 230
Tubb, 1946
Coln-Urban et al.,
1979
some
egg 16080
St I 840
Nilsson-Cantell,
1930b
Krger, 1940
Lang, 1976
21459 depending
on size of adult
Jeffries & Voris,

1983
South Africa
egg 180
cyp 750
smallest adult had
325
largest 12 777
Barnard, 1924
Zann & Harker, 1978
Atlantic, West Indies

and Ascension Is.
S. Hemisphere, Dec
egg 250
Hoek, 1883
gravid Mar-Apr
egg (200220)80
egg 20080
numerous
Hoek, 1907
Krger, 1940
South Carolina, USA

gravid in June to Oct
many of these animals measurements or counts of embryos were made but a figure of 161 m for egg length
and 164 000 for number of eggs is given. Egg number depends on the size of the parent and Rasmussen
(1980) gives a graph showing values for C. auritum ranging from about 5000 eggs at a scutum length of 6
mm up to about 300 000 at 12 mm. This compares with that given by Thorner (1967) for Lepas fascicularis.
Lang (1976) found gravid Octolasmis mlleri (probably=O. lowei) in South Carolina, USA, every month
of the year ranging from less than 10% of the population in February to March to more than 40% in August
to November. Breeding and settlement was restricted to summer and autumn as release of eggs rarely took
place at temperatures below 15C. At Beaufort in North Carolina Jeffries & Voris (1983) found gravid animals
from late May to mid-July and suggested that breeding was continuous during the summer; their sampling
was restricted to the summer. They found brood size to depend on the capitulum length of the adult, the
number of eggs ranging from about 200 at 2 mm capitulum length to 3000 at 45 mm. These same authors
(Jeffries & Voris, 1979) examined O. grayii from the Malay peninsula and found that about 20% of mature
85
adults of 3.317.3 mm capitulum length . contained ova or eggs on the dates they sampled in December to
April and in August.
Scalpelloidea
Members of the Scalpelloidea may be hermaphrodites with complemental males or females with dwarf
males. In the genera Calantica and Smilium the males have a well separated capitulum and peduncle and
resemble the free-living juvenile adults. In Euscalpellum the males are more sac-like and the distinction
between capitulum and peduncle is not obvious; they still have cirri and a mouth. Males of the genus
Scalpellum are even more degenerate being sac-like with neither peduncle nor mouth and only vestigial
cirri and digestive system. Nilsson-Cantell (1932) gives an account of the males of Scalpellum species and
the literature on those already described. The most recent and comprehensive review of the comparative
anatomy of all cirripede males has been given by Klepal (1987).
Embryonic development proceeds in egg lamellae held in the mantle cavity of the hermaphroditic or
female adult. When hermaphroditic the embryos are released as stage I nauplii and lead a planktonic life up
to the cyprid stage. Embryonic development seems to be abbreviated in adults that are female with embryos
developing to the cyprid stage before hatching or leaving the mantle cavity (see Table IX). Barnard (1974)
thought that there was no difference in life history between shallow-and deep-water Scalpellum species.
Only ova were found in two of the deepest forms he studied and only early metanauplius in a third. All
the species were, however, female with dwarf males so that it is probable that all had an abbreviated
embryonic development.
There has been some discussion on the merits or otherwise of abbreviated larval development (see
Nilsson-Cantell, 1921; Kaufmann, 1965). Advantages include the reduced chance of predation which is
present during a prolonged planktonic life and as a consequence fewer larvae need to be produced. A
disadvantage may be lack of dispersal of the species by the larvae but because
TABLE IX
Scalpelloidea: summary of literature on Scalpellum and related species, cyp=cyprid; St Istage I nauplius. St ?=stage
not known; F=female; H=hermaphrodite
Species
Place
Date collected
or breeding
Size of adult
(LB), mm
Size of young
(LB), m
Number of
young per
brood
References
Calantica
pollicipedoide
s
Acroscalpellu
m sp.
egg 340280
Krger, 1940
5815N: 48
36W
14.87.8
Newman &
Ross, 1971
6553S: 70
56W
6118S: 569
W
6351S: 62
38W
6551'S: 82
40W
St ?
(850650) to
(900750)
cyp 1300650
F, 7.70.9
cyp 750250
50 to 60
Newman &
Ross, 1971
Newman &
Ross, 1971
F, 8534.5
egg
15001000
about 300
Acroscalpellu
m africanum
A. angulare
A. darwinii
Newman &
Ross, 1971
86
MARGARET BARNES
Species
Date collected
or breeding
Size of adult
(LB), mm
Size of young
(LB), m
Number of
young per
brood
References
6755S: 90
43W
egg 420350
Krger, 1940
egg 400250
Krger, 1940
egg 800550
Krger, 1940
Kerguelen Is.
6.0
egg 900600
egg 500330
egg 430300
39
Zevina, 1974
Krger, 1940
Krger, 1940
Krger, 1940
Kerguelen Is.
6.0
S. Africa
F, 5.5
egg 500300
egg 1030870
egg 580
59 to 82
cyp 1100520
egg 470270
14
Krger, 1940
Barnard, 1924
542S: 132
25E
S.Africa
Sept
egg 420350
about 20
Hoek, 1883
F, 4.0
cyp 1000500
S.Africa
F, 10.0
cyp 750500
24
Barnard,
1924;
Thorner, 1967
Barnard, 1924
S.Africa
F, 4.0
cyp 400250
S. cancellatum S.Africa
F, 6.5
cyp 750500
S. capense
S. chiliense
Oct
F, 5.0
7.0
cyp 700400
egg 500400
S. compactum
S.Africa
3218S: 71
50W
small
number
15 to 17
21
cyp 1030
S.
compressum
255N: 124
53E
Oct
egg 800
not
numerous
Scalpellum
(Acroscalpell
um)
balanoides
S.(A.)
brevicaulis
S.(A.)
compression
S.(A.) eugenie
S.(A.) eumitos
S.(A.) gracile
S.(A.)
hexagonum
S.(A) micrum
S. (A.) regium
S.(A.) sergi
S.(A.) sessile
Scalpellum
agulhense
S. balanoides
S. bolellinae
S. brachiutmcancri
S. brevicaulis
Place
Krger, 1940
Krger, 1940
Zevina, 1974
Barnard,
1924;
Thorner, 1967
Barnard, 1924
Barnard, 1924
Zevina, 1972
NilssonCantell, 1921
Hoek, 1883
S. convexum
S. Georgia
cyp 940
egg 780
cyp 1380
numerous
S. cornutum
cyp 750
S. eumitos
S. faurei
S. gibberum
S. Africa
S. Africa
E. Falkland Is.
May
F, 10.0
F, 6.0
cyp 900600
cyp 750400
egg 1090 to
1500
S. gracile
540S: 120
45E
S. Africa
Sept
egg 500330
F, 9.0
egg 500300
S. Africa
S. Africa
3717S: 53
52W
Feb
F, 3.5
F, 6.5
cyp 600300
cyp 800400
egg 750
2404S: 70
45W
528S: 134
55E
Sept
6.0
St ? 460
20
Zevina, 1972
Dec
H, 6.34.0
egg 340280
Hoek, 1907
cyp 1250510
June
ova 600
egg 1030870
about 400
S. scalpellum
3454N: 56
38W
3529N: 50
53W
British waters
Kaufmann,
1971
Hoek, 1883,
1884
Apr to Nov.
Max inAug
St I 475431
H, 16 to 26
110 to 582
Breed 3 times
a year
H, 6.5 to 18.5
egg 500(340
to 380)
egg 433352
St I 470
S. sessile
S. sinuatum
424S: 129
49E
28 to 3569 av.
of 229
animals=402
egg 470270
Krger, 1922,
1927, 1940
Kaufmann,
1962, 1965
F, 6.0
S. slearnsi
S. micrum
S. natalense
S. ornatum
S.
parallelogram
ma
S. perlongum
S.
pollicipedoide
s
S. regina
S. regium
NilssonCantell, 1930a
less than 20
NilssonCantell, 1921,
1930a
53
small
number
12
30 or less
not
numerous
Auivillius,
1894; NilssonCantell, 1978
Barnard, 1924
Barnard, 1924
cyp 1230 to
1920
Hoek, 1907
Barnard, 1924
Barnard, 1924
Barnard, 1924
Hoek, 1883
Bassindale,
17
Hoek, 1907
small
number
eggs seen
Barnard, 1924
Hoek, 1906
87
88
MARGARET BARNES
S. stroemi
cyp 700
S. subalatum
S. Africa
F, 5.0
cyp 800500
S. triangulare
Feb
S. uncinatum
S. valvulifer
3717S: 53
52W
S. Africa
S. Africa
F, 6.0
F, 6.0
S. vetutinum
cyp 1000600
ova 500300
cyp 750400
June
H, 4.0
S.
ventricosum
S. vulgare
Mediterranean
Scalpellum sp.
Smilium
hypocrites
S. Africa
S. Africa
Smilium
pollicipedoide
s
large number
but not
numerous
small
number
full
Hoek, 1883,
Barnard, 1924
Hoek, 1883
15
up to 30
Barnard, 1924
Barnard, 1924
Barnard, 1925
cyp 1330
Several
hundred ova
ova 300
St I 625400
ova 200
Hoek, 1884
45
ova 200
H, 1.5 to 12
2030
ova 200
Barnard, 1924
at least 150
Le Reste, 1965
Thorner, 1967
Krger, 1940
Barnard, 1924
the adults are female and dwarf males are essential for reproduction this lack of dispersal ensures that an
adequate supply of cyprids capable of becoming dwarf males is always available.
There has been very little work done to determine whether there are two types of cyprids, male and
female. Stewart (1911) said there were two sizes of cyprids in S. squamuliferum, the smaller becoming
complemental males and the larger the hermaphrodites. This was confirmed for the same species by
Stubbings (1936). Svane (1986) working with S. scalpellum, an hermaphrodite with complemental males,
has made some experimental observations. He found that isolated adult animals containing no complemental
males did not produce egg lamellae and, therefore, self-fertilisation did not take place. He also found that all
cyprids were potential hermaphrodites but that only about 50% also possessed the ability to metamorphose
into males if they encountered an hermaphrodite with available receptacles. He concluded that genetic and
environmental conditions influenced the determination of sex in this species. Similar work on female adults
and dwarf males would be of value.
As with many of the Rhizocephala and Acrothoracica what information there is on egg production is
scattered throughout the literature describing material collected during expeditions. Practically no
experimental work has been done on the Scalpelloidea. Kaufmann (1965) observed copulation in S.
scalpellum in the laboratory and compared the size of the adult hermaphrodite and number of eggs in 229
cases. He found an average of 402 eggs per animal, with a range of 28 to 3569 (see Table IX), depending on
the size of adult and time of the breeding season. Krger (1927) counted eggs in the same species ranging
from 16 to 26 mm in size and found 122 to 582 eggs depending on parental size. The number of eggs in
other species can range from eight up to several hundred (Table IX). When a very small number is
recorded it is not possible to know whether any eggs were lost during collection or preservation. Indeed this
89
can apply in many cases. When a reference states 150 eggs in each lamella then one can be sure there were
300 eggs present, as in Acroscalpellum dawrinii (Newman & Ross, 1971), and in Scalpellum regium, with
approximately 200 eggs in each lamella (Hoeck, 1883) there would be a total of about 400.
The times of breeding have only been followed closely by Kaufmann (1965) for S. scalpellum found in
the Gullmarfjord, Sweden. He took regular samples and also examined animals of known age in the
laboratory. He found that in Sweden an animal can probably carry three broods a year. There were relatively
more animals with fewer eggs in the autumn than in early summer which suggests that the numbers of eggs
may depend on the food available for ovarian development. Nutrition will decline as the adults use up their
reserves and are not able to replenish them as food in this northern environment declines in late summer and
autumn. In British waters, Bassindale (1936) gives the breeding peaks for S. scalpellum as mid-April,
September, and November; Nilsson-Cantell (1978) gives the maximum in mid-August.
For several of the other genera the information on the time of breeding is very sparse (see Table IX).
Dates of collection of material in a reproductive state vary from 17 June to 20 October in the Northern
Hemisphere and 14 February to 26 December in the Southern. Much of the material is from deep water
where environmental conditions are relatively stable. Barnard (1924) was of the opinion that there was no
particular breeding season. In shallower water the effects of temperature, light, and availability of nutrients
can cause seasonal variation as shown in S. scalpellum. In general, the size of eggs produced by these
genera is larger and the number less than in the Lepadoidea with a large number of very small eggs.
Species of the genus-Pollicipes are hermaphrodites without complemental males. They are usually found
in dense groups in the intertidal zone orientated so that they can feed as the backwash of the tide rushes
over them. The length of peduncle can be adjusted to bring the capitulum into a suitable position for feeding.
The egg lamellae form two thin sheets one on either side of the prosoma in the mantle cavity. The three
main species about which there is information on the reproduction are P. polymerus from the Pacific coast of
North America, P. cornucopia from southern European shores, and P. spinosus from New Zealand. The
available data on egg sizes and numbers are given in Table X.
Smith & Weldon (1920) thought that self-fertilisation might take place in P. polymerus but this has now
been dis-proved by Hilgard (1960) and Lewis & Chia (1981). The last authors never found egg lamellae in
animals separated by 11 cm or more from the nearest neighbour. On the Pacific coast of North America the
time and length of breeding season of this species varies throughout its range of distribution (Cimberg,
1981; Lewis & Chia, 1981). Page (1986) found differences in size and age at maturity depending on the habitat.
Reproductive patterns, percentage of adults with egg lamellae and the size of the lamellae have been studied
by Page (1984). When standardised for size of adult, he found seasonal changes in the percentage of adults
carrying egg lamellae; the weight of the lamellae ranged from 4 to 21% of the body weight. He has also
investigated the effect of sea-water temperature and food on energy allocation in P. polymerus (Page,
1983).
According to Cimberg (1981) there are two physiological races of P. polym erus on the Pacific coast of
North America. The northern race shows maximum breeding activity at sea-water temperatures of 14C or
less and the southern race at 20C. He found three types of adult: Type 1, north of Point Conception, which
breeds during the summer as sea-water temperature approaches about 14C; Type 2, at Latigo Point, south
of Point Conception, which breeds during the summer as sea-water temperature increases up to 20C; and
Type 3, also found south of Point Conception, at Goleta Point and on Santa Catalina Island, which breeds
during the winter as sea-water temperature falls to about 14C. Types 1 and 3 are, therefore, breeding at the
same temperature but not in the same season and constitute the northern race; Type 2 represents the
southern race. He suggests that the similarity between Types 1 and 3 is because larvae north of Point
90
MARGARET BARNES
Conception are transported in the south-flowing California Current during the oceanic and upwelling
seasons.
Lewis & Chia (1981) have summarised data on the number of broods produced per year by P. polymerus.
It can vary between about three to four (presumably the northern race) and eight at Santa Barbara (southern
race). This figure of eight broods at Santa Barbara is given by Lewis & Chia (1981) as quoting Straughan
(1971) although the figure does not seem to be in the latter reference. The number of eggs per brood also
varies; compared with P. spinosus (New Zealand) and P. cornucopia (Europe), P. polymerus produces
TABLE X
Pollicipes and Lithotrya species: summary of breeding seasons, sizes and number of young, and number of broods per
year. St I=stage I nauplius; o.d.=oven dry
Species
Place
Breeding
season
Size of young
(LB), m
Number of
Number of
References
eggs per brood broods per year
Pollicipes
cornucopia
S. Spain and
Gibraltar
63% with
eggs in July
egg 245
15 400 per 25
mg o.d. body
wt
Policipes
polymerus
Monterey
Bay, Calif.
Santa Monica,
Calif.
April
onwards,
peaks in June,
Sept, Dec
St I 17382
ova 100127
104 000240
000
4 to 5
Hilgard, 1960
144 000288
000
24 depending
San Juan Is.
Friday Harbor,
Wash.
ova 10580
egg 250130
Santa Barbara,
Calif.
Pollicipes
spinosus
St I 207114
New Zealand
5 years to
reach maturity
15007000
Lithotrya
dorsalis
Barbados,
West Indies
egg early
600445
egg late
690565
egg 570
Lewis & Chia,

1981 on
situation
Lewis, 1975
and Bodega
Bay, Calif.
Lewis & Chia,
1981
2
short breeding
season, June
July
Collected
SeptOct
St I 320
few hundred
Lewis, 1960
St I 36225
Dineen, 1987
egg (235 to
276)98
Sewell, 1926
egg 570
Indian Key,
Florida
Lithotrya
nicobarica
Lithotrya
truncata
Philippines
Darwin, 1851;
Barnes &
Barnes, 1966,
1968
Barnes &
Barnes, 1965
Batham,
1945b, 1946
Krger, 1940
Darwin, 1851
91
many more eggs per brood and has more broods per year (Table X). It is not clear whether the low number
of 100 young produced per brood at Santa Barbara (Straughan, 1971) is due to the effect of oil seepage or a
gradual reduction towards the southern end of the range of distribution but it is 1000 times (not 100 times as
quoted by Straughan, 1971) less than the figure given by Hilgard (1960) for Monterey Bay. Lewis & Chia
(1981) say that approximately seven times as many eggs are produced per brood by P. cornucopia at Cabo
Silleiro and Gibraltar (Barnes & Barnes, 1968) compared with P. polymerus at San Juan Island. This is
incorrect: Barnes & Barnes (1968) give a figure of 15 400 eggs from a moderate size P. cornucopia in
Europe which is seven times less (not more) than found at San Juan Island. P. cornucopia at Cabo Silleiro,
Spain, contain egg lamellae in July and at Biarritz, France, 22% of the population contain egg lamellae in
April, 85 90% in July, and 16% in October (Barnes & Barnes, pers. obs.) but it is not known how many
broods are produced per year.
P. spinosus produces a very much larger egg than the European or American species (see Table X) and
the larvae are lecithotrophic. It is not surprising, therefore, that it produces fewer eggs per brood (Batham,
1945b, 1946) in an animal of about the same size as P. polymerus. In addition, P. spinosus only produces
two broods a year and so far fewer eggs per year than does P. polymerus with say three to four broods per
year. Reproduction in P. spinosus at Otago, New Zealand, begins in December to January, as sea-surface
temperature rises to about 14C, reaches a peak in February to April and by August has finished by which
time the sea-surface temperature has dropped to about 8C. This temperature compares well with that of the
northern race of P. polymerus.
Lithotyra species are generally found in tropical seas in association with soft coral reef limestone into
which they burrow. They are hermaphrodites, although Sewell (1926) says that L. nicobarica may be
protandrous and only hermaphroditic when fully adult. The body is lodged partly in the peduncle with the
ovary filling the peduncle. Darwin (1851) found eggs in L. truncata from the Philippines and remarked on
their large size. Lewis (1960) records L. dorsalis in Barbados as having a short breeding season in June and
July and producing a few hundred eggs. He says that larvae are typical cyprids and that a newly hatched
cyprid is 320 m long and 640 m after 12 hours. He presumably means that the larvae are typical cirripede
nauplii and that stage I is 320 m lone. Dineen (1987) gives the length of L. dorsalis stage I nauplius as 362
25 m The few sizes that are given in the literature are summarised in Table X.
VERRUCOMORPHA
The Verrucomorpha contains asymmetrical sessile barnacles which may have a membranous or a
calcareous base. They are hermaphrodites. Darwin (1854) recorded four species from Iceland to Cape
Horn. According to Newman (1987) the genus Verruca now contains about 60 species. They usually occur
in deep water up to near inshore and shallow area (Zevina, 1987, 1988). V. stroemia is found in depths of
10100 m in British waters and is common in northern Europe and the northern Mediterranean but has not
been recorded from the Baltic Sea (Stone & Barnes, 1973). The reproductive
TABLE XI
Verruca species: summary of breeding and sizes of young. St I=stage I nauplius
Species
Place
Notes
Sizes of young (LB), m References
Verruca striata
Verruca stroemia
Northern waters
Adriatic Sea
Larval stages in plankton
in summer
One brood per year

egg 180
egg 322252
Nilsson-Cantell, 1921,
1978
Krger, 1940
Kolosvry, 1947
92
MARGARET BARNES
Species
Millport, Scotland
Place
Larval stages in plankton

most of year except Nov.
Most in spring and early
summer
Oban, Scotland
Several broods a year,
main one in spring, ceases
breeding in October
British waters
British waters
Marseilles, France Reproduces from mid May

to August
Notes
St I 260120
St I 270120
egg 203
Sizes of young (LB), m References

Pyefinch, 1948; Barnes &
Crisp, 1956; Barnes, 1958
Stone & Barnes, 1973;

Barnes & Stone, 1973;
Barnes & Barnes, 1975
Bassindale, 1936
Darwin, 1854
Le Reste, 1965
cycle of V. stroemia in Scotland has been considered in detail by Stone & Barnes (1973, 1974), Barnes &
Stone (1973), and Barnes & Barnes (1975). Because of the asymmetry of the animal neither the ovaries nor
the egg lamellae are equal in size, nor do they lie symmetrically on either side of the mantle cavity although
both are appressed to the prosoma. The larger lamella lies above the prosoma (as this lies parallel to the
substratum) and the smaller one lies below the prosoma. The larger lamella contains about 1.5 times as
many eggs as the smaller one. Breeding ceases during the autumn and early winter in natural populations
because of lack of food but if fed in laboratory cultures breeding will continue. Breeding is not inhibited in
either constant light or dark but a temperature of 20C is lethal even over moderate periods. Because of the
lack of breeding in the natural population in the winter there is virtually complete synchronisation of the
first brood of the year in early spring. Thereafter, synchrony is gradually lost as the animals produce further
broods throughout the summer. Most authors report several broods per year in V. stroemia except Kolosvry
(1947) who records only one in the Adriatic Sea.
Verruca, being essentially a deep-water animal is subjected to a cold and relatively stable environment
and information on the breeding behaviour of other species would be of interest. Ova and egg or stage I
nauplius sizes are given in Table XI for V. stroemia from several habitats but information on only one other
species, V. striata, could be found and this has a slightly larger egg than V. stroemia.
BALANOMORPHA
Members of the Balanomorpha are sessile barnacles with bilaterally sym-metrical shells and may have a
membranous or a calcareous base. They are hermaphrodites; a very few species have been found with
complemental males. Of the five superfamilies suggested by Newman (1987) nothing could be found in the
literature regarding egg production in the Chionelasmatoidea and the Pachylasmatoidea. In contrast a
considerable literature has developed on the other three. This involves general ecological studies and also a
great amount of experimental work on the factors and conditions regulating egg production and on the
biochemistry of the eggs themselves. The general ecological aspects will be considered first.
Chthamaloidea
Within this superfamily most of the work has been done on Chthamalus a warm-water genus some of which,
such as C. fragilis, C. stellatus and C. dalli, extend into the north-temperate area. Southward & Southward
93
(1967) found C. dalli, at what is the northernmost recorded place for a chthamalid, in the Chukchi Sea. Here
the shore is only ice-free from May to October and breeding takes place at a sea-water temperature of 6C.
Some animals even attempted to copulate at 4C suggesting that low temperature is little handicap to
fertilisation. These authors found 54% of the population with egg lamellae in late July and they suggested
that there might be two broods a year. Korn & Kolotukhina (1983) found that C. dalli had two broods per
year between March (when the sea-water temperature is 2C) and June in the Sea of Japan.
TABLE XII
Chthamalus species summary of breeding seasons, sizes and number of young. St I=stage I Nauplius; o.d. =oven dry ;
+=or more
Species
Place
Breeding
Size of young
(LB), m
Number of eggs
per brood
References
C. anisopoma
Gulf of California
egg 16382
Barnes & Barnes,

1965; Malusa,
1986
C. antennatus
New South
Wales, Australia
Hakodate, Japan
Breeds all year,

at 1333C; no
seasonal pattern.
44% fertilised in
June, 52% July,
7694% Dec
Feb
80% fertilised in
Jan (summer)
Fertilised Apr
July to June and
late Aug to early
Oct. Low levels
continuous Mar
to Oct. At least 2
broods perhaps 3
at low levels
ova 11080
Wisely & Blick,

1964; Pope, 1965
Iwaki, 1975
54% with eggs in

July 1+broods a
year
Luckens, 1968,
1969
C. challengeri
Asamushi, Japan
C. dalli
Upper levels
breeds April
Chukchi Sea
Sea of Japan
Two broods a
year
Vladivostok
St I 218112
Pacific coast,
USA
C. dentatus
St I 183102
Cape Town,
South Africa
Ripe eggs Oct to

May, peak in
Mar. Ripe again
in Aug with peak
in Dec
St I 140100
Korn &
Kolotukhina,
1983
Korn &
Ovsyannikova,
1979
Barnes & Barnes,
1965
Southward &
Southward, 1967
Bokenham,
1938; Sandison,
1954
94
MARGARET BARNES
Species
Place
Breeding
Size of young
(LB), m
Number of eggs
per brood
False Bay, South

Africa
Breeds Sept to
April but not in
May to Aug
egg 191111
St I 201108
Gulf of Guinea
C. depressus
Mediterranean
egg (166 to 196)

(90 to 102)
Breeds May to
Sept
Achituv &
Wortzlavski,
1983; Achituv,
1986
Stubbings, 1961
Euraphia
depressa (=C.
depressus)
C. fissus
Ligurian Sea
1298 eggs per

0.5 mg
o.d. body wt
Le Reste, 1965;
Barnes & Barnes,
1968
Relini, 1983
egg 13095
8022640
depending on
age.
990 eggs per
0.5 mg o.d. body
wt
Hines, 1974,
1978, 1979
3 broods a year
Villalobos, 1979a
1015% with
eggs for 9
months. In
culture
submerged 80
90% had eggs all
year
Page, 1984
egg 15382
Eyed embryos in
eggs in Jan
Breeds all year
except during
monsoons July
Sept. In Jan
temp, may be too
low
C. malayensis
Papua New
Guinea
Bombay, India
Barnes & Barnes,

1965
Pope, 1965
St I 205 to 216
980 in adult of 4
mm diameter
1890 in one of 9
mm, also give
max values of
3500 and 4300
Queensland,
Australia
Eyed embryos in
eggs Nov to
Western
Australia
Eyed embryos at
end Dec
Pope, 1965;
Hines, 1966
June, peak Nov
to Feb
Pope, 1965
Ripe eggs all

year, late stages
in June to Sept
Morro Bay, Calif. Peaking breeding
June to
Sept estimated
16 broods
between Mar and
Oct
Santa Barbara,
Calif.
Goleta Pt., Calif.
California
C. intertextus
St I 200149
References
Karande &
Palekar, 1963;
Wagh, 1965;
Karande, 1967,
1974a; Karande
& Thomas, 1976;
Gaonkar &
Karande, 1980
C. montagui
Ligurian Sea
C. stellatus
Adriatic Sea
Marseilles,
France
35 broods from
June to Oct. A
few fertilised in
Mar to May
Arcachon, France Breeds from Apr
to May
Ligurian Sea
All year except
Oct and Nov
Mediterranean
Breeds Mar to
Oct
Northern waters
Great Britain
More than one
brood from June
onwards to Oct
Shetland and Fair Breeds early

Isle, GB
June to Sept
Europe in general
C. withersi
Bombay, India
Eggs all year
except Oct and

Nov
Eggs JulyDec, 2
broods
Le Reste, 1965
Dessenoix, 1962
Relini, 1983
1528
St I 220
ova 130
egg 19194
St I 19090
egg 230130
Tenerelli, 1958,
1959
Hoek, 1909
Bassindale,
1936; Crisp,
1954; Barnes &
Barnes, 1965;
Nilsson-Cantell,
1978
Powell, 1954
500 to 2500 per

0.5 mg o.d. body
wt depending on
place and shore
level
St I 205 to 215
Breeds mainly
MarJune also in
SeptNov and
FebMar
Relini, 1983
Kolosvry, 1947
95
Barnes &
Barnes, 1968
7000 max 7100
Karande &
Palekar, 1963;
Karande &
Thomas, 1976
Similarly, C. challenged has a restricted breeding season in April to July near the northern limits of its
distribution at Hakodate (Iwaki, 1975), At the northernmost limits of its distribution in Scotland C. stellatus
produces two broods annually between May and September (Crisp, 1950; Powell, 1954; Barnes, 1972;
Achituv & Barnes, 1976) but only the second reaches maturity. It should be noted that because Southward
(1976) found that some European C. stellatus should have been called C. montagui some papers referring to
C. stellatus may have been concerned with a mixture of the two species.
Chthamalids in the more southern parts of their distribution generally produce more than two broods per
year depending on temperature and availability of food but rarely is reproduction continuous. There is
spermatogenetic activity in C. malayensis throughout the year according to Karande & Palekar (1963) but it
is greatest during periods of fertilisation. The available data from various parts of the world are summarised
in Table XII. The time of breeding and number of broods may depend on shore level as in C. challenged
(Luckens, 1968, 1969). In similar situations C. malayensis has more broods than C. withersi but produces
fewer eggs per brood (Karande & Palekar, 1963; Karande, 1974a; Karande & Thomas, 1976; Gaonkar &
96
MARGARET BARNES
Karande, 1980). The 16 broods said to be produced by C. fissus in central California (Hines, 1978) is
grossly in excess of the number found in any other Chthamalus species including C. fissus at Santa Barbara
in California (Villalobos, 1979a) and may be an over-estimate. It is based on the assumption that for eight
consecutive months an animal produces a new brood immediately the previous brood has been released; it
must also be assumed that adequate food reserves and ideal environmental conditions are available.
Barnes & Barnes (1965, 1968) have recorded the size of egg and/or stage I nauplius of C. stellatus and C.
depressus on European shores as well as the number produced by both species. Egg sizes are about the same
(190200 m) in each case. C. depressus produces about 1300 eggs per 0.5 mg oven dry body weight
throughout its range of distribution in Europe whereas the number in C. stellatus varies with latitude and
intertidal position from about 500 to 2500 per 0.5 mg oven dry body weight. In general the fecundity in C.
stellatus is relatively lower in protected areas such as harbours than in more exposed situations. This may be
due to turbidity in harbours and quiet bays. There is, however, the overriding effect of nutrient supply, the
highest number of eggs being found at Arcachon, France, where there is shelter and the water is turbid but
nutrient level is very high. These numbers are comparable with those given by Hines (1974, 1978, 1979) for
C. fissus in California. The only other numbers given in the literature are for C. withersi, 7000 per brood
and C. malayensis, 4300 per brood (Gaonkar & Karande, 1980). Karande & Palekar (1963) give 980 in an
adult C. malayensis of 4 mm basal diameter and 1890 eggs in one of 9 mm basal diameter. These two
species are from Bombay waters.
Available information on other species of the Chthamaloidea is summarised in Table XIII. Chamaesipho
columna near Sydney, Australia, is said to breed mainly from June to October with no egg lamellae present
for about six months of the year (Wisely & Blick, 1964). At Leigh in New Zealand, Moore (1944), Foster
(1967), and Luckens (1970, 1976) report the same species as breeding throughout the year whereas C.
brunnea, also at Leigh, breeds only in spring and summer (November to April). The cultured stage
TABLE XIII
Chthamaloidea other than Chthamalus species: breeding seasons and sizes of young. St I=stage I nauplii
Species
Place
Breeding season
Size of young (LB),

m
References
Catophragmus
polymerus
Sydney, Australia
Wisely & Blick, 1964
Chamaesipho
brunnea
Leigh, N.Z.
New Zealand
Peak breeding
seasons Jan to Apr,
June to Sept
Breeding Sept to Feb
Moore, 1944
New Zealand
Chamaesipho
columna
Leigh, N.Z.
New Zealand
Breeds mainly in
Nov to Apr
New Zealand
Breeds all year,
settles all year at low
levels but only in
Apr to Jan at high
levels
St I 350190
St I cultured
(190 to 210) (90 to
100)
Breeds all year
Foster, 1967;
Luckens, 1970
Barker, 1976
St I 300170
Foster, 1967;
Luckens, 1970, 1976
St I cultured
Barker, 1976
Moore, 1944
Species
Place
Sydney, Australia
Breeds mainly June

to Oct Nothing for
about 6 months of
year
Cape Town, South
Africa
Octomeris angulosa
False Bay, South

Africa
Peak breeding in Aug

to Jan Egg masses
present most of year
except July
Breeding season
(200 to 230)100
Late stage eggs in

Oct After release
empty until June,
then peaks in Oct
egg 212133
Size of young (LB),

m
97
References
St I 180100
Sandison, 1954
Achituv &
Wortzlavski, 1983
I nauplii (Barker, 1976) of these two species seem to be smaller than in the natural populations (Foster,
1967). Catophragmus polymerus at Sydney has peak breeding seasons from June to September and January
to April (Wisley & Blick, 1964). In South Africa Octomeris angulosa at Cape Town contains late stage
embryos in eggs in October; there are none from February to June (Sandison, 1954). In False Bay Achituv &
Wortzlaviski (1983) found egg masses most of the year except in July; peak breeding was from August to
January.
Coronuloidea
Most information concerns the family Tetraclitidae (Table XIV) which is intertidal and found in tropical
and warm-temperate regions. It would, therefore, be expected that Tetraclita species might breed
throughout the year. Breeding seasons, however, vary and are not always continuous. For instance T.
squamosa rufotincta in the Gulf of Elat has a distinct breeding cycle with a peak in November to December;
only 0.5% of the population may be found with egg lamellae at other times of the year (Achituv, 1979;
Barnes & Achituv, 1981). According to Lewis (1960) T. s. stalactifera breeds throughout the year in
Barbados whereas in Costa Rica T. stalactifera contains lamellae with eyed embryos in October to
November (Villalobos, 1980). T. squamosa japonica breeds most of the year with eyed embryos present
from June to September in Shimizu Harbour, Japan, (Kosaka & Ishibashi, 1979).
Egan & Anderson (1988) record Tesseropora rosea as having a clearly defined breeding season in
summer and early winter in New South Wales while Denley & Underwood (1979) say there is much local
variability on the same shores. In Tetraclitella purpurascens and Austrobalanus imperator there are peaks
of breeding in New South Wales in winter to early summer in the former species and in late autumn to early
winter in the latter with some gravid animals present throughout the year in both species (Egan &
Anderson, 1988).
Villalobos (1979b) suggests that Tetraclita rubescens at Santa Barbara, California, which reaches sexual
maturity at the end of its second year may produce offspring one year when there is no somatic growth and
then grow the next year, so that in one year energy is allocated to development of gonads rather than growth.
T. squamosa rufotincta at Elat becomes mature during its second year (Achituv, 1979) as does T.s. japonica
in Japan (Kosaka & Ishibashi, 1979).
98
MARGARET BARNES
Size of late stage eggs and/or stage I nauplii are generally about 240 310 m in length. There are three
notable exceptions, T.s. rufotincta, T. (Tesseropora) pacifica, and T. divisa with eggs of 508, 527, and 840
m long (Barnes & Achituv, 1981; Crisp, 1986; Nilsson-Cantell, 1921), respectively. These three species
all produce lecithotrophic larvae. The larvae of the first two species pass through the usual six moults to the
cyprid stage but development in T. divisa is abbreviated to four stages brooded within the mantle cavity; the
cyprid is released from the mantle cavity but has a restricted larval life (Anderson, 1986).
The number of eggs produced per brood is recorded in two species in each case depending on the size of
the parent. Tetraclitella karandei from Bombay waters contains about 5900 eggs per brood (Gaonkar &
Karande, 1980) and Tetraclita squamosa japonica in Japan has 13 000 to 71 000 (Kosaka &
TABLE XIV
Tetraclita, Tetraditella and Tesseropora spacies: summary of available literature on breeding seasons, size and number
of young. cyp=cyprid; St I=stage I nauplius
Species
Place
Breeding season
Size of young
(LB), m
Number of eggs
per brood
References
Tetraclita divisa
egg 840
Nilsson-Cantell,
1921, 1978
Malay
Archipelago
Tetraclita
japonica
According to
Nilsson-Cantell
this is only
known
operculate to
develop to cyprid
within the mantle
cavity of adult
St I 620
20 to 30
Hiro, 1939
egg 300
13 000 to 71 000
Kosaka &
Ishibashi, 1979
Tetraclita
karandei
Bombay, India
Breeds most of
year, eyed
embryos in eggs
June to Sept
St I 240
5900
Tetraclita
(Tesseropora)
pacifica
Tetraclita
purpurascens
(=Tetraditella
purpurascens)
Leigh, New
Zealand
egg 527387
Karande, 1974b;
Karande &
Thomas, 1976;
Gaonkar &
Karande, 1980
Crisp, 1986
Sydney,
Australia
Foster, 1967;
Harker, 1976
Tetraclita
(Tesseropora)
rosea
Sydney,
Australia
A few nauplii
throughout year,
peak settlement
Oct to Dec
St I cultured
(290 to 310)
(130 to 140)
St I 470200
Breeds Feb to
Mar, releases in
May. Mantle
Shimizu
Harbour, Japan
Wisely & Blick,

1964; Denley &
Underwood, 1979
Wisely & Blick,

1964
Species
Place
Tesseropora
rosea
Sydney, Cape
Banks Australia
Tetraclita
rubescens
Santa Barbara,
California
Tetraclita serrata
Cape Town,
South Africa
South Africa
Breeds July to
Oct
California
Tetraclita
squamosa
rubescens
Tetraclita
squamosa
rufotincta
Gulf of Elat
Tetraclita
squamosa
stalactifera
Tetraclita
stalactifera
Barbados
Costa Rica
Gonads Apr to
Aug, eggs Oct to
Nov, releases
Nov to Dec
Gulf of
California
Breeding season
Size of young
(LB), m
Number of eggs
per brood
References
Denley &
Underwood,
1979; Otway &
Underwood, 1987
Villalobos,
1979a, 1980
St I 240170
Griffiths, 1979
Breeds June to
Sept 23 broods a
year
Breeds Nov to
Dec. One brood,
may be two per
yr
Breeds
throughout year
egg 340195
10 770 to 54 090 Hines, 1974,

depending on age 1978, 1979
St I 509336
Achituv, 1979;
Barnes &
Achituv, 1981
Lewis, 1960
Breeds in
summer, peaks in
Aug, ends in Nov
Malusa, 1986
Villalobos, 1980
cavity empty for

6 months of year
Some breeding
all year but 80%
in Apr. Local
variability
Reproduces
every 2 yr egg
lamellae Feb to
Nov
Ripe gonads Oct
to Feb none in
summer, settles
in May
St I 274154
99
Bokenham, 1938;
Sandison, 1954
Ishibashi, 1979). There is no indication as to how many broods are produced per year. In contrast T. divisa
produces 2030 eggs per adult according to Hiro (1939); this lower number is to be expected because of the
much larger egg size.
So far it does not seem to have been possible to bring about fertilisation of ova in Tetraclita species in the
laboratory even though the animals have been apparently in a suitable condition. Hines (1978) failed to get
T. squamosa rubescens to fertilise although natural populations were fertilising at that time. Achituv &
Barnes (1978a) and Barnes & Barnes (unpubl.) tried variable culture conditions with T. s. rufotincta but
although well advanced ova and spermatozoa were produced there was no copulation.
Members of the Coronulidae include Chelonibia, which according to Crisp (1983) should be spelt
Chelonobia, and Platylepas species. Chelonibia testudinaria is found in tropical and temperate seas
attached to turtles and according to Kolosvry (1947) in the Adriatic it has one brood a year. Pillai (1958)
gives the size of stage I nauplius as wide from an individual found at Kerala, India. Platylepas species are
100
MARGARET BARNES
associated with sea snakes, dugongs, and turtles. Zann & Harker (1978) compared P. ophiophilus and P.
hexastylos from northern Queensland, Australia. The length of life of the barnacles depends very much on
the frequency of moulting of the host. P. ophiophilus is mature at a diameter of 2.5 mm and produces only
one brood of 450525 eggs of length 120 m in December. The hosts, sea snakes, moult frequently and
although adult barnacles can continue to live on the cast-off skin existence is then precarious, for example
due to risk of burial in the sediment. P. hexastylos is mature at 6 mm diameter and eggs the same size as those
of P. ophiophilus are found in May and July. Some animals can have up to 6500 eggs per brood, others only
20100; the average seems to be about 14703100. Egg production is probably continuous and because the
hosts, turtles, moult less often than sea snakes the barnacles can produce more than one brood in a lifetime.
Bathylasma corolliforme is found in Antarctic seas down to about 1400 m. According to Dayton,
Newman & Oliver (1982) larvae are continuously dispersed into the McMurdo Sound region. The stage I
nauplius is relatively large, about 430 m long, and is capable of a planktonic life. It is probable that there is
a pool of larvae throughout the Ross Sea.
Balanoidea
Species of the genus Elminius are found in Australia, New Zealand, South America and Europe. There is one
recorded appearance of E. modestus in South Africa (Sandison, 1950) but it has not been found again since
then. It has generally been thought that the European species introduced from Australasia during World
War II (Bishop, 1947) was E. modestus but after examining larvae of the Australasian species and
comparing them with larval descriptions of European species, Egan & Anderson (1985) have pointed out
some anomalies which cast doubt on this. In this review the European species has been called E. modestus as
in all the published work from Europe. Foster (1982) has split what was known as E. modestus from eastern
Australia into three species, E. modestus, E. covertus, and Hexaminius popeiana. Elminius kingii occurs
exclusively in South America.
TABLE XV
Elminius and Hexaminius species: breeding seasons and size of young. St I=stage I nauplius; o.d.=oven dry
Species
Place
Breeding season
Size of young (LB),

m
References
E. covertus
Sydney, Australia
E. kingii
Chile
Egan & Anderson,

1985
Stefoni & Contreras,
1979; Arenas, 1982
E. modestus
Sydney, Australia
Auckland, New
Zealand
Leigh, N.Z.
Egg lamellae present

every month except
Apr
Breed all year
Eyed embryos for 7

months of year
St I cultured
230140
egg 250175
St I 250140
(120 to 140 also
quoted)
New Zealand
St I 360150
St I cultured (210 to
230) (100 to 110)
Moore, 1944
Foster, 1967;
Luckens, 1970, 1976
Barker, 1976
Species
Place
Breeding season
Size of young (LB),

m
Europe ien general
1800 eggs per 1 mg

o.d. body wt
Breeds at 71 8C in
May to Oct. Main
period July to Sept
Main peak July to
Aug Some from May
to Sept
Barnes & Barnes,

1968
Barnes & Barnes,
1965
Harms, 1984
Menai Bridge, North

Wales
Nauplii all year
ova 100 to 150

egg 19093
E. plicatus
New Zealand
Auckland, N.Z.
Egg lamellae every

month except Apr
Some breeding all
year
Pontevedra, Spain
Heligoland, Germany
Southern England
Leigh, N.Z.
Hexaminius
popeiana
egg 192
St I (240 to 260)
(110 to 140)
St I 490200
Knight-Jones &
Waugh, 1949;
Stubbings &
Houghton, 1964
Crisp, 1954; Wisely,
1960; Crisp & Patel,
1961
St I cultured (300 to
320) (120 to 140)
Moore, 1944
101
References
Barker, 1976
Foster, 1967;
Luckens, 1970, 1976
St I cultured 200110 Egan & Anderson,
1985
In general, where food is adequate and sea temperatures above 6C, breeding seasons seem to be
continuous, with occasional peaks, for Elminius species (Knight-Jones & Waugh, 1949; Ralph & Hurley,
1952; Skerman, 1958b, 1959; Wisely, 1960; Crisp & Patel, 1961; Wisely & Blick, 1964; Foster, 1967;
Luckens, 1970, 1976). Egan & Anderson (1985) found, however, seasonal breeding in E. covertus with
peaks in June to August (winter) and September to November (spring). In Europe breeding becomes
seasonal at the northern limits of the distribution of E. modestus where sea temperatures drop below 6C
such as in Heligoland (Harms, 1986).
Some authors give sizes of ripe eggs or stage I nauplii and these are summarised in Table XV. The only
egg counts seem to be those reported by Barnes & Barnes (1968). They found that there was no significant
difference in the numbers of eggs produced by E. modestus per given oven dry weight of body throughout
the whole range of distribution in Europefrom Scotland to Portugal. The value of 1800 eggs per 1 mg
oven dry body weight was obtained from the common regression of egg number against oven dry body
weight for all localities and refers to a moderately sized animal.
The coral-inhabiting cirripedes of the genus Pyrgoma may be found as far north as the English Channel
and southern Irish Sea although they are usually much further south. Hoek (1913) found P. jedani at Station
Jedan, containing 6080 eggs of size 270 m long140 m wide. P. anglicum breeds in summer at the
northern limit of its range of distribution producing stage I nauplii of length 280321 m. These are the same
size as those of Acasta spongites (293 320 m) which also breeds in summer in the north (Moyse, 1961).
According to Kolosvry (1947) A. spongites in the Adriatic produces one brood a year and cyprids are only
found in the spring.
102
MARGARET BARNES
Species of the genus Balanus apparently represent several diverse origins and much has been done
recently to separate these. Several species have now been separated into a new family, the
Archaeobalanidae while others still remain in the Balanidae (Newman & Ross, 1976, 1977; see also Foster,
1978). For the present purpose the original names used by the authors have been used. The vast volume of
data on Balanus species is summarised as far as possible in Table XVI. The differences depend mainly on
whether the species is boreo-arctic, warm-temperate or tropical. Those in the north breed at lower
temperatures than those further south. In many cases they only produce one brood a year with a large
number of eggs compared with southern species that produce more numerous broods containing smaller
eggs. The implications of these differences and the general conditions governing breeding and egg
production are included in the following sections.
FACTORS AFFECTING BREEDING
In an introduction to reproductive rhythms in marine invertebrates Barnes (1975) discussed synchrony, and
the loss of it, in the reproductive state. He reviewed the effect of temperature, light, and food on population
synchrony with particular reference to cirripedes.
Experimental work on the conditions affecting breeding has been carried out on several species, such as
B. amphitrite var. denticulata (Patel & Crisp, 1960b); B. balanoides (Crisp, 1959, 1964b; Crisp & Clegg,
1960; Barnes, 1963; Barnes & Barnes, 1967; Crisp & Patel, 1969); B. balanus (Crisp & Patel, 1969);
TABLE XVI
Balanus and related species: summary of some of the literature on breeding seasons, size and number of young. St
I=stage I nauplius; o.d.=oven dry
Species
Place
Breeding and
notes
Size of young
(LB), m
Number of eggs
per brood
References
Balanus alatus
B. aligcola
Sulu Sea
Table Bay, South
Africa
egg 240
St I 18098
numerous
Hoek, 1913
Bokenham,
1938; Millard,
1952; Sandison,
1954
B. amaryllis
Bombay, India
St I 240
B. a. euamaryllis
Bombay, India
June
Year round
breeding, peaks
in Sept to Dec
and Mar to June.
25% with ova all
year
Breeds all year
except Oct
St I 240
B. amphitrite
Genoa,
Tyrrhenian Sea,
Vado, Ligure Bay
St I 270140
Marseilles
Reproduces May
to Nov. Probably
up to 8 broods a
year
1718C temp
min for
fertilisation
Optimum 2223
C. Settles Mar to
Nov
Wagh, 1965;
Karande, 1974a
Karande &
Thomas, 1976
Relini, 1968;
Relini &
Giordano, 1969;
Geraci &
Romairone, 1986
Le Reste, 1965
Species
Place
Breeding and
notes
Size of young
(LB), m
Goa, India
3380 to 18 700 in Harkantra et al.,

adults 3.8 to 9.5 1977
mm diam
Paul, 1942
Weiss, 1948b
Europe
Egg lamellae all

year but best in
pre-and postmonsoon when
salinity is high
Matures in 16
days
Breeds at above
20C, peaks in
Mar, May, June,
Oct. No breeding
in winter at less
than 20C
B. a. albicostatus
Japan
4800 per 3 mg
o.d. body wt
St I 240140
Barnes & Barnes,

1968
B.a. amphitrite
Bombay, India
St I cultured 225
18 700 4607 per

1.3 mg o.d. body
wt
Cochin, India
Andaman Is.,
Indian Ocean
St I cultured
180120
Sydney,
Australia
Breeds all year,

particularly in
Jan to May
2568% with
ripe eggs from

June to Jan. Main
release Nov to
Mar
Kalyanasundara
m & Ganti, 1975
Karande, 1978
Wisely & Blick,

1964
Species
Place
Breeding and
notes
Size of young
(LB), m
Number of eggs
per brood
References
B. a. communis
Cochin, India
250300
Pillay & Nair,

1972
Bombay, India
Breeds in warmer
months but not in
May if temp is
above 33C.
Peaks usually in
Two peaks of
breeding in Dec
and May. No
breeding in July
and Aug
St I cultured 180
Wagh, 1965;
Karande, 1967;
Karande &
Thomas, 1971
Madras, India
Florida, USA
Number of eggs
per brood
103
References
Ishida & Yasugi,

1937
Karande, 1973,
1974c; Karande
& Thomas, 1976;
Gaonkar &
Karande, 1980;
Rege, Joshi &
Karande, 1980
104
MARGARET BARNES
Species
Kerala
backwaters, India
Adriatic Sea
B. a. cirratus
Port Jackson,
Australia
B. a. denticulala
Place
Mar to Apr and
Oct
Breeds all year
but max in dry
season Dec to
Apr. Breeding
reduced in May
to Aug if salinity
is reduced to 6
7%o
Only one brood a
year
Auckland, New
Zealand
Seasonality in
breeding, never
more than 50% at
a time. Min in
June to Aug,
increase in Sept
to Feb. A few
breeding Apr to
May Smallest
gravid animal 6
mm diam
Cape Town,
South Africa
Swansea, UK
More than one

brood a year
North Carolina,
USA
B. a. hawaiiensis
Bombay, India
Breeds in warmer
months but not
above 33C.
Peaks in Mar to
Apr and in Oct
Breeds all year.
Max in Feb to
July
Manila Bay,
Philippines
Japan
Breeding and
notes
Size of young
(LB), m
Number of eggs
per brood
St I 210150
Pillai, 1958;
Karande &
Palekar, 1963;
Pillay & Nair,
1970
Kolosvry, 1947
Settles Nov to
Mar. Probably
mature and
breeding within 2
months
St I 220
Egan &
Anderson, 1986
Ripe eggs in
Sept. No
development
during winter
ova 120
egg 15090
St I 210140
St I (160240)
(140200)
Crisp, 1954;
Patel & Crisp,
1960b
Costlow &
Bookhout, 1957
St I cultured
190100
Karande, 1967
Rosell, 1976
References
Skerman, 1959
Sandison, 1954
Hudinaga &
Kasahara, 1942
Species
Place
Breeding and
notes
Size of young
(LB), m
Number of eggs
per brood
References
B. a. variegatus
Bombay, India
Breeds all year

including during
monsoons
35 000
B. balanoides
Bangor, UK
Fertilises Nov.
Releases in
spring 1 brood a
year
ova 210
egg 305160
St I 34189
Karande &
Palekar, 1963;
Gaonkar &
Karande, 1980
Crisp, 1954,
1962, 1964b,
1968a
Great Britain
Northern Europe
(plankton)
Port Erin, UK
St I 370
5000 to 10 000 in Moore, 1935;

Barnes &
mature adults;
4008000 per l.5 Barnes, 1968
mg o.d. body wt
Hoek, 1909
Fertilises in Nov
Scotland
Fertilises Nov.
One brood a year
St I (340350)
220
25004000, max
13 000
4008000 per 1.
5 mg o.d. body wt
Herdla, Norway
Fertilises end Oct
Hammerfest,
Norway
Spitsbergen
Fertilises Sept
1000 per 1.5 mg

o.d. body wt
Fertilises end
Aug to Oct
depending on
place
Nauplii released
end May-June
Zevina, 1963a
Arnold, 1977
egg 392186
egg 338180
4200 in 2nd yr
animal, diam
Crisp. 1968a
Crisp, 1968a
egg 341178
Crisp, 1964a
4007160 per 1.
5 mg o.d. body wt
Barnes &
Barnes, 1968
Scotland
Fertilises about
Feb. One brood a
year
St I 370210
Greenland
White Sea,
Russia
New Brunswick,
Canada
Newfoundland
Woods Hole,
USA
New England,
USA
EuropeSweden
to Spain excl
Great Britain
B. balanus
Moore, 1935
Pyefinch, 1948;
Barnes &
Barnes, 1965,
1968
Runnstrom,
19241925
Barnes &
Barnes, 1968
FeylingHanssen, 1953
Hpner Petersen,
1966
Barnes &
Costlow, 1961;
105
106
MARGARET BARNES
Barnes &
Barnes, 1965
Bangor, UK
B. calceolns
B. crenatus
South of
Salawati Is.
Puget Sound,
Wash., USA
Scotland
Bangor, UK
Sea of Japan
Settles in spring
and autumn, a
few in summer
Species
Place
White Sea,
Russia
Breeds
continuously
depending on
food and temp
Breeds Mar to
Nov
Woods Hole and
Long Is., USA
B. cariosus
Puget Sound,
Wash., USA
San Francisco
Bay, USA
B. eburneus
North Carolina,
USA
Florida, USA
Seasonal
breeding, low in
mid winter, peak
in Oct
Breeds May to
Oct. Nauplii
present June
onwards, settles
mainly in
summer
Genoa, Vada
Ligure Bay, Po
estuary, Tarante
Med. Sea
ova 225
egg 307168
Collected in Aug
50 000
Crisp, 1954, 1962
egg 170
Hoek, 1913
One brood a year

in early spring
Main breeding
Apr to May, but
also later in year ;
a few broods per
year
ova 170
egg 237120
St I cultured
263124
St I 285146
St I 280162
Branscomb &
Vedder, 1982
Pyefinch, 1948,
1949; Barnes &
Barnes, 1965
Crisp, 1954
Ovsyannikova &
Korn, 1984a,b
Breeding and
notes
Size of young
(LB), m
Number of eggs
per brood
References
Nauplii present
Zevina, 1963a
Branscomb &
Vedder, 1982
egg 190120
St I 220120
Breeds all
summer, 60 days
to maturity. First
release in June
St I (190 to 230)
(160 to 180)
Herz, 1933
Costlow &
Bookhout, 1957;
Barnes & Barnes,
1965
Weiss, 1948b
St I 315151
Relini, 1968;
Relini &
Giordano, 1969;
Lepore, Scisciola
& Gherardi,
1979; Relini &
Fasciana, 1982;
Grave, 1933;
Landau, Finney
& dAgostino,
1979
Species
Place
Breeding and
notes
Size of young
(LB), m
Adriatic Sea
Black Sea and
Sea of Azov
Caspian Sea
One brood a year

Breeds only at
end of summer
Egg lamellae in
June-July
Breeds July and
Sept at 2129C.
Releases Aug to
Sept
La Jolla and
Catalania Is.
Calif., USA
ova 13080
Yasuda, 1970;
Honma &
Nakajima, 1973
Breeds
continuously.
Has a
complemental
male
2 major broods a
year, in May and
Sept. May be
more. No
settlement from
Nov to May
Molenock &
Gomez, 1972;
Gomez, 1974
egg 220125
St I 244 153
2000 to 12 000
depending on
size of adult
Johnson &
Miller, 1935;
Barnes & Barnes,
1956, 1965; Wu
& Levings, 1979;
Branscomb &
Vedder, 1982
Uchiura Bay and

Sado Is., Japan
B. galeatus
Number of eggs
per brood
Geraci &
Romairone, 1986
Kolosvry, 1947
Zevina, 1957,
1963b
Zevina, 1957
107
B. glandula
British Columbia
and Puget Sound,
USA
Morro Bay,
Calif., USA
6 broods a year in eggs 245175

winter and
spring, limited by
heat
Great Britain
Fertilises early
Jan, releases
early Mar. One
brood a year
3417 to 30 090
depending on
age of adult
Hines, 1974,
1978, 1979
ova 265
egg 385205
St I 442232
100 000
Friday Harbor,
USA
Sydney, Australia
St I 265129
Eyed embryos
for 11 months of
year. Some
release in Mar to
Apr
B. hameri
B. hesperius
B. imperator
B. improvisus
West coast
Sweden
Fertilises May to
June, more than
60% with egg
lamellae in June
to Sept, decreases
to 10% in Nov to
References
Moore, 1935;
Crisp, 1954,
1962; Patel &
Crisp, 1960a;
Barnes & Barnes,
1965
Barnes & Barnes,
1959c, 1965
Wisely & Blick,
1964
Blom, 1965
108
MARGARET BARNES
Cuxhaven and
Kiel, Germany
Dec. 23 broods a
year
St I (160 to 200)
(80 to 100)
Mediterranean
Sea
Breeds May to
Oct or Nov until
temp is less than
10C
Female gonads
present all year.
Egg lamellae May
to Oct until temp
is less than 10C
Two breeding
seasons, June to
July and Sept
Breeds May to
Dec
Great Britain
ova 123
egg 16193
St I 195111
Northern waters
egg 12090
St I 190
Relini, 1980;
Relini, Matricardi
& Diviacco, 1980;
Relini &
Fasciana, 1982
Crisp, 1954; Jones
& Crisp, 1954;
Barnes & Barnes,
1965
Hoek, 1909;
Krger, 1940
Zevina 1957,
1963b
Zevina, 1957
Yasuda, 1970
Weiss, 1948a,b
Early stage
embryos in Sept,
settles only in
spring
St I 200135
Karande, 1979
Millard, 1952;
Sandison, 1954
St I 266157
Breeds all year,

probably 23 to 33
broods
Breeds in dry
season when
5900 to 74 400
from adults of 11
to 28 mm diam
Barnes & Barnes,

1959d, 1965
Hurley, 1973
Netherlands
Arcachon, France
Black Sea and Sea Breeds all year

of Azov
Caspian Sea
Egg lamellae in
June to July
Uchiura Bay,
Breeds early Mar
Japan
to late June at 14
2C. Peak in June
at 1822C
Florida, USA
Breeds in pulses
rather than
continuously all
year
B. kondakovi
E.coast India
B. maxillaris
Cape Town,
South Africa
B. nubilus
B. pacificus
B. pallidus
stutsburi
Friday Harbor,
Wash., USA
Baja California
and S.Calif.
Lagos, Nigeria
Buchholz, 1951;
Khl, 1966
Breeman, 1934
Dessenoix, 1962
Sandison, 1967
B. perforatus
S.W.Great Britain
Species
Arcachon, France
Marseilles, Med.
Sea
Genoa, Vado,
Ligure Bay,
Taranto
B. reticulatus
B. rostratus
B. terebratus
B. tintinnabulum
tintinnabulum
B. trigonus
salinity is high. 3
to 4 broods a year
ova 160
egg 221115
St I 279130
Northern waters
Rarely fertilises
before mid June,
releases same
month, settles late
July to Sept
St I 280
Hoek, 1909
Place
Breeding and
notes
Adriatic
One brood a year,

cyprids in winter
Dessenoix, 1962
Le Reste, 1965
St I 402160
egg 250150
Relini, 1968;
Relini &
Giordano, 1969;
Lepore, Sciscioli
& Gherardi,
1979; Geraci &
Romairone,
1982, 1986
Depends on temp Yan & Chen,
1980; Cai Rusing
and size adult.
& Huang
More at higher
Zongguo, 1981
temp and bigger
animals
10 00015 000 in Korn, 1985
adults 2 cm diam.
100 000 to 500
000 at 56 cm
diam
Hoek, 1913
Wagh, 1965
St I 375171
Relini, 1968;
Relini &
Giordano, 1969;
Breeds in
summer, May to
June and Aug are
main peaks
Three periods of
reproduction,
summer, autumn,
winter at 1324
C. Probably 10
broods a year
Larvae in June to
Sept Mainly
settles in summer
Max fertilisation
at 2225C and
release in Aug
East and South

China Sea
Breeding begins
mid Apr at above
17 to 18C, ends
Dec. Peak May to
Oct
Peter the Great
One brood a year.
Bay, Sea of Japan Fertilises in Sept
at 1718C.
About 2 weeks
incubation
Kei Is.
Egg lamellae in
Dec
Bombay, India
Breeds during
SW monsoon in
July to Sept and
Mar to Apr
Genoa, Vado,
Settles June to
Ligure Bay
Oct
Size of young
(LB), m
Norris & Crisp,

1953; Barnes &
Barnes, 1965
109
St I cultured
(256 to 275)
(143 to 187)
ova 120150
Number of eggs
per brood
References
Kolosvry, 1947
110
MARGARET BARNES
Species
Place
Breeding and
notes
Size of young
(LB), m
Number of eggs
per brood
References
Geraci &
Romairone, 1986
Sydney,
Australia
Leigh, New
Zealand
Table Bay, South
Africa
Uchiura Bay,
Eyed nauplii for

7 months,
releases Jan and
July
Summer
breeding, settles
Nov to Mar
Sporadic
breeding all year,
mainly late
summer
(Millard). Once a
year (Sandison)
Breeds May to
July and
Wisely & Blick,

1964
St I cultured
(210 to 230)100
St I 370190
St I 240140
Skerman, 1959;
Foster, 1967;
Harker, 1976
Millard, 1952;
Sandison, 1954
Yasuda, 1970
Sept to Nov at
1719C. Peaks
late May to late
June at 1824C
egg 17090
Breeds all year,

max in spring and
autumn.
Probably many
broods a year
Bombay and
Indian harbours
Krger, 1940
Werner, 1967
St I 240
Breeds all year,

peaks in Jan to
May
Some seasonality
in breeding.
Never more than
50% with egg
lamellae, Min in
June to Aug
increasing to
peak in Sept to
Feb Smallest
gravid animal 7
mm diam
Karande, 1978
St I 200
Egan &
Anderson, 1986
Japan
Florida, USA
B. variegatus
Andaman Is.
Port Jackson,
Australia
Karande, 1974c;
Karande &
Thomas, 1976;
Gaonkar &
Karande, 1980
B.v. cirratus
Leigh, New
Zealand
Chile
Nauplii from
June to Apr
Breeds Apr to
June at 1422C.
Max in June at
1822C
Predominately
winter breeding
Chile
B.M. rosa
Tanabe Bay,
Japan
B.M. volcano
Tanabe Bay,
Japan
Sydney,
Australia
Breeds Mar to
May with temp
rising
Breeds July to
Oct at max temp
Some breeding
all year but main
peaks in late
autumn and early
spring
Breeds all year
but peaks in
spring and
autumn. Reaches
max size of 8 mm
in 35 days. Can
produce larvae
30 days after
settling
Reproduces all
year with max in
Nov to Dec and
July to Aug
B. venustus
B. vestitus
B. Austrobalanus
flosculus
B. Megabalanus
psittacus
Austromegabala
nus nigrescens
Sydney,
Australia
Uchiura Bay,
Japan
Notomegabalanu
s algicola
South Africa
Solidobalanus
hesperius
Sea of Japan
S.h. hesperius
Vladivostok
Wisely & Blick,

1964
Yasuda, 1970
St I 550200
Foster, 1967
egg 280160
St I 330140
Stefoni &
Contreras, 1979
Stefoni &
Contreras, 1979
111
egg 150(70 to
100)
St I 290140
Yamaguchi, 1973
St I 270150
Egan &
Anderson, 1987
Branch &
Griffiths, 1988
Ovsyannikova &
Levin, 1982
St I cultured
17785
Korn &
Ovsyannikova,
1981
Yamaguchi, 1973
B. crenatus (Crisp & Patel, 1969); B. eburneus (Landau, Finney & dAgostino, 1979); B. glandula (Hines,
1978); B. perforatus (Patel & Crisp, 1960b); Chthamalus fissus (Hines, 1978); Elminius modestus (Patel &
Crisp, 1960b); Pollicipes polymerus (Hilgard, 1960); Verruca stroemia (Barnes & Barnes, 1975).
Chthamalus stellatus breeds earlier at a lower than higher tidal level (Crisp, 1950) and is controlled by
temperature whereas Balanus balanoides breeds first at higher and later at lower levels (Crisp, 1959) and
may be controlled by light (Barnes, 1963) and possibly air temperature (Barnes & Barnes, 1976). It seems,
therefore, that breeding in intertidal species begins at the shore level having the longest exposure to the
changing controlling factors.
112
MARGARET BARNES
Temperature
A temperature shock has been suggested as a possible agent synchronising the fertilisation in Balanus
balanoides over a considerable section of the eastern North American coast. This may be the final stage of
long-term temperature changes which have ensured that all the gonads are available when conditions for
fertilisation are favourable. The timing of such conditions may vary slightly from year to year so a shock
device is essential to ensure that full advantage is taken of them each year. In general reproductive
processes are sensitive to temperature.
Some cirripedes will breed over a wide temperature range whereas others will not breed until a certain
critical temperature is reached; they are eurythermic or stenothermic, respectively. This critical temperature
may be above or below that of their natural environment for most of the year. Boreo-arctic species have an
upper temperature barrier and warm-water or tropical species have a lower temperature barrier. Temperature
may, therefore, set limits to reproduction and thus become ecologically important in the latitudinal
distribution of cirripedes. The effect of temperature may also enable two closely related species to exist in
the same region without being in competition. In Tanabe Bay, Japan, for example, Yamaguchi (1973) gives
the breeding season of Balanus (Megabalanus) rosa as March to May when sea-water temperature is rising
and that of B. (M.) volcano in July to October when temperatures are falling.
In those species with a lower temperature barrier to breeding, and living at the northern limit of their
distribution, once this barrier is crossed the whole population is released and may fertilise synchronously.
Such is the case in B. perforatus at Arcachon, France, released from a low critical temperature in May when
about 90% of the mature population fertilises. As more broods are produced throughout the summer the
synchrony is lost, because of individual variation between animals, until in October breeding ceases as the
temperature barrier is once again imposed (Barnes & Barnes, unpubl. obs.). Landau, Finney & dAgostino
(1979) found that by keeping B. eburneus at 8C (or below) they could prevent fertilisation for up to 12
months; when the low temperature barrier was removed fertilisation took place.
In northern latitudes where animals have an upper temperature barrier temperature, food, and light show
marked seasonal variations that are repeated more or less regularly. It is in these regions that cirripedes tend
to have restricted breeding cycles which in extreme cases are reduced to one per year. This breeding is
timed so that nauplii are released at the most favourable time when food is available for them (Barnes,
1957, 1962; Barnes, Barnes & Finlayson, 1963). B. balanus has a reproductive cycle very similar to that of
B. balanoides (Barnes, Barnes & Finlayson, 1963) but the timing is different even though both species
release nauplii about March to April. Crisp (1954) considers that a gradual fall in sea-water temperature in
the autumn and early winter initiates the final ripening of the gonads in a sublittoral species such as B.
balanus. Copulation then takes place at the appropriate time irrespective of any further external stimulus.
This may also be the case in other sublittoral species such as B. hameri. B. balanoides needs the shock
device because of its intertidal habitat and in the far north fertilisation must take place before the shores
become ice-bound. If B. balanoides is maintained above 10C and in continuous light fertilisation can be
prevented indefinitely; when the temperature is reduced to below 10C and the light to no more than 12
hours in 24 fertilisation takes place in about four weeks (Barnes, 1963; Tighe-ford, 1967).
In more tropical regions where temperature, light, and possibly food are more constant or only fluctuate
slightly around mean values, breeding might be expected to be asynchronous in a population. Within the
optimum temperature range and in relatively stable conditions there is some evidence of seasonal breeding
periods superimposed on a general continuous low level of reproduction, for example in Elminius modestus
and E. plicatus in New Zealand (Moore, 1944; Foster, 1967) and Chthamalus anisopoma in Baja California
(Malusa, 1986). Hines (1978) found temperature to be the controlling factor in the breeding of Balanus
glandula in California.
113
Latitude
The effect of latitude on the onset of breeding is difficult to separate from the effect of temperature and it
has been most extensively studied on Balanus balanoides in both Europe and North America. As mentioned
above boreoarctic cirripedes, whether intertidal or sublittoral, with their southern limits in northern Europe
normally have one main breeding season a year, for example, Balanus balanoides (Moore, 1935; Pyefinch,
1948), B. balanus (Barnes & Barnes, 1954), and B. hameri (Moore, 1935; Crisp, 1962). Crisp (1959) gives
dates of fertilisation for population of B. balanoides in Europe ranging from 50 to 80N. There is a trend
from north to south with fertilisation in Spitsbergen (Feyling-Hanssen, 1953) being two to three months
earlier than in the southwest of Britain. There is also a difference of some days between the east and west
coasts of Britain at similar latitudesprobably related to temperature. In eastern Canada at St Andrews,
New Brunswick, fertilisation of B. balanoides begins in October (Bousfield, 1954) whereas in the Hudson
Strait region it begins in September (Bousfield, 1955). In this region B. balanus also probably fertilises in
September (Bousfield, 1955).
In Frobisher Bay and Cumberland Sound there may be only one annual brood in B. crenatus as it is near
its northern limit (Bousfield, 1955); further south there are two. In Europe, B. crenatus (Pyefinch, 1948) and
Verruca stroemia (Barnes & Stone, 1973; Stone & Barnes, 1974; Barnes & Barnes, 1975) have one major
breeding period followed by several lesser ones during the season.
Warm-water species with their northern limits of distribution in Europe may have more than one breeding
cycle in the warmer months but the number is less than in the same species further south. For example,
Balanus improvisus produces two to three broods a season on the west coast of Sweden (Blom & Nyholm,
1961; Blom, 1965) but five to six in Florida (Weiss, 1948a). In their normal habitats warm-water species
may breed continuously as long as conditions are favourable, for example B. amphitrite in southern India
(Daniel, 1958; Pillai, 1958). Breeding in this species is seasonal in the warmer months in temperate regions
(Hudinaga & Kasahara, 1942; Sandison, 1954; Costlow & Bookhout, 1958; Wisely & Blick, 1964; Egan &
Anderson, 1986). Chamaesipho columna in the region of Sydney, Australia breeds for about six months of
the year with release of nauplii from June to October (Wisely & Blick, 1964) whereas in warmer waters at
Leigh in New Zealand there is some breeding throughout the year (Moore, 1944; Luckens, 1970, 1976).
Light
The uniformity of the date of fertilisation of Balanus balanoides in the same area each year suggests that
reduction in day length may be a controlling influence (Crisp, 1959). At the same latitude this is the one
factor that remains constant from year to year. This explains why animals in shaded situations as well as those
on the upper shore, in which light is reduced except when the opercular valves are open under water,
fertilise first. Older animals also have more opaque shells (and hence less light penetration) than young
ones; older animals fertilise first. The inhibition of fertilisation in B. balanoides by keeping them in
continuous light has already been mentioned above (Barnes, 1963).
Light probably becomes less important in species from southern regions. In central California, Hines
(1978) found that photoperiod had no effect on the reproduction of Chthamalus fissus and Balanus glandula.
Feeding
Orientation of adult cirripedes, particularly in those species that feed by holding their cirral net in the backwash
of water, can affect their ability to feed efficiently. In adverse feeding situations Otway & Underwood
(1987) found that there was no reduction in the number of Tesseropora rosea carrying egg lamellae nor in
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the weight of egg lamellae produced. There was, however, a reduction in body weight of the parents
presumably caused by some starvation due to non-efficient feeding. This agrees with the results of Page
(1983) on Pollicipes polymerus. Cimberg (1981) found a higher percentage of P. polymerus breeding at
higher than lower tidal levels although the maximum brooding activity was the same at both levels. Because
of the way this animal feeds those higher on the shore may be better stimulated to feed. Hines (1978) found
food to be the dominating factor in the breeding of Chthamalus fissus in California.
Barnes & Barnes (1967, 1975) have shown that the time at which egg lamellae are produced can be
controlled by feeding on Balanus balanoides and Verruca stroemia. In the latter species it is poor nutrient
conditions that cause breeding to cease in October at Oban in Scotland. As a result, during the subsequent
months all the population reaches the same reproductive state and the first fertilisation in the spring is
synchronous with 100% of the adults containing egg lamellae. Subsequent broods are not so synchronous
the second has 70% of the population with egg lamellae at the same time. Later broods are even less
synchronous so that by June or July breeding is asynchronous until it ceases in October. At this time the
temperature is still above that at which reproduction takes place earlier in the year (Barnes & Stone, 1973).
By feeding V. stroemia continously Barnes & Barnes (1975) showed that breeding could be maintained
asynchronously throughout the year.
In a cirripede producing more than one brood a year the time between the laying down of egg masses is
important. A longer time due to low food reserves would mean a reduction in the number of broods per
year. Hines (1978) has shown that a delay of up to five days between broods in Balanus glandula can
reduce the number of broods from six to five in the six months of the breeding season. As far as energy
budgets are concerned Wu & Levings (1978) have shown that in this species the production of eggs takes
second place after respiration followed by production of shell and body tissue.
Crisp & Lewis (1984) have listed the factors affecting the cold tolerance of B. balanoides as reduced
metabolism, reduced temperature, and reduced day lengthall factors associated with the onset of
fertilisation in this species (Crisp & Ritz, 1967). This resistance to cold protects both the parent and the
developing egg lamellae and is vital in northern regions. Increased feeding in the spring is sufficient to end
the cold tolerant state (Cook & Lewis, 1971). Tooke & Holland (1985) and Tooke, Holland & Gabbott
(1985) have compared cold tolerance in B. balanoides and Elminius modestus.
Moulting
Patel & Crisp (1961) found that in Balanus crenatus and Elminius modestus the moulting phase had no
detectable influence on successful copulation. In Balanus balanoides, however, animals which had recently
moulted appeared to copulate more readily than those that had moulted more than seven days previously.
The moulting cycle in all species is affected by the presence of egg lamellae as a period of reproductive
anecdysis follows copulation (Barnes, 1962). The length of this depends on the species. Moulting while egg
lamellae are present in the mantle cavity may be a disadvantage although it does occur in boreo-arctic
species which have long incubation times. In warm-water species which breed continuously the danger is
reduced if the incubation time falls within an intermoult period. This has been found to be so for B.
amphitrite, B. crenatus, B. perforatus, Chthamalus stellatus, Lepas anatifera, and Verruca stroemia (Patel &
Crisp, 1961). Hatching in these species removes the inhibition to further breeding since oviposition never
takes place while egg lamellae are pesent. It also removes any inhibition to moultingso that the animals
moult and are inseminated again. Thus, while able to copulate at any part of the moulting cycle, warmwater cirripedes probably do so most frequently immediately after a post-hatching ecdysis.
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Age and Size

The size reached by adult barnacles depends on the species and therefore the size at which maturity is
reached can only be compared intraspecifically. In warm-water species producing several broods a year
those settling early in the year will reach maturity and will themselves reproduce during that year. The age
of Chthamalus species when first reproductively active is variable. C. anisopoma in the Gulf of California
may be reproductively mature at an age of about six weeks (Malusa, 1986). C. fissus in California first
reproduces about two months after settlement (Hines, 1978). C. stellatus in Europe and C. fragilis on the
Atlantic coast of North America are about nine months old before they first reproduce (Connell, 1961;
Wethey, 1983).
The much larger warm-water Tetraclita does not reproduce until much older. T. stalactifera in the Gulf
of California does not reproduce until it is about 20 months old (Malusa, 1986). Villalobos (1980) found that
T. panamensis in Costa Rica did not reproduce until it was two years old, nor did T. squamosa rubescens in
California (Hines, 1978) and T. s. rufotincta in the Gulf of Elat (Achituv & Barnes, 1978a).
The age when first reproductive in Balanus species can vary from one to two months as, for example, in
B. amphitrite saltonensis (Linsley & Carpelan, 1961), B. trigonus (Werner, 1967), B. pacifica (Hurley,
1973), B. improvisus (Breeman, 1934; Blom, 1965), and B. eburneus (Grave, 1933) to one to two or even
three years as, for example, in B. balanoides (Runnstrm, 19241925; Barnes, Barnes & Finlayson, 1963),
B. balanus (Barnes & Barnes, 1954; Crisp, 1954), B. hameri (Moore, 1935), and B. restrains (Korn, 1985).
In B. balanoides populations of first year adults fertilise later than those consisting of older animals no
matter what the tidal level (Crisp, 1959).
Age can also affect the numbers of eggs produced by an adult. In the boreoarctic B. balanoides has only
one breeding season and animals can reach maturity at the end of their first season of growth. In the early
weeks after settlement food resources are used for somatic rather than gonadal growth and so only limited
gonadal material is available for reproduction at the end of the first year when adult basal diameter is 56
mm. Such animals of about 79 mm basal diameter produce only 200600 eggs whereas second year
animals of only 6 mm basal diameter produce about 4200 eggs in Passamaquoddy Bay, Canada. Thus, the
adults may be reproductively mature at the end of the first year but the number of eggs produced is only
about 10% of the number produced by older animals of a similar size (Arnold, 1977). Crisp (1954) found
that the weight of egg masses and number of eggs compared with the weight of the adult was less in small
(younger) animals than in larger (older) ones. There is also some indication of this in Elminius modestus
(Crisp & Patel, 1961). Age as well as size is therefore important in egg production.
Crowding
If breeding is connected with food supply then it seems that crowding of the adults, which could cause
competition for a limited food supply, might be expected to reduce breeding in some way. Crisp & Davies
(1955) and Crisp & Patel (1961) found that the onset of breeding in E. modestus was delayed in slower
growing crowded populations by about four weeks. It was also found that in such conditions the male
reproductive organs developed at a smaller size and egg lamellae were found in smaller animals than in less
crowded situations. Chthamalus dalli and Balanus balanoides produce more eggs per somatic weight when
crowded (Wethey, 1984).
Wu (1981) found however, that in B. glandula the incidence of cross fertilisation was not increased by
decreasing the distance between mature adults. The energy partition of individual barnacles depended on the
degree of crowding and this affected the energy channelled into egg production. Uncrowded B. glandula
with adequate energy transfer more into egg production than do crowded individuals (Wu, Levings &
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MARGARET BARNES
Randall, 1977; Wu, 1980; Wethey, 1984). In their first year B. glandula transfer about 50% of their energy
production into egg production; this ensures the propagation of the species and counteracts the high
mortality that the adults suffer in their first year after settlement (Wu & Levings, 1978). If the whole
population of B. glangula is considered, as distinct from individual animals, then in crowded populations in
which the animals may have become elongated the egg production per unit area is higher than in uncrowded
areas even though the animals in those areas may be contiguous (Wu, 1980). It should be mentioned that
this may not be of great ecological value as such over-crowded populations tend to be self-destructive
(Barnes & Powell, 1950).
Crisp (1964a) found reduced fecundity in high population densities of B. balanoides.
Seaweed cover
Crisp (1959) found that in B. balanoides local topography had an effect on the percentage of fertilised
animals. Fertilisation takes place first in animals at high levels on the shore and becomes progressively later
by about 12 days down the shore. Fertilisation was earlier on the underside of boulders, in crevices, and
under clumps of seaweed than in open situations although the differences of about three days were not so
great as those caused by tidal level. Jernakoff (1985) found that there was no reduction in the weight of egg
lamellae produced by Tesseropora rosea overgrown by seaweed compared with those free of cover in the
Cape Banks Marine Scientific Research Area of Australia. As this species can contain egg lamellae at all
times of the year the effect of cover on the date of fertilision was masked.
Salinity
The effect of salinity on the breeding season is particularly important in estuarine habitats where freshwater
run-off due to river discharge or monsoons is excessive at certain times of the year. In Indian estuaries and
harbours Balanus amphitrite amphitrite and B. a. hawaiiensis can breed throughout the year except during
the monsoon months when salinity is low (Paul, 1942; Daniel, 1954; Ganapati, Lakshmana Rao &
Nagabushanam, 1958; Pillai, 1958; John, 1964; Karande, 1967; Pillay & Nair, 1972; Fernando &
Ramamoorthi, 1975). B. variegatus also breeds throughout the year except at very low salinities during the
monsoon when the water is also very turbid. B. pallidus in the Vellar estuary does not breed during the
summer and early monsoon when salinity is high; there is a slight decrease in breeding during the height of
the monsoon at extremely low salinities. This agrees with Sandison (1966, 1967) who reports B. pallidus in
Lagos Harbour, Nigeria, as being sensitive to both low and high salinities.
In a West Indian mangrove swamp egg masses were found in most adult B. eburneus all the year. There
was no indication that the number of eggs was reduced during periods of low salinity but there was
evidence that the survival of the hatched nauplii depended on the salinity experienced by the parents during
the pre-liberation period (Bacon, 1971). In the Po estuary, Italy, breeding of B. eburneus is more influenced
by increase of fresh water than is that of B. improvisus (Relini, 1980; Relini, Matricardi & Diviacco, 1980;
Relini & Fasciana, 1982). In B. amphitrite communis in Kerala backwaters in India embryos can be held in
the egg lamellae in the mantle cavity of the adult during the rainy season until the salinity becomes more
favourable (Daniel, 1958; Pillai, 1958); this was confirmed experimentally. Khl (1966) found that at
Cuxhaven, Germany, B. improvisus would not breed in salinities below 5%o which agrees with the increase
of this species in the Baltic when salinity increases to 6%o in some years. Chthamalus malayensis and C.
withersi do not breed during the low salinity periods of the monsoons in July to September in India
(Karande, 1967).
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Bergen (1968) found that egg lamellae of Balanus glandula were less tolerant than adults to reduced
salinity. They are, however, protected from low salinity because the adults close their opercular valves in
50% sea water. Crisp & Costlow (1963) investigated the effect of salinity on the in vitro development of
egg lamellae in B. eburneus, B. amphitrite amphitrite, and Chelonobia patula; at salinities between 15 and
25%o and between 40 and 60%o development of egg lamellae was delayed and hatching was impaired.
Pollution
A direct effect of pollution on egg production was found by Rege, Joshi & Karande (1980) in Balanus
amphitrite amphitrite at Bombay, India. The time of the breeding season was not affected but in an animal
of 1.3 mg oven dry body weight the number of eggs produced was reduced from 4607 in an unpolluted
control area to 3458 and 2710 in a moderately and highly polluted area, respectively. Wu & Levings (1980)
also found reduced egg production in B. glandula due to bleached kraft pulp mill effluent in British Columbia.
Crisp (1959) found that B. balanoides in stagnant or polluted water fertilised earlier than might be expected
because of their lower metabolic rate compared with animals on wave-exposed shores.
Parasites
Johnson (1958) found a marine fungus, Lagenidium chthamalophilum parasitic on the eggs of Chthamalus
fragilis var. denticulata. Early stage eggs may be completely destroyed leaving a mass of egg cases filled
with fungus mycelium. If, however, the egg lamellae are more mature and the embryos differentiated then
some embryos escape infection and hatch normally. Lagenidium callinectes has been found in egg lamellae
of Chelonibia patula by Johnson & Bonner (1960). Echiniscoides sp. feeds on egg lamellae of Chthamalus
malayensis (Karande, 1967). Peltogaster paguri, a rhizocephalan cirripede, may be rendered sterile by the
presence of a female Liriopsis pygmaea (Reinhard, 1942b).
Parasitic castration caused by association with gregarian protozoans and an isopod Hemioniscus balani
has been reported by several workers (Henry, 1938; Barnes, 1953; Sandison, 1954; Crisp, 1968b). Species
susceptible to such infection include Balanus algicola, B. amphitrite amphitrite, B. balanoides, B. balanus,
B. glandula, B. hameri, B. improvisus, Chthamalus dalli, C. dentatus, and Eliminius modestus (Crisp,
1968b). Although Sandison (1954) found as many as seven female Hemioniscus in one Balanus algicola
she found no apparent deleterious effect. This is unexpected and is not in agreement with Crisp (1968b).
Barnes (1953) found that release of nauplii was delayed in a B. balanus heavily parasitised by a protozoan
but the nauplii themselves were unaffected when teased out into sea water.
RELEASE OF EMBRYOS
The actual hatching of cirripede eggs is not within the scope of this article. What is of interest here is the timing
of the release of nauplii. The terms nauplii and release of embryos are preferred to the commonly used
spawning because in many invertebrates spawning refers, as it should, to the release of gametes. The use
of the word spawning to describe the release of embryos in cirripedes has led to confusion and some
misunderstanding.
The time of release can vary within the same species depending on its habitat and geographical
distribution. At Leigh in New Zealand Luckens (1970) found that Chamaesipho brunnea released nauplii
during periods of spring tides, stormy weather, and rough seas. Although eggs may have been ready to hatch
release was withheld during neap tides and in calm weather.
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MARGARET BARNES
More often release is tied to the presence of plankton in the sea water thus ensuring that the nauplius
stages have adequate food supplies. Thus, in Chthamalus challengeri near the northern limits of its
distribution at Hakodate, Japan, release is in March to April at the time of a diatom outburst in that region
(Iwaki, 1975). Korn (1985) reports a similar finding for Balanus rostratus in Peter the Great Bay, Sea of
Japan. Fertilisation of the population is in the latter part of September and October, incubation lasts about
two weeks and nauplii are found in the plankton in late October to December during an autumn bloom of
Skeletonema costatum.
Most information is, as usual, available for Balanus balanoides. In this species there is a long time
between fertilisation and release of nauplii and the embryos are ready to hatch long before there is a diatom
outburst. This readiness is obvious from the in vitro development of egg lamellae as found by Barnes &
Barnes (1963). In nature there must, therefore, be some inhibiting factor preventing release until external
conditions are favourable. This inhibition is removed once the adult animals start to feed in the spring. In
European waters there is a diatom bloom in the spring and the release of nauplii is initiated to coincide with
this (Runnstrm, 192425; Barnes, 1957). Delay of a few weeks in the outburst can cause a similar delay in
the release of the barnacle nauplii (Barnes, 1956, 1957, 1962). At Woods Hole, USA fertilisation is slightly
earlier than in Europe and the embryos are ready and are released in late autumn because here there is
abundant planktonic food available throughout the winter (Barnes, 1959; Barnes & Barnes, 1959a).
In regions where the intertidal region of the shore is not permanently frozen during the winter B.
balanoides nauplii are released first from animals on the upper shore followed by those on the lower shore a
little later. In areas where the intertidal area is permanently frozen for several months each winter the
animals at the upper levels will remain frozen longer than those at the lower levels. The development of the
egg lamellae on the upper shore may, therefore, be arrested, and more so in colder than in less cold winters,
because the parents are frozen. The onset of spring feeding by the adults will also be delayed compared with
those on the lower shore. In such cases the animals on the lower shore release their nauplii first. Such
conditions are found in the Murman region of Russia (Rzepishevsky 1959, 1962). Release here also
coincides with the phytoplankton increase in spring.
Shore and sea ice can also affect the reproductive timing in B. balanoides in Greenland and Spitsbergen.
In Greenland animals fertilise from August to the end of October depending on the place and release begins
in March and may continue until August. In some places it may not even start until July and in extreme
conditions some nauplii may not be released at all in that year. Embryonic development has to be completed
before the formation of the ice foot and there can be no release until it has broken away (Hpner Petersen,
1966). A whole generation can also be lost at Spitsbergen if severe local conditions prevent release of
nauplii so long that there is no time to complete the life cycle and fertilise before the onset of the next
winter (Feyling-Hansen, 1953).
EGGS
The number of eggs produced, their size and shape as well as their chemical composition are all of interest.
Chemical composition
Several studies have been made of the biochemistry of cirripede eggs: B. balanus and B. balanoides
(Barnes, 1965; Dawson & Barnes, 1966; Barnes & Evens, 1967; Barnes & Blackstock, 1975); Chthamalus
stellatus (or probably C. montagui) (Achituv & Barnes, 1976); Balanus perforatus, Pollicipes cornucopia,
and Tetraclita squamosa rufotincta (Achituv & Barnes, 1978b; Gilboa-Garber, Achituv & Mizrahi, 1983);
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Chthamalus dentatus and Octomeris angulosa (Achituv & Wortzlavski, 1983); Pollicipes polymerus
(Eastman, 1968). The oxygen uptake of the egg lamellae of Balanus balanoides and Pollicipes polymerus
has been discussed by Barnes & Barnes (1959b). Lucas & Crisp (1987) were principally concerned with
energy metabolism of Balanus balanoides eggs during embryogenesis. Detailed consideration of these
papers is, however, not within the scope of this article.
Number of eggs
Barnes & Barnes (1968) defined some of the terms used in discussing reproduction in cirripedes. Egg
number denotes the total number of eggs in the egg lamellae carried by an adult at any one time. In
crustaceans this is a function of the size of the parent. Comparisons should therefore be made between
animals of the same size. From graphs relating egg number to size of parent a standard animal can be
arbitrarily selected for the purposes of comparison. The number of eggs produced by such a standard animal
can be used to compare environmental conditions within a restricted habitat or over widely separated
regions.
The term fecundity is often used loosely but in the case of cirripedes it is best defined as the number of
eggs produced per standard animal per unit time when comparing the same species or, when comparing
different species, as the number of eggs produced per unit time by a given increment of body tissue. Other
conditions being constant this number will be inversely proportional to egg size. Thus, per unit body weight
increment the fecundity of Chthamalus stellatus is several times greater than that of Balanus balanoides.
When populations are concerned the age structure must, amongst other factors, be considered so that the
population fecundity of Chthamalus stellatus compared with that of Balanus balanoides and possibly B.
perforatus and Elminius modestus at equal population densities is lower because of its smaller adult size
(Barnes & Barnes, 1968).
In both Pollicipes polymerus and Chthamalus fissus the reproductive effort increases with lower tidal
level. Usually, however, most C. fissus are found above this level because of poor survival at lower levels.
The higher reproductive effort of which this species is capable at low levels may be to offset the high
mortality (Page, 1984). In central California Hines (1974) found that the weight specific fecundity of C.
fissus was higher than in Balanus glandula or in Tetraclita squamosa in that order, but that fecundity over
an individuals life is highest in T. squamosa followed by Balanus glandula and then Chthamalus fissus, yet
population fecundity was highest in C. fissus followed by Balanus glandula and then Tetraclita squamosa.
Of the three species Balanus glandula was only highest in population reproductive productivity followed by
Tetraclita squamosa and then Chthamalus fissus.
Using the volume (V) of the egg just prior to hatching or that of the stage I nauplius and the number (N)
of eggs produced per 50 g oven dry body weight, Barnes & Barnes (1968) used NV values for a range of
species from different habitats to compare the relative weights of eggs produced per standard increment of
body weight. This emphasised the contrast between boreo-arctic species with NV values between 1500
and 3500 and those of less than 500 for all other species tested. In order to compare what Barnes & Barnes
(1968) called the metabolic efficiency of egg production but what Hines (1978) prefers to call
reproductive output or reproductive effort the product NVB should be used, where B is the number of
broods produced by an animal per year. Barnes & Barnes (1968) thought that metabolic efficiency of a wide
variety of species was similar. From the data collected in the intervening years it is now known that
reproductive effort can vary within a species in different habitats and also between species (Hines, 1978;
Page, 1984). Chthamalus fissus has a high reproductive effort and a rapid response to available food.
Pollicipes polymerus, on the other hand, reacts more slowly, perhaps because of its specialised feeding
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MARGARET BARNES
behaviour (Barnes & Reese, 1959, 1960), and has a lower reproductive effort (Page, 1984). It behaves more
like Tetraclita squamosa rubescens (Hines, 1978). These last two species channel more energy into a large
adult before reaching maturity and so have to use more energy to maintain that size at the expense of
reproduction.
Cirripedes incubate their eggs in the mantle cavity and so it is obvious that the volume of this cavity must
regulate the number of eggs that can be accommodated. Animals with the same weight of soft tissue but
thick shells will have a smaller space for egg lamellae than thinner walled animals of the same basal
diameter. Some of the mantle cavity in both cases will be occupied by the prosoma and muscles. Species
that remain small can only increase the number of eggs produced by reducing the egg size or by increasing
the number of broods produced in a lifetime.
The number of eggs produced may be influenced by latitude as well as the position of the adults in the
intertidal zone (Crisp, 1959; Barnes & Barnes, 1965, 1968; Cimberg, 1981; Lewis & Chia, 1981). In the
East and South China Sea Cai Rusing & Huang Zongguo (1981) found that the number of eggs in Balanus
reticulatus depended on temperature as well as on shell diameter. Arnold (1977) said that B. balanoides in
Passamaquoddy Bay, Canada, produces more eggs than the same species in Europe giving figures of 4200
for an animal of 6 mm diameter and 19 000 for one of 19 mm diameter. No mention was made of the oven
dry weight of these animals. The figures quoted by Barnes & Barnes (1968) were adjusted to 1.5 mg oven
dry body weight so that they were all comparable. An animal of about 6 mm basal diameter would have this
body weight and so the figure of 55008000 for Millport, Scotland is greater than that given by (1977) and
4200 for animals further north at Corpach, Scotland is about the same as Arnolds. Egg number in this
species varies with shore level, from place to place, and from year to year. There is also considerable
individual variation and so care is needed when making comparisons. Optimal egg numbers seem to be
reached, where conditions are fully marine but where there is some protection, even at the southern limits of
its distribution in Spain (Barnes & Barnes, 1968).
B. pacificus is found on small objects on sandy bottoms in California and Baja California and matures in
two to three months at a basal diameter of 10 mm. Egg lamellae of a single brood contain on the average 15
000 eggs and are ready for release in 8 to 11 days. Hurley (1973) calculates that this barnacle is capable of
producing 23 to 33 broods a year; at an average of 28 this amounts to 420 000 eggs per year; no egg size is
given. This enormous annual egg production is no doubt related to the rather hazardous existence of the
adult and ensures that at least a few cyprids may find a suitable settling site.
Egg size and shape
The size and shape of cirripede eggs has recently been reviewed by Crisp (in press) and little can be added
to his summary. He lists the volume of a series of cirripede eggs including and extending those given by
Barnes & Barnes (1968). The egg increases in size during development of the contained embryo and when
comparing egg sizes in the considerable literature available care must be taken to use data referring to the
same stage of development. This is not always possible as the stage may not be given. Sometimes only the size
of the first nauplius stage is available and so that rough comparisons can be made this may be assumed to reflect
closely that of the final egg size before hatching (Groom, 1894; Barnes & Barnes, 1968).
Apart from the stage of development of the embryo, temperature, genetic differences, individual variation,
and variations within an egg lamella can affect the size of the egg within a species. Variations within an egg
lamella are really differences in stage of development as eggs at the outer edges of large lamellae, having
more access to oxygen, tend to be further advanced, and hence larger, than those in the centre.
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Crisp (1959) and Barnes & Barnes (1965) have discussed the influence of temperature on egg size and
have recorded differences due to latitude in B. balanoides. Barnes & Barnes found the largest (396 m long)
eggs of this species at Murmansk and the smallest (263314 m long) in Great Britain. Within these
extremes the relationship of egg size and latitude is not close. Animals from places with severe winters
(during which the embryos are developing) have large eggs irrespective of latitude. For example, eggs at
Murmansk (6900N) were 396 m long and those at St Johns, Newfoundland (4734N) were 386 m long.
Sizes (348 m long) at St Andrews on the Canadian eastern coast (4505N) were similar to those (356 m
long) at Disko, Greenland (6920N). These places all have severe winters compared with Great Britain. In
areas with less severe winters, after taking any local variations into account, there is little connection
between latitude and egg size. For example, at Pornic, France (4707N) the egg length was 282 m which
comes within the range found in Great Britain some 10 degrees of latitude further north. It seems that eggs
of B. balanoides are largest where winters are severe and summers relatively cold irrespective of latitude.
Latitude has not been shown to have a striking effect on the size of eggs of Chthamalus stellatus (Barnes
& Barnes, 1965) in Europe; sizes range from 158186 m long at latitudes from 36 to 48N. At the extreme
northern limit of this species in Fair Isle (5932N) Powell (1954) quotes a length of 230 m. The size of C.
dalli eggs is given by Barnes & Barnes (1965) as 183 m long on the Pacific coast of North America (about
40N) and by Korn & Ovsyannikova (1979) as 218 m long at Vladivostok (43 N) at about the same
latitude. Given adequate food in controlled experiments Patel & Crisp (1960b) found that temperature
affected egg size in several warm-water species. Under these conditions the animals were breeding
continuously and an increase in temperature caused a decrease in egg size. Lucas & Crisp (1987) explained
this as an increase in the metabolic rate of eggs during development resulting in extra consumption of food
reserves.
Crisp (in press) regards the egg size of Balanus balanoides as being genetically controlled in the
different races of this species but taking the animals at Boothbay Harbor, Maine, as typical of the
American E.coast race seems to neglect the obvious differences found in egg size and rate of embryonic
development found by Barnes & Barnes (1965, 1976) for this species further south on the American coast.
Barnes & Barnes (1965) found that within limits larger B. balanoides (up to about 10 mm basal diameter)
produced larger eggs. Crisp (in press) has shown that it is the relative amount of tissue available for egg
production that determines the egg size. At Boothbay Harbor small animals in probably poor nutrient
conditions had smaller eggs than larger animals but at Menai Bridge, North Wales, in good nutrient
conditions egg size was the same throughout the size range of adults.
Eggs of boreo-arctic species are large compared with practically all others; there are a few exceptions
that will be mentioned later. This large size is mainly an adaptation to boreo-arctic conditions and the
survival value of producing a large nauplius capable of dealing with the available planktonic food (Barnes &
Barnes, 1965). Crisp (in press) suggests that it may also be related to greater dispersal of larvae having a
long planktonic life and the time needed to find suitable substrata for settlement. Moyse & Knight-Jones
(1967) say that the smaller eggs in warm-water species are related to shorter planktonic lives and probably
the quick turnover of food supplies by adults producing numerous broods per year.
Although many cirripede nauplii are pelagic and planktotrophic some are pelagic and lecithotrophic while
some are merely lecithotrophic and develop to the cyprid stage within the mantle cavity of the parent.
Animals producing lecithotrophic nauplii usually produce broods of fewer than usual eggs of a larger size
than normal. The rhizocephalans are an exception. The eggs are small and numerous. Cyprids of these parasitic
cirripedes do not, however, need excessive reserves of yolk because as soon as a suitable host is found for
settlement then ample nutrient is available for further development. Many of the acrothoracicans also have
lecithotrophic larvae but the eggs are much bigger and fewer in number than in the rhizocephalans.
122
MARGARET BARNES
In the Thoracica several species produce lecithotrophic larvae. In the Lepadomorpha Ibla quadrivalvis
(Anderson, 1965), I. cumingi (Karande, 1974a; Klepal, 1985) and I. idiotica (Batham, 1945a) are all known
to have large eggs and only relatively few per brood. Anelasma squalicola (Darwin, 1851; Hoek, 1909,
Krger, 1940) has a very large egg of about 500 m length, much larger than in other Heteralepadoidea
(about 200 m in length). All the deep-water Scalpellum and Acroscalpellum species on which there is
adequate information form lecithotrophic larvae. Pollicipes (Mitella) spinosus (Batham, 1946) has a very
large egg (690 m long) immediately before release of larvae compared with about 250 m length in
planktotrophic P. polymerus and P. cornucopia. P. spinosus also produces far fewer eggs per brood.
In the Balanomorpha there are striking examples of lecithotrophy in the Coronuloidea in Tetraclita
species. Three species produce lecithotrophic larvae while the rest, as far as is known are planktotrophic.
The three exceptional species are T.squamosa rufotincta (Achituv & Barnes, 1978a; Barnes & Achituv,
1981), T. (Tesseropora)pacifica (Crisp, 1986), and T. divisa (Nilsson-Cantell, 1921; Anderson, 1986). The
volume of the egg of T. squamosa rufotincta when ready to hatch is ml compared with ml for T. squamosa,
ml for T. rubescens, and ml for T. serrata. It also greatly exceeds that of boreo-arctic species such as B.
balanoides and B. balanus with volumes of and ml, respectively (Barnes & Achituv, 1981).
The shape of a cirripede egg has been dealt with fully by Crisp (in press). Suffice it to say here that the
general shape is ovoid with the variable short diameter being longer at one end than the other giving a
tapering shape. Eggs producing lecithotrophic larvae are much more globular than those giving
planktotrophic larvae presumably due to the yolk reserves carried in the former right through to the cyprid
stage and maybe beyond. The increased amount of yolk retards the rate of embryonic development
(Anderson, 1965). At 23C Ibla quadrivalvis eggs take about 17 days to hatching and at 14 15C those of
Pollicipes spinosus take about 32 days. In contrast Balanus perforatus and B. eburneus eggs produce
planktotrophic larvae and take about 8 and 11 days, respectively at 15C.
CONCLUSIONS
In order to exist an animal must reproduce itself successfully. Models of reproductive methods in marine
benthic invertebrates proposed by Vance (1973a,b) have caused some controversy (Underwood, 1974;
Vance, 1974). Steele (1977) and Strathmann (1977) have attempted to resolve the arguments. In nature,
however, things are always more complicated and interrelated; the situation in cirripedes is no exception.
Steele & Steele (1975) report that in crustaceans egg size and duration of embryonic development are
correlated. This is often the case in cirripedes.
At high latitudes with low environmental temperatures optimal conditions for larval life and survival of
young adult barnacles is short. The time of releasing larvae is critical and must be timed to coincide with the
spring outburst of phytoplankton. Only a single brood can be produced each year because a second brood
cannot be reared successfully as young would be released when conditions were unfavourable. In the far
north ice-bound shores limit the time available for fertilisation and embryonic development. Large eggs
ensure that sufficient nutrient is available during the long period waiting for optimal conditions for release
when the ice thaws. Smaller eggs are produced at low latitudes where temperatures are higher and
favourable conditions last longer. Embryonic development is quicker and there is no delay in release of
nauplii except in a few cases, for example where there is a sudden drastic reduction in salinity. Many broods
can be produced in quick succession providing adequate food is available and other environmental
conditions remain favourable.
The production of many broods increases the chance of reproductive success especially in cases where a
whole generation may fail or where there is excessive predation of the planktonic stages. Such prdation can
123
be avoided by incubation to the cyprid stage within the mantle cavity or the reduced necessity of a long
planktonic life because the adults provide the eggs with sufficient nutrient to carry the young through until
metamorphosis, that is, the larvae are lecithotrophic. This mode of life seems to have been developed
independently in several groups of cirripedes and almost always with some advantage to the species
concerned or as an adaptation to the local environment. It usually means the production of much larger eggs
to accommodate the large amount of stored yolk. As has been said above this is not necessary in
rhizocephalans. Lecithotrophy is no doubt an advantage in deep-water species such as Acroscalpellum and
Scalpellum. In these species an abbreviated nauplius development within the mantle cavity is also an
advantage. The cyprid when released remains in the vicinity of the parent group; restricted dispersal in a
habitat with few suitable substrata for settlement is advantageous.
At first it is not why the three species of Tetraclita should behave differently from conspecifics which
produce the usual planktotrophic larvae. Achituv & Barnes (1978a) thought that the large nauplii of T.
squamosa rufotincta might be an adaptation to feeding on large particles such as may be the case in boreoarctic species. Barnes & Achituv (1981) found, however, that the nauplii did not feed and compared them with
other non-feeding nauplii. This species and T. (Tesseropora) pacifica (Crisp, 1986) live in the vicinity of
coral reefs and where the water is very and nutrients are limited. The lecithotrophic nauplii seem, therefore,
to be an adaptation to environmental conditions. That this is extended further to an abbreviate nauplius
development in T. divisa may be because planktonic dispersion would be a disadvantage in this insular and
cave-living species (Crisp, 1986). According to Anderson (1986) the cyprid of this last species contains no
yolk reserves and immediate settlement in the vicinity of the parent stock is favoured. Although this species
is insular it is also circumtropical, thus dispersal must be by adults attached to floating objects. Rapid
settlement of newly released cyprids will then ensure quick colonisation of any new sites.
In Anelasma squalicola the abbreviate nauplius development ensures that cyprids when released are in
the immediate vicinity of a suitable substratum, in this case members of the same shoal of fish.
Lecithotrophy in Ibla species presents a problem unless it is again connected with lack of nutrients in the
water such as with I. cumingi at Elat. Moyse (1987) has suggested that it may be habit carried over from an
earlier deep-sea existence.
From the foregoing it is evident that in cirripedes, egg production, egg sizes and numbers as well as
number of broods produced and the breeding cycles and seasons cannot be divorced from the life style and
general ecology of the animal concerned.
ACKNOWLEDGEMENTS
It is a pleasure to acknowledge the help of many colleagues, particularly Univ. Doz. Dr W.Klepal, in the
preparation of this review. Miss E.Walton and Miss R.Gow helped in tracing some of the references and
ProfessorD. J.Crisp supplied me with a proof of his paper on the shape and size of cirripede eggs. I appreciate
the care taken by Mrs M.Fletcher in the typing of the manuscript.
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133

BIOLOGY OF MARINE HERBIVOROUS FISHES*

MICHAEL H.HORN
Department of Biological Science, California State University, Fullerton, California
92634, and Ocean Studies Institute, Long Beach, California 90840, USA
ABSTRACT iF s hes that feed on benthic algae occur as solitary individuals, members of roving
groups or defenders of territories containing their algal food. They may be broadly classified as
browsers or grazers , the latter if sediment is ingested during feeding. nO tropical re efs, the
Acanthuridae, Scaridae, Siganidae, and oP macen tridae have abundant and ecologically important
herbivorous members. In temperate waters the Aplodactylidae, G irellidae, dO acidae, and
Stichaeidae contain or consist solely of plant-eating species. The K yphosidae and Sparidae contain
herbivorous species in both temperate and tropical waters. uN merous herbivorous fishes select
relatively tender and palatable algae, and apparently are deterred by combinations of
morphological and chemical defences found in many seaweeds. N evertheless, some species
regularly consume tough and chemically defended seaweeds.
H erbivorous fishes can assimilate algal material, but few growth studies have been done. M ost
herbivores have longer guts than carnivores and relatively high ingestion rates and fast gut transit
times. Several species, however, feed more intermittently and retain food longer. H erbivorous
fishes apparently do not produce cellulases to break down plant cell walls but gain access to the
contents by lysing the cells in a highly acidic stomach, grinding the food in a muscular stomach
or pharyngeal mill or harbouring microbes that ferment the food in a hindgut caecum. eH rbi vorous
and detritivorous fishes maintain large populations on their low protein diets and have evolved
several specialisations similar to those of terrestrial herbivores to cope with the low nitrogen
content of their diets.
rF e e-ranging herbivorous fishes, especially surgeonfishes and parrotfishes, markedly affect
coral reef ecosystems by contributing to erosion and sedimention as well as affecting the
abundance and composition of benthic algal communities. Because of their mobility these fishes
decrease the spatial variability of herbivore effects on community structure but often appear to
have smaller local effects on seaweed communities than grazing s ea urchins. Territorial
damselfishes by defending and maintaining algal patches strongly affect the abundance, diversity,
and productivity of seaweed communities on coral reefs. iL mited evidence suggests that
herbivorous fishes might also influence community structure of temperate algae.
BIOLOGY OF MARINE HERBIVOROUS FISHES
135
H erbivores constitute a small proportion of marine fishes and most are eP rci formes, a large and
almost certainly polyphyletic assemblage of teleosts. They are largely confined to coastal habitats
between 40N and 40S and are so mewhat more diverse in southern rather than northern temperate
habitats. Inexplicably, herbivorous fishes are more species-rich in tropical than in temperate
waters. aL ti tudinal differences in abundance (density) are less obvious, but too few data are
available to draw any conclusions about reasons or consequ ences.
INTRODUCTION
Fish herbivory in the sea is an important ecological subject because the trophic interactions at the base of
food webs, the energetic requirements and physiological capabilities of fishes and the role of fishes in the
flow of energy through marine communities are involved. A diet of seaweeds or seagrasses confers on
fishes a set of basic physiological problems that has made fish herbivory an intriguing and provocative topic
for a continuing series of investigators. Like other herbivorous animals, plant-eating fishes face seemingly
formidable difficulties concerning the quality of, and access to, the nutrients available in the seaweeds they
consume. Animals have much greater nitrogen requirements than plants and also use nitrogen less
efficiently (Mattson, 1980). Therefore, herbivores must consume relatively large quantities of food and
assimilate it efficiently in order to meet their nitrogen (and energy) requirements (Mattson, 1980; Crawley,
1983). These challenges are hard to meet partly because plants, as stationary organisms, defend themselves
against herbivore attack in a variety of ways and partly because plant nutrients are components of, or are
contained within, relatively indigestible cell walls.
Several major questions surround herbivory by fishes in the marine environment, and consideration of
these questions forms the framework of this review. They are as follows. (1) How do herbivorous fishes
select their diets from an array of seaweeds (and seagrasses) that vary in availability, nutritional quality,
thallus (leaf) toughness, secondary chemistry, and digestibility? (2) How do these fishes obtain an adequate
diet from a food source relatively low in nitrogen and, hence, protein? In other words, what morphological
and physiological specialisations allow herbivorous fishes to gain access to and assimilate the nutrients locked
inside plant cell walls? (3) What ecological impacts do herbivorous fishes have on seaweed populations and
on nearshore marine communities in general? (4) Why are there so few strictly herbivorous fishes in
temperate and polar latitudes as compared with tropical latitudes? To consider these questions, the review is
divided into four main sections: (1) Food and feeding; (2) Digestion and digestive mechanisms; (3)
Ecological impacts; and (4) Distribution, diversity and abundance. The protein requirements of herbivorous
fishes and the evolutionary responses of herbivorous fishes to nitrogen shortage form two additional
sections that complete the review.
A few definitions and restrictions are necessary at the outset to provide the boundaries for the review.
Coverage is limited to those species of marine fishes that consume benthic plants: macroalgae (seaweeds),
diatoms or seagrasses. Fishes that feed on phytoplankton are not included except where their mention
contributes in a comparative way to the herbivores of interest. Emphasis is placed on fishes that appear to be
dependent on seaweeds, diatoms or seagrasses for most of their energy and nutritional requirements during
at least part of their life histories. This focus is qualitative and imprecise, however, because fishes in general
are often catholic and notoriously opportunistic in their food habits. Nevertheless, it is important to try to
*Contribution No. 61 from the Ocean Studies Institute
136
MICHAEL H.HORN
limit discussion to those fishes feeding primarily on the plant end of the food spectrum; otherwise, the
review grades into an appraisal of omnivores, which are common in many coastal marine habitats (Bakus,
1969).
What topics have been emphasised to date in studies of marine herbivorous fishes? The literature on
marine fish herbivory is far less voluminous than that on terrestrial herbivores, especially insects and
mammals, but also less so than that on marine invertebrate herbivores, particularly sea urchins and
gastropod molluscs. Among the reasons for the latter disparity, aside from the abundance and ecological
importance of these two invertebrate groups, is that fishes are more mobile and therefore more difficult to
study. The advent of SCUBA and related diving gear and techniques, however, has led to rapid
developments in the in situ study of coastal fishes, especially on coral reefs (Sale, 1980), where herbivorous
fishes are particularly abundant and diverse. Studies of fish communities in tropical waters (e.g. Hiatt &
Strasburg, 1960; Randall, 1967; Hobson, 1974) included accounts of the feeding behaviour and food habits
of the herbivorous components and recognised that although herbivorous fishes made up a minor proportion
of the total diversity, they were often among the most abundant species. In temperate waters, true
herbivores have been viewed as rare or non-existent in both earlier (e.g. Quast, 1968) and more recent (e.g.
Moreno & Jara, 1984) studies of temperate-zone fish assemblages even though several species were found
to contain substantial amounts of macroalgae in their stomachs. The notion has prevailed until very recently
that even fishes whose guts were packed with seaweeds were not digesting the algal material but actually
gaining their nutrition from the epibionts on the plant surfaces (e.g. Wheeler, 1980). Only in recent years
has it become apparent that year-round herbivores occur in the temperate waters of both the northern (e.g.
Horn, Murray & Edwards, 1982) and southern (e.g. Russell, 1983) hemispheres and that fishes from both
regions can digest macroalgae (e.g. Edwards & Horn, 1982; Anderson, 1987). It is of interest that
herbivores in the southern hemisphere, especially in the waters around New Zealand and southern Australia,
are more diverse than those in the northern hemisphere (e.g. see Burchmore et al., 1980; Stephens & Zerba,
1981) and make up large proportions of the total fish biomass of rocky reef communities (e.g. Russell, 1983).
In the last decade, an increasing number of studies have shown that herbivorous fishes in tropical waters,
particularly on coral reefs, have profound influences on individual seaweed populations and community
structure (e.g. Hixon, 1986). Damselfishes, in particular, have been shown in a continuing series of papers
to have a marked effect on the abundance and species composition of seaweeds in their territories (e.g.
Hixon, 1983). Also in tropical waters, the morphological and chemical defences of seaweeds have been
intensively studied of late and shown to affect strongly the food selection of certain herbivorous fishes (e.g.
Hay & Fenical, 1988). Greater recognition has been given in recent years to the differences in herbivore
diversity in temperate compared with tropical latitudes (e.g. Choat, 1982; Gaines & Lubchenco, 1982;
Thayer et al., 1984), but little progress has been made in providing and testing explanatory hypotheses.
Although anatomical specialisations of herbivorous fishes have long been recognised (e.g. Suyehiro, 1942;
Al-Hussaini, 1947) and their digestive physiology generally summarised more recently (e.g. Kapoor, Smit &
Verighina, 1975; Lobel, 1981; Pandian & Vivekanandan, 1985), much remains to be known about the
physiological and biochemical mechanisms by which fishes break down and absorb seaweed material. The
synthesis of cellulolytic enzymes by fishes remains unproven (see Lewis & Peters, 1984; Urquhart, 1984),
but a microbial fermentation system is known to occur in at least two herbivorous fishes (Rimmer & Wiebe,
1987). Greater knowledge of the digestive physiology of herbivorous fishes may be a key to understanding
the differences in diversity and abundance of these species in tropical and temperate habitats (Clements &
Bellwood, 1988).
To my knowledge, this review represents the first attempt to provide a comprehensive account of marine
fish herbivory on a worldwide basis. Previously published review articles on herbivorous fishes have
137
concentrated either on their ecological roles (Ogden & Lobel, 1978; Hixon, 1983) or their digestive
mechanisms (Lobel, 1981). Many other reviews that were focused on larger or peripheral topics such as
plant-herbivore interactions (e.g. Lubchenco & Gaines, 1981; Gaines & Lubchenco, 1982; Hay & Fenical,
1988), fish feeding (e.g. Hyatt, 1979; Choat, 1982; Hixon, 1986) and fish digestion and energetics (e.g.
Kapoor et al., 1975; Brett & Groves, 1979; Fange & Grove, 1979; Pandian & Vivekanandan, 1985) have
included information on herbivorous fishes.
FOOD AND FEEDING
Even though most herbivorous fishes consume a variety of seaweeds, they still must select from dozens to
hundreds of the different plant species available to meet their nutritional requirements. How is this
accomplished and what are the outcomes of the process? In the words of Howe & Westley (1988), few
questions in ecology are of more fundamental and practical interest than why do different herbivores eat
different plants? Food choice is still poorly known for fish herbivores but deserves further attention
because, for example, preferences often determine (Lubchenco & Gaines, 1981) the role of the animal in
community organisation. This section considers the feeding behaviour of herbivorous fishes, their food
habits and preferences and the factors influencing diet selection.
FEEDING BEHAVIOUR
Fishes that eat algae usually have short, blunt snouts with closely set teeth that form a cropping edge
(Ogden & Lobel, 1978). In their extreme form, the teeth are fused to form a beak as in the parrotfishes
(Scaridae), most of which bite into the inorganic substratum and obtain algal mat and endolithic algae
(Ogden & Lobel, 1978). Odacids (Odacidae) use the beak to bite pieces out of the thalli or reproductive
structures of laminarian and fucoid algae (Clements, 1985; Clements & Bellwood, 1988).
Herbivorous fishes can be classified as either grazers or browsers (Hiatt & Strasburg, 1960; Jones, 1968;
Backus, 1969; Ogden & Lobel, 1978). Grazers pick up inorganic substratum while feeding by scraping or
sucking, whereas browsers bite or tear more upright macroalgae and rarely ingest any inorganic material
(Jones, 1968). Grazers tend to feed non-selectively because their algal food is small and closely affixed to
the substratum, whereas browsers take whole or parts of individually recognisable seaweeds and, therefore,
are more selective (Lobel, 1981; Choat, 1982).
In tropical reef communities, herbivorous fishes are daytime feeders and are among the species that seek
shelter within the reef as twilight progresses and remain inactive at night (e.g. Earle, 1972). Travel between
foraging areas and slumber sites occurs in both temperate (Meekan, 1986) and tropical species (Fishelson,
Montgomery & Myrberg, 1987) and seems to be prevalent in habitats where food supply and hiding places
are spatially separated (Fishelson et al., 1987). During the day, herbivorous fishes, especially those
associated with coral reef habitats, forage in one of three ways: (1) territorial defence; (2) group foraging, or
(3) individual home ranges (Ogden & Lobel, 1978).
Territorial defence in tropical species
The most obvious holders of feeding territories on coral reefs are herbivorous damselfishes (Pomacentridae)
(Hixon, 1983). Their territories are readily identified as patches of algae frequently of a particular colour
and consistency. These fishes have important effects on the reef itself and on other herbivorous fishes in
138
MICHAEL H.HORN
their habitat. The behaviour and ecology of territorial damselfishes have been the subject of intensive study
over the past 15 years.
Other tropical reef fishes including blenniids (Nursall, 1977), scarids and acanthurids (Foster, 1985a) are
also known to hold feeding territories. These territories vary in time, space and intensity with which they are
defended. Some overlap and are shared between unrelated species; others are defined by the morphological
limitations of the holder. This range of territorial situations provides a glimpse into the complexities of
biological interactions in coral reef communities. The following examples illustrate this spectrum of
territorial relationships.
The parrotfish Scarus croicensis holds territories that appear to serve the dual functions of feeding and
reproduction (Ogden & Buckman, 1973; Buckman & Ogden, 1973) and defends against both conspecifics
and other benthic feeding fishes (Robertson, Sweatman, Fletcher & Cleland, 1976). In the San Bias Islands
(Panama), however, some individuals of this species hold permanent feeding territories while others form
feeding schools (Robertson et al., 1976). In St Croix, US Virgin Islands, S. croicensis does not hold
territories (Buckman & Ogden, 1973), possibly because of a more dispersed food supply (Ogden & Lobel,
1978).
The Caribbean blenny Ophioblennius atlanticus fiercely defends small feeding territories on exposed
surfaces of coral rock against conspecifics but weakly against other species (Nursall, 1977, 1981). Its
territory often lies within the larger territory of the damselfish Eupomacentrus dorsopunicans and, although
these two species overlap in diet, they interact little with each other. Nursall credits this lack of interaction
to the benthic habits, non-aggressive behaviour and time-minimised use of the algal food resource by the
blenny. A third species, the damselfish Microspathodon chrysurus, uses the same zone as a foraging area
and together with the more aggressive Eupomacentrus dorsopunicans protects the space including the
territory of the blenny against roving grazers and other potential invaders.
On the Great Barrier Reef, another blenny-damselfish pair has been shown to occupy overlapping
territories and share the algal turf food resource with little mutual interference (Roberts, 1987). The
damselfish Pomacentrus flavicauda and the blenny Salarias fasciatus had similar diets except that
the former fed to some degree on plankton. Removal experiments by Roberts (1987) failed to provide
evidence of exploitation competition between these species or of changes in levels of interference
competition by the damselfish after blenny removal. Damselfish were unable to exclude blennies from their
territories because the blennies took refuge in holes. The feeding activities of the blennies appeared not to
be detrimental to Pomacentrus flavicauda, at least in the short-term. This result is intriguing given the
estimates in other studies (Hatcher, 1981; Walker, 1984) that blennies seem to exert the greatest pressure
among grazers on algal turf in areas dominated by territorial fishes. Some damselfish populations, however,
may not be at the carrying capacity of the habitat (Robertson, Hoffman & Sheldon, 1981) and, in certain
cases, limited more by recruitment than resource availability (Wellington & Victor, 1985).
A three-species system involving the symbiotic sharing of feeding territories and algal food has been
described for coral reef fishes at Aldabra in the Indian Ocean (Robertson & Polunin, 1981). A damselfish
(Stegastes fasciolatus) occurs in the feeding areas of two much larger surgeonfishes (Acanthurus lineatus
and A. leucosternon). All three defend feeding areas against conspecifics and other fishes with similar diets
but show little aggression toward each other. Like the blennies in the above examples, the damselfish
provides little of the interspecific defence and cannot be excluded by the surgeonfishes because it can take
refuge in holes. The authors argue that the cost to the surgeonfishes of having the damselfish in their
feeding areas is small because the damselfish has a low biomass density, a slightly different diet and
contributes even if in a minor way to the defence of the shared feeding territories. Long-term experiments
are required, as they are in the study by Roberts (1987) described above, to sort out the costs and benefits of
139
the relationship to each species. Such a relationship may represent a mechanism by which some of the
numerous coral reef fish species can coexist with little apparent competition on the same potentially limiting
resources.
In another study at Aldabra involving the same two acanthurids, Robertson, Polunin & Leighton (1979)
claimed that morphological limitations dictated differences in territoriality and food habits between these two
species. They reasoned that A. leucosternon, with its smaller size, smaller mouth, more ovoid body with
larger median fins and more truncate tail, has greater flexibility in its feeding behaviour than A. lineatus and,
therefore, can feed more efficiently on smaller, more sparsely distributed algae and small growths in
crevices. A. leucosternon then, exploits food unavailable to other species but is restricted to poorer quality
habitat by more dominant species. A. lineatus, on the other hand, must eat food that has to be defended
against many other species, and it forms large colonies in which individual fish defend small territories
containing thick algal mats. Like Jones (1968), these authors maintain that the several acanthurid species on
a given reef coexist through resource partitioning and interspecific dominance hierarchies.
Territorial defence in temperate species
In general, few of the herbivorous fishes in temperate waters appear to defend feeding territories. Many
temperate species seem to be roving browsers or grazers (see Table I) or relatively inactive and secretive
species such as the
TABLE I
Names, feeding types and diets of herbivorous species in 14 shallow marine fish communities; species were included if
stomach contents were more than 50% plant material by volume, mass or, in some cases, frequency of occurrence; if no
quantitative data were available, herbivore designation was based on information from other sources; see Table VIII for
numbers and proportions of herbivorous fishes in these communities
Familyspecies
Feeding type
Main dietary items
France (Mediterranean, rocky littoral), Gibson (1968)

Blenniidae
Blennius sanguinolentus
Grazer
Filamentous and foliose algae
California (rocky intertidal), Grossman (1986)
Cottidae
Clinocottus globiceps
Browser
Foliose green and red algae, sea anemones
California (rocky intertidal), L.G.Allen & M.H.Horn, unpubl. data
Stichaeidae
Cebidichthys violaceus
Browser
Foliose green and red algae
Xiphister mucosus
Browser
New Zealand (rocky subtidal), Russell (1983)
Aplodactylidae
Aplodactylus arctidens
Grazer
Turf-forming red, brown and green algae
Girellidae
Browser/grazer
Turf-forming red algae and large brown algae
Girella tricuspidataa
Kyphosidae
Kyphosus sydneyanus
Browser
Large brown algae
Odacidae
140
MICHAEL H.HORN
Familyspecies
Feeding type
Odax pullus
Browser
Pomacentridae
Parma alboscapularis
Browser/grazer
Australia (rocky subtidal), Burchmore et al. (1985)b
Acanthuridae
Acanthurus xanthopterus
Grazer
Prionurus microlepidotus
?
Aplodactylidae
Crinodus lophodon
Grazer
Girellidae
Girella elevata
Browser/grazer
Girella tricuspidata
Browser/grazer
Odacidae
Olisthops cyanomelas
Browser
Pomacentridae
Mechanichthys immaculatus
Browser/grazer?
Parma microlepis
Browser/grazer?
Parma oligolepis
Browser/grazer?
Parma polylepis
Browser/grazer?
Parma unifasciata
Browser/grazer?
Siganidae
Browser
Siganus spinus
Familyspecies
Main dietary items

Large brown algae
Turf-forming red algae, foliose green algae, invertebrates
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Feeding type
California (rocky subtidal), Stephens & Zerba (1981)

Girellidae
Girella nigricans
Browser/grazer
Scorpididae
Medialuna californiensis
Browser/grazer
California (kelp bed), Quast (19681)
Girellidae
Girella nigricans
Browser/grazer
Kyphosidae
Hermosilla azurea
Browser/grazer
Scorpididae
Medialuna californiensis
Browser/grazer
Mexico (rocky intertidal), Thomson & Lehner (1976)
Girellidae
Girella simplicidens
Browser/grazer
Kyphosidae
Main dietary items
Algae
Algae
Red, green and brown algae; invertebrates

Algae, invertebrates
Familyspecies
Feeding type
Main dietary items
Hermosilla azurea
Browser/grazer Algae, invertebrates
Mugilidae
Mugil curema
Grazer
Diatoms, blue-green algae, detritus, mud and silt
Pomacentridae
Eupomacentrus rectifraenum
Grazer
Algae
South Africa (rocky littoral), Berry et al. (1982)
Acanthuridae
Acanthurus triostegus
Browser
Filamentous algae
Acanthurus lineatus
Browser
Filamentous algae
Mugilidae
Valamugil buchanani
Grazer
Detritus, diatoms
Scorpididae
Neoscorpis lithophilus
Browser
Sparidae
Sarpa salpa
Browser
Kermadec Islands (rocky subtidal), Schiel, Kingsford & Choat (1986)
Aplodactylidae
Aplodactylus etheridgi
Grazer
Turf-forming red, brown and green algae
Girellidae
Browser/grazer Algae
Girella cyaneaa
Browser/grazer Algae
Girella fimbriatusa
Kyphosidae
Kyphosus fuscus
Browser
Algae
Pomacentridae
Parma alboscapularis
Grazer/browser Turf-forming red algae, foliose green algae, invertebrates
Parma polylepis (=P.kermadecensis) Grazer/browser Algae, invertebrates
Grazer
Algae, detritus
Stegastes fasciolatus
Familyspecies
Feeding type
Hawaii (coral reef), Jones (1968)

Acanthuridae
Acanthurus achilles
Browser
Acanthurus glaucopareius
Browser
Acanthurus guttatus
Browser
Acanthurus leucopareius
Browser
Acanthurus nigrofuscus
Browser
Acanthurus sandvicensis
Browser
Acanthurus nigroris
Browser/grazer
Acanthurus dussumieri
Grazer/browser
Acanthurus mata
Grazer
Main dietary items
Filamentous algae
Filamentous algae
Filamentous algae
Filamentous algae
Filamentous algae
Filamentous algae
Filamentous algae, diatoms and detritus
Diatoms, detritus and filamentous algae
Diatoms and detritus
141
142
MICHAEL H.HORN
Familyspecies
Feeding type
Main dietary items
Acanthurus olivaceus
Grazer
Grazer
Ctenochaetus hawaiiensis
Grazer
Ctenochaetus strigosus
Grazer
Naso brevirostris
Browser
Foliose algae
Naso lituratus
Browser
Foliose algae
Naso unicornis
Browser
Foliose algae
Zebrasoma flavescens
Browser
Filamentous algae
Zebrasoma veliferum
Browser
Filamentous algae
Hawaii (coral reef), Hobson (1974)
Balistidae
Melichthys niger
Browser/grazer
Foliose algae, coralline algae
Blenniidae
Cirripectus variolosus
Grazer
Filamentous algae and detritus
Canthigasteridae (Tetraodontidae)
Canthigaster amboinensis
Grazer
Coralline algae, filamentous algae
Chaetodontidae (Pomacanthidae)
Centropyge potteri
Grazer
Filamentous algae and detritus
Kyphosidae
Kyphosus cinerascens
Browser
Benthic algae, drifting algal fragments
Monacanthidae (Balistidae)
Cantherines sandwichiensis
Grazer
Filamentous and coralline algae
Pomacentridae
Abudefduf sindonis
Grazer
Algae, including diatoms, detritus
Abudefduf sordidus
Grazer
Algae, including diatoms, detritus
Pomacentrus jenkinsi
Grazer
Algae, including diatoms, detritus Scaridae
Scarus rubroviolaceus
Grazer
Algal scrapings from rock surfaces, calcareous powder, sand
Scarus sordidus
Grazer
Algal scrapings from dead coral, calcareous powder, sand
Scarus taeniurus
Grazer
Algal scrapings from rock surfaces, calcareous powder, sand
Puerto Rico/Virgin Islands (coral reef), Randall (1967)
Acanthuridae
Acanthurus bahianus
Grazer
Algae and detritus, seagrasses
Acanthurus chirurgus
Grazer
Browser
Acanthurus coeruleus
Familyspecies
Balistidae
Melichthys niger
Blenniidae
Blennius cristatus
Feeding type
Main dietary items
Browser/grazer
Algae, invertebrates, seagrasses
Grazer
Algae and detritus
Familyspecies
Feeding type
Main dietary items
Blennius marmoreus
Grazer
Algae and detritus, invertebrates
Entomacrodus nigricans
Grazer
Algae and detritus
Ophioblennius atlanticus
Grazer
Algae and detritus
Chaetodontidae (Pomacanthidae)
Centropyge argi
Grazer/browser Algae and detritus
Gobiidae
Gnatholepis thompsoni
Grazer
Coryphopterus glaucofraenum
Grazer
Hemiramphidae
Hemiramphus brasiliensis
Browser
Seagrasses, fishes
Kyphosidae
Kyphosus incisor
Browser
Brown algae
Kyphosus sectatrix
Browser
Brown and red algae
Alutera schoepfi
Browser
Seagrasses and algae
Mugilidae
Mugil curema
Grazer
Diatoms, blue-green algae, detritus, mud and silt
Pomacentridae
Abudefduf taurus
Browser
Brown, green and red algae
Microspathodon chrysurus
Browser/grazer Filamentous red and blue-green algae, silt
Pomacentrus fuscus
Grazer
Algae and detritus, invertebrates, silt
Scaridae
Scarus coelestinus
Grazer
Algae, inorganic sediment
Scarus croicensis
Grazer
Scarus guacamaia
Grazer
Algae, seagrasses, inorganic sediment
Scarus taeniopterus
Grazer
Scarus vetula
Grazer
Sparisoma aurofrenatum
Grazer
Sparisoma chrysopterum
Grazer
Sparisoma rubripinne
Grazer
Sparisoma radians
Browser
Seagrasses, algae
Sparisoma viride
Grazer
Sparidae
Archosargus rhomboidalis
Browser/grazer Seagrasses, algae
Diplodus caudimacula
Grazer
Algae, invertebrates, sand
Marshall Islands (coral reef), Hiatt & Strasburg (1960)
Acanthuridae
Acanthurus achilles
Browser
Filamentous algae
Acanthurus aliala
Browser
Acanthurus gahhm
Grazer
Filamentous algae, sand
143
144
MICHAEL H.HORN
Familyspecies
Feeding type
Main dietary items
Acanthurus guttatus
Acanthurus lineatus
Acanthurus mata
Acanthurus nigroris
Acanthurus triostegus
Browser/grazer
Browser
Grazer
Browser/grazer
Grazer
Browser
Foliose and filamentous algae

Filamentous algae
Calcareous, filamentous and foliose algae, calcareous powder
Filamentous algae
Familyspecies
Feeding type
Grazer
Ctenochaetus striatus
Grazer
Naso lituratus
Browser
Naso unicornis
Browser
Zebrasoma veliferum
Browser
Balistidae
Rhinecanthus rectangulus
Grazer
Rhinecanthus aculeatus
Grazer/browser
Melichthys vidua
Grazer
Blenniidae
Cirripectus variolosus
Grazer
Cirripectus sebae
Grazer
Exallias brevis
Grazer
Istiblennius coronatus
Grazer
Istiblennius paulus
Grazer
Canthigasteridae (Tetraodontidae)
Canthigaster solandri
Grazer
Chaetodontidae
Chaetodon ephippium
Browser
Chaetodon reticulatus
Grazer
Kyphosidae
Kyphosus cinerascens
Browser
Mugilidae
Crenimugil crenilabis
Grazer
Neomyxus chavtali
Grazer
Pomacanthidae
Centropyge flavissimus
Browser/grazer
Pomacentridae
Abudefduf amabilis
Grazer/browser
Abudefduf biocellatus
Browser/grazer
Abudefduf dicki
Browser/grazer
Abudefduf glaucus
Grazer
Main dietary items

Algal scrapings and filaments, calcareous powder
Foliose and filamentous brown algae
Foliose brown algae
Algal scrapings and filaments, calcareous powder
Algal scrapings, foliose algae, coralline algae
Filamentous and foliose algae, sand, calcareous powder
Filamentous algae, detritus
Filamentous algae, detritus, sand
Algal scrapings and filaments, detritus, sand
Foliose and filamentous algae, calcareous powder
Coral polyps, filamentous algae
Filamentous algae
Detritus, blue-green algae, diatoms
Diatoms, desmids, filamentous algae
Filamentous and foliose algae, foraminiferans
Foliose and filamentous algae, invertebrates, fish
Filamentous algae, fish, detritus and sand
Filamentous algae, invertebrates, fish
Familyspecies
Feeding type
Main dietary items
Abudefduf lacrymatus
Abudefduf saxatilis
Abudefduf septemfasciatus
Abudefduf sordidus
Pomacentrus albofasciatus
Pomacentrus jenkinsi
Pomacentrus nigricans
Pomacentrus vaiuli
Browser
Browser
Browser
Grazer
Grazer
Browser/grazer
Grazer
Browser
Filamentous algae, foraminiferans, invertebrates

Filamentous and foliose algae, invertebrates
Foliose algae, invertebrates
Algal scrapings and invertebrates
Algal filaments and scrapings, sand
Filamentous and foliose algae, algal scrapings
Filamentous algae, fish, invertebrates
Familyspecies
Feeding type
Main dietary items
Scaridae
Cryptotomus spinidens
Scarus bicolorc
Grazer
Grazer
Scarus sordidusc
Grazer
Scarus spp.c (7 unidentified species)
Grazers
Filamentous algae, calcareous powder

Coral polyps, filamentous algae, calcareous
powder
powder
powder
Siganidae
Siganus rostratus
Tanzania (coral reef), Talbot (1965)
Acanthuridae
Acanthurus bariene
Acanthurus bicommatus
Acanthurus fuliginosus
Acanthurus leucosternon
Acanthurus lineolatus
Ctenochaetus striatus
Naso brevirostris
Naso lituratus
Zebrasoma scopas
Zebrasoma veliferum
Pomacanthidae
Apolemichthys trimaculatus
Centropyge bispinosus
Scaridaec
Calotomus spinidens
Scarus aeruginosus
Scarus africanus
Browser
Algal fronds and filaments,
Grazer?
Grazer?
Grazer?
Grazer?
Grazer?
Grazer?
Grazer?
Browser?
Browser?
Browser?
Browser?
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Grazer?
Grazer?
Algae
Algae
Grazer?
Grazer?
Grazer?
Algae
Algae
Algae
145
146
MICHAEL H.HORN
Familyspecies
Feeding type
Main dietary items
Scarus bipallidus
Scarus forsteri
Scarus globiceps
Scarus guttatus
Scarus harid
Scarus javanicus
Scarus microrhinos
Scarus niger
Scarus pectoralis
Scarus scaber
Scarus sordidus
Scarus vermiculatus
Siganidae
Siganus oramin
Siganus stellatus
Grazer?
Grazer?
Grazer?
Grazer?
Grazer?
Grazer?
Grazer?
Grazer?
Grazer?
Grazer?
Grazer?
Grazer?
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Algae
Browser?
Browser?
Algae
Algae
This species was placed in the Kyphosidae by the author (s).

Designation of herbivorous species was aided by M.J.Kingsford (pers. comm.).
c All scarids were classified as coral feeders by Talbot (1965); 9 scarids were classified as omnivores by Hiatt &
Strasburg (1960).
b
aplodactylids (Clements, 1985) and stichaeids (Ralston & Horn, 1986). Exceptions to this generality include
mainly those species that belong to primarily tropical families such as the Pomacentridae and Blenniidae.
As examples, the Australian damselfish Parma microlepis (Moran & Sale, 1977), the New Zealand
damselfish Parma alboscapularis (Choat & Ayling, 1987) are territorial, and the Mediterranean blenny
Parablennius sanguinolentus loosely defends a feeding territory (see Taborsky & Limberger, 1980).
Another pomacentrid, Hypsypops rubicunda, which occurs in waters off southern California, maintains and
defends a red algal turf nest but relies mainly on animal food (Quast, 1968; Clarke, 1970; Foster, 1972).
Group foraging
Foraging groups are common in tropical waters especially among members of the Acanthuridae and
Scaridae (Ogden & Lobel, 1978). These groups may be made up of one to several species. If multispecific,
the aggregations often consist of several herbivorous species and a few carnivorous ones that apparently
consume the invertebrates and smaller fishes disturbed by the feeding activities of the foraging group
(Ogden & Buckman, 1973; Hobson, 1974; Alevizon, 1976; Robertson et al., 1976). Although participation
in these groups may confer any of several advantages on the individual species, the major benefit seems to
be to overwhelm the defences of territorial damselfishes and thereby gain access to the algal patches
maintained within damselfish territories. Robertson et al. (1976) and Foster (1985a,b) argue that territorial
damselfishes, as abundant and aggressive defenders of space on tropical reefs, promote the widespread
habit of group foraging among non-territorial herbivores. This behaviour may be likened to the pack hunting
of carnivores (Foster, 1985a,b). The occurrence of aggregations seems to increase (and incidence of solitary
individuals decrease) with increase in density of territorial herbivores (Barlow, 1974a; Doherty, 1983). The
biting rate of individual participants increases with group size, apparently because individuals in large
147
groups are attacked less frequently by damselfish (Foster, 1985a). A damselfish at first attacks the invaders,
but soon the attack rate per fish in the aggregation declines and the damselfish waits passively for the group
to move away.
In the parrotfish Scarus croicensis schooling is a mechanism for circumventing the territoriality of
competitors (Robertson et al., 1976). Some individuals hold permanent territories while others form feeding
schools. Territorial parrotfish inhibit the feeding of non-territorial conspecifics, but both types of
individuals are subordinate to the omnivorous, territorial damselfish Eupomacentrus planifrons. Nonterritorial Scarus croicensis in schools feed at higher rates and are attacked by territory holders less often
than are non-schooling, non-territorial individuals. Non-schooling S. croicensis seem to make up that
portion of the population unable to acquire feeding territories, probably because of the aggressiveness of
Eupomacentrus planifrons. Schooling, therefore, helps maintain the coexistence of territorial and nonterritorial individuals.
Group foraging as a means to obtain algal food inside damselfish territories is expected to be rare in
temperate waters because herbivorous fishes in general, and herbivorous, territorial damselfishes in
particular, are rare at temperate latitudes (see Quast, 1968; Choat & Ayling, 1987). Sites of such activity
may, however, exist in southern Australia and New Zealand where territorial pomacentrids and girellids,
which feed as roving browsers or grazers, co-occur (Burchmore et al., 1985; Choat & Ayling, 1987) and
overlap somewhat in diet (Russell, 1983).
Home ranges
Home ranges of coral reef fishes appear to differ from feeding territories in at least three ways (Ogden &
Lobel, 1978): (1) home ranges do not increase the productivity of the food resources even if stronger
defences are applied; (2) home ranges are defended only against closely related species and possibly
competitors for shelter or spawning sites; and (3) home range behaviour develops where the food resource
is neither limiting nor widely used by other species. A variety of reef fishes are known to limit their
movements to specific areas of the reef where their feeding is concentrated (Reese, 1973; Sale, 1977;
Bouchon-Navaro & Harmelin-Vivien, 1981; Russ, 1984a). To some extent, fishes using home ranges are
intermediate between species such as certain scarids and acanthurids that feed over relatively wide areas in
mixed-species schools and species such as many pomacentrids and some acanthurids that actively defend
feeding territories. Species using home ranges may belong to these same families or even the same species.
Local-scale heterogeneity in reef structure may cause site-associated variations in feeding behaviour and
territorial defence such that a fish may defend a territory at one site but only occupy a home range at
another (see Choat & Bellwood, 1985).
Little information is apparently available on home range use by temperate herbivorous fishes. The highly
restricted areas used by the stichaeid Cebidichthys violaceus in a rocky intertidal habitat may indicate that
this fish occupies a home range, but more data are required to test this possibility (Ralston & Horn, 1986).
Comparative feeding behaviour of three herbivorous fishes
Recent studies on a tropical parrotfish (Scaridae), a temperate odacid (Odacidae) and a temperate
aplodactylid (Aplodactylidae) (Clements, 1985; Clements & Bellwood, 1988) provide an opportunity to
compare the feeding behaviours and mechanisms of three distinctly different herbivores.
Scarus rubroviolaceus, a tropical grazer This parrotfish and the odacid share the morphological features
of (1) a fused dental structure, with the premaxillary and dentary bones forming a beak, (2) an opposable
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MICHAEL H.HORN
pharyngeal jaw, and (3) the lack of a gastric stomach (Clements & Bellwood, 1988). The Scaridae and the
Odacidae along with the Labridae form a monophyletic assemblage of pharyngognathous acanthopterygian
teleosts (Liem & Greenwood, 1981). S. rubroviolaceus occurs from eastern Africa to Baja California and
exhibits a typical parrotfish feeding behaviour of scraping algae from the surface of rocks and coral rubble
(Rosenblatt & Hobson, 1969).
S. rubroviolaceus is described (Clements & Bellwood, 1988) to feed in an oblique head-down position,
scraping the surface of the turf-covered substratum. Each bite produces a pair of narrow parallel scrapes
marked by dislodged algae, but substratum scarring occurs only occasionally. Bites, about 1520 per
minute, are grouped into short feeding bouts with little or no searching behaviour within or between bouts.
The jaw morphology and feeding behaviour of S. rubroviolaceus indicate a strong scraping bite but a weak
sucking action. The pharyngeal apparatus appears to be capable of a great deal of movement, and a
powerful grinding action is produced by the broad, flat dentigerous surfaces of the pharyngeal bones. Once
ingested, algae are triturated by the action of the pharyngeal jaws, The intestinal contents consist of finely
ground algal material and large amounts of calcium carbonate particles, attesting to the grinding efficiency
of the pharyngeal apparatus. The gut is modified with unusual intestinal sacculae, which may increase the
holding capacity and also retention times by reducing laminar flow rates.
Odax pullus, a temperature browser Odacids are temperate fishes endemic to Australia and New
Zealand, and O. pullus is found only in New Zealand waters (Gomon & Paxton, 1985). This species
displays a variety of feeding methods depending on the food type and appears to be a more selective feeder
than the parrotfish; the main foods are primarily laminarian (i.e. Ecklonia radiata) and fucalean (i.e.
Carpophyllum spp.) brown seaweeds (Clements, 1985; Clements & Bellwood, 1988). When the fish feeds
on Ecklonia radiata, the oral surface is applied to the lamina and held there by opercular suction, and a disc
of algal tissue is excised. The bite is usually taken from the tips and centres of the secondary laminae where
the sori are located in the reproductive season. When feeding on Carpophyllum spp., Odax pullus removes
the reproductive bunches and thalli with a bite and a sideways flick of the head. Bites, two or fewer per
minute, are grouped into bouts, which are punctuated by searching behaviour. The feeding rates are highest
during the first two hours after dawn. Like Scarus rubroviolaceus, Odax pullus is a strictly diurnal feeder
and, like numerous tropical reef species (Fishelson, Montgomery & Myrberg, 1987) and some other
temperate fishes, especially of tropical affinities (Ebeling & Bray, 1976), seeks shelter at night.
After each feeding bout, the fish hangs in a tail-down position and pharyngeal mastication occurs, as
evidenced by the raising and lowering of the hyoid apparatus. The jaw morphology and feeding behaviour of
O. pullus indicate a relatively weak bite but a strong sucking action. The sharp, finely serrated oral jaws
provide a cutting action that is enhanced by the narrow cutting edges of the dentigerous surfaces of the
pharyngeal apparatus. Once ingested, algae are shredded into small pieces but left uncrushed as they pass
into the intestine. No carbonate material is found in the gut because O. pullus feeds on large upright
seaweeds and not on turf or encrusting algae. The simple intestine is shorter than would be expected for a
herbivore and, overall, how O. pullus digests seaweeds is an intriguing question.
Aplodactylus arctidens, a temperate browser Aplodactylids are temperate fishes found only in coastal
waters of Peru, Chile, New Zealand and Australia (Nelson, 1984), and A. arctidens is confined to the latter
two regions (Clements, 1985). A. arctidens is apparently a crepuscular species, preferring to feed during the
early morning and late evening (Doak, 1978). The feeding behaviour of this species as described here
follows that of Clements (1985). A. arctidens is a sluggish, negatively buoyant fish that feeds primarily on
red turfing algae growing on rocky reefs. Its relatively weak jaws, weakly implanted jaw teeth and lack of
opposable pharyngeal jaws limit this fish to a diet of relatively tender, low growing seaweeds. Larger fish,
however, eat a higher proportion of tougher, foliose algae. Clements (1985) calls A. arctidens a non-
149
selective grazer, more like the parrotfish than the highly selective odacid in this comparison. Unlike either
the parrotfish or the odacid, this fish does not grind nor shred its food, but it does have a distinct, muscular
stomach. The three fishes clearly must have different mechanisms for digesting algae, a topic to be
addressed in the next section (p. 197).
DIETS AND FOOD PREFERENCES
The food habits of many herbivorous fishes indicate that collectively these fishes consume a great variety of
the plant material in the sea (Table I). Although red and green macroalgae seem to predominate in the diets
of the majority of herbivorous fishes, virtually all types of algae from diatoms to large kelps are eaten as
well as several species of seagrasses. At first glance, the food habits of plant-eating fishes might seem to be
merely representative of the widely reputed versatility and opportunism exhibited by fishes in general.
Closer examination, however, reveals a much more complex, and still incompletely understood, picture of
dietary patterns in these fishes. Herbivorous species are constrained morphologically, for example, by the
relatively small gapes that characterise most of them (Ogden & Lobel, 1978) and by differences in their jaw
teeth and pharyngeal apparatus (e.g. Clements & Bellwood, 1988). Although most herbivorous fishes are
diurnally active (Ogden & Lobel, 1978), they may variously feed throughout the day (Earl, 1972), primarily
during twilight hours (Doak, 1978), or reach peaks of feeding intensity early in the morning (Meekan, 1986)
or late in the afternoon (Taborsky & Limberger, 1980). Some species, especially those in temperate waters
(Horn, Murray & Edwards, 1982; Horn, 1983), often shift their diets with the season, and many species in
both temperate and tropical latitudes show ontogenetic changes in their food habits (Montgomery, 1977;
Barton, 1982; Horn, Murray & Edwards, 1982; Clements, 1985; Meekan, 1986). These latter species
commonly begin life as carnivores then become herbivores as adults. Still another source of variation is that
some herbivorous fishes have different diets in different parts of their geographic range (e.g. Odum, 1970;
Collins, 1981), perhaps mainly a result of changes in food availability but possibly because of other factors
as well. Also, a number of seaweed species, including seemingly palatable forms, are avoided by
herbivorous fishes (Montgomery & Gerking, 1980).
Relatively few studies have been completed in which: (1) the availability of the algal resource was known
so that food selectivity in nature could be quantitatively determined, or (2) fishes were presented with an
array of seaweeds, either in the field or laboratory, so that food preferences could be established. Emerging
studies of herbivorous fishes, however, including those on functional morphology and digestive physiology
and on their responses to seaweed defences, are beginning to shape a clearer understanding of the
complexity in dietary patterns and to provide a better answer to the question of why do herbivores eat what
they eat.
The purpose of this portion of the food and feeding section is first to summarise information on the diets,
food selectivity and dietary preferences of the herbivorous members of several tropical and temperate fish
families and then to evaluate the factors that appear to influence diet choice in herbivorous fishes. A
compilation of the diets and feeding modes of the herbivorous species encountered in several major studies
of tropical and temperate fish communities is presented in Table I.
Tropical families
Acanthuridae Acanthurids (surgeonfishes) comprise one of the most abundant and diverse fish families on
tropical reefs. Although a few species are zooplankton feeders, most are either grazing or browsing
herbivores (Jones, 1968). In a study of 20 species of Hawaiian and Johnston Island acanthurids, Jones
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MICHAEL H.HORN
(1968) found that two were planktivores, feeding on zooplankton, six were grazers of diatoms and detritus
and 12 were browsers, three feeding on foliose brown algae and nine on smaller, filamentous red and, to a
lesser extent, green algae. Five major algal divisions, Cyanophyta (blue-greens), Chrysophyta (diatoms),
Chlorophyta (greens), Rhodophyta (reds) and Phaeophyta (browns) were represented in the diets of these 18
herbivorous surgeonfishes. Although they consumed a wide variety of algae, the 12 species of browsers still
fed selectively on a rather small range of seaweeds. Of the 160 algal genera available to browsing
acanthurids in Hawaii, Jones (1968) found only 40 in the fish stomachs he examined. If he omitted rarely
occurring genera, the number was reduced to 32 or 20% of those species available in the habitat. More
specifically, 2 of 24 (8%) available blue-greens, 9 of 27 (33%) greens, 15 of 97 (15%) reds and 6 of 16
(38%) browns were eaten. A further indication of dietary selectivity was that one of the browsers of large,
foliose algae, Naso lituratus, apparently preferred to eat brown algae in the genus Pocockiella because the
genus was found in all 37 fish examined and made up the entire stomach contents of 25 of these specimens.
In a laboratory study of one of the above surgeonfishes, Acanthurus trio stegus sandvicensis (=A.
sandvicensis), Randall (1961a) showed that this fish preferred the red alga Polysiphonia sp. and the green
alga Enteromorpha sp. over a variety of other algae even though numerous other filamentous species and
diatoms were found in stomach contents. Randall (1961a) believed that many of the algae, including the
blue-greens, were consumed by the fish incidentally according to their abundance in the habitat.
Recent field studies, including algal transplant experiments (Lewis, 1985), observations of tagged fishes
(Wolf, 1985), preference tests (Lewis, 1986) and experiments to assess the effectiveness of algal secondary
compounds in deterring herbivores (Paul, 1987; Hay et al., 1988a; Wylie & Paul, 1988) have all shown
acanthurids to be selective feeders.
Scaridae Scarids (parrotfishes) are abundant and diverse residents of tropical reefs (Hiatt & Strasburg,
1960; Randall, 1967; Hobson, 1974), and some species also occur in adjacent seagrass beds (Randall, 1967;
Ogden, 1976). Although earlier studies (Al-Hussaini, 1947; Gohar & Latif, 1959; Hiatt & Strasburg, 1960;
Talbot, 1965) considered parrotfishes to be primarily coral feeders, subsequent investigations (Randall,
1967; Hobson, 1974; Smith & Paulson, 1974) cast doubt on this conclusion, and these fishes are now
classified as virtually exclusive herbivores (Russ, 1984b; Randall, 1986). With their fused jaw teeth and
pharyngeal mill they are able to graze on a variety of algae on reef surfaces (Randall, 1967; Lobel, 1981)
and to browse on seagrasses (Randall, 1967; Ogden 1976). Although most parrotfishes are grazers (Ogden,
1976), Sparisoma radians is a seagrass browser and a characteristic member of Caribbean seagrass
communities (Thayer et al., 1984).
Two relatively recent studies on S. radians constitute almost all the experimental work on parrotfish food
preferences except for some more general field experiments on food choice in tropical herbivores that
included parrotfishes (see below). The first of these studies showed that the seagrass Thalassia testudinum
was the most abundant item in the field diet and, with epiphytes, the top-ranking plant species in laboratory
preference tests (Lobel & Ogden, 1981). Nevertheless, fish fed a mixed diet including all seagrasses and
algae in the preference hierarchy provided the greatest certainty of survival. Lobel & Ogden speculated that
Sparisoma radians eats a variety of plants to maintain a balanced diet. In a subsequent study, Targett, Targett,
Vrolijk & Ogden (1986) showed that the three least preferred food genera in Ogden & Lobels experiments,
the green algae Caulerpa, Halimeda and Penicillis, contain terpenoid secondary compounds that deter
feeding by Sparisoma radians. Coating Thalassia blades with crude extracts of Halimeda incrassata
reduced the fishs bite rate on, and consumption of, the seagrass to the same level as that for H. incrassata.
The results of this study indicate that secondary metabolites can play an important role in food selection by
herbivorous fishes. Feeding observations corroborate this dietary selectivity in that Sparisoma radians prefers
151
the epiphytised tips of Thalassia, which are lower in protein but also lower in phenolic compounds than
younger, basal leaves (Thayer et al., 1984).
Recent field studies including algal transplant experiments (Lewis, 1985, 1986), observations on tagged
fishes (Wolf, 1985) and experiments to assess the role of algal secondary compounds in deterring
herbivores (Hay et al., 1988a) have all shown that scarids are selective feeders, but often with different
responses than acanthurids.
Siganidae Siganids (rabbitfishes) are Indo-Pacific herbivores that feed as grazers on filamentous algae or
as browsers on larger, foliose seaweeds (Hiatt & Strasburg, 1960; Lundberg & Lipkin, 1979). They are
locally abundant around tropical reefs (Tsuda & Bryan, 1973), and some species are harvested (Bryan, 1975)
and cultured (Bryan, 1975; Avila, 1986) for human consumption. Bryan (1975) reported that the foliose
alga Gelidiopsis intricata and the filamentous algae Boodlea composita, Sphacelaria tribuloides, and
Centroceras clavulatum were the most abundant items in the stomachs of Siganus spinus captured in waters
around Guam. In a study of three siganids in the northern Red Sea, Lundberg & Lipkin (1979) found that
these fishes ate green, red and brown algae in different proportions and also consumed small quantities of
blue-green algae and seagrasses. Their conclusion that all three species fed selectively was based on
comparisons of stomach contents with availability of the seaweeds and seagrasses in the habitat.
Several other studies have shown that siganids feed selectively in nature or prefer certain algae in the
laboratory. Tsuda & Bryan (1973) observed that the green algae Enteromorpha, Caulerpa, Boodlea, and
Cladophoropsis were the first seaweeds to disappear from the reef flats of Guam following the invasion of
huge schools of Siganus restrains and S. spinus. Their preference experiments showed that the algae chosen
were also grazed heavily in the field. Other preference studies on siganids (Westernhagen, 1974; Bryan,
1975) have shown that Enteromorpha is a highly preferred algal type. Enteromorpha, however, was only of
intermediate importance in the siganid stomachs examined by Bryan (1975). This discrepancy could be a
result of differential digestibility or local availability of the alga at the time the fish were captured (Ogden &
Lobel, 1978). The latter notion is corroborated by the importance of Enteromorpha in the diets of two
rabbitfishes in a Red Sea location where the alga was abundant in the habitat (Lundberg & Lipkin, 1979). In
multiple choice feeding trials with 5060 seaweed species, juvenile Siganus rostratus and S. spinus rejected
26 species whereas only 12 were never consumed by adults (Tsuda & Bryan, 1975). Bryan (1975) claimed
that the adults but not the juveniles were physically able to ingest the larger, tougher algal species and that
this limitation was a factor in the high mortalities of starving juveniles recorded by Tsuda & Bryan (1975)
after an invasion of the juveniles caused the depletion of filamentous algae from the reef flats of Guam.
Siganids were among the coral reef herbivores whose foraging was often deterred by secondary
compounds extracted from chemically defended seaweeds and applied to the surface of otherwise palatable
and preferred Enteromorpha plants in field experiments on Guam (Paul, 1987; Paul et al., 1987; Paul & Van
Alstyne, 1988). It is of interest that elatol, a terpenoid compound extracted from the red alga Laurencia
obtusa, has been shown in field experiment to deter parrotfish feeding in the Caribbean (Hay, Fenical &
Gustafson, 1987b). L. obtusa, however, along with two other species of Laurencia pre-dominated in the
diets of Siganus rivulatus in the Red Sea (Lundberg & Lipkin, 1979). These findings suggest that different
herbivores react differently to seaweed secondary chemicals, an increasingly recognised source of variation
in recent field experiments.
Pomacentridae Pomacentrids (damselfishes) are widespread, conspicuous and ecologically important
fishes on tropical reefs around the world (Emery & Thresher, 1980). They are solitary or form small to
dense aggregations depending upon the species, and they range in food habits from strict carnivores to
omnivores to almost exclusive herbivores, with most maintaining an omnivorous diet (Hiatt & Strasburg,
1960). The territorial species, which are usually omnivores or herbivores, exert profound and well-
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MICHAEL H.HORN
documented effects on the social organisation of other herbivorous reef fishes and on the structure of algal
communities in tropical waters. Some pomacentrids also occur in warm temperate waters where a few are
herbivores (Russell, 1983) and others are omnivores (Quast, 1968; Moran & Sale, 1977) or planktivores
(Quast, 1968).
The herbivorous damselfishes are reef-dwellers and feed primarily on turfing red and green algae. Much
attention has been given to their diets because of the impacts their defence of a feeding territory have on
other fish herbivores and on the algal populations within their territories. Two studies that focused on
feeding ecology in particular serve to illustrate the diets and food selectivity in herbivorous pomacentrids.
Montgomery (1980b), despite acknowledged small sample sizes, found that two co-occurring species in the
southern Gulf of California, Eupomacentrus rectifraenum and Micro-spathodon dorsalis, have somewhat
similar diets in that both consume highly productive, foliose red and green algae but ignore brown and
calcareous seaweeds. The two species, however, differ in feeding behaviour. The smaller Eupomacentrus
rectifraenum feeds intensively and selectively on a defended algal mat, choosing primarily the green alga
Ulva and secondarily red algae, especially Gracilaria. Montgomery argued that the recruitment rate and
productivity of Ulva must be high to persist under the heavy grazing pressure. In contrast, Microspathodon
dorsalis feeds less intensively and non-selectively on its defended algal mat, foraging without close
inspection of the substratum by tearing a large circular patch of algae from the mat. Its diet and the mat
inside its territory are dominated by the red alga Polysiphonia, not because this alga is selected, but
presumably because it is the only alga with a growth rate sufficient to persist under the influence of heavy,
nonselective grazing pressure. Thus, maintenance of the species composition in the algal mats of both fishes
requires high primary productivity and rapid growth rates of the dominant species. In the second study,
Lassuy (1984) showed that Stegastes lividus in Guam shifted from omnivory as juveniles to herbivory as
adults. Both ontogenetic stages were classed as browsers. Red algae, particularly those in the genera
Polysiphonia, Gelidiopsis and Ceramium, were the main plant components of the diet of all size classes.
Enteromorpha and Cladophora were the most common green algae in the stomachs examined. Brown algae,
mainly Ectocarpus and Sphacelaria, and blue-green algae were recorded in smaller quantities; the
proportion of the latter type in the diets decreased with size of the fish.
Tropical-temperate families
Kyphosidae Kyphosids (rudderfishes) and their relatives do not classify easily into either phylogenetic
arrangements or latitudinal categories. This family is sometimes considered to be made up of three
subfamilies, Kyphosinae, Girellinae and Scorpidinae, but in other cases these taxa are raised to family status
(Nelson, 1984). The three taxa are treated here as separate families. All three families contain herbivorous
species, but discussion is limited in this section to the kyphosids and girellids because, unlike the
scorpidids, essentially all their members are herbivorous and because their herbivorous habits are better
known than those of the plant-eating scorpidids. Kyphosids occur in both tropical and temperate waters
(Nelson, 1984) and are therefore considered in this tropical-temperate subsection, whereas girellids are
temperate species and thus included in that subsection.
Kyphosids, in particular the genus Kyphosus, occur worldwide in tropical to temperate (mainly warm
temperate) seas (see Nelson, 1984). They browse in small to large schools on red and brown algae (Hiatt &
Strasburg, 1960; Randall, 1967; Hobson, 1974), and are also known to feed near the surface on drifting
seaweeds in tropical (Randall, 1967; Hobson, 1974; Littler, Taylor & Littler, 1983b) and temperate
(Rimmer, 1986) waters. They consume cleanly-bitten pieces of algae and pass the material with little or no
trituration into the stomach (Russell, 1983; Rimmer, 1986). Kyphosus sydneyanus, a south temperate
153
species, feeds mainly on brown algae in both New Zealand (Russell, 1983) and Australian (Rimmer &
Wiebe, 1987) waters, whereas K. cornelii, another Australian species, feeds chiefly on red algae (Rimmer
& Wiebe, 1987). Several species of Kyphosus seem to prefer brown algae, a notion reinforced in an
anecdotal way by the practice (see Titcomb, 1972) of some Hawaiian fishers who bait their hooks with
brown seaweeds, especially Sargassum, to catch Hawaiian rudderfishes as well as the acanthurid, Naso
unicornis, another brown algae eater. The food and feeding ecology of Hermosilla azurea, a warm
temperate species occurring in waters off southern California and northern Mexico, is poorly known but
appears to consume a variety of red, green and brown seaweeds (Quast, 1968). Kyphosids have complex
digestive tracts, and the two south temperate species mentioned above have recently been shown to have a
microbial fermentation system in their hindguts (Rimmer & Wiebe, 1987).
Sparidae Sparids (porgies) are active fishes commonly associated with reefs, seagrass beds and other
coastal benthic habitats in tropical to warm temperate regions around the world (Smith & Smith, 1986). As
a group, sparids have extremely varied diets, and many undergo complex, ontogenetic changes in food
habits that are often correlated with age-related changes in dentition and gut morphology (Christensen,
1978; Stoner, 1980; Stoner & Livingston, 1984). Porgies are of interest in the context of this review because
many are omnivorous, consuming both animal and plant material during their lives. The use of plant
material varies with age, season and location but is usually greater in adults (Adams, 1976; Christensen,
1978; Stoner, 1980; Livingston, 1982; Gerking, 1984; Ogburn, 1984; Stoner & Livingston, 1984). Sparids
variously graze on filamentous algae or browse on larger, foliose algae or seagrasses (Randall, 1967;
Christensen, 1978; Stoner, 1980; Gerking, 1984; Ogburn, 1984; Stoner & Livingston, 1984). In Lagodon
rhomboides (Stoner, 1980) and Sarpa salpa (Christensen, 1978) canine teeth are replaced in older fish by
incisors, which are apparently better suited for taking bites of the plant material that becomes a larger part
of the diet with age in these fishes. The powerful molariform teeth in the sides of the jaws of many sparids
may not be used to crush algal cell walls because Ogburn (1984) found only whole and completely intact
algae in the stomachs of Archosargus probatocephalus. Sarpa salpa, a species found in the Mediterranean
and along western and southern African coasts (Smith & Smith, 1986), is probably as an adult as close to being
a complete herbivore as any of the sparids, even though animals still supplement the red and green algae that
make up the bulk of the diet. Not only does the gut lengthen and the teeth become incisiform with age in
S.salpa (Christensen, 1978), but the fish has been shown to have relatively high assimilation efficiencies
when fed the green alga Ulva lactuca (Gerking, 1984). Nevertheless, the fish lost weight on a strict Ulva
diet in the laboratory (Gerking, 1984), as did another sparid, Archosargus rhomboidalis, when fed only a
single algal species (Vaughan, 1978). These results suggest that the two species require animal food and
perhaps accurately reflect the omnivorous habits of most sparids.
Recent field and laboratory experiments have shown that the feeding selectivity of two sparids, Dlplodus
holbrooki and Lagodon rhomboides, is influenced by unpalatable (i.e. not consumed, probably because of
taste or texture) seaweeds and seaweed secondary compounds. Both fishes were found to feed at
significantly higher rates on the palatable red algae Hypnea and Spyridia occurring alone than on these
algae attached to the unpalatable brown seaweed Sargassum (Hay, 1986) and to be deterred from feeding by
a secondary chemical extracted from Dictyota dichotoma, a brown alga little preferred by these two fishes
(Hay, Duffy, Pfister & Fenical, 1987a; Hay, Renaud & Fenical, 1988b).
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MICHAEL H.HORN
Temperate families
The food and feeding behaviour of herbivorous members of two south temperate fish families, the
Aplodactylidae and the Odacidae, were described in an earlier part of this section of the review to illustrate
nonselective grazing and selective browsing and are not included here.
Girellidae Girellids (nibblers) are widespread in the warm temperate waters of the north Pacific and south
Pacific (Nelson, 1984) where they feed in small to large schools as grazers or browsers on rocky substrata
or in kelp bed habitats (Quast, 1968; Russell, 1983). The close-set, cuspate incisors of girellids are movable
and seem to allow these fishes to be efficient grazers of rock surfaces (Norris & Prescott, 1959), perhaps
more so than the related kyphosids, which have fixed but otherwise similar teeth (Thomson, Findley &
Kerstitch, 1979). Girellids, however, are also able to browse on foliose algae including kelps, for they
remove clean bites from a variety of seaweeds and pass the material with little or no trituration into the stomach
(Bell, Burchmore & Pollard, 1980; Russell, 1983). Most girellids consume at least some invertebrate prey,
either intentionally or incidentally, but the bulk of the diet, at least in adults, is usually made up of macroalgae
(Williams & Williams, 1955; Quast, 1968; Bell et al., 1980; Russell, 1983). Nevertheless, the mixed diets
of girellids led to the impression (Williams & Williams, 1955; Quast, 1968) that these fishes gained most of
their nutrition from animal material despite the large amount of algae in their guts. Only recently has it been
demonstrated (Anderson, 1987) that a girellid, the Australian Girella tricuspidata, can assimilate nutrients,
including those in the cell wall, from algal material. Much remains to be learned about feeding and
digestion in girellids and the related kyphosids and scorpidids, especially in north temperate waters.
Stichaeidae Stichaeids (pricklebacks) are elongate, bottom-dwelling fishes that occur in cold temperate,
primarily inshore waters of the Northern Hemisphere (Eschmeyer, Herald & Hammann, 1983). Of the 23
stichaeid species recognised for the eastern North Pacific (Eschmeyer et al., 1983), only two, Cebidichthys
violaceus and Xiphister mucosus, are considered to be herbivores (Barton, 1982; Horn, Murray & Edwards,
1982). Once these two species shift from carnivory to herbivory (as small juveniles of about 45 mm
standard length), they feed selectively in the rocky intertidal zone on red and green algae and avoid
encrusting, calcareous and brown seaweeds (Horn et al., 1982). Laboratory experiments have shown that
Cebidichthys violaceus prefers three species of red algae that have the highest protein contents among the
eight species making up the bulk of the diet. This result combined with rather consistently high assimilation
efficiencies shows that the preferred species provide the greatest amount of protein per bite to the fish (Horn
& Neighbors, 1984). These three algae, however, are annuals and available mainly during the summer
(Horn et al., 1982). Diet selection from a seasonally changing array of seaweeds in the habitat results in
both C.violaceus and Xiphister mucosus consuming carbohydrate-rich, protein-poor algae in the winter and
protein-rich, carbohydrate-poor algae during the rest of the year (Horn, Neighbors & Murray, 1986). The
small amounts of animal material in the gut of fish beyond the dietary transition phase (Montgomery, 1977;
Horn et al., 1982; Miller & Marshall, 1987), the highly acidic stomach that apparently is effective in
releasing nutrients from algal cells (Urquhart, 1984) and the assimilation of radioactively labelled algal
material (Horn, Neighbors, Rosenberg & Murray, 1985) demonstrate that Cebidichthys violaceus is a
herbivore. Although less intensively studied, Xiphister mucosus seems to be equally dependent on algal
foods. These two stichaeids appear to be among the very few year-round herbivorous fishes in cold
temperate waters. They may be matched in diet and thermal environment (approximately 815C annual
range of sea surface temperatures) only by the aplodactylids and odacids in southern New Zealand waters
(see Ayling & Cox, 1982).
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FACTORS AFFECTING DIET SELECTION

What are the factors that account for the food selectivity seen among herbivorous fishes and are these
predictive for unstudied species and plant-eating fishes in general? The question is difficult and complex
even when stated in the simpler terms of why herbivorous fishes eat what they eat. Morphological and
behavioural constraints (e.g. mouth size, tooth type, swimming mode and buoyancy) certainly limit the
dietary range. For instance, the blades of a large kelp may be too large or too tough for a fish to bite effectively
or too far into the water column for a negatively buoyant, benthic fish to acquire safely or economically.
Also, availability of potential dietary items may vary in time and space because of, for example, abiotic
factors, algal life history patterns or the feeding actions of other herbivores. This variation obviously
influences food habits: absent plants are not eaten, and very rare ones usually contribute little to the total
diet. At the same time, however, extremely abundant seaweeds do not necessarily predominate in
herbivorous fish diets.
Although fish morphology and food availability are important influences on fish herbivore diets, the
selectivity exhibited by plant-eating fishes seems to be governed by more than just these factors. For
example, as many as 15 or 20 or even dozens of algal species have been recorded from the stomach contents
of a herbivorous fish such as Cebidichthys violaceus (e.g. Horn et al., 1982; Miller & Marshall, 1987), but
only a few species make up the bulk of the diet, and these are not consumed in proportion to their
abundance in the habitat (Horn et al., 1982). Moreover, only two or three species of brown algae constitute
almost the entire diet of Odax pullus even though many more seaweeds are available in the habitat (Russell,
1983; Clements, 1985; Meekan, 1986; Clements & Bellwood, 1988). Clearly, selectivity is practised by
herbivorous fishes. But what drives this selectivity besides the feeding abilities of the fishes and the
availability of the plants? Are diets more the result of positive or of negative selection (i.e. avoidance)?
The answers to these questions are explored below in the context of other factors that may influence diet
selection. Emphasis is placed on the chemical and morphological features of the seaweeds and seagrasses that
are potential food sources for herbivorous fishes.
Food quality
Herbivorous fishes might be expected to choose seaweeds high in nutritional quality, i.e., high in energy and
especially protein, given the low levels of this nutrient in macroalgae. The cues that would allow fishes to make
such choices remain obscure (see Stephens & Krebs, 1986), but if food quality as defined here were
correlated with other features of the algae such as colour, texture, toughness or taste then fishes could have
evolved to make such an association. In any case, is nutritional quality predictive of food choice regardless
of the cues? The answer seems to be yes, at least in part.
Optimal foraging theory including models of optimal diets is represented by a large and growing body of
literature (Schoener, 1971; Pyke, Pulliam & Charnov, 1977; Hughes, 1980; Pyke, 1984) but remains
controversial (Gray, 1987; Pierce & Ollason, 1987; Schoener, 1987; Stearns & Schmid-Hempel, 1987). This
body of thought and conflict has stimulated research on the diet and feeding behaviour of a variety of animals.
The basic assumption of foraging theory is that energy is the currency to be optimised leading to the energy
maximisation premise (Townsend & Hughes, 1981). Most tests of the model, including the optimal diet
component, have been consistent with the theory (Schoener, 1987); the theory was, however, developed
with carnivores in mind (Stenseth & Hansson, 1979), and few studies have been done on marine herbivores
(Hughes, 1980). Although Hughes (1980) concluded that the diets of marine herbivorous browsers largely
meet the expectations of optimal diet theory, he mentioned few studies, and none was on fishes. Hughes
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MICHAEL H.HORN
further concluded that foraging behaviour could not be adequately understood solely on the basis of the
energy maximisation premise.
In one of the few studies to examine the diets of herbivorous fishes in the context of optimal diet theory,
Horn (1983) found the diets of the stichaeid fishes Cebidichthys violaceus and Xiphister mucosus to be
partially consistent with the three most important predictions (Schluter, 1981) of the model. (1) The
prediction that at high food densities a forager should concentrate solely on the energetically most valuable
items was incompletely met by these two fish species. Cebidichthys violaceus and Xiphister mucosus
increased their consumption of energy-rich annual seaweeds during periods (summer and fall) of high food
abundance, but still continued to take a mixed diet. (2) The prediction that abundance of lower-valued foods
does not determine their inclusion in the diet was largely upheld by the feeding habits of these two intertidal
fishes. The probability of an item being consumed apparently depends upon its abundance as well as its
chemical composition. (3) The prediction that foragers will generalise as food abundance declines was largely
met by the two fishes because their diets broadened noticeably during periods (especially winter) of reduced
food supply. An overriding outcome of this and other studies indicates that optimal diet models cannot be
based solely on energy maximisation but should also include nutrient constraints in order to account more
completely for the seasonally fluctuating, mixed diets of these fishes and other generalist herbivores.
Foliage-eating herbivores (generalists) face nutrient constraints because foliage often varies greatly in
abundance and in chemical composition, both within species on a seasonal basis and between species
(Westoby 1974, 1978). According to Westoby (1974, 1978) variety in the diets of such generalist herbivores
might best be explained by sampling and, hence, diet mixing by the animal in order to keep pace with
seasonal changes and thereby maintain a nutritionally adequate diet. The food preferences and seasonal
diets of herbivorous stichaeids are relevant in the context of diet mixing. The seaweed species most highly
preferred by Cebidichthys violaceus and Xiphister mucosus are the annual red algae Microcladia coulteri,
Porphyra perforata and Smithora naiadum (Horn, et al., 1982), which have the highest protein contents of
the seaweeds in the diets of these fishes (Horn & Neighbors, 1984). Thus, these two fishes prefer the
seaweeds that yield the most protein per bite. Furthermore, in the winter when these preferred annuals are
scarce or absent, Cebidichthys violaceus and Xiphister mucosus feed selectively on those perennial
seaweeds, especially the red alga Iridaea cordata var. cordata (as I. flaccida), that provide them with greater
carbohydrate and, therefore, greater energy return than would the other algae contributing to the bulk of the
diet (Horn et al., 1986). These results mean that the two stichaeids consume carbohydrate-rich, protein-poor
algae in the winter and protein-rich, carbohydrate-poor algae during the rest of the year. Thus, contrary to an
expectation of optimal diet theory, energy intake was increased by selectivity only during the winter,
whereas protein intake was increased at the expense of energy intake at all other times of the year (Horn et
al., 1986). The recently documented dietary shift with season in a tropical surgeonfish, Acanthurus
nigrofuscus, appears to be tied to the nutritional requirements of the fish during the reproductive cycle
(Fishelson, Montgomery & Myrberg, 1987) and may be another example in support of Westobys (1974,
1978) proposition of seasonal diet mixing by herbivores to meet nutritional requirements.
At this point, it is pertinent to describe the use of protein (P) and energy (E) contents together in ratio
form (the P/E ratio) as an indicator of food quality and, in turn, of fish growth. In a series of publications on
detritivorous and herbivorous freshwater fishes in the family Cichlidae, Bowen (1979, 1982, 1984b) has
demonstrated the application of the P/E ratio. The P/E ratio as used by Bowen is defined as the amount of
assimilable protein per unit of assimilable energy. P/E ratios required for maintenance and for maximum
growth appear (Russell-Hunter, 1970) to be remarkably uniform across a wide range of animal taxa. Bowen
(1984b) cited these ratios as being about 4 mg digestible protein per kJ of digestible energy for maintenance
and 20 30 mg of protein per kJ for maximum growth (Fig 1). He found growth of goldfish (Carassius auratus)
157
Fig1.Predicted bimonthly growth rates of the stichaeid fishes Cebidichthys violaceus (months listed above curve) and
Xiphister mucosus (months listed below curve) as a function of the amount of assimilable protein relative to the amount
of assimilable energy (P/E ratio) obtained from consumption of eight species of algae; theoretical growth curve for
different P/E values from Bowen (1982); figure slightly modified from Horn, Neighbors & Murray (1986).
between maintenance and maximum growth levels to be directly proportional to protein concentration in the
diet (Bowen, 1984b). Growth rates predicted by the Bowen (1982) model for Cebidichthys violaceus and
Xiphister mucosus (Fig 1) based on P/E ratios calculated from assimilation of protein and energy by the
fishes from major dietary species are, as expected, lowest and near maintenance levels during the winter and
increase but do not reach maximum growth levels at other times of the year (Horn et al., 1986). Such
growth predictions can provide the basis for actual growth experiments using diets with modified P/E ratios.
Comparison of the potential food quality among different algal groups offers important but somewhat
limited clues to dietary selectivity in herbivorous fishes. Montgomery & Gerking (1980) analysed the ash,
energy and nutrient contents of 16 species to assess the food quality of fleshy red, green, brown and
calcareous red algae. On the basis of ash, calories, total protein, and total lipid contents, they concluded first
that fleshy algae should be superior to calcareous algae as foods for fishes and secondly that green algae
should be superior to brown algae and brown algae superior to red algae. When Montgomery & Gerking
considered the digestibility of storage and extracellular carbohydrates, they predicted that green and red
algae should be superior to brown algae as food for fishes. Montgomery & Gerking then cited two Gulf of
California damselfishes, Eupomacentrus rectifraenum and Microspathodon dorsalis, as examples of
herbivores that feed as predicted by algal biochemistry in that they eat red and green algae, assimilate
nutrients from both types and ignore brown and calcareous algae. As mentioned above, most herbivorous
fishes probably do seem to eat mainly red and green algae, and to this extent, these predictions are valuable.
Caution, however, is required in expanding the model because of within-group variation in chemical
composition of red and green algae (see Horn et al., 1986). Moreover, several different types of herbivorous
fishes, including kyphosids, odacids and certain acanthurids and siganids, feed selectively on brown algae,
which also exhibit (Steinberg, 1985; Ragan & Glombitza, 1986; Estes & Steinberg, 1988) large withingroup variation in chemical composition, especially secondary metabolites.
The discussion of food quality and diet prediction to this point indicates that energy content alone does
not account for herbivore diets and that energy and nutrient contents together are better predictors but still
deficient. It is important to emphasise that data showing that stichaeids prefer the seaweeds of highest
protein content (Horn & Neighbors, 1984) and that these fishes feed selectively for greatest protein or
carbohydrate return (Horn et al., 1986) distinguish only among dietary species. Non-dietary seaweeds were
not studied. So the question is not just which species are preferred among a larger set that constitutes the
total diet, but also which species are avoided and why or under what circumstances. The answers require
greater understanding of seaweed defences, a subject that has received increasing attention in recent years,
and of fish digestive mechanisms, a subject that has yet to receive adequate study. These topics are taken up
in sequence below.
Seaweed defences
Traits of seaweeds that may deter herbivores include low digestibility, calcified or otherwise tough (leathery
or rubbery) thalli and toxicity resulting from the synthesis and sequestering of secondary compounds. The
evidence that these characteristics defend against marine herbivores, especially fishes, is summarised
below.
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MICHAEL H.HORN
Low digestibility Differential digestibility of carbohydrates, which comprise most of the bulk and
available energy in macroalgae, has been cited (Montgomery & Gerking, 1980) as a factor influencing, or at
least correlated with, dietary patterns in herbivorous fishes. Fishes in general have carbohydrases capable of
breaking alpha-linked but not beta-linked polymers of monosaccharides (Fange & Grove, 1979). All plants
contain beta-linked polymers (cellulose and structurally similar compounds) in their cell walls (Mackie &
Preston, 1974), and presumably, therefore, these compounds cannot be digested enzymatically by fishes. A
major difference among plant groups occurs in the linkages of their polysaccharide storage products. Green
and red algae and seagrasses produce alpha-linked storage compounds (Craigie, 1974). Thus, digestibility
apparently does not explain why, for example, the stichaeids Cebidichthys violaceus and Xiphister mucosus
do not consume (Horn et al., 1982) red algae such as Endocladia muricata or Prionitis lanceolata and the
seagrass Phyllospadix scouleri. Brown seaweeds, however, contain beta-linked polysaccharides (Craigie,
1974), so digestibility (or lack of it) may help to explain why these algae are avoided by the stichaeids
(Horn et al., 1982) and also by certain pomacentrids (Montgomery & Gerking, 1980). In support of the
apparent indigestibility of brown algae, Cebidichthys violaceus did not assimilate carbon from either
Macrocystis integrifolia or Fucus distichus when force-fed these two brown seaweeds in the laboratory
(Horn et al., 1985). As has already been mentioned, however, a variety of fishes such as certain acanthurids
(Jones, 1968), siganids (Lundberg & Lipkin, 1979), kyphosids (Russell, 1983; Rimmer & Wiebe, 1987) and
odacids (Russell, 1983; Clements, 1985; Meekan, 1986; Clements & Bellwood, 1988) regularly eat brown
seaweeds as a major portion of their diets and almost certainly are able to digest these algae. There are
distinct differences in digestive capabilities among herbivorous fishes, therefore, and further study should
be undertaken on the digestion of various algal carbohydrates by herbivorous fishes.
Calcification and toughness Calcified thalli appear to be effective in deterring herbivorous invertebrates
and fishes (Paine & Vadas, 1969; Littler, 1976; Montgomery & Gerking, 1980; Lewis, 1985; Paul & Hay,
1986). The strong negative correlations between ash and both energy and nutrient content in calcareous
seaweeds suggest that avoidance of these species would be of selective value for most herbivorous fishes
(Montgomery & Gerking, 1980). The diets of only a few herbivorous fishes appear to contain substantial
amounts of calcareous algae (see Table I, p. 173). Corallina officinalis, a heavily calcified red alga, fits the
pattern of avoidance in that it is not eaten by Cebidichthys violaceus or Xiphister mucosus (Horn, Murray &
Edwards, 1982). Steneck (1983) has argued that diversity of herbivores and the intensity of their grazing
activities have escalated over geological time and that the conspicuousness and frequent dominance of
coralline algae on hard substrata in shallow marine communities is due in part to their ability to withstand
and adapt to deep grazing (i.e. excavating) herbivores such as parrotfishes.
Toughness refers to the resistance to breaking or tearing of the thallus or leaf (if on a seagrass) when
pulled or bitten. It is a morphological characteristic of seaweeds and seagrasses that can deter feeding by
marine herbivores such as fishes and sea urbins (Littler, Taylor & Littler, 1983) and molluscs (Steneck &
Watling, 1982). Toughness alone, however, is frequently not sufficient to explain the dietary selectivity of
herbivorous fishes but is a trait that often appears to be part of a combination of morphological and chemical
defences present in seaweeds (see p. 197).
Secondary compounds Many marine plants produce secondary metabolites, and increasing numbers of
these compounds are now known to have a role in deterring herbivorous invertebrates and fishes (see Ragan
& Glombitza, 1986; Hay & Fenical, 1988). Deterrence of herbivorous fishes by a variety of these
chemicals, either as extracts or purified compounds, has been demonstrated in numerous recent field or
laboratory studies (Paul, Sun & Fenical, 1982; Paul & Fenical, 1983; Sun, Paul & Fenical, 1983; Hay,
1986; Paul & Hay, 1986; Targett et al., 1986; Hay et al., 1987a; Hay, Fenical & Gustafson, 1987b; Paul,
1987; Paul et al., 1987; Hay et al., 1988a; Hay, Renaud & Fenical, 1988b; Paul & Van Alstyne, 1988;
159
Wylie & Paul, 1988). Although the incidence of defensive chemicals appears to be more common in
seaweeds of herbivore-rich tropical and subtropical waters (Hay & Fenical, 1988), some temperate algae
produce secondary metabolites that deter herbivorous invertebrates (Steinberg, 1984, 1985) and fishes
(Hay, 1986; Hay et al., 1987a). Brown seaweeds in north temperate seas have been shown (Steinberg, 1985)
to produce phlorotannins in high concentrations (order Fucales) or in low concentrations (order
Laminariales). Fucalean and other brown seaweeds in tropical habitats all appear to be low in phlorotannins
(Steinberg, 1986). Interestingly, common species of fucoid algae in temperate Australia and New Zealand
appear to have phlorotannin concentrations two to three times those of phlorotannin-rich species in
California waters (Estes & Steinberg, 1988; Steinberg, 1988). This striking difference intensifies the
mystery of how the southern hemisphere odacid and kyphosid fishes, whose diets often are made up mostly
of these fucoids, tolerate and digest such seemingly heavily defended algae. In California, the girellid
Girella nigricans and the scorpidid Medialuna californiensis are known (Quast, 1968; Harris, Ebeling, Laur
& Rowley, 1984) to eat varying quantities of the phlorotannin-poor laminarian kelps, but no fish in the
northern hemisphere is known to consume fucoid algae.
The rapid progress that has been made in collecting, handling, purifying and applying the often unstable
secondary compounds from seaweeds (Norris & Fenical, 1985) has fuelled the recent surge of studies on the
deterrent effects of these chemicals on fishes and other marine herbivores. An especially useful and
rewarding technique has been to coat pieces of a palatable seaweed with an extract or pure metabolite of
another alga known or expected to be unpalatable. The coated piece is then offered along with pieces of the
same seaweed coated only with the solvent (control) to a particular herbivore species in the laboratory (e.g.
Targett et al., 1986; Hay et al., 1987a; Wylie & Paul, 1988), or to populations of several different
herbivores (e.g. parrotfishes, surgeonfishes and rabbitfishes) in the wild (e.g. Hay et al., 1987b; Paul & Van
Alstyne, 1988). Experimental and control pieces are then either counted or weighed after short-term
(minutes to hours) feeding trials to calculate the deterrent effect of the extract or metabolite on the
herbivores in question. This technique has been limited to non-polar extracts and metabolites (e.g. terpenoids)
because, being lipid soluble, they adhere to the algal surface after the solvent evaporates and are not quickly
lost to sea water. Polar secondary compounds, especially phlorotannins, have not been studied with this
technique because their separation and identification is more complex (Norris & Fenical, 1985) and, being
water soluble, they are subject to greater loss in sea water.
Recent experiments involving secondary compounds show that seaweeds vary in their production of these
metabolites and that different herbivores respond differently to the same compounds. Some of these
findings are as follows. (1) Palatable seaweeds are eaten less when growing on, or in association with,
herbivore-resistant species (Hay, 1986; Littler et al., 1986). (2) Different metabolites from the same
seaweed confer different levels of resistance against different herbivores (Hay et al., 1987a; Paul, 1987; Paul
et al., 1987; Hay et al., 1988a; Paul & Van Alstyne, 1988). (3) Extracts from some populations of the green
alga Halimeda in areas of high herbivore activity appear to be more effective deterrents against herbivorous
fishes than extracts from populations of the same species in habitats subject to lower rates of herbivory (Paul
& Van Alstyne, 1988). (4) The secondary compounds of the brown alga Dictyota dichotoma that deter
feeding by herbivorous fishes do not deter, or may even increase, feeding by small, sedentary grazers such
as amphipods and polychaetes (Hay et al., 1987a; Hay et al., 1988b). Hay and co-workers suggested that the
small herbivores that live on plants are more resistant to chemical defences than are large, mobile
herbivores like fishes that move among many plants and that prdation and herbivory by fishes may be
major factors selecting for amphipods that can live on and eat seaweeds unpalatable to fishes.
These last statements might be interpreted as evidence that plant-herbivore relationships in the sea are the
products of coevolution. Hay & Fenical (1988), however, argue that fundamental differences in marine and
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MICHAEL H.HORN
terrestrial communities make the potential for coevolution less likely in the marine environment. The major
difference between the herbivore communities in the two environments is the manner in which juveniles
locate their host plants. The adults of many specialised insects are not tied to the food plant but search
widely and lay eggs on appropriate hosts. In contrast, herbivorous fishes and sea urchins have planktonic
larval stages that spend time developing in the pelagic community before returning to coastal habitats where
they settle, metamorphose into juveniles and begin eating seaweeds either immediately as small juveniles or
perhaps in most cases, especially for fishes, as larger juveniles. Although some larvae settle selectively in
response to general habitat cues (Marliave, 1977; Butman, 1987), they are unlikely to respond only to
inconspicuous seaweed hosts because these would be rarely encountered. Moreover, larvae approaching shore
are subject to intense prdation (Gaines & Roughgarden, 1987) and unlikely to have the opportunity of
multiple entries to find a rare host seaweed. These factors should select for generalist feeders that can use
whatever seaweeds they encounter as they join coastal communities. Such constraints would not appear to
promote coevolution between herbivores and seaweeds and may explain why specialists appear to be rarer
in marine than terrestrial communities. Hay & Fenical (1988) further reason that the potential for
coevolution between seaweeds and small sedentary grazers such as amphipods is limited because of the
minor impact of these grazers on plant fitness relative to the major effects of herbivorous fishes and sea
urchins. These reservations about coevolution between seaweeds and herbivores reinforces the cautionary
note sounded by Meekan (1986) that the chemical and morphological traits of seaweeds may have evolved
in response to a variety of biotic and abiotic influences, not just herbivorous animals.
Despite all the recent investigations of seaweed secondary metabolites, including pharmacological
assays, the physiological effects of these compounds on herbivores remain virtually unknown (Hay &
Fenical, 1988). When Hay et al. (1987a) fed pinfish (Diplodus holbrooki) a diet containing 1 %
pachydictyol-A from the brown alga Dictyota dichotoma, the fish grew half as rapidly as control fish over a
three-week period. The physiological basis for this reduced growth, however, was not investigated. Fishes
such as odacids and kyphosids that consume large amounts of brown algae would be important subjects for
the study of the physiological effects of secondary compounds on herbivorous fishes. Lobel (1981) has
suggested that the neutral or weakly alkaline environment of the alimentary tracts of some fishes may
dissociate the proteintannin complexes formed by the digestion of algae with high phlorotannin
concentrations. Interestingly, the gut pH of the stomachless Odax pullus is alkaline (Clements & Bellwood,
1988), whereas the stomach pH is strongly acidic and the intestine weakly acidic to alkaline in Kyphosus
cornelii and K. sydneyanus (Rimmer & Wiebe, 1987). This area of fish herbivory requires further study and
promises to yield exciting discoveries. Combined defences In a study of herbivory on a Caribbean reef,
Littler, Taylor & Littler (1983b) presented evidence that seaweeds grouped according to a functional-form
model (Littler & Littler, 1980) increasingly resisted fish and sea urchin herbivory in the following order of
six morphological types: sheet, filamentous, coarsely-branched, thick-leathery, jointed-calcareous and
crustose groups. A combination of chemical and morphological defences (toxicity, low calorific content,
calcified or otherwise tough thalli) appears to be present in the most resistant functional-form groups
(Littler et al., 1983b). Moreover, several recent studies (Hay, 1984a; Lewis, 1985; Wolf, 1985; Paul & Hay,
1986; Hay et al., 1988a; Paul & Van Alstyne, 1988) show the difficulty of distinguishing between the
effects of these two types of deterrents in tropical algae. For example, Lewis (1985) found that alleged
defences were prevalent in some algal species that are nevertheless highly susceptible to fish grazing. She
found that the brown algae Sargassum polyceratium and Turbinaria turbinata, which are tough and leathery
and contain phlorotannins, and another brown alga, Padina jamaicensis, which is lightly calcified, to be
highly preferred by parrotfishes in the genus Sparisoma but avoided by the surgeonfishes Acanthurus
bahianus and A. coeruleus, both with weaker jaw structure and dentition than the parrotfishes. Both Lewis
161
(1985) and Wolf (1985) stressed that algal defences must be interpreted with respect to individual
herbivores.
Multiple defences might be expected among seaweeds in habitats of high herbivore diversity such as coral
reefs where no single defence is apt to be effective against all the herbivores that encounter these plants
(Paul & Hay, 1986). These combinations of deterrents may undergo dramatic temporal shifts in tropical
algae in response to the diel activity patterns of herbivores. According to Hay et al. (1988a) new growth in
the green alga Halimeda is produced at night when herbivorous reef fishes are inactive, and although
chemically defended, is susceptible to damage by herbivores. Older plant portions (more than 48 hours old),
which are exposed to daytime herbivory, have lower concentrations of the terpenoid feeding deterrent but
are lower in food value and more highly calcified, thus relatively resistant to herbivory. Hay et al. (1988a)
speculate that coordinating diel patterns of growth with rapidly mobilisable defences could be an important
component of the ecology of not only Halimeda but other seaweeds and marine phytoplankton as well.
Seaweeds in temperate waters, predictably, may lack the combined defences of algae in tropical habitats
because of the lower intensity of herbivory, especially by fishes, in higher latitudes. Little is known,
however, about seaweed deterrence against fish herbivores in temperate habitats. Comparison of the
defensive traits of algae in north temperate latitudes with those in south temperate waters, especially around
Australia and New Zealand where brown algae are known (Estes & Steinberg, 1988; Steinberg, 1988) to
have high concentrations of certain secondary compounds, should make a rewarding study.
DIGESTION AND DIGESTIVE MECHANISMS
EVIDENCE FOR DIGESTION AND ASSIMILATION OF ALGAL MATERIAL
The ability of herbivorous fishes to digest and assimilate algal material is apparent and convincing for many
species, but the most compelling evidence for herbivory (i.e. growth on an algal diet) is limited to only a few
species. The kinds of evidence, in order of increasing confirmation of herbivory, are as follows: (1) diets
largely of seaweeds; (2) specialised morphology of the alimentary canal; (3) assimilation of seaweed
compounds; and (4) growth on a seaweed diet. These topics are discussed in turn below.
Diets largely of seaweeds
This evidence is usually obtained from observations of feeding behaviour or analyses of gut contents of
fishes or both. Many fishes in tropical waters (e.g. Hiatt & Strasburg, 1960; Randall, 1967; Jones, 1968;
Hobson, 1974) and fewer in temperate habitats (e.g. Quast, 1968; Gibson, 1968; Horn, Murray & Edwards,
19c2; Russell, 1983) have been shown to have such diets (see Table I, p. 173). But whether browser or
grazer, a plant-eating fish is always going to ingest some animal material simply because many species of
small invertebrates live in close association with seaweeds. Herbivorous fishes do not appear to winnow out
the animals before swallowing morsels of algal foods, so it seems that no marine fishes are herbivores in the
strictest sense. Does the ingested animal material contribute significantly to the fishs nutrition? This
question remains largely unanswered, but because the digestive enzymes of carnivorous and herbivorous
fishes are about the same, differing mainly in concentration (Kapoor, Smit & Verighina, 1975; Fnge &
Grove, 1979), the animal matter probably contributes to the total assimilated material. In fishes that seem to
be unequivocal herbivores the proportion of animal material can be exceedingly small. Proportions of
animal material in the guts of both tropical (e.g. Randall, 1967) and temperate (e.g. Russell, 1983) species
may be less than 1 % by volume. Diets of the stichaeids Cebidichthys violaceus and Xiphister mucosus are
162
MICHAEL H.HORN
usually less than 2% animal material by dry weight (Horn et al., 1982), an amount that does not change the
P/E ratio of the total diet for the two species and therefore does not alter their predicted growth rates (Horn,
Neighbors & Murray, 1986; see Fig. 1, p. 192). The diet of X. mucosus, however, occasionally contains as
much as 8% animal material, which increases the P/E ratios of assimilated matter by 2050% but still does
not change the predicted growth pattern of the fish (Horn et al., 1986; see Fig 1).
Specialised morphology of the alimentary canal
Further evidence for herbivory is apparent in the morphological specialisations of the digestive tract of
fishes whose diets are made up largely of algal material. The beak-like jaws and pharyngeal mill of
parrotfishes, one of the most abundant groups of tropical herbivorous fishes (Randall, 1967, 1986), allow
these fishes to scrape epilithic algae from rock substrata and dead coral and grind the material into a mass of
fine particles (Randall, 1967; Clements & Bellwood, 1988) presumably available for enzymatic action and
subsequent assimilation. Other plant-eating fishes such as acanthurids (Jones, 1968), girellids (Norris &
Prescott, 1959) and odacids (Clements & Bellwood, 1988) have jaw teeth that appear to be specialised for a
herbivorous diet. The stomachs of several species of grazing herbivorous fishes, especially the mugilids
(Thomson, 1954) and certain acanthurids (Jones, 1968), are muscular and function as gizzards to grind
filamentous algae and diatoms into fine particles apparently ready for chemical breakdown and subsequent
absorption. The intestine or entire gut of herbivorous fishes is usually longer than that of their noncarnivorous relatives (e.g. Al-Hussaini, 1947; Barton, 1982; Goldschmid, Kotrschal & Wirtz, 1984; Hallacher
& Roberts, 1985). Finally, the hindguts of at least two species of kyphosids are enlarged and specialised as
fermentation chambers (Rimmer & Wiebe, 1987). These morphological specialisations are discussed in
greater detail under Digestive Mechanisms (see p. 207).
Assimilation of seaweed compounds
Assimilation efficiencies obtained by both direct (i.e. measurement of food consumed and faeces produced)
and indirect (i.e. use of an indigestible marker) methods for a variety, but still a relatively small number, of
herbivorous fishes (Table II) indicate strongly that these fishes are digesting and absorbing carbohydrate,
lipid and protein from their seaweed diets. Herbivores are expected to have low assimilation efficiencies
because of the relatively large amounts of indigestible plant material contained in their diets (Kapoor et al.,
1975; Brett & Groves, 1979; Knights, 1985), and this expectation is often met as the values in Table II
reveal. Nevertheless, these efficiencies are highly variable as a whole because they range from values below
10% for lipid or carbohydrate assimilation in certain fishes (Montgomery & Gerking, 1980; Horn et al.,
1986) to values for protein assimilation in the 9598% range (Horn et al., 1986). These latter efficiencies
match those recorded for carnivorous fishes (Kapoor et al., 1975). Within- and between-species differences
in assimilation efficiencies among herbivorous fishes are driven by an enormous range of factors including
temperature, type of food eaten, age of the fish, recent history of feeding, gut morphology and transit time
of food through the gut. Two examples illustrate intraspecific variation. (1) Nitrogen assimilation efficiency
in the damselfish Stegastes lividus increases from 36% in juveniles to 79% in adults, in accord with the
ontogenetic shift from omnivory to herbivory in this species (Lassuy, 1984). (2) Periods of food deprivation
cause reduced assimilation efficiencies for carbon, nitrogen, lipid and protein in the girellid Girella
tricuspidata, with a 4-day deprivation period having a greater effect than a 24-h deprivation period
(Anderson, 1988).
163
Because of the differences in the direct and indirect methods of determining assimilation efficiencies and
because of criticisms of the latter method, it is appropriate at this point to compare the two techniques. Most
studies of assimilation efficiency in fishes including herbivores have used an indirect method of
determination because of the difficulty of collecting faeces quantitatively (Talbot, 1985). The procedural
advantage of the indirect method is that nutrient assimilation can be calculated without measuring food
intake or faeces output. An indicator or marker substance is added to the diet, or an integral, naturally
occurring component of the diet is used as an indicator or marker. Ideally, indicators should be completely
indigestible and evacuated at the same rate as the other gut contents. Internal indicators, i.e., naturally
occurring constituents of the diet, are preferable because assimilation of
TABLE II
Assimilation efficiencies of some marine herbivorous fishes
Familyspecies Food item
Assimilation efficiency
Method
Temperature C Reference
Acanthuridae
Acanthurus
guttatus
Natural diet,
filamentous
algae
Natural diet,
diatoms &
detritus?
Natural diet,
filamentous
algae
Natural diet,
diatoms &
detritus?
37%
Total
11%
Indirect (ash
marker)
2829
Charlock, 1983
Total
16%
Indirect (ash
marker)
2829
Chartock, 1983
Total
14%
Indirect (ash
marker)
2829
Charlock, 1983
Total
20%
Indirect (ash
marker)
Nelson &
Wilkins, 1988
Enteromorpha
sp. (green alga)
% 14C recovered
in fish tissue of
that
administered in
whole or
fractionated
alga (force fed):
1.4
4.2
Carbon-14
20
Anderson, 1987
Acanthurus
olivaceus
Acanthurus
triostegus
Ctenochaetus
striatus
Nitrogen
Girellidae
Girella
tricuspidata
Control
Cell walls (16 h
after feeding)
Cell walls (5 d
after feeding)
Protoplasts (16
h after feeding)
Whole alga (16
h after feeding)
6.8
9.8
15.0
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MICHAEL H.HORN
Girella
tricuspidata
Lipid
Total nitrogen
Protein
nitrogen
Total carbon
(decline in
efficiencies
with food
deprivation)
Hemiramphidae
Hyporhamphus
melanochir
Heterozostera
tasmanica
Enteromorpha
intestinalis
(green alga)
20 to 55%
53 to 83%
42 to 79%
Whole alga
18 to 78%
Direct
20
Anderson, 1988
Organic matter
38%
Indirect (lignin
marker)
17
Klumpp &
Nichols, 1983
Carbon
8%
Carbon-14
uptake
Conacher,
Lanzing &
Larkum, 1979
22%
Carbon-14
uptake
Nitrogen
85%
Direct
19 & 28
Menzel, 1959
24%
Indirect (ash
marker)
Montgomery &
Gerking, 1980
26 to 82%
Natural
seagrass diet,
Protein
Lipid
Energy
Monacanthus
Microdictyon
chinensis
umbilicatum
(green alga)
Posidonia
Carbon
australis
(seagrass)
Pomacanthidae
Holacanthus
Enteromorpha
bermudensis
salina &
Monostroma
Carbohydrate
oxysperma
(green algae)
Energy
78%
Pomacentridae
Eupomacentrus Natural diet,
rectifraenum
green & red
algae
Protein
88%
Lipid
56%
2%
Carbohydrate
50%
76%
28%
72%
Total
165
Family
species
Food item
Assimilation efficiency
Method
Temperature
C
Reference
Microspathodo
n dorsalis
Natural diet,
Polysiphonia
(red alga)
57%
46%
37%
Enteromorpha
clathrata
(green alga)
Total
Indirect (ash
marker)
Montgomery &
Gerking, 1980
Total 29%
(juveniles)
Indirect (ash
marker)
28
Lassuy, 1984
Natural algal
turf diet
Nitrogen 92%
(winter)
Indirect (ash
marker)
Polunin, 1988
Direct &
Indirect?
Lobel &
Ogden, 1981
Carbon-14
uptake
Bryan, 1975
Direct
25
Vaughan, 1978
Protein
Lipid
Carbohydrate
Stegastes
lividus
Total 72%
(adults)
Nitrogen 36%
(juveniles)
Nitrogen 79%
(adults)
Plectroglyphid
odon
lacrymatus
20%
77% (summer)
Carbon 78%
(winter)
58% (summer)
Phosphorus
61% (summer)
Scaridae
Sparisoma
radians
Siganidae
Siganus spinus
Carbon 6 to
39% (adults)
Sparidae
Archosargus
rhomboidalis
Enteromorpha
flexuosa (green
alga)
Polysiphonia
subtilissima
(red alga)
Seven different
algae &
seagrasses
Total
(depending on
item eaten)
Enteromorpha
compressa
(green alga)
Carbon 9 to
60% (juveniles)
Total
48%
Total
58%
7 to 81%
166
MICHAEL H.HORN
Sarpa salpa
Total (ash free
dry weight)
Protein
Energy
Stichaeidae
Cebidichthys
violaceus
Protein
Lipid
Carbohydrate
(depending
upon alga fed)
Cebidichthys
violaceus
Nitrogen
(depending
upon alga fed)
Cebidichthys
violaceus
Four algae,
epibionts
reduced (2
browns, 1
green, 1 red)
Four algae (2
browns, 1
green, 1 red)
Nitrogen
(depending
upon alga fed)
Cebidichthys
violaceus
Carbohydrate
(depending
upon alga fed)
Xiphister
mucosus
Ulva lactuca
(green alga)
59%
Total (dry
weight)
61%
Direct
19
Gerking, 1984
Four dietary
algae (2 greens,
2 reds)
43 to 81%
21 to 44%
46 to 62%
Total
31 to 52%
Indirect
(ash marker)
15
Edwards &
Horn, 1982
Eight dietary
algae (2 greens,
6 reds)
71 to 84%
Protein
77 to 95%
Indirect
(ash marker)
15
Horn &
Neighbors, 1984
Three algae,
epibionts not
reduced (1
brown, 1 green,
1 red)
Carbon
(depending
upon alga fed)
Carbon
(depending
upon alga fed)
0 to 37%
Carbon-14
uptake
15
Horn et al., 1985
1 to 13%
Carbon-14
uptake
Carbon
14 to 68%
Indirect
(ash marker)
Eight dietary
algae (2 greens,
6 reds)
18 to 83%
Lipid
0 to 59%
Indirect
(ash marker)
15
Horn, Neighbors
& Murray, 1986
Eight dietary
algae (2 greens,
6 reds)
Protein
69 to 98%
Indirect
(ash marker)
15
Horn, Neighbors
& Murray, 1986
81%
65%
0 to 80%
Lipid
Carbohydrate
(depending
upon alga fed)
167
6 to 78%
11 to 74%
natural foods can be determined in both laboratory and field situations (Talbot, 1985). A large number of
the assimilation studies on herbivorous fishes have used the ash component of the food as an internal
indicator (Montgomery & Gerking, 1980; Edwards & Horn, 1982; Horn & Neighbors, 1984; Lassuy, 1984;
Horn et al., 1985, 1986) stemming from its original use in assimilation studies with zooplankton (Conover,
1966). Any removal of ash from the food upon passing through the gut would result in under-estimation of
assimilation efficiency. In certain studies (Buddington, 1980) some of the ash has been shown to be
absorbed and, as a result, its use as an indicator or marker has been criticised (Bjorndal, 1985). Several
other natural dietary substances including hydrolysis-resistant organic matter (Buddington, 1980; De Silva
& Perera, 1983), hydrolysis-resistant ash (De Silva & Perera, 1983), lignin (Klumpp & Nichols, 1983) and
acid-insoluble ash (Atkinson, Hilton & Slinger, 1984) have been used with varying degrees of success, but
none seems to be without limitations. Both Gerking (1984) and Anderson (1988) used direct methods, i.e.,
quantitative measurement of food consumed and faeces produced, to determine assimilation efficiencies and
obtained values generally similar to those estimated by indirect methods.
Even more convincing evidence for assimilation of algal compounds by fishes is provided by data
showing that radioactively labelled (14C) algal material is absorbed from the digestive tract into the fishs
body. Such evidence is available for at least four species of marine herbivorous fishes (Table II). The study
on the stichaeid Cebidichthys violaceus (Horn et al., 1985) was the first to demonstrate uptake of
radioactively labelled algal material by a cold-temperate marine fish. Moreover, this work showed that the
fish could assimilate 14C from macroalgae largely free of epibionts (diatoms and bacteria) and from a
nondietary brown alga (Macrocystis) as well as dietary species. Andersens (1987) study was the first to
show that a herbivorous fish can assimilate the cell wall components of a seaweed although the mechanism
remains unknown.
Growth on a seaweed diet
Finally, the most compelling evidence for complete herbivory would be growth and maintenance of good
health by fish on a strictly algal diet. Few such growth experiments have been done, and less than definitive
results have been obtained in the studies completed. When Menzel (1959) fed Monostroma to the
predominantly herbivorous angelfish Holacanthus bermudensis at 28cC, the fish gained some weight, but
when the fish were given Enteromorpha at 19C, they lost weight. The weight gain at 28C was attributed
to deposition of lipids not proteins. Menzel expressed doubt that Holacanthus bermudensis could grow on
algal matter alone unless consumption rates were much higher in nature than those seen in captivity.
Similarly, weight losses were recorded for the sparids Archosargus rhomboidalis (Vaughan, 1978) and
Sarpa salpa (Gerking, 1984) when fed unialgal diets in the laboratory. Much of the understanding of growth
of marine fishes on strictly herbivorous diets is based on the results of these three studies, but they are
misleading for two reasons. First, the fish used in each case was more an omnivore than a strict herbivore
and, secondly, unialgal diets were used, which are unnatural and probably do not provide a sufficiently
balanced diet for growth. Other studies suggest that fishes survive better on multispecies diets than on
unialgal diets. Although they did not measure growth, Lobel & Ogden (1981) found that survival in the
strictly herbivorous parrotfish Sparisoma radians was higher on a mixed plant diet than on any single
168
MICHAEL H.HORN
dietary item, including the most preferred species. Fry of Chanos chanos, a euryhaline herbivore and widely
cultured fish in tropical Asia, also survive better on a combined diet of two kinds of freshwater algae than
on either one alone (Pantastico, Baldia & Reyes, 1986). The maintenance ration calculated by Gerking
(1984) for Sarpa salpa apparently represents the first and only such estimate for a marine herbivorous fish.
Clearly, more studies of growth in marine herbivorous fishes are needed, not only to provide a greater
understanding of their digestive capabilities but also to derive estimates of food consumption in nature.
DIGESTIVE ENZYMES
The major emphasis in enzymatic studies of herbivorous fishes has been on the search for cellulolytic
enzymes, while research on the action of the basic digestive enzymes in these fishes has largely been neglected.
These two topics are discussed in turn below.
Assays for endogenous celluloses
One of the most lingering and troublesome questions in fish herbivory is whether any fishes produce a
cellulase to break down the cell walls of the plants they consume. Numerous papers have been published on
the subject with generally mixed and inconclusive results. Broad surveys have shown that cellulase activity
is unrelated to food habits and produced by the intestinal microflora (Stickney & Shumway, 1974; Stickney,
1975) or related either to the amount of highly processed plant detritus in the gut (Prejs & Blaszczyk, 1977)
or a diet of invertebrates that contain cellulase or a cellulolytic micro-flora (Niederholzer & Hofer, 1979;
Lindsay & Harris, 1980). Cellulase activity has been reported in the intestinal tracts of the sparid Lagodon
rhomboides (Weinstein, Heck, Giebel & Gates, 1982), and the clupeid Brevoortia tyrannus (Lewis & Peters,
1984), but the authors in each case refrain from claiming the existence of an endogenous cellulase system
for their fish. Neither Klumpp & Nichols (1983) studying the south temperate hemirhamphid Hyporhamphus
melanochir nor Urquhart (1984) studying the north temperate stichaeid Cebidichthys violaceus found
significant cellulase activity in the guts of these plant-eating fishes. Unlike Klumpp & Nichols (1983) and
most other investigators who have measured the degradation of methylor carboxymethyl cellulose by an
enzyme extract, Urquhart (1984) assayed for glucose production from native, crystalline cellulose when the
latter was subjected to homogenates of gut tissue and gut contents prepared from specimens of C. violaceus.
He reasoned that native crystalline cellulose was a more appropriate substrate for the assay because it and
not methylor carboxymethyl-cellulose occurs in plant cell walls (Mackie & Preston, 1974). Future studies
should attempt to standardise the assay techniques and probably should use crystalline cellulose as a
substrate.
Other enzymes
The uncertainty surrounding cellulolytic enzymes is paralleled to a certain degree for the other digestive
enzymes known to occur in herbivorous fishes. Plant-eating fishes appear to produce the complement of
digestive enzymes found in other fishes although in different concentrations (Kapoor et al., 1975; Fange &
Grove, 1979), but a general lack of knowledge persists about digestive enzymes and their action in fish
herbivores, especially among marine species. A few general statements can be made, based on the reviews
of Kapoor et al. (1975) and Fange & Grove (1979), but even here inconsistencies expose the fragmentary
knowledge of enzymology in these herbivores. The gastric protease, pepsin, has optimal proteolytic activity
around pH2 but often has another maximum between pH3 and pH4. Pepsin is probably found in all fishes
169
except stomachless species. Apart from the appropriate pH of the stomach contents, proteolytic gastric
digestion is enhanced by a high pepsin concentration, high temperatures and intense stomach motility.
Other enzymes such as lipases, trypsin or its analogs, and several carbohydrases including amylase are
produced either in the pancreas or intestine and require a neutral or slightly alkaline environment for
activity. Enzyme production seems to be correlated with the composition of the diet, in particular, that
carbohydrases are produced in larger amounts in herbivores and proteases in greater quantities in carnivores.
For example, amylase activity is much higher in the freshwater herbivore Tilapia than in Perca, a carnivore
(Fish, 1960), and proteolytic activity is weak in the herbivorous surgeonfish Acanthurus triostegus
sandvicensis (Randall, 1961a). Moreover, stomachless fishes, which lack a pepsin, tend to be herbivores or
omnivores (Kapoor et al., 1975) and have nearly neutral or slightly alkaline guts (Klumpp & Nichols, 1983),
whereas carnivorous fishes, according to Kapoor et al. (1975), possess a true stomach in which peptic
digestion takes place. This statement helps to explain the weakly acidic to slightly alkaline digestive tracts of
such stomachless herbivores as odacids (Clements & Bellwood, 1988), scarids (Gohar & Latif, 1961b;
Smith & Paulson, 1974; Lobel, 1981) and hemiramphids (Klumpp & Nichols, 1983) because acidic guts in
these fishes would impede the action of intestinal enzymes. The Labridae, however, one of the largest
marine fish families (Nelson, 1984), is composed of species almost all of which are carnivorous, yet they
too are stomachless (Suyehiro, 1942; Al-Hussaini, 1947; Gohar & Latif, 1959) and have alkaline digestive
tracts (Gohar & Latif, 1961b). All carnivorous fishes, therefore, cannot be characterised as having true
stomachs and peptic digestion.
One of the most detailed series of studies on fish digestive enzymes is that by Gohar & Latif who
described the morphology (Gohar & Latif, 1959) and histology (Gohar & Latif, 196la) as well as trie
carbohydrases (Gohar & Latif, 1961b), lipases (Gohar & Latif, 1961c) and proteolytic enzymes (Gohar &
Latif, 1963) of the digestive tracts of some labrid and scarid fishes. These investigators found that the scarids
had much stronger amylase activity and somewhat greater lipase and protease activities than the labrids, a
pattern not completely in accord with the hypothesis of a close correlation between enzyme production and
diet. Gohar & Latif considered the labrids they studied to be carnivores, especially adept at crushing
mollusc shells in their pharyngeal jaws, and the scarids to be coral-feeders despite describing several structural
features of the digestive systems (grinding pharyngeal teeth, long intestine, large gut mucosal area) of these
fishes that suggest herbivorous habits.
DIGESTIVE MECHANISMS
How is the nutrition from seaweeds obtained? In other words, what mechanisms are found among
herbivorous fishes that allow them access to the nutrients locked inside algal cells? The emphasis here is on
the morphological and physiological specialisations of the herbivore gut. The available information is
placed into an expanded and somewhat modified version of Lobels (1981) framework of alimentary canal
types based on the relationship between their morphology and physiology and the digestibility of different
kinds of algae. Preceding this framework are discussions of gut length and the transit time of algal food
through the digestive tract, two measurable gut characteristics important for understanding the complexities
of food processing in herbivorous fishes. Following the discussion of alimentary canal types, the digestive
mechanisms of herbivorous fishes are analysed in the light of broader conceptual or comparative studies
involving both herbivorous and non-herbivorous animals. The subjects of these studies are animal guts as
chemical reactors, intestinal nutrient transport in different vertebrates, protein requirements of fishes and the
evolutionary responses of herbivores to plant nitrogen content.
170
MICHAEL H.HORN
Gut length
One of the most consistent and widely recognised features of herbivorous fishes is that with few exceptions
their digestive tracts are longer than those of non-herbivorous species of equivalent size. This pattern is seen
in several fish families exhibiting a variety of feeding modes including the Blenniidae (Goldschmid,
Kotrschal & Wirtz, 1984; Kotrschal & Thomson, 1986), Gobiidae (Geevarghese, 1983), Pomacentridae
(Emery, 1973) and Stichaeidae (Barton, 1982). Increased gut length is also reported in those species that
represent the only taxa that resort to occasional or seasonal herbivory in otherwise carnivorous fish families
such as the Myctophidae (Robison, 1984) and Scorpaenidae (Hallacher & Roberts, 1985). Most herbivorous
fishes begin life as carnivores or omnivores (White, 1985) before adopting a stricter plant diet as adults. Not
surprisingly, increased gut length accompanies the ontogenetic shift to herbivory as has been documented
for a variety of plant-eating taxa including odacids (Clements, 1985), pomacentrids (Emery, 1973; Lassuy,
1984), sparids (Christensen, 1978; Ogburn, 1984; Stoner & Livingston, 1984) and stichaeids (Montgomery,
1977; Barton, 1982). Relative gut length, however, does not always continue to increase with size, but may
level off or even decline slightly when the fish reaches a certain length (Emery, 1973; Montgomery, 1977;
Lassuy, 1984; Ogburn, 1984; Stoner & Livingston, 1984) and may reflect a critical period in the dietary
shift to herbivory.
Gut length is a convergent feature of herbivorous fishes in that taxonomically unrelated plant-eating fishes
share the characteristic of a relatively long digestive tract. Al-Hussaini (1947) in a still frequently cited
study arranged 60 species of Red Sea fishes into four categories based on their food habits and relative gut
lengths (defined as the distance from the posterior end of the pharynx to the anus divided by the distance
from the tip of the snout to the insertion of the caudal fin). Plankton-feeders had the shortest relative gut
lengths (0.50.7), carnivores the next (0.62.4), then omnivores (1.34.2) and herbivores the longest
relative gut lengths (3.76.0). Attempts to place species other than those studied by Al-Hussaini into this
framework can be misleading, and, for several reasons, precautions are required in deriving the trophic
status of fishes from their gut lengths (see Table III). First, many fishes now known to be rather strict
herbivores have shorter guts than those in Al-Hussainis herbivore category including parrotfishes, which he
considered to be coral-feeders. Stomachless herbivorous fishes, in particular, have relatively short guts. For
example, Odax pullus has a relative gut length of around 1.5 and Scarus rubroviolaceus one of about 2.0
(Clements & Bellwood, 1988). A more extreme example is the hemiramphid Hyporhamphus melanochir,
which has a relative gut length of 0.5 (Robertson & Klumpp, 1983). This species is an omnivore but
consumes large quantities of plant material, especially seagrasses, which it can digest with moderate
efficiency (Klumpp & Nichols, 1983). Other herbivorous fishes with true stomachs but relative gut lengths
less than 3.0 include the stichaeids Cebidichthys violaceus and Xiphister mucosus (Barton, 1982) and the
aplodactylid Aplodactylus arctidens (Clements, 1985). A second precaution is that gut length can vary with
nutritional status of the fish. Montgomery & Pollak (1988) showed that the relative gut length of the
surgeonfish Acanthurus nigrofuscus decreases by 3050% during periods of starvation of only several hours
to about two days. The mullet Mugil cephalus appears to grow a longer gut when consuming a diet
relatively high in detritus compared to algal material (Odum, 1970) although Collins (1981) found the
reverse pattern, and the cyprinid Cyprinus carpio has a longer intestine when fed a diet containing increased
amounts of glucose (Buddington, 1987). A third precaution is that the surface area of the intestinal mucosa
per body weight or volume may actually decrease with size in some herbivorous fishes (Al-Hussaini, 1949;
Gohar & Latif, 1959; Montgomery, 1977). These reported declines in absorptive surface area may be related
to the lower metabolic rates of larger fish, but further studies using additional specimens and other species are
required before definitive conclusions can be drawn about this relationship.
171
What is the importance of increased gut length in herbivorous fishes? The pervasiveness of this trait
among plant-eating fishes suggests that it is important for the digestive processes of these fishes. Sibly &
Calow (1986) argued on theoretical grounds that animals eating relatively poor quality food should have
larger digestive chambers, other factors being equal. The net rate of obtaining energy is a product of (1) the
weight of material in the digestive tract and (2) the amount of energy yielded from the material for a given
retention period. The second quantity in the product is lower for a poorer quality food. So, for a given
nutritional requirement, the animal must carry a greater weight of digesta (the first quantity in the product
above). This relationship, according to Sibly & Calow (1986), provides an explanation for the widespread
observation that animals sustaining themselves on poorer quality food have larger guts. The food processing
actions of herbivorous fishes with a long, coiled or looped intestine seem to be consistent with this model in
that the large quantities of high fibre, low nutrient food they ingest are distributed along the extensive
surface area of the intestine to maximise
TABLE III
Relative gut lengths of some marine herbivorous fishes
Familyspecies
Feeding type
Relative gut length
Acanthuridae
Acanthurus achilles
Acanthurus glaucopareius
Acanthurus guttatus
Acanthurus leucopareius
Acanthurus sandvicensis
Acanthurus nigroris
Acanthurus dussumieri
Acanthurus mata
Browser
Browser
Browser
Browser
Browser
Browser
Browser/grazer
Grazer/browser
Grazer
5.2
4.9
4.6
6.9
4.0
5.8
4.4
3.0
3.8
Dimensions of ratio
Reference
Jones, 1968
Jones, 1968
Jones, 1968
Jones, 1968
Jones, 1968
Jones, 1968
Jones, 1968
Jones, 1968
Jones, 1968
Familyspecies
Feeding type
Relative gut length Dimensions of ratio Reference
Ctenochaetus
hawaiiensis
Naso brevirostris
Naso lituratus
Naso unicornis
Zebrasoma flavescens
Zebrasoma veliferum
Grazer
Grazer
3.4
3.5
Jones, 1968
Jones, 1968
Grazer
Browser
Browser
Browser
Browser
Browser
Browser
3.5
2.2
3.2
3:2
3.7
3.7
3.0 (08001600 h)
Jones, 1968
Jones, 1968
Jones, 1968
Jones, 1968
Jones, 1968
Jones, 1968
Montgomery & Pollak,
1988
2.3 (18000600 h)
1.4 (starved 48h)
1.9 (starved and fed)
172
MICHAEL H.HORN
Aplodactylidae
Aplodactylus arctidens
Blenniidae
Salarias fasciatus
Blennius sanguinolentus
Entomacrodus chiostictus
Ophioblennius steindachneri
Girellidae
Girella elevata
Girella tricuspidata
Gobiidae
Boleophthalmus pectinorostris
Awous stamineus
Pseudogobius javanicus
Familyspecies
Hemiramphidae
Hyporhamphus melanochir
Kyphosidae
Kyphosus tahmel
Kyphosus cornelii
Kyphosus sydneyanus
Mugilidae
Mugil auratus
Aldrichetta forsteri
Liza argentea
Liza dussumieri
Mugil cephalus
Grazer
1.61.8
Clements, 1985
Grazer
Grazer
Grazer
Grazer
4.1
2.4
2.5
4.8
Al-Hussaini, 1947
Goldschmid, Kotrschal & Wirtz, 1984
Kotrschal & Thomson, 1986
Kortschal & Thomson, 1986
Browser/grazer
2.1 (adults)
Browser/grazer
1.7 (juveniles)
Bell, Burchmore & Pollard, 1980
1.92.9
Anderson, 1986
Grazer?
Grazer?
Grazer?
6.0
1.5
1.3
Suyehiro, 1942
Geevarghese, 1983
Geevarghese, 1983
Feeding type Relative gut length Dimensions of ratio Reference

Browser
0.5
Robertson & Klumpp, 1983
Browser?
Browser
Browser
4.1
4.6
4.0
Al-Hussaini, 1947
Rimmer & Wiebe, 1987
Grazer
Grazer
Grazer
Grazer
Grazer
3.7
5.55.7
5.55.7
5.55.7
5.55.7
Al-Hussaini, 1947
Thomson, 1954
Thomson, 1954
Thomson, 1954
Thomson, 1954
Mugil georgii
Myxus elongatus
Mugil cephalus
Grazer
Grazer
Grazer
Liza dumerilii
Liza richardsonii
Liza tricuspidens
Mugil cephalus
Grazer
Grazer
Grazer
Grazer
Odacidae
5.55.7
5.55.7
3.25.5
(depending on diet)
2.42.5
2.52.7
2.12.5
4.55.2
(slightly longer in smaller fish)
Thomson, 1954
Thomson, 1954
Odum, 1970
Marais, 1980
Marais, 1980
Marais, 1980
Marais, 1980
Odax pullus
Pomacentridae
Stegastes lividus
Plectroglyphidodon lacrymatus
Scaridae
Pseudoscarus ghobbam
Browser
1.5
Clements & Bellwood, 1988
Browser
Grazer
4.4
8.510.0
Lassuy, 1984
Polunin, 1988
Grazer
1.41.6
Gohar & Latif, 1959
173
Familyspecies
Feeding type Relative gut length
Dimensions of ratio Reference
Pseudoscarus harid
Scarus rubroviolaceus
Siganidae
Siganus fuscescens
Siganus spinus
Sparidae
Sarpa salpa
1.4 (juveniles)
2.7 (adults)
2.3 (adults)
Archosargus
probatocephalus
2.02.1 (adults)
Stichaeidae
Xiphister mucosus
Grazer
Grazer
1.61.9
2.1
Gohar & Latif, 1959

Clements & Bellwood, 1988
Browser
Browser
2.53.0
3.54.0
Suyehiro, 1942
Bryan, 1975
Browser
0.9 (small juveniles)
Christensen, 1978
Browser
Gerking, 1984
1.7 (juveniles)
Ogburn, 1984
Browser
Browser
1.1
0.8
Barton, 1982
Barton, 1982
digestion and assimilation (see Buddington, Chen & Diamond, 1987). Intestinal surface area is, of course,
constrained by the size of the body cavity and the size and shape of the fish (Montgomery, 1977). Kotrschal
& Thomson (1986) speculated that, although the smallest reef fishes (e.g. chaenopsids) should be grazers
like certain blennies (Nursall, 1981) because such a feeding habit minimises handling time and thereby reduces
the threat of predators, these species are not herbivores probably because gut length is constrained by the
small body size. Another possible function of a long intestine in herbivorous fishes is reabsorption of
proteolytic enzymes thereby conserving protein, which is often in short supply for plant-eating animals.
Hofer & Shiemer (1981) found evidence for active reabsorption of these enzymes in some herbivorous and
omnivorous freshwater fishes. The efficiency of reabsorption reached an optimum at relative gut lengths of
2.53.0. This avenue of research might be usefully extended to marine species.
Gut transit times
Gut transit time, or gut retention time, is the interval of time required for a particle of food to pass through
the digestive tract and the undigested portion voided as faeces. Gastric evacuation time is a component of this
interval, and both are often expressed as rates (Fnge & Grove, 1979). Methods used to measure the rate of
movement of food through the digestive tract include serial killing of individuals in an experimental
laboratory population, monitoring of food translocation by X-radiography of an ingested opaque marker and
174
MICHAEL H.HORN
recording the time of appearance of coloured faeces after a dye has been incorporated into the food (Fange
& Grove, 1979). Gut transit time is a critical component in food processing by fishes because it influences
assimilation efficiencies and helps determine food consumption rates. The appetite offish appears to return
as the digestive tract empties (Fange & Grove, 1979; Grove & Crawford, 1980). Gut transit time (or rate)
varies with temperature, meal size, food type, fish size, method of feeding and feeding history of the fish
(Fange & Grove, 1979).
The frequently cited scenario that herbivorous fishes consume large quantities of plant material by
continuous feeding, pass the material rapidly through the gut and assimilate it with moderate efficiency
(Ogden & Lobel, 1978; Brett & Groves, 1979; Gerking, 1984; Pandian & Vivekanandan, 1985; Buddington
et al., 1987) is more fully understood in the context of herbivore diversity and the exceptions to the pattern.
Herbivores do appear to have shorter gut transit times although the data are sparse. The summaries of
gastric evacuation and total gut emptying times compiled by Fnge & Grove (1979) are heavily dominated
by carnivorous species, and almost all of the few herbivorous species are freshwater forms, both sets of data
reflecting the historical bias in species chosen for study. Although the values are strongly temperature
dependent, the total gut emptying times range from 10 to 158 h for carnivores and are mostly less than 10 h
for herbivores. Gut retention times for the few marine herbivores that have been studied are mostly tropical
species, and these times are also below 10 h (Table IV).
This mode of food processing, which involves the passing of ingesta across the large surface area of an
extended intestine, apparently results in a more favourable cost/benefit ratio for herbivores than the more
carnivore-like
TABLE IV
Time required for food to pass through the gut of some marine herbivorous fishes
Transit time, h
Familyspecies
Stomach Entire gut
Acanthuridae
Acanthurus triostegus sandvicensis
Hemiramphidae
Hyporhamphus melanochir
Kyphosidae
Kyphosus sydneyanus
Mugilidae
Mugil cephalus
Liza dumerilii
Liza falcipinnis
Pomacentridae
Stegastes lividus
Plectroglyphidodon lacrymatus
Scaridae
Scarus gibbus
Scarus jonesi
Temperature, C Reference
Randall, 1961a
4.4 (seagrass diet)

8.3 (crustacean diet)
17
Klumpp & Nichols, 1983
21
23
26
2026
?
?
Odum, 1970
Payne, 1978
Payne, 1978
4.5 (1 juvenile)
9.7, 9.9 (2 adults)
56
28
Lassuy, 1984
Polunin & Koike, 1987
46
46
?
?
Smith & Paulson, 1974

Smith & Paulson, 1974
3
3
175
Transit time, h
Familyspecies
Stomach Entire gut
Siganidae
Siganus spinus
Sparidae
Sarpa salpa
Stichaeidae
38
Temperature, C Reference
1.5 (juveniles)
23 (adults)
Bryan, 1975
Several
19
Gerking, 1984
53
15
Urquhart, 1984
actions of intermittent consumption, longer retention times and higher assimilation efficiencies. Studies on
feeding and digestion in the hemiramphid Hyporhamphus melanochir (Robertson & Klumpp, 1983;
Klumpp & Nichols, 1983) are instructive for this comparison. This warm temperate Australian fish feeds on
seagrass during the daytime but switches to crustaceans at night. It is a continuous feeder, and the seagrass
passes through the short tubular gut twice as fast as the crustacean food (4.4 compared with 8.3h; see
Table IV). The crustaceans are available only at night when they emerge into the water column; thus,
seagrass is much more available during the day than the crustaceans. The dilution of food quality by
inorganic material has been shown to increase ingestion and egestion rates in fishes, i.e., to decrease gut
emptying times (Rozin & Mayer, 1964; Lee & Putnam, 1973). Similarly, other studies, but on carnivores
with stomachs, have shown that gastric emptying times are faster in fish on low energy diets than those
consuming high energy meals (Jobling, 1980, 1987). Klumpp & Nichols (1983) argued, therefore, that the
indigestible fibre in seagrass may have the same effect on gut transit time in H. melanochir. Thus, rapid
passage of the seagrass material through the fishs short gut apparently results in the low assimilation
efficiencies (only 50% for protein) reported by these authors. Night-time consumption of crustaceans then
becomes, according to Klumpp & Nichols calculations, a necessary source of protein for the fish. H.
melanochir and other stomachless herbivores such as the odacids and scarids may be limited to rapid gut
transit times because of their short, simple guts although it is difficult to sort out the effects of this factor
from other influences. Clements & Bellwood (1988) speculated that the intestinal folds of Scarus
rubroviolaceus may slow laminar flow rates and thereby increase food retention times.
Exceptions to the above scenario are instructive and help illustrate the diversity of feeding modes and
food processing among marine herbivorous fishes. The cold temperate stichaeid Cebidichthys violaceus has
a gut transit time of greater than 50 hours (Urquhart, 1984; see Table IV), possibly the longest reported for a
herbivorous fish, and moderately high assimilation efficiencies (Edwards & Horn, 1982; Horn &
Neighbors, 1984; Horn, Neighbors & Murray, 1986). This sluggish fish is an intermittent feeder, apparently
consuming algae in its rocky intertidal habitat only on the incoming tide and then becoming inactive for
most of the diel cycle (Ralston & Horn, 1986). The time and energy required to digest and assimilate its
seaweed food at low temperatures may limit the fishs scope for activity. The warm temperate rudderfish
Kyphosus sydneyanus also appears to be an intermittent feeder and to have a relatively long gut transit time,
but for reasons different from those of Cebidichthys violaceus. Kyphosus sydneyanus has been shown to
have a microbial fermentation system in its hindgut (Rimmer & Wiebe, 1987). The gut retention time of 21
h (Rimmer & Wiebe, 1987; see Table IV) and feeding activity limited apparently to crepuscular periods
(Russell, 1983) seem to be traits appropriate to allow time for a batch of seaweed food to be broken down
by a microbial colony in the fishs caecum.
176
MICHAEL H.HORN
Fig 2.Digestive tracts of four species of fishes, each representing one of four types of alimentary canals in marine
herbivorous fishes; gut lengths but not other dimensions are drawn to the same scales as the fishes; salient features of
the four canal types are lettered consecutively; a=upper and lower jaw teeth of Acanthurus nigrofuscus; b=stomach of A.
nigrofuscus, consisting of a thin-walled, distensible cardiac region and a thin-walled but more muscular pyloric region;
c=close-set, sieve-like gill rakers of Mugil cephalus; d=thick-walled, muscular pyloric region (shaded) of the stomach
of M.cephalus; e=fused upper and lower jaw teeth of Scarus rubroviolaceus; I=lateral view of the upper and lower
pharyngeal bones of S. rubroviolaceus; g=hindgut caecum of Kyphosus sydneyanus, separated by valves (shaded areas)
from the intestine and the rectum; pyloric caeca, located at the junction of the stomach and intestine, range in number in
these four fishes from none in Scarus rubroviolaceus, to 2 in Mugil cephalus, to 5 in Acanthurus nigrofuscus to an
uncounted mass in Kyphosus sydneyanus; information for drawings: Acanthurus nigrofuscus (Jones, 1968); Mugil
cephalus (Thomson, 1966); Scarus rubroviolaceus (Clements & Bellwood, 1988); Kyphosus sydneyanus (Rimmer &
Wiebe, 1987); see Table V for further details and additional representative species of the four alimentary canal types.
TYPES OF ALIMENTARY CANALS

A central question in fish herbivory is how fishes gain access to the nutrients inside plant cell walls. Based
on the apparent absence of endogenous cellulolytic enzymes and a fermentative microflora in herbivorous
fishes, Lobel (1981) claimed that fish can digest seaweeds only if breakage of the cell occurs so that the fishs
regular complement of enzymes can react with the cell contents. He proposed that such breakage can occur
by either (1) lysis, resulting from acidic stomach secretions, or (2) mechanical action, resulting mainly from
trituration in a pharyngeal mill or gizzard-like stomach. Based on Lobels (1981) findings and those of more
recent studies, four types of alimentary canals are discussed below.
Highly acidic stomach (Type I)
Herbivorous fishes with thin-walled stomachs and no trituration mechanism other than the jaw bite appear
to use highly acidic stomach fluids to lyse algal cell walls (Fig 2; Table V). Acid lysis as a means of
releasing plant cell contents was first suggested by Fish (1960) and has since been demonstrated by
Moriarty (1973) and Bowen (1976) for freshwater cichlids and by Lobel (1981) and Urquhart (1984) in
laboratory tests simulating the acidic gastric pH environment of several herbivorous marine fishes. Gastric
pH levels drop to as low as 1.31.5 in the cichlids and are apparently sufficient to lyse the cells of bluegreen algae (Moriarty, 1973) and detrital bacteria (Bowen, 1976) eaten by these fishes. Lobel (1981) found
that the stomach pH of certain acanthurids, pomacanthids and pomacentrids ranged from 2.4 to 4.3
(Table V), acidities seemingly as effective as trituration in releasing the cell contents of some algal species.
He used spectrophotometry to measure the concentrations of cell contents released into the medium by the
acid treatments and noted that algae were differentially susceptible to acid lysis. This finding indicates that
an alga might be available but not digestible to a particular consumer. Urquhart (1984) obtained stomach pH
values of 2.22.5 (Table V) for the stichaeid Cebidichthys violaceus, and his laboratory simulations
TABLE V
Characteristics of four types of alimentary canals in marine herbivorous fishes with a list of representative species and
their gut pH values; first three types based on information in Lobel (1981); see Fig 2 for illustrations of these alimentary
canal types
Representative fishes
Family
Species
Stomach pH
Intestinal pH
Reference
I. Digestive mechanism: primarily chemical; acid lysis in stomach releases cell contents Gut morphology: thin-walled
stomach; long intestine Feeding type: mainly browsing
177
Representative fishes
Acanthuridae
Acanthurus lineatus
Acanthurus
triostegus
Zebrasoma
rostratum
Acanthurus
nigrofuscus
Chanidae
Pomacanthidae
Centropyge
flavissimus
Pomacentridae
Eupomacentrus
planifrons
Sparidae
Acanthurus
glaucopareius
4.2
4.3
4.2
7.3
3.2
7.07.2
3.76.2 (pyloric)
(depending on time
of collection &
feeding state)
Chanos chanos
(pyloric caeca)
Eupomacentrus
nigricans
2.4
Lobel, 1981
Lobel, 1981
Lobel, 1981
2.95.7 (cardiac)
Apolemichthys
xanthopunctatus
3.1
Lobel, 1981
1.96.6
(depending on diet)
3.0
Montgomery &
Pollak, 1988
Lobel, 1981
7.6
Lobel, 1981
Lobel, 1981
2.7
6.9
5.6
Lobel, 1981
Lobel, 1981
Archosargus
2.0
Ogburn, 1984
probatocephalus
Stichaeidae
Cebidichthys
3.0
7.37.9
Edwards & Horn,
violaceus
1982
2.22.5
Urquhart, 1984
II. Digestive mechanism: primarily mechanical; food ground in thick-walled, gizzard-like stomach; sediment ingested
to aid in grinding process Other gut morphology: long intestine Feeding type: mainly grazing
Acanthuridae
Acanthurus bleekeri 6.7
Lobel, 1981
Acanthurus gahhm
7.4
Lobel, 1981
Lobel, 1981
Acanthurus guttatusa 6.3
Acanthurus mata
6.5
Lobel, 1981
Acanthurus olivaceus 6.7
Lobel, 1981
Acanthurus
7.0
Lobel, 1981
xanthopterus
Ctenochaetus
7.1
Lobel, 1981
striatus
7.3
Lobel, 1981
Ctenochaetus
cyanoguttatus
Aplodactylidae
Aplodactylus
arctidensb
Clements, 1985
178
MICHAEL H.HORN
Mugildae
Crenimugil
7.9
6.8
Lobel, 1981
crenilabis
Liza dumerilii
7.08.5
8.5
Payne, 1978
Liza falcipinnis
2.05.0
8.5
Payne, 1978
Mugil cephalus
3.57.0
Moriarty, 1976
8.5
8.5
Payne, 1978
7.2
Lobel, 1981
Mugil curema
8.5
8.5
Payne, 1978
III. Digestive mechanism: primarily mechanical; food ground in pharyngeal mill; sediment ingested by grazers
Gut morphology: no stomach; moderately long intestine
Feeding type: grazing or browsing
Hemiramphidae
Hyporhamphus
6.57.0
Klumpp & Nichols,
melanochir
1983
Odacidae
Odax pullus
>8.1
Clements &
Bellwood, 1988
Gohar & Latif, 1961b
Scaridae
Pseudoscarus
6.16.8 (duodenum)
ghobbam
6.47.9 (posterior
limbs)
Pseudoscarus harid
6.16.8 (duodenum)
Gohar & Latif, 1961b
6.17.8 (posterior
limbs)
Scarus gibbus
6.4 (pyloric caecum)
Smith & Paulson,
6.46.5 (intestine)
1974
7.5 (rectum)
Smith & Paulson,
Scarus jonesi
1974
6.97.5 (intestine)
8.2 (rectum)
(feeding)
7.57.6 (intestine)
(nonfeeding)
Sparisoma radians
8.4 (anterior
Lobel, 1981
intestine)
8.6 (posterior
intestine)
IV. Digestive mechanism: primarily chemical; hindgut caecum for fermentation; acidic stomach but cell lysis not
apparent Other gut morphology: well-defined stomach; long intestine Feeding type: bro owsing
Kyphosidae
Kyphosus cornelii
2.93.9
5.77.5 (intestine)
Rimmer & Wiebe,
6.16.2 (caecum)
1987
6.4 (rectum)
2.83.0
6.48.2 (intestine)
Rimmer & Wiebe,
Kyphosus
6.36.7 (caecum)
1987
sydneyanus
6.57.0 (rectum)
a
b
This species is described as a browser with a thin-walled stomach by Jones (1968).

This species is reported not to ingest sediment (Clements, 1985).
179
showed that acid lysis of the cell walls of the green alga Ulva lobata significantly increased the
concentration of protein and carbohydrate in the medium compared to control solutions. Carbohydrates
leached into acidic solutions simulating the stomach fluids, whereas proteins leached into solutions
simulating the slightly alkaline environment of the intestine after the alga had been treated with acidic
solutions simulating those in the stomach.
The exact mechanism by which low pH causes cell lysis is poorly understood. Increased acidity appears
to weaken the hydrogen bonds between the cellulose units in terrestrial plant cell walls and, in effect, to
loosen or expand the cell walls (Wilkins, 1984), which presumably would allow the cell contents to leach
out through the cell wall. A similar mechanism may operate in seaweeds. As mentioned above, marine algae
are differentially affected by acidic conditions (Lobel, 1981). These differences may result from differences
in cell wall structure among the various groups of seaweeds.
Gut pH in fishes is influenced by a variety of factors and conditions. Lobel (1981) found that fishes with
thin-walled (non-gizzard-like) stomachs had more acidic stomach contents (mean pH of 3.4) than fishes
with thick-walled (gizzard-like) stomachs (mean pH of 7.0). Moreover, a thin-walled stomach increases in
acidity as it is filled and becomes distended (Randall, 196la; Smit, 1967, 1968; Moriarty, 1973; Norris,
Noms & Windell, 1973; Kapoor, Smit & Verighina, 1975; Lobel, 1981). Assimilation efficiency is
positively correlated with stomach fullness and acidity in the cichlid Tilapia nilotica (Moriarty, 1973).
Stomach pH also can vary with the type of food eaten. For example, Lobel (1981) reported a gastric pH of 1.
9 in the milkfish, Chanos chanos, when it had been feeding on green algae and a pH of 6.6 when the fish
had been eating invertebrates.
The stomach pH of carnivorous fishes, although not as acidic as in herbivores, may enable them to digest
algae to a certain degree or to take advantage of the filling effect of ingested seaweeds to lower acidity and
thereby enhance digestion of animal prey. Lobel (1981) has even proposed that gastric acidity in such fishes
may preadapt them to herbivory. Only moderate character evolution, such as an increase in gut length or a
change in jaw tooth shape or number, might allow increased herbivory in species belonging to otherwise
carnivorous families. For example, relatively long guts and increased consumption of algae distinguish
Ceratoscopelus warmingii from the other, carnivorous myctophid fishes (Robison, 1984) and Sebastes
mystinus from the other, carnivorous scorpaenid fishes in the genus Sebastes (Hallacher & Roberts, 1985).
Also, some carnivorous fishes are known to consume seaweeds when animal prey is scarce.
Zooplanktivorous damselfishes in the genera Amblyglyphidodon, Chromis and Pomacentrus eat drifting
algae where zooplankton is in low abundance (Hobson & Chess, 1978), and the scorpaenid Sebastes
mystinus, which feeds primarily on zooplankton during the upwelling season, consumes large quantities of
macroalgae during the non-upwelling season (Hallacher & Roberts, 1985).
In summary, acid lysis appears to be one of the principal mechanisms whereby certain herbivorous fishes
gain access to the nutrients inside algal cell walls. The alimentary canals of these fishes are perhaps the
least morphologically specialised of the plant-eating marine species. Algal types suitable as food for fishes
with this kind of alimentary canal should be primarily green and red algae with large cell sizes (Lobel,
1981). Lobel (1981) asserted that fishes with acidic stomachs are browsers rather than grazers so as to
minimise ingesting sand while feeding and thereby prevent the rapid buffering of stomach contents by
calcium carbonate material. All 12 species of acanthurids recognised as browsers by Jones (1968) have thinwalled stomachs. Other fishes in this category include the chanid, pomacentrids, pomacanthids, sparids and
stichaeids (Table V). Siganids have thin-walled stomachs and long intestines (Bryan, 1975) and may belong
in this category, but gastric pH apparently has not been measured in these fishes. Herbivorous blenniids
have long, coiled intestines and anterior intestinal swellings but lack a true stomach (Al-Hussaini, 1947;
Goldschmid, Kotrschal & Wirtz, 1984). These fishes may also belong in this category but, again, digestive
180
MICHAEL H.HORN
tract acidity apparently has not been recorded. It is of interest that the luderick Girella tricuspidata is the
only fish studied to date that has the ability to assimilate components of algal cell walls (Anderson, 1987).
The highly acidic (pH as low as 2) and muscular stomach of this fish (Anderson, 1986) probably contributes
to this ability. In having both of these traits, G. tricuspidata is intermediate between herbivorous fishes with
thin-walled, highly acidic stomachs and those with muscular, less acidic stomachs discussed below. Whether
the pharyngeal apparatus of G. tricuspidata, mentioned by Kaufman & Liem (1982), aids in rupturing cell
walls remains unknown.
Gizzard-like stomach (Type II)
A thick-walled, gizzard-like stomach represents one of the two mechanical means by which herbivorous
fishes rupture algal cell walls (Lobel, 1981). The proposed function of such a heavily muscularised stomach
is trituration of bacteria, blue-green algae, diatoms, and macroalgae, especially filamentous green and red
forms, ingested with sand or other inorganic material. Mugilids and certain acanthurids are the main groups
of herbivorous fishes with this type of alimentary canal (Fig 2; Table V). The mullet Mugil cephalus
typically feeds either by sucking up the surface layer of mud or by grazing on submerged rock or plant
surfaces (Odum, 1970). Sand or other sediment particles may comprise more than 50% of the stomach
contents (by weight) of M. cephalus (Collins, 1981). Grazing surgeonfishes in the genus Acanthurus can
commonly be seen moving in schools over the bottom picking up mouthfuls of sand (Jones, 1968). That the
gizzard-like stomach is a grinding organ is based upon observations of the condition of food before and
after passage through the stomach (Al-Hussaini, 1947; Pillay, 1953; Jones, 1968; Odum, 1968, 1970;
Payne, 1978).
Mullets (Mugilidae), perhaps the best known group of fishes with a gizzard-like stomach, seem to rely
solely (Payne, 1978) on the muscular, grinding action of the pyloric portion of the stomach and the abrasion
of sand grains to lyse the cells of bacteria and blue-green algae. Payne cites methods in microbiology that
tend to corroborate the effectiveness of the mullet grinding mechanism for lysing cells. Wet attrition milling
with the use of abrasives is known to lyse bacterial cells, and the resultant particle size can be as small as 0.
02 mm (Hughes, Wimpenny & Lloyd, 1971). Such milling is said to be particularly effective when the
abrasive is continually added as would be the case in feeding mullet. Furthermore, the uniform size of the
sand grains ingested (Odum, 1968) may increase the milling efficiency (Payne, 1978). Changes in
permeability resulting from the formation of cracks in the cell envelope during the grinding process may be
sufficient to lyse the cells (Hughes et al., 1971). The stomach contents of mullets become enveloped in a
stiff mucous membrane that Payne (1978) claims is a protective device for the stomach epithelium during
the grinding process.
Herbivorous fishes with thick-walled stomachs appear to have slightly acidic to slightly alkaline stomach
fluids (Table V). Although more highly acidic pH values (3.54.5) have been recorded for the mullets Liza
falcipinnis and Mugil cephalus, such acidities are thought to be insufficient to cause cell lysis (Moriarty,
1976; Payne, 1978). Gizzard-like stomachs have been reported to lack acid-secreting cells and proteolytic
enzymes (Ishida, 1935, 1936), but these findings are controversial (Lobel, 1981) because pepsin-producing
glands apparently have been found in a species of mullet (Pillay, 1953) and moderately low pH levels have
been recorded for two other mullets as noted above.
Fishes with gizzard-like stomachs tend to have shorter guts than species with thin-walled stomachs, at least
within the Acanthuridae. Among the herbivorous surgeonfishes studied by Jones (1968), four species with
thick-walled stomachs had a mean relative gut length of 3.6 ( 0.2SD), whereas 12 species with thin-walled
stomachs had a mean length of 4.3 ( 1.3SD) Intestinal length in mullets may be greater than in those fishes
181
with thin-walled stomachs (see Fig 2, p. 219), but gut length in mullets varies according to diet although the
pattern is not clear. Odum (1970) found that a population of Mugil cephalus feeding chiefly on plant
detritus in a salt marsh had longer intestines than a population consuming mainly diatoms in a seagrass bed.
Odum reasoned that a longer intestine is required to digest and assimilate detritus than diatoms. In contrast,
Collins (1981) reported that M.cephalus populations with a greater proportion of algae (mostly diatoms) in
their diets had longer intestines than those ingesting mainly detritus. The basis for this discrepancy between
intestinal length and diet data is unknown but might result from variations in importance of detrital amino
acids or differential digestibility of algae in the diets of mullets from different localities (Collins, 1981).
In summary, herbivorous fishes with thick-walled stomachs consume algae and microorganisms along
with quantities of sand or other sedimentary material, which apparently aids in the rupture of cells during
the grinding process in the stomach. Fishes in this category are considered to be grazers (Lobel, 1981), and
they fit Jones (1968) definition of the term in that inorganic material is ingested in the feeding process. In
addition to the mullets and certain surgeonfishes, aplodactylids may also belong to this category (see
Table V, p.220). Clements (1985) reported that Aplodactylus arctidens has a muscular stomach and
tentatively classified the species among Lobels (1981) fishes with gizzard-like stomachs. Clements noted,
however, that gut pH data are lacking for A.arctidens and that, although the species is a non-selective
grazer, it does not swallow sand to aid in food preparation.
Pharyngeal mill (Type III)
A specialised pharyngeal apparatus represents the second of the two mechanical means by which
herbivorous fishes rupture algal cell walls (Lobel, 1981). In addition to the pharyngeal mill, fishes with this
type of alimentary canal have slightly acidic to alkaline digestive tracts and no stomach (Fig 2; Table V).
These alimentary canal features are found in scarids (Gohar & Latif, 1961b; Smith & Paulson, 1974; Lobel,
1981; Clements & Bellwood, 1988), odacids (Clements & Bellwood, 1988) and hemiramphids (Klumpp &
Nichols, 1983). Scarids are reported to lack acid-secreting cells (Gohar & Latif, 196la), so the slight acidity
of their intestines may result from bile secretions (Gohar & Latif, 1961b). The relative gut lengths of fishes
with pharyngeal mills are generally shorter than either those with highly acidic, thin-walled stomachs or
gizzard-like stomachs (Lobel, 1981; see Fig 2).
Scarids are the best known of the herbivorous fishes with a pharyngeal mill. As already indicated, they
use their fused jaw teeth either to graze algae from reef surfaces (Randall, 1967; Ogden, 1977; Lobel, 1981;
Clements & Bellwood, 1988) or to browse on seagrasses (Randall, 1967; Ogden, 1976; Thayer et al., 1984),
and then use their powerful pharyngeal apparatus to grind the food into small particles before it is passed
into the intestine (Randall, 1967; Ogden, 1977; Clements & Bellwood, 1988). The pharyngeal mill in
scarids is similar to that in cichlids, which like the scarids are members of a monophyletic assemblage of
pharyngognathous perciform fishes (Liem & Greenwood, 1981; Kaufman & Liem, 1982), but cichlids have
retained a thin-walled acidic stomach (Lobel, 1981). The inorganic material ingested by parrotfishes is
mostly calcium carbonate, whereas that which might be swallowed by the freshwater cichlids while feeding
is inert silica (Lobel, 1981).
Odacids are labroid fishes closely related to scarids. Both taxa have been included in the Labridae (Liem
& Greenwood, 1981; Kaufman & Liem, 1982) based primarily on osteological and myological characters
associated with the feeding apparatus. Richards & Leis (1984), however, advocated separate family status
for labrids, scarids and odacids based on early life history characters. In either case, odacids have fused jaw
teeth like scarids and a true diarthrosis in the pharyngeal jaws (Kaufman & Liem, 1982) characteristic of the
labroid lineage. Odax pullus, the only herbivorous odacid in which food and feeding have been studied in
182
MICHAEL H.HORN
detail, browses on brown macroalgae and shreds but does not grind its food in the pharyngeal apparatus
(Clements, 1985; Clements & Bellwood, 1988). Its gut is relatively short and simple, and apparently no
sedimentary material is ingested. The alkaline fluids (pH>8.1) of the intestine may dissociate protein-tannin
complexes (Lobel, 1981) and allow O. pullus to feed mainly (Clements, 1985; Meekan, 1986; Clements &
Bellwood, 1988) on the brown seaweeds known (Estes & Steinberg, 1988) to have high phlorotannin
concentrations.
Hemiramphids are included in this category because, although they are mostly omnivorous, some species
eat seagrasses as a major portion of the diet (Thomson, 1959; Randall, 1967; Coetzee, 1981; Robertson &
Klumpp, 1983) and triturate the ingested plant material in a pharyngeal mill (Klumpp & Nichols, 1983).
The family is defined taxonomically by the third pair of upper pharyngeal bones being ankylosed into a
plate (Collette, McGowen, Parin & Mito, 1984). This plate is part of the pharyngeal apparatus, which is
similar in function to that of the unrelated labroid fishes but different in structure. In Hyporhamphus
melanochir, the gut is extremely short, a stomach is lacking and the intestinal pH ranges from slightly acidic
to neutral (Klumpp & Nichols, 1983).
Hindgut fermentation chamber (Type IV)
A fourth type of alimentary canal found in herbivorous fishes was not described by Lobel (1981), but he
recognised the possibility that intestinal microorganisms might be found in certain species with the ability to
digest plant cell walls. Since the publication of Lobels study, compelling evidence has been provided
(Rimmer & Wiebe, 1987) that two species of kyphosids in warm temperate to subtropical Australian waters
contain a hindgut microflora that can fermentatively digest seaweed material ingested by these fishes. The
two species, Kyphosus cornelii and K. sydneyanus, are large (60 80 cm in lenght), strictly herbivorous
fishes with long, coiled intestines and thin-walled caecum-like pouches near the posterior end of the intestine
(Fig 2; Table V). The capacity of these pouches is about 1.52 times the stomach volume. The pouches
were found to be well vascularised and separated by valves from the adjacent parts of the gut. In K.
sydneyanus the caecal pouch is single-lobed, whereas in K. cornelii the pouch contains two blind, lateral
sacs connected by valves to the median lobe. A short, vascularised rectum is separated by a distal valve from
the caecum. Food material taken from caecal pouches contained an abundant and diverse microflora of
bacteria and ciliated and flagellated protozoans, which were undetectable in the anterior part of the gut.
Rimmer & Wiebe (1987) claimed they found conclusive evidence of fermentation by recording the presence
of volatile fatty acids (VFAs) in the material sampled from the caecal pouch of these two fishes and the
rectum of K. sydneyanus. (VFAs are the assimilable, anaerobic degradation products following hydrolysis
of polysaccharides (e.g. cellulose) to their constituent sugars by the microfloral symbionts in the gut; see Smith
& Douglas, 1987). The VFA concentrations were slightly lower than those reported for the rumen contents
of sheep and cattle.
Several basic requirements must be met in order for a vertebrate to maintain an efficient gut microflora
(Bjorndal, 1987). These requirements include (1) constant, preferably elevated, body temperature; (2)
constant food supply; (3) slow passage of digesta to allow sufficient time for microbial reproduction; (4)
anaerobic conditions; (5) control of gut pH; and (6) removal of fermentation waste products. Most of these
requirements seem to be readily met by the two kyphosid fishes. The staples of their diets, red and brown
seaweeds, are abundant in their habitat. Gut transit time is a relatively slow 21 h, anaerobic conditions most
likely prevail in the caecal pouches and the caecal pH values measured by Rimmer & Wiebe were in a fairly
narrow range 6.16.2 for K. cornelii and 6.36.7 for K. sydneyanus. Samples from the rectum contained
many more lysed bacteria than did anterior regions of the gut, perhaps indicative of waste product removal.
183
The temperature requirement seems to be the most restrictive because these fishes live at latitudes where
temperatures would be expected to fluctuate to some extent with the season. Water temperatures, however,
varied only 4C (2226C) over the year at Rimmer & Wiebes (1987) collection site in coastal waters of
Western Australia (Rimmer, 1986). Apparently this temperature range is sufficiently narrow to allow
effective microbial fermentation in the digestive tracts of K. cornelii and K. sydneyanus.
The digestive tracts of the two kyphosids do not appear to fit readily into any of the three other types of
alimentary canals discussed above and first described by Lobel (1981). Pieces of algae are bitten off cleanly
and swallowed intact without trituration. Although the stomach fluids are strongly acidic in both K. cornelli
(pH 2.93.9) and K. sydneyanus (pH 2.83.0), lysis of algal cells was not apparent to Rimmer & Wiebe
(1987). Algae were softened but retained their natural colour and intact appearance before passing from the
stomach to the intestine. K. cornelii is known (Rimmer, 1986) to have a specialised gut by the time it settles
on to the reef as a juvenile and to have a resident microflora at sizes less than 40 mm fork length. The fishs
gut lengthens rapidly during the transition from an omnivorous to a strictly herbivorous diet.
Kyphosids, especially species in the genus Kyphosus, occur worldwide in warm temperate to tropical
waters and frequently eat brown seaweeds that are considered to be (Littler, Taylor & Littler, 1983b; Estes
& Steinberg, 1988) among the most chemically defended of marine plants. Comparison of digestive
mechanisms among kyphosid taxa and investigation of their apparent tolerance to seaweed defences should
be highly rewarding.
Symbiotic microorganisms have also been found in the guts of surgeonfishes, especially Acanthurus
nigrofuscus, in the Red Sea (Fishelson, Montgomery & Myrberg, 1985). The symbionts included bacteria,
flagellates and an undescribed protozoan that attains extremely high densities in the gut. Fishelson and coworkers found no evidence of fermentation, but reasoned that the location of the protozoan near the gut
lining and not in the food bolus meant that it is not involved in primary digestion. Two to three days of
starvation in A. nigrofuscus caused the elimination of the symbiont, and subsequent feeding by starved fish
that were released and observed foraging with other surgeonfishes did not re-establish the protozoan in the
gut (Montgomery & Pollak, 1988).
Small, unidentified flagellates have been found in the intestinal contents of Mugil cephalus by Odum
(1970) who thought they probably served to break down the cellulose walls of plant detritus particles. When
the flagellates disappeared from the gut after the fish was starved for 12 days, Odum concluded that they
were digested by the fish. He quoted earlier speculation that the intestinal tracts of many fishes become
sterile during periods when no food is ingested. Further study is required to understand the role of microbial
symbionts in the guts of mugilids, acanthurids and other fishes.
Conclusions on the types of alimentary canals
The four kinds of alimentary tracts discussed above provide a general framework for most of the different
groups of herbivorous fishes in the sea. Much more information, however, needs to be obtained on all of
these groups, and further research will undoubtedly lead to modification and greater resolution of this basic
model of digestive mechanisms. Gut pH seems certain to continue to be an important parameter of
herbivore alimentary canals, both as an instantaneous signal of food processing conditions and as a
predictive indicator of digestive function. Techniques should be devised to monitor continuously the pH in
the different parts of the herbivore digestive tract without causing undue stress to the fish. Recent work
showing that gut pH and even intestinal length are subject to short-term and local variations (Montgomery &
Pollak, 1988) emphasises the dynamic nature of fish digestive systems and underscores the need for more
detailed studies on the physiology and biochemistry of digestion in herbivorous fishes.
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MICHAEL H.HORN
HERBIVORE GUTS AS CHEMICAL REACTORS

One approach that holds promise for providing the needed greater resolution and precision on the
functioning of alimentary canals in herbivorous fishes is that of treating the gut as chemical reactor. This
avenue has recently been taken for animal guts in general and for deposit feeding invertebrates and
mammals with fermentative digestion in particular (Penry & Jumars, 1986, 1987). The purpose here is not
to provide a new analysis of the digestive tracts of herbivorous fishes in the context of chemical reactor
models but rather to describe briefly the general classes of reactors and suggest which herbivore digestive
mechanisms fit each of these classes. These tentative pairings might then serve as springboards for future
research.
An animals net rate of energy and nutrient gain are determined by foraging and digestion, two stages of a
single process (Penry & Jumars, 1986, 1987). Optimality models have stressed foraging but neglected
digestion, although, as Penry and Jumars indicate, digestive parameters are increasingly being taken into
account (e.g. Milton, 1981; Taghon, 1981; Troyer, 1984; Horn, Neighbors & Murray, 1986). Penry &
Jumars (1986) suggested that principles of chemical reactor theory can be used to formulate optimisation
constraints in a general theory of digestion and then followed those principles (Penry & Jumars, 1987) to
develop explicit models of digestion. These authors used performance equations and kinetic models of both
enzymatic catalysis and fermentative digestion to reveal functional relationships among initial
concentrations of the limiting food component, gut volume, gut retention time and digestive reaction kinetics.
An optimality approach that combines foraging and digestion seems especially relevant to herbivore studies
because food quality becomes a composite of a number of different measurable factors including
concentration of limiting components, susceptibility to degradation by the animals enzymes or microbes,
cost of producing enzymes or maintaining microbes and costs of adding new body tissues from breakdown
products of particular foods.
Three ideal theoretical models form the basis of all chemical reactor design: (1) batch reactors; (2) plugflow reactors; and (3) continuous-flow stirred-tank reactors. Batch reactors are filled with reactants,
continuously stirred during the reaction, and then emptied of products after a given reaction period. In plugflow reactors, reactants enter continuously and products exit continuously with no mixing along the flow
path. In continuous-flow stirred-tank reactors, reactants enter continuously and products continuously exit a
stirred vessel. The guts of animals eating discrete meals can be classified as batch reactors and those of
animals that eat continuously as either plug-flow or continuous-flow stirred-tank reactors.
Herbivorous fishes with thin-walled acidic stomachs or with gizzard-like stomachs seem to fit best the
continuous-flow stirred-tank model. In both of these groups ingestion and egestion rates are high in most
cases, and the food is subjected either to acid lysis or trituration in the stomach (the stirred tank) before
being passed into the rather long intestine. An apparent exception is the stichaeid Cebidichthys violaceus,
which has a thin-walled acidic stomach. This fish seems to represent more closely the batch reactor model
because of its intermittent feeding schedule, long gut retention times and generally sluggish lifestyle.
Although Penry & Jumars (1987) claimed by their analysis that batch processing is an undesirable digestive
mode, they admitted that a variety of animals use such a method, especially those with low metabolic
requirements and those that are time minimisers constrained to widely separated foraging intervals. They
listed hydras, hydroids, jellyfishes, sea anemones, corals, combjellies, some glycerid polychaetes, brittle
stars, starfishes and chaetognaths as animals that can be modelled as having batch-reactor guts.
Herbivorous fishes with a pharyngeal mill and no stomach seem to fit the plug-flow reactor model. These
fishes have high ingestion rates, relatively short guts and brief gut transit times. Food is apparently neither
stirred nor stored on route from the pharyngeal mill to the anus although intestinal peristalsis may provide
some stirring action. Penry & Jumars (1987) pointed out that an animal dependent on its own digestive
185
enzymes should function as a plug-flow reactor. The digestive tracts of geese, corophiid amphipods and
deposit-feeding polychaetes with simple tubular guts approximate plugflow reactors (Penry & Jumars,
1986).
Animals fermenting refractory materials (i.e. plants) should combine the continuous-flow stirred-tank and
plug-flow reactors in series (Penry & Jumars, 1987). Foregut fermenters should begin digestion with the
continuous-flow stirred-tank type of reactor, whereas hindgut fermenters should operate starting with the
plug-flow type. Therefore, the kyphosid fishes with a hindgut fermentation chamber have guts that are best
modelled as a combination of a plug-flow reactor and a continuous-flow stirred-tank reactor in sequence.
The distinctions between foregut and hindgut fermenters are incomplete in the Penry-Jumars analysis,
probably a reflection of the complexity of guts with both catalytic and fermentative modes of digestion.
This brief account tentatively shows that all four of the chemical reactor models and combinations are
represented among the alimentary types found in herbivorous fishes. A more detailed analysis of herbivore
digestive mechanisms in the context of these models should be rewarding.
INTESTINAL NUTRIENT TRANSPORT IN HERBIVOROUS FISHES
A component of digestive mechanisms in herbivorous fishes not yet considered in this review is that of
nutrient uptake across the intestinal wall. Does the uptake rate for different nutrients, in particular,
carbohydrate and protein, vary between herbivores and carnivores? First of all, uptake rates in general are
lower for fish intestines than those for mammal, bird and reptile intestines (Karasov, Buddington &
Diamond, 1985). Moreover, intestinal glucose absorption appears to be highest in herbivores, intermediate
in omnivores and lowest in carnivores within several vertebrate classes (Karasov et al., 1985) including
fishes (Ferraris & Ahearn, 1983). These findings indicate that the rate of intestinal glucose transport is
correlated with the carbohydrate content of the natural diet of each species.
More recently, Buddington, Chen & Diamond (1987) studied the ratio of proline to glucose uptake in two
carnivores (the salmonid Salmo gairdneri and the percichthyid Morone saxatilis), two omnivores (the
ictalurid Ictalurus punctatus and the acipenserid Acipenser transmontanus) and four herbivores (the
cyprinids Cyprinus carpio and Ctenopharyngodon idella, the cichlid Tilapia zillii and the stichaeid
Cebidichthys violaceus). The sole marine herbivore was C. violaceus, which was treated both as a carnivore
and a herbivore depending upon size because it is known (Montgomery, 1977; Barton, 1982; Horn, Murray
& Edwards, 1982) to undergo an ontogenetic shift from carnivory to herbivory. The authors fed all eight
species on the same manufactured diet and determined the uptake of proline and glucose by an in vitro,
everted intestinal sleeve technique. They found that the ratio of proline to glucose uptake decreased from
carnivores to omnivores to herbivores and that the intestines uptake capacity for glucose, a non-essential
nutrient, was much higher in the herbivores than in the carnivores. This result suggests, as do the earlier
studies cited above, that glucose transport is matched to the carbohydrate content of the natural diet. Proline
uptake, however, varied less among the eight species, apparently because species with different natural diets
still have similar protein requirements. Buddington et al. (1987) drew the conclusion that the species
differences in uptake are genetic adaptations not phenotypic responses because all the species were fed the
same diet.
This study seems to have shown real differences in intestinal uptake among fishes of different trophic
levels. The results, however, for the only marine herbivore in the study, Cebidichthys violaceus, are
problematical because of the experimental conditions used and because of the interpretation of results for
different-sized fish. C. violaceus was maintained in the laboratory at 19C, and the in vitro experiments
were performed at 20C. These temperatures would seldom if ever be experienced by this fish in its cold
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MICHAEL H.HORN
temperate coastal habitat (see Horn, Murray & Seapy, 1983; Murray & Horn, 1989), and C. violaceus is
known to show increased stress and mortality at these temperatures in other laboratory experiments (Riegle,
1976). The size range of C. violaceus examined was approximately 100370 mm total lenght (= fork lenght
in this case). Although Buddington et al. (1987) designated for unexplained reasons fish shorter than 120
mm as carnivores and longer than 120 mm as herbivores, stomach content data (Montgomery, 1977;
Barton, 1982; Horn et al., 1982) would indicate that all the fish they examined were herbivores. The diets of
fish as small as about 55 mm (total length) appear to consist almost totally of macroalgae (Horn et al.,
1982). The ratio of proline to glucose uptake for C. violaceus varied greatly, especially in the 100120 mm
size range, in which the highest values were 34 times greater than the lowest values. Perhaps this variation
in the ratio of proline to glucose uptake represents, at the level of the gut wall, the rapid shift from a
carnivore to a herbivore gut, but it leaves in question how presumably fast-growing juveniles in the size
range between 55 mm and 100120 mm survive as herbivores.
The conclusions drawn by Buddington et al. (1987) about fish herbivory seem to be over generalised
based on their examination of three freshwater species and one marine species. They state that herbivores
distribute their absorptive tissue along the surface of a long thin intestine, whereas carnivores concentrate it
in a short thick intestine or allocate much of it to the pyloric caeca. They then suggest that these differences
in allocation of absorptive tissue between carnivores and herbivores arise from the herbivores very high
food ingestion rates and fast intestinal transit times. Buddington and his co-workers reasoned that allocation
of absorptive tissue to pyloric caeca is incompatible with fast transit times because food material would
have to travel in and out of the blind caeca whereas the material transits the intestine only once. Nutrients
would have little time to diffuse down to the deeper absorptive cells of the thick mucosa of the caeca and
would thus be inefficiently assimilated. This scenario, however, is too narrow to accommodate the diversity
and complexity of herbivore alimentary canals and digestive mechanisms surveyed in the foregoing parts of
this review. Just two examples help to illustrate this point. First, all herbivores do not have fast gut transit
times. C. violaceus, the marine herbivore studied by Buddington et al. (1987), requires more than 50 h to
evacuate its digestive tract at 15C (Urquhart, 1984), and Kyphosus Sydney anus, a hindgut fermenter,
requires about 21 h at 23C (Rimmer & Wiebe, 1987). Secondly, although herbivores do commonly have
only a few (less than 10) pyloric caeca (see Suyehiro, 1942; Al-Hussaini, 1947) as Buddington et al. imply,
these caeca are numerous in kyphosids (Al-Hussaini, 1947; see Fig 2, p. 219) and number more than 100 in
girellids (Suyehiro, 1942; Bell, Burchmore, & Pollard, 1980; Anderson, 1988). Finally, on a more general
point, all herbivores do not have long thin intestines; some species have relatively short, apparently thicker
intestines (see Fig 2). As Penry & Jumars (1987) show in their plug-flow model, radial elaboration of
absorptive surface area and lengthening of the gut are not equivalent tactics if the gut is considered to be a
chemical reactor. A radial increase in the absorptive surface increases the uptake of digestive products at
any point along the gut. Both a radial increase and an elongation of the gut increases the surface area, but
lengthening increases the total gut volume as well. All other factors being equal, the resulting increase in
retention time increases the extent to which food materials are converted to digestive products. Increase in
surface area thus affects only the extent of absorption, whereas lengthening the gut influences both the
extent of absorption and the extent of reaction. Studies of a wider range of herbivorous fishes are required
before broad generalisations about digestive mechanisms in these fishes can be established.
PROTEIN REQUIREMENTS OF HERBIVOROUS FISHES
Do herbivorous fishes require as much protein in their diet as carnivorous species? This seems to be a
reasonable question to ask given the low protein content of plants (Mattson, 1980) and the low rates of
187
amino-acid transport in the intestines of herbivores (Buddington et al., 1987). Fishes, in general, have
traditionally been considered to require more dietary protein than other vertebrate animals (Cowey &
Sargent, 1979; Millikin, 1982; Pandian & Vivekanandan, 1985; Tacon & Cowey, 1985; Wilson & Halver,
1986). Whereas birds and mammals usually attain maximum growth on diets of 1225% protein, fishes are
reported to require diets with 3555% protein to achieve maximum growth rate. Pandian & Vivekanandan
(1985) argued that the low cost of maintaining body temperature and position in water, the ease with which
nitrogenous waste is excreted as ammonia in water and the capacity to digest protein efficiently regardless of
feeding habit have led to the high protein requirement and therefore to carnivory in the majority of fishes.
They concluded that omnivorous, herbivorous and detritivorous fishes have the same high protein needs as
carnivores, thus perpetuating the widely held view that herbivores and detritivores must digest
microorganisms attached to their algal and detrital food to satisfy this high protein requirement.
This view has recently been challenged by Bowen (1987) who, while not denying that herbivores may
use attached microorganisms, cited examples (Dabrowski, 1982; Bowen, 1984a,b) indicating that many
fishes that specialise as herbivores and detritivores in freshwater ecosystems maintain very large
populations on low protein diets. The same can be said for marine herbivorous fishes on tropical (Odum &
Odum, 1955; Hiatt & Strasburg, 1960) and temperate reefs (Russell, 1977, 1983). In a careful reassessment
of the protein requirements of fishes and terrestrial homeotherms, Bowen (1987) concluded that the two
animal groups differ only in relative protein concentration in the diet required for maximum growth rate. This
difference can be explained by the greater energy requirement of birds and mammals and does not reflect
absolute differences in protein requirement among these three vertebrate groups. Other measures of protein
requirement examined by Bowen suggest that these groups are remarkably similar in their use of protein as
a nutritional resource.
According to Bowen (1987), two circumstances have led to the conclusion that fishes have high protein
requirements (Bowen, 1987). First, the requirement for diets relatively high in protein has been
misinterpreted as a requirement for higher absolute amounts of protein. Bowens analysis, however,
indicates that the difference in dietary requirement of fishes and terrestrial homeotherms is in their need for
energy, not protein. To clarify the relationship between protein and energy requirements, nutritionists
working with vertebrates other than fishes have used protein, the less variable quantity, as the denominator
to form an E/P ratio (e.g. Sell, Hasiak & Owings, 1985) rather than the P/E ratio often used by fish
nutritionists such as Bowen (1984b). Second, most studies of digestive physiology and nutrition in fishes
have focused almost entirely on carnivorous species, yet the results have often been generalised to fishes of
all trophic levels. As more comparative studies similar to that by Buddington et al. (1987) are completed,
the digestive and metabolic specialisations of different taxa and trophic levels can be better understood.
According to Bowen (1987) the explanation for why many fishes on low protein diets achieve rapid
population growth probably resides not in unique nutritional requirements but in food choice and digestive
specialisations. Thus, the need for further research on the digestive mechanisms of herbivorous (and
detritivorous) fishes is expressed again in this review.
EVOLUTIONARY RESPONSES TO NITROGEN SHORTAGE
In an article focused primarily on terrestrial herbivores (insects and vertebrates), Mattson (1980) reviewed
the evidence that nitrogen is scarce and perhaps a limiting nutrient for many herbivores and that in response
to this selection pressure many herbivores have evolved behavioural, morphological, physiological and other
adaptations to cope with and use the nitrogen available in their environments. The responses in Mattsons
list are: (1) ability to find and use the most nitrogen-rich plants or plant parts; (2) increased consumption
188
MICHAEL H.HORN
rates; (3) prolonged periods of feeding, digestion and development; (4) specialised alimentary canals and
digestive systems that rely on the presence and activity of endosymbionts or ectosymbionts; (5) occasional
carnivory (cannibalism and predation); (6) switching among plant parts and plant species; (7) regulation of
plant chemistry; and (8) evolution of larger body size. The purposes here are to consider briefly each of
these responses in turn for marine herbivorous fishes and thereby provide a concise and somewhat
speculative appraisal of the feeding behaviour and digestive mechanisms of these fishes in the context of
nitrogen limitation.
Some evidence is available to indicate that herbivorous fishes feed on the most nitrogen-rich plants or
plant parts. Other factors, however, complicate food choice, as has been discussed earlier in the review. For
example, the parrotfish Sparisoma radians feeds preferentially on the upper, older portions of turtlegrass
blades with microalgal epiphytes (Lobel & Ogden, 1981). These parts of the plant are lower in nitrogen but
also lower in phenolic compounds than the younger, basal leaf parts (Thayer et al., 1984).
Many, if not most, plant-eating fishes have higher consumption rates than those of non-herbivorous
species. These higher rates are usually accompanied by relatively short gut transit times. Important
exceptions to this pattern have been discussed earlier in this review.
Prolonged periods of feeding generally go together with increased consumption rates. Again, there are
exceptions, as in the intermittently feeding stichaeids and kyphosids. Apparently, prolonged periods of
digestion are not common in herbivorous fishes because the majority of species have short gut transit times.
Food material is retained in the gut for relatively long periods in cold temperate species (stichaeids) and
those with microbial fermentation (kyphosids), but no herbivorous fishes are known to have gut retention
times as long as the 5.5- to 7-day periods of iguanid lizards (Nagy & Shoemaker, 1984; Troyer, 1984) and
the 13-day period of the gopher tortoise (Bjorndal, 1987). A cellulolytic microflora is found in most, if not
all, tropical iguanids and this temperate tortoise (Bjorndal, 1987). Prolonged periods of development, such
as the extended life cycles of certain insects like the cicadas (Mattson, 1980), are not obvious features of
herbivorous fishes, but many plant-eating fishes are relatively large (see p. 234) and may be long-lived and
slow growing. For example, a 600-mm specimen of Kyphosus sydneyanus was estimated to be 49 years old
based on counts of otolith growth rings (Ayling & Cox, 1982).
Specialised alimentary canals and digestive systems that rely on endosymbionts are known for two
species of kyphosid fishes. Microbes are also abundant in the intestines of mullets and certain acanthurids.
Direct or indirect rles of gut microbes in the digestive physiology of herbivorous fishes will probably
become increasingly apparent as more species are studied in detail. Ectosymbionts, i.e., microorganisms
living on the surfaces of seaweeds and seagrasses, most likely contribute directly to the nutrition of
herbivorous fishes that consume these plants, but they also may play an important rle by breaking down
plant material and making it more usable to herbivores. Little definitive work has been done to demonstrate
either of these processes for marine herbivorous fishes although mullets have been shown to digest bacteria
and detritus and to have a resident microflora.
Several lines of evidence suggest that occasional carnivory is a response to nitrogen shortage and
therefore important to the nutrition of herbivorous fishes. First of all, carnivory on a small scale is inevitable
for virtually all herbivorous fishes whether they are browsers or grazers because small animals encrust or
otherwise dwell on the surfaces of foliose seaweeds or occur in close association with filamentous algae or
diatoms on the substratum. The contribution of these small amounts of animal material to the nutrition of
herbivorous fishes is essentially unknown. Omnivory, in which the diet is frequently composed of
substantial proportions of both plant and animal material, is widespread among fishes and perhaps could be
considered to be a response to nitrogen shortage but may also serve to dilute toxic materials that are
ingested. Conversely, consumption of algal material by largely carnivorous fishes with acidic stomachs
189
might serve as a filler that enhances digestion of animal material by stimulating flow of acid and thus
lowering gastric pH. Perhaps the most telling evidence of all that carnivory is a response to nitrogen shortage
is that all herbivorous fishes, with a few apparent exceptions such as the gobiescocid Sicyases sanguineus
(Cancino & Castilla, 1988), probably begin life as carnivores. Even in Kyphosus cornelii, which apparently
acquires its intestinal microflora as a small juvenile, some animal material contributes to the diet at this
stage before the fish shifts to strict herbivory (Rimmer, 1986). White (1985) has gone so far as to assert that
with few exceptions the young of all herbivores are not herbivores. Rather, they have near total dependence
on access to animal or microbial protein for survival and growth. Finally, on a more anecdotal level,
herbivorous fishes such as Girella nigricans and Medialuna californiensis (North, 1973), Odax pullus
(Clements, 1985) and certain scarids (Bakus, 1969; Hay, 1981a) have been observed to feed on animal material
offered to them in nature or captivity.
Switching among plant species or plant parts has not been well demonstrated in herbivorous fishes apart
from spatial or temporal changes in diet that seem largely driven by availability of preferred foods. In some
cases these foods are richer in nitrogen and protein but, again, the reasons for switching are often influenced
by a variety of factors.
Herbivorous fishes are not known to regulate plant chemistry in a manner parallel to certain insects and
ungulate mammals that secrete agents in their saliva that alter plant metabolism or promote plant growth
(see Mattson, 1980). Nevertheless, like terrestrial herbivores, fishes, especially those such as territorial
damselfishes, can enhance primary productivity presumably by their grazing or browsing activities
(Klumpp, McKinnon & Daniel, 1987) and may increase local nitrogen concentrations within their territories
through excretion and defaecation (Polunin & Koike, 1987).
Circumstantial evidence for the evolution of larger body size in herbivorous fishes is seen in data on diet
and maximum body length compiled for three families, Odacidae, Pomacentridae and Stichaeidae, each
composed of members with different feeding habits (Table VI). In each case the largest two or three species
are herbivores, whereas the smallest species are carnivores. Other vertebrates, including reptiles (Pough,
1973; Rand, 1978), birds (Morton, 1978) and mammals (Eisenberg, 1978), also show such a relationship
between body size and dietary mode.
Larger body size confers several advantages on the animal, and these may all be necessary on a nitrogenpoor diet (Mattson, 1980). Mattson cites the following advantages of increased body size. (1) Larger body
size increases
TABLE VI
Maximum body lengths of species in three marine fish families with carnivorous, herbivorous and omnivorous
(Pomacentridae only) members
Familyspecies
Trophic position
Maximum body length, mm Remarks
Odacidae, Australia and New Zealand. Gomon & Paxton. 1985

Odax pullus
Herbivore
750
All sizes are standard

lengths except total length
for O.pullus from Ayling &
Cox (1982). The list of
herbivorous species is from
M.J.Kingsford (pers.
comm.). S.argyrophanes is
an extremely slender
species. All species in the
family are listed.
190
MICHAEL H.HORN
Familyspecies
Trophic position
Siphonognathus
Carnivore
argyrophanes
Odax cyanoallix
Herbivore
Odax cyanomelas
Herbivore
Haletta semifasciata
Carnivore
Odax acroptilus
Herbivore
Siphonognathus radiatus
Carnivore
Neoodax balteatus
Herbivore
Siphonognathus attenuatus Carnivore
Siphonognathus beddomei
Carnivore
Siphonognathus tanyourus Carnivore
Siphonognathus caninus
Carnivore
Pomacentridae, Florida Keys, Emery, 1973
Abudefduf taurus
Herbivore

400
350
350
290
240
180
140
120
120
110
100
250
Microspathodon chrysurus Herbivore

200
Abudefduf saxatilis
Omnivore
180
Chromis multilineata
Carnivore (zooplanktivore) 165
Eupomacentrus fuscus
Omnivore
150
Eupomacentrus planifrons Herbivore
125
Eupomacentrus variabilis
Omnivore
125
Chromis cyanea
Eupomacentrus partitus
Herbivore
100
Eupomacentrus
Omnivore
100
leucostictus
Chromis enchrysurus
Chromis insolatus
Chromis scotti
Stichaeidae, Alaska to Baja California, Eschmeyer, Herald & Hammann, 1983
Herbivore
760
All sizes are total lengths

from Randall (1968) or
Robins, Ray & Douglass
(1986). All species studied
by Emery (1973) are listed
except an unidentified
species of Eupomacentrus.
All sizes are total lengths,

C. violaceus and X.
mucosus are known to be
herbivores (Horn, Murray
& Edwards, 1982; Barton,
1982). All other species are
listed as carnivores because
of lack of evidence of
herbivory. The species
listed include all those
Familyspecies
Trophic position
Xiphister mucosus
Lumpenus sagitta
Chirolophis decoratus
Stichaeopsis sp.
Lumpenella longirostris
Bryozoichthys marjorius
Xiphister atropurpureus
Poroclinus rothrocki
Stichaeus punctatus
Anoplarchus purpurescens
Phytichthys chirus
Herbivore
Carnivore
Carnivore
Carnivore
Carnivore
Carnivore
Carnivore
Carnivore
Carnivore
Carnivore
Carnivore
191

reported by Eschmeyer,
Herald & Hammann (1983)
to occur in the region.
580
510
420
320
310
300
300
250
220
200
200
Familyspecies
Trophic position
Maximum body length, mm
Plagiogrammus hopkinsii
Lumpenus maculatus
Chirolophis nugator
Anisarchus medius
Kasatkia sp.
Plectobranchus evides
Anoplarchus insignis
Allolumpenus hypochromus
Carnivore
Carnivore
Carnivore
Carnivore
Carnivore
Carnivore
Carnivore
Carnivore
200
180
150
140
140
130
120
75
Remarks
efficiency of locomotion thus permitting wider foraging for higher volume consumption. (2) Larger animals
have lower mass-specific energy requirements and therefore need to extract less energy per unit of ingested
material than do smaller animals. (3) Lower respiration rates mean that on equivalent diets larger animals
should have higher food conversion efficiencies than smaller species. (4) Larger size may also confer
mechanical advantages in foraging because low nitrogen levels usually accompany increased toughness of
plant tissues. (5) Finally, larger body size may be necessary for the development of complex digestive
systems important for breaking down nitrogen-poor, refractory plant foods. Both Demment & Van Soest
(1985) and Penry & Jumars (1987) provide evidence to show that the extent to which refractory plant
material is digested increases with body size. All of these advantages seem as applicable to fish herbivores
as to other plant-eating vertebrates.
ECOLOGICAL IMPACTS OF HERBIVOROUS FISHES
Herbivorous fishes by their grazing and browsing activities affect shallow water benthic communities,
especially those of tropical reefs, in a variety of ways. Their scrapings and excavations of hard substrata
192
MICHAEL H.HORN
contribute to erosional and sedimentary processes and their intensive cropping of algal stands influences the
composition, abundance and spatial patterns of seaweed populations. In addition, territorial defence,
especially as exhibited by damselfishes, protects algal stands from other, roving herbivorous species and
creates a mosaic of lush algal growth inside territories and heavily cropped zones outside the territories.
These ecological impacts in coral reef habitats represent perhaps the most intensively studied topic in all of
fish herbivory over the past 1520 years (see recent reviews by Sale, 1980; Borowitzka, 1981; Lubchenco &
Gaines, 1981; Gaines & Lubchenco, 1982; Hixon, 1983, 1986; Chapman, 1986). This section of the present
review is divided into tropical and temperate segments and concentrates on tropical habitats, especially
coral reefs, where the great majority of the studies have been conducted. The topics discussed are the
contribution of herbivorous fishes to bioerosion and sedimentation on coral reefs, the distributions of
herbivorous fishes across the reef environment, the impacts of roving (largely non-territorial) fish
herbivores on the structure of seaweed communities, the relative importance of grazing by fishes and sea
urchins in reef habitats and the effects of territorial damselfishes on the diversity and abundance of algal
assemblages and other reef inhabitants.
TROPICAL HABITATS
Bioerosion and sediment formation
Grazers were defined earlier in the review as those fishes (and invertebrates) that in the course of feeding
ingest some inorganic material from the substratum. They bite, rasp or scrape off pieces of the substratum
and subsequently excrete the material as sediment. The effects of this grazing on the erosion of coral reefs
and on the production of carbonate sediments has been documented for fishes (Cloud, 1959; Bardach, 1961;
Gygi, 1969; Glynn, 1973; Randall, 1974; Ogden, 1977; Hutchings, 1986; Sammarco, Carleton & Risk,
1986) and for a variety of invertebrates (Scoffin et al., 1980; Hutchings, 1986).
Parrotfishes and surgeonfishes are the major bio-eroders and sediment producers among herbivorous
fishes (Hiatt & Strasburg, 1960; Randall, 1967, 1974; Gygi, 1969, 1975; Ogden, 1977; Frydl & Stearn,
1978, Sammarco et al., 1986). With their heavy beaklike jaws and pharyngeal mill, parrotfishes break down
pieces of dead coral skeleton and calcareous red and green algae into fine sand and silt (Ogden, 1977). They
digest the algal tissue and void as faeces the fine, inorganic material, which has been shown to comprise an
average of 70% of the dried gut contents of Caribbean scarids (Randall, 1967). Their high ingestion rates
and fast gut transit times are typical of many tropical herbivorous fishes and result in the frequent passage
(Hiatt & Strasburg, 1960) of faeces as great masses of calcareous powder. Ogden (1977) determined that at
Isla Pico Feo in Caribbean waters of Panama Scarus croicensis fed 8 h each day (data from Ogden &
Buckman, 1973) and defaecated 50 mg (dry weight) in each of 20 defaecations per day. Based on an
estimated population of 3200 at Pico Feo, S. croicensis would deposit 7300 kg/year of sediment on the reef.
Assuming that half of the carbonate material deposited consists of sediment already present on the reef,
Ogden calculated that the fish produces new carbonate sediment at the rate of 0.49 kg.m2.yr1. This
estimate, however, was considerably lower than those he calculated for the sea urchins Diadema antillarum
(4.6 kg.m2.yr1) and Echinometra lucunter (3.9 kg.m2.yr1). Although Ogden (1977) admitted that
estimates of turnover for both fish and sea urchin grazers were subject to some major sources of error, he
concluded that such grazers are important contributors to geological and biological processes on coral reefs
and therefore to the physical structure of reef ecosystems.
The surgeonfishes that ingest sand are grazers on filamentous algae, diatoms and detritus (Jones, 1968).
These fishes have thick-walled, muscular stomachs in which they presumably use the inorganic material to
193
grind the food into finer particles to make more of the cell contents available for digestion (Hiatt &
Strasburg, 1960; Randall, 1967; Jones, 1968).
Surgeonfishes in the genus Ctenochaetus are sediment feeders and have long, flexible teeth with spatulate
tips, gill rakers bearing many very fine teeth and bristles and a muscular, gizzard-like stomach (Jones,
1968). The teeth on the upper and lower jaws function as opposing brooms, and the fishes appear to use
them to sweep and suck up fine material from the reef. The flexibility of the teeth apparently allows the fish
to scrape irregular rock surfaces and comb attached algal thalli to remove adhering detritus and diatoms
(Jones, 1968).
A member of the genus Ctenochaetus, C. striatus, recently has been reported to reduce the sizes of
ingested carbonate particles on the reef flat at Moorea, French Polynesia (Nelson & Wilkins, 1988). Mean
particle size in stomach samples of this fish were smaller than those in the feeding area, and particle sizes in
the rectal contents were smaller than those in stomach samples. Nelson & Wilkins hypothesised that
grinding of ingested materials by the muscular stomach of C. striatus was responsible for the observed
reduction in size of particles as the particles pass through the gut. This view is consistent with that of
Randall (1974) who asserted that particle size is undoubtedly reduced in the stomach of surgeonfishes with
muscular stomachs. That particle size is smaller in the rectum than in the stomach of C. striatus is the
expected result of grinding action in the stomach, but the reduction in particle size from the sediments to the
stomach could also occur if the fish selects smaller particles when feeding. Nelson & Wilkins acknowledged
this possibility but failed to mention the elaborate, finely divided gill raker apparatus of C. striatus that
Jones (1968) proposed would be highly effective in handling the fine particulate matter ingested. Mullets,
which also have an average particle size in their stomachs that is smaller than those in the sediments,
apparently feed selectively on the smaller, nutrient-rich particles (Odum, 1968; Marais, 1980). Mullets have
a pharyngeal filtering device (Ebeling, 1957) that they use to select the very fine particles from sediments of
various sizes (Odum, 1968). Whether the surgeonfish C. striatus selectively ingests smaller particles or
mechanically reduces particle size in the stomach or both remains an important but unanswered question.
Regardless of the process, C. striatus produces smaller particles than those found in ingested sediments
and, therefore, probably has a local impact on the particle-size distributions of sediments within reef and
lagoon habitats. Nelson & Wilkins (1988) found that C. striatus has relatively low assimilation efficiencies
(Table II) for total organic matter (20%) and nitrogen (37%) but cited evidence (Barlow, 1974b) that
Ctenochaetus species have high feeding rates, which may compensate for the low assimilation efficiencies.
Species in this genus are also known to be among the most abundant fishes on tropical reefs (e.g. Jones,
1968; Bouchon-Navaro & Harmelin-Vivien, 1981; Robertson & Gaines, 1986). Thus, given the high
abundance and probable high feeding rate of C. striatus, it is reasonable to predict that the fish significantly
influences particle size distributions in coral reef habitats. One consequence of particle size reduction is that
finer sediments have more surface area available for microbial colonisation, which enhances sediment
productivity (Moriarty et al., 1985; Yamamoto & Lopez, 1985).
Impacts of roving herbivorous fishes
Free-ranging herbivorous fishes are not uniformly distributed across tropical reefs, and the spatial patterns
they form are relevant to a consideration of the impacts of these fishes on algal communities. Spatial
distributions on coral reefs Plant-eating fishes are most common at the shallower depths on tropical reefs.
Ranges of 06 m (Gosline, 1965) and 010 m (Bakus, 1969) have been given as the depths of greatest
abundance although some species can be found at considerably greater depths. In a survey of deep reefs (30
180 m) by small submersible at Enewetak, Marshall Islands, Thresher & Colin (1986) found that
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MICHAEL H.HORN
Fig 3.Abundances of five guilds of herbivorous fishes in five sections of six different coral reefs on the central Great
Barrier Reef; black bars represent midshelf reefs, white bars represent outershelf reefs; suckers and scrapers are types of
grazers, and croppers are browsers; suckers of fine sediments include surgeonfishes in the genus Ctenochaetus; sand
suckers include the surgeonfishes Acanthurus dussumieri, A.mata and A.nigricauda; scrapers include several species of
parrotfishes in the genus Scarus, e.g. S. brevifilis, S. gibbus, and S. rivulatus; large croppers include the surgeonfishes
Acanthurus lineatus and Naso lituratus and the rabbitfish Siganus doliatus; small croppers include the surgeonfishes
Acanthurus glaucopareius and A. nigrofuscus; from Russ (1984b).
herbivorous fishes were most abundant at the shallowest depth (30 m) of the survey and disappeared by 90
m. Although space limitations or limited recruitment rates have been proposed (Sale, 1980) as more
important than food abundance in affecting the distribution and abundance of reef fishes, Thresher & Colin
(1986) asserted that the depth distributions of herbivores (and coralivores) are ultimately constrained by
their food supply, i.e., by light-dependent organisms.
Acanthurids and scarids, the two major groups of large, roving herbivorous fishes associated with coral
reefs, have generally different depth distributions. Acanthurids tend to predominate in shallow habitats,
whereas scarids occur more prominently in deeper zones. This pattern has prevailed in studies in the
Caribbean (Randall, 1963; Lewis & Wainwright, 1985), Red Sea (Bouchon-Navaro & Harmelin-Vivien,
1981) and Indo-Pacific (Bradbury & Goeden, 1974; Jones & Chase, 1975) and, therefore, may be typical of
acanthurid and scarid distributions in many reef systems. These depth differences combined with
differences in feeding behaviour and food preferences of these two major members of the roving herbivore
guild suggest that algal populations in different depth zones are subject to different grazing and browsing
pressures.
The non-uniform spatial distributions of mobile herbivorous fishes, however, are not explained simply by
reef bathymetry, but also by reef topography, local availability of food resources and other physical features
and biological interactions (Lewis & Wainwright, 1985). Recent studies on reefs in widely separated
geographic regions lend support to this statement. On the central Great Barrier Reef, Russ (1984a) found
inshore reefs to have fewer individuals and species of acanthurids and scarids than mid- and outershelf reefs
and proposed that changes in food availability across the shelf may be the best explanation for the pattern.
The assemblage studied by Russ fed primarily on filamentous and highly productive turf-forming algae that
predominate on the mid- and outershelf reefs. Inshore reefs were characterised by larger, probably less
palatable seaweeds such as the brown algae Sargassum and Turbinaria. In a related study focusing on five
reef zones, Russ (1984b) found distinctive assemblages of herbivorous fishes on reef slopes, reef flats, reef
crests, and over sandy areas in both lagoon and back reef zones. Acanthurids and scarids generally had
higher numbers of species and individuals on reef crests and in lagoons than on reef flats or reef slopes,
whereas siganids were more diverse and abundant in lagoons and back reefs. Different guilds of
herbivorous fishes were also distributed differently among the zones (Fig 3): (1) suckers feeding on fine
sediments were most abundant near windward and leeward edges of reefs; (2) suckers feeding over sand
were most abundant in back reefs and lagoons; and (3) croppers and scrapers were more numerous in
shallow zones (reef crest, reef flat, lagoon) than in deep zones (reef slope, back reef).
Interspecific interactions and local-scale heterogeneity further complicate spatial distributions of
herbivorous fishes as seen in a study (Choat & Bellwood, 1985) on the Great Barrier Reef of the territorial
surgeonfish Acanthurus lineatus, one of the large croppers in the studies of Russ (1984a,b) described above.
This reef-crest species is strongly site-attached and aggressive toward other herbivorous fishes. Behavioural
observations of these fishes at two adjacent sites of high A.lineatus abundances revealed a complex pattern
of interactions among species. Large scarids, including Scarus gibbus, a scraper (Russ, 1984b), fed within
Acanthurus lineatus territories at one site but were rare at the other. A.nigrofuscus, a small cropper (Russ,
195
1984b) and a consistent target of aggression by A.lineatus, was moderately common at one site but rare at
the second site. Ctenochaetus striatus, an abundant surgeonfish and a sucker of fine sediments (Russ, 1984b),
was present in high densities at both sites and fed within Acanthurus lineatus territories. Although the
degree of aggression by A. lineatus seems to be somewhat related to feeding guild membership of the other
species, Choat & Bellwood (1985) emphasised the importance of small but consistent differences in reef
structure at each site. They hypothesised that localised differences in the within-habitat component of
acanthurid and scarid abundances and distributions reflect site-associated variability in recruitment, postrecruitment mortality or behaviour independent of the activities of A. lineatus.
In the Red Sea (Gulf of Aqaba), acanthurids were found to dominate on the reef flat, whereas scarids
were more abundant on the outer reef slope (Bouchon-Navaro & Harmelin-Vivien, 1981). In this study the
observed complexity in the spatial distributions of fish herbivores was related in large part to differences in
social structure of the fishes according to reef biotope. Surgeonfishes formed dense schools in the reef
zones nearshore, smaller schools seaward and behaved as solitary individuals on the outer slope. Parrotfishes
displayed similar but less marked patterns of schooling versus solitary behaviour in the different reef zones.
The occurrence of both schooling and solitary individuals within the same species has been reported in
other studies of acanthurids (Randall, 196la; Barlow, 1974b; Vine, 1974) and scarids (Ogden & Buckman,
1973; Barlow, 1975; Robertson et al., 1976). The schools of both acanthurids and scarids generally
comprised adults at the Red Sea site (Bouchon-Navaro & Harmelin-Vivien, 1981). Juvenile acanthurids
were concentrated in shallow (less than 10 m) waters primarily as solitary individuals, whereas young
scarids occurred in the shallows but also as deep as 30 m on the outer reef slopes, either as solitary
individuals or in small aggregations.
Another complicating factor in the equation for explaining the spatial distributions of fish herbivores on
tropical reefs is the risk of predation. Although relatively few data are available, Hay (1985) pointed out
that predators could have a strong impact on the spatial patterns of habitat use by herbivorous fishes (and
sea urchins) and thus indirectly help form the mosaic pattern of grazing on reefs. Grazing and browsing
fishes may avoid deep sections of reefs because of the reduced algal food supply, as discussed above, but
also because of the heightened risk of predator attack at decreased light levels (see Hobson, 1972).
Herbivorous minnows avoid both shallow areas of streams where they be attacked by aerial or terrestrial
predators (Power, 1984) and areas near large predatory fishes (Power & Matthews, 1983). Similar
behaviour by marine herbivorous fishes is suggested by the results of several studies. For example,
herbivorous fishes may avoid structurally simple reef flats (Hay, 1984a), deep sand plains (Earle, 1972;
Dahl, 1973; Hay, 1981b; Hay, Colburn & Downing, 1983) and shallow sandy lagoons (Randall, 1965; Hay,
198la, 1984b) because they provide few hiding places and, therefore, leave these fishes more vulnerable to
predators. On the other hand, Hay (1985) also provided evidence that herbivore feeding rates are higher in
more open reef areas than areas near overhangs, which may provide ambush sites for predators. In terms of
seaweed distributions, such a predatory threat to herbivores may result in small safe patches for seaweeds to
colonise even though they would be rapidly eaten in immediately adjacent areas.
In summary, these studies illustrate some of the complex interactions that are involved in determining the
spatial distributions of roving herbivorous fishes across reef habitats. They provide an appropriate
background for the following discussion of the effects of these herbivores on coral reef algal communities.
Effects on algal communities Two striking features of coral reefs are the abundance of animals and the
scarcity of conspicuous plants (see Randall, 1967; Earle, 1972; Menge & Lubchenco, 1981). What are the
causes of such a low standing biomass of seaweeds and the prominence of small plants in these highly
productive tropical habitats? Gaines & Lubchenco (1982) discuss this question at length and identify two
main causal factors: low nutrient levels and intensive feeding by herbivorous fishes and sea urchins. They
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MICHAEL H.HORN
concluded that nutrient levels may set limits on the total size (and thus biomass) of algae, but that herbivory
can limit algal size and biomass well below the constraints imposed by low nutrients. Fishes and sea
urchins, by their foraging on larger, upright seaweeds, can prevent crustose and small filamentous algae
from being overgrown by the erect species.
The free-ranging herbivorous fishes, in particular, parrotfishes, surgeonfishes and rabbitfishes, appear to
have great overall impacts on reef-inhabiting algal communities. Gaines & Lubchenco (1982) drew
attention to their well-developed visual capabilities, large and powerful feeding apparatus and high potential
mobility as traits making fishes important tropical herbivores. Roving fishes are thus able to decrease
spatial variability in the effects of herbivory on community structure. More specifically, they can reduce
between-habitat algal diversity across the range of reef habitats where they occur as compared to areas with
less mobile herbivores. Ogden & Lobel (1978) suggest that fishes with these traits and capabilities are
similar to herbivorous mammals in a number of ways. For example, these fishes have diversified their diets
and probably learn quickly to feed mainly on familiar foods. Nevertheless, they can be expected to remain
flexible in order to cope with temporal changes in seaweed availability. They appear to be able to tolerate
some algal secondary compounds because they consume certain chemically defended species. Recent
studies of food preferences show, however, that herbivorous fishes tend to choose plants species or plant
parts with small amounts of secondary metabolites.
That these mobile herbivorous fishes are intensive feeders and greatly affect the abundance, diversity and
distribution of reef algae has been demonstrated in numerous field experiments (see reviews by Sale, 1980;
Borowitzka, 1981; Hixon, 1983, 1986). A few representative studies are discussed here. Two of the earliest
experimental studies were by Stephenson & Searles (1960) in the intertidal zone at Heron Island on the
Great Barrier Reef and Randall (1961b) in shallow subtidal waters on the island of Hawaii. In both cases
algal populations showed rapid and conspicuous increases in standing crop when protected by exclosures
from herbivorous fishes. At Heron Island, rabbitfishes were the most important of several species of grazing
and browsing fishes on intertidal beach rock, and on Hawaii, surgeonfishes were the main species
controlling algal density. Within 48 h after removal of the exclosures rabbitfish toothmarks were visible in
all the formerly caged areas. Several other investigations have shown that algal abundances are reduced by
foraging fishes (John & Pople, 1973; Wanders, 1977; Montgomery, Gerrodette & Marshall, 1980; Miller,
1982; Hatcher & Larkum, 1983; Lewis, 1986). Grazer-resistant crustose forms have been observed to
become dominant on grazed surfaces in many studies (John & Pople, 1973; Wanders, 1977; Brock, 1979;
Hixon & Brostoff, 1981, 1985; Lewis, 1986). Miller (1982), however, recorded increased coverage by
filamentous blue-green algae and a diatom-bacterial film in a heavily grazed area of an intertidal reef at
Enewetak, Marshall Islands. Reduced algal density is common, but algal diversity can also vary as a
function of fish browsing and grazing as has been documented in several studies (Stephenson & Searles,
1960; John & Pople, 1973; Day, 1977). Algal diversity varied according to different intensities of scarid
grazing pressure (as measured by different fish densities) in experiments conducted by Brock (1979). At low
fish densities, algal diversity was low because of dominance by a few species; at intermediate densities, the
highest algal species richness was obtained; and at high fish densities, low algal diversity developed. Brock
(1979) suggested that parrotfish may serve as keystone species (sensu Paine, 1966) on some Hawaiian
reefs.
Factors that seem to influence the distributions of herbivorous fishes on coral reefs in turn affect the
spatial distributions of algal species. Lubchenco & Gaines (1981) pointed out that some seaweed species
normally excluded from many reef slopes by fish grazing often persist on reef flats where shallow water
restricts fish foraging (Hay & Goertemiller, 1983), on sand plain areas that lack protection from predators
for many herbivorous fishes (Earle, 1972; Dahl, 1973; Hay, 1981b; Hay et al., 1983) or in areas of intense
197
wave action or surge that also limit fish feeding (Van den Hoek, Breeman, Bak & Van Buurt, 1978; Ruyter
van Steveninck, Kamermans & Breeman, 1988). The narrow zone of bare sand often seen between patch
reefs and seagrass beds in the Caribbean appears to be the result of heavy grazing by parrotfishes and
surgeonfishes (Randall, 1965) or by sea urchins (Ogden, Brown & Salesky, 1973) that stay close to the reefs
for shelter from predatory fishes. Finally, territorial fishes, especially damselfishes, strongly influence the
foraging ranges of the roving herbivorous fishes and the spatial mosaic of seaweed species.
The responses of seaweeds to the distributional patterns and feeding activities of herbivorous fishes
appear to be more extensive than just variations in spatial distributions and population densities. Transplant
experiments have shown that algal species characteristic of low-herbivory spatial refuges are highly
susceptible to being eaten by surgeonfishes and parrotfishes (Lewis, 1986). Conversely, algae from habitats
of high herbivore feeding intensity seem to be resistant to fish browsing and grazing (Hay, 1981a, 1984a;
Littler, Littler & Taylor, 1983a; Lewis, 1985). Lewis (1986) saw these results as consistent with the
hypothesis of a trade-off in algal resource allocation between competitive ability and herbivore resistance as
has been proposed for other prey assemblages (Lubchenco, 1978; Littler & Littler, 1980; Hay, 1981b;
Lubchenco & Gaines, 1981). Morphological plasticity as seen in the brown alga Padina jamaicensis has
been interpreted as another kind of response to different herbivore grazing pressures (Lewis, Norris &
Searles, 1987). This alga persists in a prostrate, turf morphology under high grazing intensity but responds
rapidly (96 h) to reduced herbivory by shifting to an erect foliose morphology. The latter morphology was
shown to be consumed preferentially by parrotfishes in transplant experiments. Thus, P.jamaicensis has the
phenotypic plasticity enabling it to respond rapidly to temporal or spatial fluctuations in herbivory.
Comparative impacts of roving herbivorous fishes and sea urchins
Numerous studies have clearly established that mobile herbivorous fishes, especially acanthurids and
scarids, and echinoids, especially those in the genus Diadema, exert strong influences on algal communities
in coral reef habitats. On the Great Barrier Reef, the fishes appear to be the major grazers (Stephenson &
Searles, 1960; Day, 1977; Borowitzka, 1981; Hatcher, 1981; Russ, 1984a,b; Sammarco, 1983). In the
Caribbean, both fishes and sea urchins have been recognised as playing important roles as primary consumers
(cf. Ogden et al., 1973; Sammarco, Levinton & Ogden, 1974; Ogden, 1976; Sammarco, 1982a,b; Carpenter,
1981, 1983, 1986, 1988; Steneck, 1983; Hay, 1984a,b; Hay & Taylor, 1985; Foster, 1987; Hughes, Reed &
Boyle, 1987; Levitan, 1988). On the Great Barrier Reef, Hatcher (1981) estimated that about 60% of the
daily algal production was removed by herbivores, with fishes being the only significant consumers. On a
Virgin Islands reef, in contrast, Carpenter (1986) reported that of the 97% removal of algal production by
herbivores, the urchin Diadema antillarum removed a slightly larger proportion than did the herbivorous
fishes (mainly juvenile parrotfishes). The percentage of the primary production entering the grazing food
chain on this Caribbean reef is the highest reported for any ecosystem (Carpenter, 1986; see Wiegert &
Owen, 1971).
The relative magnitude of the grazing impacts of fishes and sea urchins varies with the locality and other
conditions. This variation has led to different interpretations and to controversy about the relative influence
of these two herbivore groups on Caribbean reefs. Hay (1984a,b) stirred debate (see Hixon, 1985) when he
questioned earlier studies (e.g. Ogden et al., 1973; Sammarco, 1982a,b) purporting to show that sea urchins,
especially D. antillarum, were the most important grazers on typical coral reefs. Hay proposed that the
results obtained at the particular sites of these studies were atypical because they were on reefs heavily
overfished by humans, thus resulting in unusually high densities of sea urchins that had been from predation
by and perhaps competition with fishes. Using strips of the seagrass Thalassia testudinum as a field
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MICHAEL H.HORN
bioassay for the intensity of herbivory, Hay found that on seven lightly fished reefs scattered throughout the
Caribbean grazing intensity decreased with depth and almost all the herbivory resulted from fish grazing.
Sea urchin densities were low on these reefs. In contrast, he found the opposite, traditional pattern on four
heavily fished Caribbean reefs. Hay stressed that on reefs affected by human activity many patterns may be
recent, having existed only for the past few hundred years, and therefore that positing evolutionary
implications from ecological studies conducted on heavily fished reefs is unjustified. These assertions,
however, have been criticised (see Hixon, 1985), and the Thalassia bioassay technique has been shown to
produce results contradictory to other measurements of herbivory (Steneck, 1983). Hay (1984a) himself
admitted that the technique under-estimated browsing by smaller herbivores such as damselfishes and
young surgeonfishes because it is difficult for them to bite through the Thalassia blade.
The mass mortality of Diadema antillarum, which occurred throughout the Caribbean in 19831984
(Lessios, Robertson & Cubit, 1984), provided a unique opportunity to compare the impacts of grazing sea
urchings and fishes. Studies following this mass mortality (Hughes et al., 1987; Carpenter, 1988; Levitan,
1988) appear to reinforce the earlier impression that D. antillarum can have a dramatic influence on coral
reef habitats, perhaps often greater than that of herbivorous fishes in localised areas. For example,
Carpenter (1988) showed that within five days after the die-off at St Croix, Virgin Islands, algal biomass
increased by 20%, algal community primary productivity dropped by 37% (per unit area) and 61% (per unit
biomass), and algal biomass removed by herbivores declined by 50%. These changes in the algal
community were accompanied by increases in the rates of grazing by herbivorous fishes (mostly juvenile
scarids), suggesting that exploitative competition for food occurs between Diadema and some herbivorous
fish species.
The criticisms and controversy surrounding the studies comparing the impacts of fishes and urchins led
Hixon (1985) to identify three basic goals for future studies of coral reef communities: (1) make greater use
of properly controlled field experiments; (2) undertake long-term field studies; and (3) include several study
sites in order to determine the extent of observed patterns at a single site. Spatial and temporal variations in
reef habitats and in the relative abundance of the different resident herbivores provide strong support for
Hixons recommendations.
Impacts of territorial damselfishes
Unlike the roving herbivorous fishes, territorial pomacentrids closely tend a patch of the reef substratum and
maintain a growth of algae in the territory that is suitable as food. As a result of these habits, damselfishes
exert a pronounced influence on the structure of benthic algal communities on coral reefs. These fishes are
conspicuous and frequently pugnacious residents of shallow water reef habitats. Thus, they are readily
accessible for study and have been the focal point of a large number of manipulative field experiments
carried out over the past 15 years. Their abundance alone suggests that they play an important role in coral
reef communities. For example, as much as 40% to 50% of the surface of certain reef habitats can be under
the influence of a single species of territorial damselfish (Sammarco & Williams, 1982; Klumpp, McKinnon
& Daniel, 1987).
By establishing and defending distinct algal mats, territorial damselfishes affect (1) coral recruitment,
growth, and bioerosion; (2) local microfaunal abundance; (3) nitrogen fixation by blue-green algae; and (4),
algal abundance and local diversity (Hixon, 1983). Each of these effects are discussed in turn below,
followed by an account of recent studies on the effects of these fishes on algal productivity.
The effects of territorial damselfishes on coral recruitment, growth and bioerosion are varied and
complex. Birkeland (1977) reported that algal mats inhibit settlement by corals, and Potts (1977) speculated
199
that the scarcity of the coral Acropora palifera at a Great Barrier Reef site was caused primarily by the
territoriality of the damselfish Dischistodus perspicillatus. By encouraging the growth of filamentous algae,
D. perspicillatus presumably inhibits settlement and then suppresses the growth of the young coral
survivors. Both Vine (1974) and Lobel (1980) claimed that inhibition of coral growth inside territories could
lead to a weakening and eventual collapse of the basal reef network. Moreover, Risk & Sammarco (1982)
found that pieces of staghorn coral (Acropora) inside the territories of two damselfish species were
significantly more eroded than coral pieces outside territories, with most of the destruction caused by boring
sponges and sipunculids. They suggested that bioerosion is accelerated within territories as a result of
reduced grazing and predation on the borers by fishes. Irvine (1982) observed that Eupomacentrus
planifrons actually kills corals by its biting activity and thereby opens up new substrata for algal
colonisation. Wellington (1982) showed that the coral killing activities of E. acapulcoensis reduces or
eliminates the massive coral Pavona from shallow waters thus promoting establishment of the branching
coral Pocillopora, which it does not attack.
In contrast to the foregoing studies that largely report negative effects of territorial damselfishes on
corals, other works have revealed positive or neutral effects. Sammarco & Carleton (1981) found that the
density of coral spat within damselfish territories was about five times higher than on exposed surfaces and
in caged areas at 1011 m and that diversity of coral spat was greater in these defended areas. And, although
territories may be sites of high local mortality of coral spat, these defended areas may also serve as refuges
for rare species (Sammarco & Williams, 1982). The net effect would be an overall increase in coral
diversity in the community. Finally, in studies on the Great Barrier Reef, external bioerosion (i.e. erosion
caused by grazing fishes) was found to be effectively reduced within the borders of damselfish territories
(Sammarco, Carleton & Risk, 1986), whereas total rates of internal bioerosion as caused by invertebrate
borers was found not to vary significantly with changes in grazing pressure (Sammarco, Risk & Rose,
1987). Regional differences in the abundance and diversity of algae, invertebrates and fishes may account
for some of the variation in the effects of territorial fishes on corals. Further research seems necessary to
sort out the apparent conflicts in published results.
Although relatively few studies have been published on the effects of territorial damselfishes on local
microfaunal (invertebrate) abundance, the available data indicate that densities are generally higher inside
than outside the defended areas. Lobel (1980) reported that the number of small, motile invertebrates is greater
within the territories of two damselfish species, Eupomacentrus planifrons from the Caribbean and E.
nigricans from the central Pacific. He concluded that the territories function as refuges for juvenile benthic
invertebrates, such as crabs and sea stars, and demersal plankton. Hixon & Brostoff (1982) showed that
increased grazing on Hawaiian reefs causes a decrease in the biomass of erect algae and the abundance of
associated small invertebrates and an increase in coverage of crustose coralline and prostrate algae.
Invertebrate density inside territories of Stegastes fasciolatus was intermediate (34.3 per plate) between that
outside of territories (1.7 per plate) and that within fish exclusion cages (48.8 per plate). Zeller (1988) found
that densities of invertebrates (crustaceans, mainly copepods and amphipods) were greater on experimental
plates inside than outside territories of S. apicalis on the Great Barrier Reef.
Territorial damselfishes may indirectly affect nitrogen fixation by blue-green algae on reefs, but the data
that are available appear to be in conflict. Lobel (1980) and Hixon & Brostoff (cited in Hixon, 1983) both
found more blue-green algae inside than outside territories on Hawaiian reefs. Wilkinson & Sammarco
(1983), however, reported that rates of nitrogen fixation at a Great Barrier Reef site were directly
proportional to the extent of fish grazing and inversely proportional to total algal biomass. In other words,
rates were lowest in caged areas, intermediate in damselfish territories and highest in areas fully exposed to
fish grazing. More recently, Ruyter Van Steveninck (1984) found no difference in the amounts of
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MICHAEL H.HORN
Fig 4.A, diversity of algae after one year on substrata within fish exclusion cages (left), inside territories of the
damselfish Stegastes fasciolatus (centre) and exposed outside territories (right) on Hawaiian coral reefs; vertical and
horizontal lines through means represent 95% confidence limits; results support the hypothesis shown in B. B, graph of
the intermediate-disturbance hypothesis, showing that a keystone species can enhance local diversity either by
increasing predation intensity from point 1 toward point 2 (classic type), or by decreasing overall predation intensity
form point 3 toward point 2 (reverse type as exemplified by the damselfish); slightly modified from Hixon & Brostoff
(1983).
filamentous blue-green algae inside and outside damselfish territories on a reef in the Florida Keys. These
contradictory results may reflect regional differences in the local abundances of blue-green algae.
Many studies involving removal or caging experiments have shown that algal biomass is greater inside
than outside damselfish territories (Vine, 1974; Brawley& Adey, 1977; Lassuy, 1980; Hixon & Brostoff,
1981, 1982; Williams, 1981; Sammarco, 1983; Ruyter Van Steveninck, 1984; Hinds & Ballantine, 1987;
Klumpp et al, 1987; Russ, 1987; Zeller, 1988). Although this effect of territoriality seems to be clearly
established, a few studies have provided exceptions. Montgomery (1980a) showed that the non-selective
feeding of Microspathodon dorsalis maintains a near monoculture of the red alga Polysiphonia in its
territory. Polysiphonia appears to be the only alga that can grow fast enough to persist under the influence
of this fishs intense, nonselective grazing. This alga is more productive than the multispecies algal mat
outside the territory but of much lower standing biomass. Also, Foster (1987) found that while Stegastes
dorsopunicans can effectively defend its territory against most solitary fishes, it is unable to prevent the sea
urchin Diadema antillarum from grazing in its territory. As a result, this damselfish exerts a minor impact
on algal biomass in the habitat, unlike Diadema, or the more aggressive damselfish, Stegastes planifrons,
which canexclude sea urchins from its territory.
Several studies have shown that algal diversity is also higher inside than outside damselfish territories. In
an exhaustive study carried out on Hawaiian reefs, Hixon & Brostoff (1981, 1982, 1983) tested the
intermediate disturbance hypothesis (Connell, 1978), which proposes that as the intensity or frequency of
disturbance progressively increases from zero, the species diversity of the affected community will initially
increase then subsequently decrease. Hixon & Brostoffs results supported the hypothesis in that substrata
located within the defended territories of the damselfish S. fasciolatus were subjected to intermediate
grazing intensity and, as a result, showed greater algal diversity than substrata either protected within fish
exclusion cages or exposed to intense fish grazing outside territories (Fig 4). Similar experimental studies in
Guam (Lassuy, 1980), Australia (Sammarco, 1983) and Puerto Rico (Hinds & Ballantine, 1987) have all
shown that algal diversity is greatest inside damselfish territories. Hixon & Brostoff (1983) labelled S.
fasciolatus a keystone species (sensu Paine, 1966) in reverse because it maintains high diversity of algae by
decreasing rather than increasing the overall predation intensity on the algae. Also, Williams (1980) has
referred to a damselfish, Eupomacentrus planifrons, on Jamaican reefs as a non-carnivorous keystone
species because it acts as a selective predator by its stronger response to the more invasive (Diadema
antillarum) of two competing sea urchin species (D. antillarum and Echinometra viridis) in its territory.
Thus, Eupomacentrus planifrons apparently stabilises competitive interactions and reduces the potential
competitive exclusion of sea urchin species, actions primarily attributed to predatory keystone species.
Territorial damselfishes, however, do not always conform to the intermediate disturbance hypothesis.
Grazing intensity can be greater inside than outside territories, as in those species that actively weed certain
species from the defended algal mats (Lassuy, 1980; Irvine, 1982). Moreover, as mentioned on page 247,
the Gulf of California damselfish Microspathodon dorsalis maintains an almost pure stand of an algal
species in its territory (Montgomery, 1980a). A model (Fig 5) relating the intensity of non-selective grazing,
like that of M. dorsalis, to productivity of algal assemblages has been proposed by Montgomery (1980a),
who considers the model a special case and extension of the disturbance-dependent models of Connell &
201
Fig 5.Graphical model of the relationship between nonselective grazing by territorial damselfishes and algal
productivity, both represented in the same units (e.g. biomass removed or produced per unit time); increased levels of
grazing intensity (represented by higher Roman numerals) would progressively remove all but the most productive or
all the algal assemblages (represented by lower case letters), whereas decreased grazing intensity would allow
succession to occur toward the least productive assemblages; from Montgomery (1980a).
Slatyer (1977). Grazing, which is expressed in the same units as productivity, is seen as a function of the
fishs requirements and largely independent of the composition of algal communities. Grazing at the lowest
intensity (I in Fig 5) will not lead to the terminal algal assemblage (i) because the grazing rate is too small to
remove a significant amount of the production. The next level of grazing (II) would remove assemblages
with lower productivity than the grazing rate (fi), whereas grazing at level III would eliminate all but the
most productive assemblage (a). Montgomery argues that this is the situation that occurs in territories of M.
dorsalis and various other damselfishes. Even higher grazing rates would remove all erect algae and result
in the overgrazing commonly observed, particularly on coral reefs (e.g. Randall 1961b; Earle, 1972).
Reduction in grazing intensity would allow succession of algal assemblages to proceed.
Finally, at least two studies have reported that damselfish territories are zones of high algal productivity
relative to surrounding epilithic algal communities. As mentioned above, Montgomery (1980a) found that M.
dorsalis by its non-selective grazing maintains a near monoculture of the red alga Polysiphonia in its
territory. On a per unit biomass basis, this alga was 34 47 times as productive as the algal mat outside the
territory. More recently, Klumpp et al. (1987) have shown that the algal communities inside the territories
of four species of damselfishes on the coral reefs of the Great Barrier Reef and Papua New Guinea were 1.5
3.4 times more productive (per unit biomass) than algae growing outside the territories. These authors
offered three possible explanations for the high primary productivity of damselfish territories: (1)
weeding activities of the damselfishes promote more highly productive algal species or forms; (2)
cropping action of the damselfishes, as distinct from other fish grazers, keeps algae in an exponential phase
of growth; and (3) the damselfishes fertilise the algae with their waste products. Weeding has been
reported for three damselfish species. Lassuy (1980) found that both Eupomacentrus lividus and
Hemiglyphidodon plagiometopon remove the larger, tougher, and presumably less palatable and less
productive seaweeds from their territories leaving the more preferred, lower ash content forms for
consumption. Irvine (1982) reported that Eupomacentrus planifrons weeds out less preferred algae, which
opens up space for settlement and growth of preferred species. Preferred algae were Polysiphonia spp. and
diatoms, whereas those removed were primarily filamentous green algae and the brown alga Dictyota
bartayresii. Whether the preferred algae are more productive was not determined. Damselfishes feed
predominantly upon the algae in their territories (Klumpp et al., 1987) and, in terms of the rate of removal of
algal tissue, may feed more intensively than the herbivorous fishes outside their territories (Russ, 1987).
Whether such feeding maintains the algae in an exponential growth phase and that by roving herbivores
outside the territories does not is apparently yet to be discovered. Temporal and spatial focusing of the
release of nitrogenous wastes occurs in Plectroglyphidodon lacrymatus, a territorial damselfish on coral
reefs of Papua New Guinea (Polunin & Koike, 1987; Polunin, 1988). Polunin & Koike found that most
defaecation by this fish occurred at a single site in each territory and was far more important than excretion
in the generation of nitrogen by the fish. Nearly all of the nitrogen defaecated, and perhaps one-third of that
excreted, was transferred initially to the reef framework below the fishs territory. Polunin (1988) showed
that P. lacrymatus ingests 91% of the nitrogen incorporated into the algal community and thus spatially
focuses the transfer of nitrogen within its territory. All three of these explanations are intriguing and deserve
further study. Nevertheless, it is still possible that damselfish territories are highly productive because the
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MICHAEL H.HORN
fishes are somehow able to establish their territories in areas more suitable for algal growth (see Eakin,
1987; Zeller, 1988).
TEMPERATE HABITATS
On hard substrata in temperate waters the dominant herbivores are molluscs, echinoderms and crustaceans
(Gaines & Lubchenco, 1982). In California waters, for example, gastropod molluscs (especially limpets and
trochids) appear to be the major intertidal herbivores and sea urchins the principal subtidal herbivores
(Foster & Schiel, 1985). Knowledge is meagre at best about the impacts of plant-eating fishes on seaweed
and seagrass communities in temperate waters (Choat, 1982; Gaines & Lubchenco, 1982; Thayer et al.,
1984; Hixon, 1986; Castilla & Paine, 1987; Santelices, 1987), but the prevailing notion is that fishes may
have negligible effects on benthic algal abundance and diversity (Limbaugh, 1955; Bakus, 1964, 1969;
Earle, 1972; Ogden & Lobel, 1978; Lubchenco & Gaines, 1981; Menge & Lubchenco, 1981; Hixon, 1986).
This impression has emerged for at least two reasons: (1) herbivorous fishes have been perceived as rare in
kind and numbers in temperate waters and (2) individual algae and algal standing stocks are often large in
temperate latitudes and, based on general observations, seem little affected by grazing or browsing fishes.
The observations leading to this opinion have been made largely in north temperate regions, especially the
eastern North Pacific.
The small amount of evidence, however, that does suggest that plant-eating fishes may have some effect
on temperate-zone seaweeds has until recently come from these same north temperate regions, mostly from
California coastal waters. Here, three species, the girellid Girella nigricans, the kyphosid Hermosilla azurea
and the scorpidid Medialuna californiensis, are known to consume a variety of seaweeds, including
Macrocystis, the giant kelp (Quast, 1968). Girella nigricans and Medialuna californiensis are the most
common of the three species in southern California. Their herbivorous tendencies are well known because
they eat young Macrocystis plants that have been transplanted as part of kelp restoration (North, 1972, 1973)
and artificial reef (Grant, Wilson, Grover & Togstad, 1982) projects. Gill nets have been used to reduce the
number of Girella nigricans and Medialuna californiensis around kelp transplant areas (North, 1973),
which attests to the seriously detrimental effects of their grazing on young Macrocystis sporophytes.
The potential or actual impacts of these two fishes have been recognised in other studies in California
kelp beds. Three of these studies are summarised as follows.
(1) Leighton (1971) attributed the reduction in fleshy green and red algae relative to a caged treatment to
the action of herbivorous fishes. He reached this conclusion largely because the experimental block was
placed in a location where invertebrate herbivores were absent and because the green alga Ulva occurred in
appreciable amounts only in the guts of Girella nigricans among those of six fish species examined in an
attempt to find the responsible grazing agent.
(2) Foster (1975) found increased growth in the red algae Gigartina spp. in cage treatments at a giant kelp
forest site. Although Foster observed that Girella nigricans and Medialuna californiensis were common in
the area and that control plants bore evidence of structural damage from fish feeding, he presented no data
to link the two observations. An alternative explanation, which possibly diminishes the role of herbivorous
fishes in affecting seaweed biomass, stems from work by Kennelly (1983) in a kelp forest habitat near
Sydney, Australia. He found that exclusion of fishes from settlement plates and the natural substratum
resulted in less not more algal cover during colonisation. Kennelly hypothesised that exclusion of
carnivorous fishes led to an increase in the abundance of small invertebrate grazers, especially amphipods,
that caused reduced algal stands inside cages. Perhaps similar grazers avoided Gigartina and ate other algae
inside the cages used by Foster, or perhaps they modified algal abundance inside the cages by eating spores
203
or germlings. The other algae could also have been outcompeted for space by sessile animals in the low light
conditions of the habitat (Foster, 1975). Kennelly, however, presented no data or observations on
herbivorous fishes, several species of which are known to occur at least in the general vicinity of his study area
(see Bell, Burchmore & Pollard, 1980; Burchmore et al., 1985).
(3) In one of the only studies designed to determine the impacts of temperate herbivorous fishes on
seaweed populations, Harris et al. (1984) found that Girella nigricans and Medialuna californiensis can be
important grazers on young Macrocystis plants on a small scale. These workers manipulated early
colonising, fast-growing algal stands after a severe storm had denuded a southern California kelp bed habitat
to test for the role of filamentous brown algae in helping sporophytes survive fish grazing. Grazing affected
59% of small plants (less than 10 cm tall) concealed in a turf of the filamentous algae on new surfaces,
whereas 94% of the sporophytes amidst shorter turf on old surfaces had fish bites. These results indicate
that young kelp plants growing within stands of filamentous algae receive some protection from
herbivorous fishes. Larger plants were unaffected, perhaps because of a size refuge. The grazing resulted in
a small-scale change in the dispersion pattern of juvenile giant kelp on the reef. Harris et al. (1984), however,
did not mention the feeding behaviour of the fishes or report their abundances in the habitat.
Several other southern California fish species occasionally consume small amounts of algae, including two
species of surfperches (Embiotocidae) (Bray & Ebeling, 1975) and the labrid Oxyjulis californica (Bray &
Ebeling, 1975; Bernstein & Jung, 1979). The latter species, although not a herbivore, can apparently have
an impact on Macrocystis by removing blade portions encrusted with a bryozoan, one of its preferred foods
(Bernstein & Jung, 1979). Algae had the third highest utilisation index among food categories of kelp bed
fishes recognised by Quast (1968), which he attributed to be mostly a result of accidental ingestion with
animal prey.
A recent study, on a North Carolina rock jetty, also suggests that temperate fishes can have an impact on
seaweed abundance. Hay (1986) reported that palatable seaweeds such as Hypnea musciformis, Chondria
spp., Gracilaria spp., Enteromorpha spp. and Ulva spp. that are common during most of the year on the
jetty decrease sharply in abundance during midsummer when algae-eating fishes such as the sparids
Diplodus holbrooki and Lagodon rhomboides and that monacanthid Monacanthus hispidus are most
prevalent. In the spring and late fall when these fishes are rare or are feeding on invertebrates instead of
algae, most of the palatable seaweeds are growing on primary substratum. In midsummer, on the other
hand, when the fishes are numerous and feeding on algae, the palatable seaweeds are mostly epiphytes on
unpalatable brown algae such as Sargassum and Padina.
These tantalising accounts in the North Pacific and North Atlantic offer hints of the importance of
herbivorous fishes in temperate regions, but in virtually all cases the studies from which they emerged were
focused on other objectives. I am aware of no study in north temperate waters that was designed to
investigate rigorously the impacts of herbivorous fishes on algal populations or communities.
In the southern hemisphere, especially in the temperate waters around New Zealand and southern
Australia, recent studies show signs that herbivorous fishes may affect algal communities. First of all,
herbivorous fishes are surprisingly diverse in both the Australian (Coleman, 1980; Burchmore et al., 1985)
and New Zealand (Doak, 1978; Ayling & Cox, 1982; Russell, 1983; Choat & Ayling, 1987) regions.
Moreover, species such as Girella tricuspidata are highly abundant and can constitute as much as 51% of the
total fish biomass in dense kelp cover in New Zealand coastal waters (Russell, 1977). The zone of short
algal turf on shallow rocky reefs in northeastern New Zealand may be at least partially maintained by browsing
and grazing fishes (Russell, 1983).
Neither of the two studies of which I am aware that provide data on the impacts of herbivorous fishes on
algal abundance, however, show evidence of an important influence by fishes. Conacher, Lanzing &
204
MICHAEL H.HORN
Larkum (1979) concluded that browsing by the monacanthid Monacanthus chinensis had little impact on
algal or seagrass production rates in Botany Bay, New South Wales, and Meekan (1986) found that
browsing by the odacid Odax pullus imparted no more than a minor cost to the brown alga Ecklonia radiata
in shallow waters off northern New Zealand.
Meekans (1986) study is one of the most detailed yet completed on the relationship between a
herbivorous fish and its major food plant. He found that browsing damage on Ecklonia radiata was closely
correlated with abundance patterns of Odax pullus. Most browsing activity was concentrated on adult plants
and was selective within plants. Generally, only the secondary laminae of Ecklonia radiata were consumed,
and a higher proportion of reproductive tissue than vegetative tissue of these laminae was eaten by Odax
pullus. Meekan cited evidence that reproductive tissue consumed by the fish may survive digestion.
Browsing damage on Ecklonia radiata varied spatially between reef types, localities, transects, sites, plants
within a site, and, temporally, on individual plants. Moreover, browsing damage experiments and
monitoring of individuals over a three-month period suggested that Odax pullus kills few plants and that the
plants rapidly recover from either fish browsing or artificially imposed damage. A longer-term study that
would assess the fishs impact on other seaweeds in its diet (e.g. the fucoid algae Carpophyllum spp.)
should be rewarding.
DISTRIBUTION, DIVERSITY AND ABUNDANCE OF HERBIVOROUS FISHES

GENERAL PATTERNS OF DISTRIBUTION AND DIVERSITY
Herbivorous fishes are largely confined to shallow-water coastal habitats. They are limited in their vertical
and horizontal distributions because they depend directly on light-requiring organisms for food. As
mentioned in the previous section, tropical species occur as deep as 90 m (Thresher & Colin, 1986) but
mainly live in the shallowest 10 m of inshore waters (Bakus, 1969). Temperate species show essentially the
same, if not shallower, bathymtric pattern (see Quast, 1968; Russell, 1983; Burchmore et al., 1985).
Offshore, herbivorous fishes are restricted because the substratum becomes too deep for benthic plants to
survive. Moreover, the browsing and grazing fishes considered in this review are not equipped
morphologically to feed on phytoplankton in the water column. High seas herbivores are exceedingly rare,
apparently because phytoplankton populations are too sparse in the open ocean to support filter-feeding
fishes. The main phytoplanktivorous fishes in the sea are filter-feeding clupeoids such as menhaden and
some species of anchovies and sardines, and they are confined to coastal regions in various parts of the
world (see Blaxter & Hunter, 1982). Like other herbivorous fishes, these clupeoids begin life as carnivores
then through early ontogeny develop an elaborate set of gill rakers, epibranchial organs and a longer gut as
the diet becomes increasingly made up of phytoplankton. An unusual case of open ocean herbivory is seen
in the myctophid Ceratoscopelus warmingii, a dominant midwater fish in the oligotrophic North Pacific
Gyre (Robison, 1984). This fish feeds on the dense diatom mats (Rhizosolenia spp.) that form in the upper
30 m of the water column. The intestine of Ceratoscopelus warmingii is longer than that of other
myctophids, but Robison noted that the fish is only an occasional herbivore and feeds otherwise on
zooplankton.
Browsing and grazing herbivorous fishes make up only a small proportion of the total diversity of coastal
fishes. About 19 families contain almost all of the herbivorous fishes in the sea (Table VII). Thus, herbivore
diversity is concentrated in only about 5% of the 409 recognised (Nelson, 1984) families of teleostean
fishes. Moreover, 15 of the 19 families belong to the Perciformes (Table VII), the largest traditionally
205
recognised order of teleosts, but one more recently viewed (Lauder & Liem, 1983; Johnson, 1984) as a
polyphyletic assemblage. At the species level, it is difficult to estimate with any reasonable degree of
accuracy the total number of marine herbivorous fishes because for most of the families the proportions of
herbivorous fishes cannot be determined with available information (see Table VII). For example, little is
known about the feeding habits of many species in the large, diverse families such as the Blenniidae and
Gobiidae.
LATITUDINAL PATTERNS
Diversity
One of the most striking and widely recognised (Bakus, 1964, 1969; Medd, 1970; Earle, 1972; Ogden &
Lobel, 1978; Choat, 1982; Gaines & Lubchenco,
TABLE VII
Principal teleostean fish families containing marine herbivorous species ; order, suborder, family distribution and total
species from Nelson (1984)
Order
Suborder
Family
Family
distribution
Total no. species
Estimated no.
herbivorous
speciesb
Gonorynchiform
es
Atheriniformes
Perciformes
Chanoidei
Chanidae
Tropical
Exocoetoidei
Percoidei
Hemiramphidae
Sparidae
Tropical
Tropical/
temperate
Temperate
Tropical/
temperate
Tropical/
temperate
Tropical
Tropical/
temperate
Temperate
Tropical/
temperate
Temperate
Tropical
Temperate
Tropical/
temperate
Tropical/
temperate
Tropical
Tropical
80a
100
?
?
20
10
20
10
15
74
235
?
?
5
70a
5
70
12
68
60
3o1a
5
68
2
?
1500a
76
25
7
25
Girellidae
Kyphosidae
Scorpididae
Pomacanthidae
Pomacentridae
Mugiloidei
Labroidei
Aplodactylidae
Mugilidae
Zoarcoidei
Blennioidei
Odacidae
Scaridae
Stichaeidae
Blenniidae
Gobioidei
Gobiidae
Acanthuroidei
Acanthuridae
Siganidae
206
MICHAEL H.HORN
Order
Suborder
Family
Family
distribution
Total no. species
Estimated no.
herbivorous
speciesb
Tetraodontiform
es
Balistoidei
Balistidae
Tropical/
temperate
Tropical
135
Tetraodontoidei
Tetraodontidae
118a
?
include freshwater species.
sEstimates are included where all species are expected to be herbivores with two exceptions. Total number of species in
the Odacidae is from Gomon & Paxton (1985) and the number of herbivorous odacids from Choat & Ayling
(1987) and M.J. Kingsford (pers. comm.). The minimum number of herbivorous stichaeids is based on Horn,
Murray & Edwards (1982).
aTotals
1982; Estes & Steinberg, 1988) yet enigmatic distributional patterns in coastal marine waters is the rarity of
strictly herbivorous fish species in temperate latitudes as compared to the much larger numbers of such species
in tropical waters. Bakus (1969) estimated that coral reef fish communities are composed of 22%
herbivores, 69% carnivores and 9% omnivores, whereas rocky reef and kelp bed fishes in southern
California are roughly 33% carnivores and 67% omnivores. In other words, he recognised no temperate
herbivores in this warm temperate region of the eastern North Pacific. Although Bakus under-estimated
temperate-zone herbivory, a survey of 19 studies of shallow marine fish communities (Table VIII) shows
that the occurrence of herbivores is inversely correlated with latitude in terms of both the absolute numbers
and the proportions of herbivorous species in the community. Furthermore, the Table shows that the fish
communities at the highest latitudes contain no herbivores. Thus, strictly
TABLE VIII
Numbers and proportions of herbivores in shallow marine fish communities at different latitudes; see Table I for list of
herbivorous species in those communities where they occur
Locality (habitat)
Latitude Total no. species studied Herbivores Reference
No. vores
Antarctica (rocky subtidal)

Scotland (rocky intertidal)
Chile (kelp bed)
Auckland Islands (rocky
subtidal)
France (Atlantic, rocky
intertidal)
France (Mediterranean, rocky
littoral)
California (rocky intertidal)
California (rocky intertidal)
61S
56N
55S
51S
9
15
18
8
0
0
0
0
0
0
0
0
49N
13
Targett, 1981
R.N.Gibson, unpubl. data
Moreno&Jara, 1984
Kingsford, Schiel & Battershill,
1988
Gibson, 1972
42N
19
Gibson, 1968
38N
36N
15
28
1
2
7
7
New Zealand (rocky subtidal)

Australia (rocky subtidal)
California (rocky subtidal)
California (kelp bed)
36S
34S
33N
32N
50
102
46
45
5
12
2
3
10
12
4
7
Grossman, 1986
L.G.Allen & M.H.Horn, unpubl.
data
Russell, 1983
Burchmore et al., 1985
Stephens & Zerba, 1981
Quasi, 1968
207
Locality (habitat)
Latitude Total no. species studied Herbivores Reference
No. vores
Mexico (rocky intertidal)

South Africa (rocky littoral)
Kermadec Islands (rocky
subtidal)
Hawaii (coral reef)
Puerto Rico/Virgin Islands (coral
reef)
Marshall Islands (coral reef)
Tanzania (coral reef)
31N
30S
29S
25
66
45
4
5
7
16
8
16
Thomson & Lehner, 1976

Berry et al., 1982
Schiel, Kingsford & Choat, 1986
19N
18N
120
212
30
31
25
15
Jones, 1968; Hobson, 1974

Randall, 1967
10N
8S
233
106
52a
30b
22
28
Hiatt & Strasburg, 1960

Talbot, 1965
aTotal
bTotal
includes 9 scarids not listed as herbivores by Hiatt & Strasburg (1960).

includes 15 scarids not listed as herbivores by Talbot (1965).
herbivorous fishes appear to be limited to a range of latitude from about 40N to about 40S. An exception
may be the stichaeid Xiphister mucosus, a year-round herbivore in central California waters (Horn, Murray
& Edwards, 1982) that occurs as far north as southeastern Alaska (Eschmeyer, Herald & Hammann, 1983)
at a latitude of at least 55N. Whether X. mucosus is still a herbivore at this latitude is, however, unknown.
A few fishes living beyond the 40-degree belt are known to consume algae on a seasonal or facultative
basis. For example, filamentous algae were found in the stomach contents of most fish species in a kelp bed
habitat at 55N in southern Chile (Moreno & Jara, 1984). The authors, however, believed that this plant
material was consumed simultaneously with invertebrate prey and, therefore, was not evidence for
herbivory. Also, the nototheniid Notothenia neglecta was found (Daniels, 1982) to crop macroalgae and
harvest diatom mats during the spring and summer at 61S in an Antarctic habitat. The fish switches from
being an omnivore in the spring and summer to a carnivore through the autumn and winter.
Several hypotheses have been offered to explain the rarity of herbivorous fish species in temperate,
boreal and arctic latitudes (Gaines & Lubchenco, 1982). These are discussed in turn.
(1) Insufficient time has lapsed to allow cold-adaptation and range expansion to temperate and polar seas.
Medd (1970) observed that the Perciformes, the largest order of teleostean fishes, dominates the tropical
marine fauna, especially that of coral reefs, and that the diversity and abundance of these fishes decline
sharply poleward away from the tropics. He speculated that the explosive radiation of the group in the
tropics was mainly the result of the development of the ability to eat and digest benthic plant material.
Those perciform families in which herbivorous capabilities evolved (e.g. Acan thuridae, Scaridae,
Siganidae) appear to be just the forms that have not radiated in any major way into temperate seas. Mead
believed the perciform radiation to be a relatively recent phenomenon (i.e. in the Cenozoic) and argued that
time favours cold adaptation even if it is not the driving force. His analysis suggested that the highly diverse
tropical Indo-Pacific region was the major colonising source for temperate waters off Australia and New
Zealand. The relatively close proximity of the Indo-Pacific to Australia and New Zealand through the
Cenozoic may help explain the higher herbivore diversity in these regions as compared to that in the eastern
North Pacific (see Table VIII). Meads analysis, however, is largely untestable and weakened because it
was based on the evolution and radiation of the Perciformes, which is now considered to be a polyphyletic
assemblage (Lauder & Liem, 1983; Johnson, 1984). Cladistic analyses of apparently related groups that
contain both herbivorous and carnivorous species and whose distributions span both tropical and temperate
regions should prove to be valuable.
208
MICHAEL H.HORN
(2) The effects of low temperature on fish digestive physiology may largely exclude herbivorous fishes
from temperate and higher latitudes. Gaines & Lubchenco (1982) proposed that if digestive efficiency is
dramatically reduced relative to energy demands in colder waters, a primarily herbivorous diet would be
energetically infeasible. This hypothesis is unstudied and appears to be testable, but it could also be testable
if gut transit time rather than digestive efficiency were the focus of the hypothesis as follows. If the rate of
movement of food through the gut is reduced at low temperatures, as expected, so that the stimulus to feed
is decreased, thereby reducing the consumption rate, then energy intake from an algal diet could be
inadequate to meet the fishs requirements.
(3) Regions where suitable plant food is seasonally unavailable may be habitable only by invertebrate
herbivores. If herbivorous fishes are more limited than invertebrates in the length of time they can persist
without food, then non-migratory, strictly herbivorous fishes might be excluded from such regions. This
hypothesis is weakened by at least two observations. First, many temperate shores have large standing stocks
of seaweeds throughout the year and may even be more productive during the winter months (Mann, 1973;
Chapman & Lindley, 1980). Secondly, even though brown algae, the seaweeds usually comprising the bulk
of the winter biomass in these localities, has been considered to be inferior to green and red algae as fish
food and seldom consumed by fishes (Montgomery & Gerking, 1980), several species of herbivorous fishes
regularly eat brown seaweeds in both north (e.g. Harris et al., 1984) and south (e.g. Russell, 1983)
temperate waters.
(4) Latitudinal differences in algal toughness, chemical defences or nutritional quality may restrict
temperate fish herbivory. Little or no evidence exists to provide convincing support for this hypothesis.
Although Bakus (1969) suggested that the toughness of the larger temperate seaweeds might deter feeding
by fishes, several relatively tough brown algae make up a large part of the diets of temperate herbivores
such as girellids, kyphosids and odacids (Russell, 1983). Moreover, toughness and calcification seem to be
important though variable deterrents to fish feeding in a variety of tropical seaweeds (Littler, Taylor &
Littler, 1983b; Lewis, 1985; Paul & Hay, 1986). The incidence of defensive chemicals appears to be more
common in seaweeds of tropical and subtropical waters than in those of temperate habitats (Hay & Fenical,
1988). Nevertheless, temperate brown algae, especially the fucoids, are rich in phlorotannins that are known
to deter feeding by herbivorous invertebrates (Steinberg, 1984, 1985). They may deter some herbivorous
fishes because no north temperate fish is known to consume fucoid algae. In Australian and New Zealand
waters, however, where phlorotannin concentrations in fucoid algae are two to three times as great as those
in north temperate fucoids (Estes & Steinberg, 1988; Steinberg, 1988), kyphosid and odacid fishes consume
these algae as major portions of their diets (Russell, 1983). The lack of predation by sea otters or other
marine mammals on invertebrate herbivores, especially sea urchins, in the temperate South Pacific as
compared to the eastern North Pacific during recent earth history has been proposed (Estes & Steinberg,
1988) as the cause of the phlorotannin-rich brown algal flora in Australia and New Zealand. Sea urchins,
unchecked by predators, would have fed intensively on the algae and provided the selective pressure for the
algae to evolve increased chemical defences. In turn, the herbivores would have developed greater
tolerances to the seaweed defences. Herbivorous fishes may have been part of these tightly coupled plantherbivore interactions, which could explain the apparently high tolerances of kyphosid and odacid fishes to
the phlorotannins and other secondary chemicals in the brown algae they regularly consume. Finally, with
regard to nutritional quality, no strong evidence is available to suggest that temperate seaweeds are less
nutritious than tropical species although the quality and digestibility of brown algae in both temperate and
tropical regions deserves
TABLE IX
209
Densities of marine herbivorous fishes in 7 temperate and 14 tropical habitats

Latitude Habitat
No. per 1000 m2
References
Temperate
New Zealand (Pacific)
California (Pacific)
North Carolina (Atlantic)
California (Pacific)
New South Wales (Tasman)
37S
36N
36S
36S
35N
34N
34S
Rocky subtidal
Rocky intertidal
Rocky subtidal
Rocky subtidal
Rock jetty
Kelp bed
Seagrass bed
039
230
100
0270
7640
938
10430
15
230
100
63
7640
25
170
Choat & Ayling, 1987

Jones, 1981
Meekan, 1986
Russell, 1977
Hay, 1986
Ebeling et al., 1980
Conacher, Lanzing &
Larkum, 1976
Tropical
Bermuda Islands (Atlantic)
Gulf of Aqaba (Red)
32N
29N
Coral reef
Coral reef
32a
44234
32a
127
Hawaii (Pacific)
Hawaii (Pacific)
Virgin Islands (Caribbean)
Puerto Rico (Caribbean)
Tahiti (Pacific)
Belizean Barrier Reef
(Caribbean)
Dahlak Archipelago (Red)
21N
19N
18N
18N
18S
17N
Coral reef
Coral reef
Coral reef
Coral reef
Coral reef
Coral reef
1100a
172848a
172279a
114152a
312663a
88398
1100a
530a
225a
133a
488a
211
Bardach, 1959
Bouchon-Navaro &
Harmelin-Vivien, 1981
Brock, 1979
Hobson, 1974
Randall, 1963
Barlow, 1975
Galzin, 1977
Lewis & Wainwright, 1985
16N
Coral reef
55a
55a
Great Barrier Reef (Pacific)

Guam (Pacific)
Enewetak Atoll (Pacific)
Aldabra Atoll (Indian)
15S
13N
11N
9S
Coral reef
Coral reef
Coral reef
Coral-reef
137366
57214a
8a
557a
277
130a
8a
557a
Phoenix Islands (Pacific)
4S
Coral reef
176700a 1839a
Locality (ocean/sea)
Range Mean
aDensities
Clark, Ben-Tuvia & Steinitz,

1968
Choat & Bellwood, 1985
Jones & Chase, 1975
Bakus, 1967
Robertson, Polunin &
Leighton, 1979
Grovhoug & Henderson,
1978
are from Bouchon-Navaro & Harmelin-Vivien (1981).
further investigation. Comparative studies and manipulative experiments are required before the latitudinal
differences in the diversity of herbivorous fishes can be better understood.
Abundance
A prevalent opinion is that herbivorous fishes are not only more diverse but more abundant in tropical
waters than in temperate seas (Bakus, 1969; Medd, 1970; Earle, 1972; Ogden & Lobel, 1978; Gaines &
Lubchenco, 1982). Examination of the crude densities of herbivorous fishes compiled from the data on a
variety of temperate and tropical habitats (Table IX), however, reveals no sharp or obvious differences
210
MICHAEL H.HORN
between abundances in the two regions. Almost a 1000-fold difference in densities of fish herbivores is
represented in the 21 localities, but the data are insufficient to allow rigorous comparisons. The large range
of variation shown in the densities from both low and high latitude habitats most likely reflects differences
in fish and habitat characteristics, in sampling methods, and in the conditions under which the density
values were obtained. Conditions more often associated with temperate habitatsreduced visibility,
turbulent waters and low temperaturesmay have lead to under-estimates of herbivore densities in higher
latitudes. On the other hand, the more uniformly warm temperatures in the tropics probably means that
herbivorous fishes are more consistently abundant in the habitat on a year-round basis. The continuous
presence of herbivorous fishes on a tropical reef may be a major reason for the apparently greater impacts
of these fishes on algal community structure than those of their temperate counterparts. Temperate
herbivores may achieve densities rivaling those of tropical species primarily during the summer months. For
example, the high densities of herbivores recorded (Hay, 1986) for a North Carolina rock jetty (Table IX)
were reached in midsummer by a single species, the sparid Diplodus holbrooki. This species and several
other seaweed-eating fishes become more omnivorous during other parts of the year and most individuals
move offshore during the winter (Hay, 1986). That temperate herbivorous fishes can achieve densities as
high as those of tropical species, if only on a seasonal basis, is consistent with the limited evidence
presented earlier (p.251) that these higher latitude herbivores exert some influence on the structure of algal
communities.
RECOMMENDATIONS FOR FUTURE RESEARCH
Virtually all aspects of marine fish herbivory would benefit from further investigation. The following topics
seem particularly important for expanding knowledge of the biology of herbivorous fishes in the sea.
(1) Factors affecting food choice. Diet selection is a complex process in herbivorous fishes. The relative
importance of food quality and antiherbivore defences ought to be carefully assessed. Food preference
studies should examine the roles of vision and chemosensory organs in the food selection process by fishes.
Such an approach might reveal whether fishes can assess food quality directly and how chemically defended
seaweeds are evaluated. In other words, the mechanisms and relative importance of acceptance and
avoidance could be determined.
(2) Physiological effects of seaweed secondary compounds. Although the recent evidence that secondary
metabolites deter feeding by herbivorous fishes is convincing, almost nothing is known about the effects of
these chemicals on the digestive and other systems of herbivorous fishes. This topic is important for
investigation because herbivorous fishes appear to vary greatly in their reaction to, and tolerance of, these
compounds.
(3) Physiology and biochemistry of digestion. Our understanding of digestive mechanisms in herbivorous
fishes is superficial and rudimentary. Much more information is required on the importance of gut pH,
endogenous enzymes and microbial symbionts before an understanding can be reached on how the great
variety of seaweeds consumed by fishes are digested and their nutrients assimilated. Increased knowledge
of digestive physiology should aid in explaining how secondary compounds are tolerated or perhaps
neutralised by certain herbivorous fishes.
(4) Growth. Almost nothing is known about growth in herbivorous fishes. Growth experiments combined
with studies of digestive physiology should be designed to determine whether these fishes feed to satisfy an
energy or a protein requirement, how efficiently they use available protein and how they achieve such rapid
population growth on a low protein diet.
211
(5) The ecological importance of small herbivorous fishes in warm water habitats. Small plant-eating
fishes such as certain blenniids and gobiids, are often highly abundant on tropical and subtropical reefs but
their cryptic behaviour and small size make it difficult to assess their impacts on algal communities.
(6) The ecological impacts of temperate-zone herbivorous fishes. Recent studies show that fish
herbivores in both north temperate and south temperate latitudes reach high abundances, but these
investigations have only provided hints of the potential influence of such fishes on algal community
structure. Experiments should be designed with the specific objective of assessing the role of these fishes in
temperate communities.
(7) The impacts of territorial damselfishes on algal production and herbivore consumption. The relative
effects of weeding, cropping and fertilising by damselfishes on the productivity of algae in their territories
are poorly understood but required for a greater understanding of the influence of these fishes on coral reef
communities. Moreover, studies of the impacts of territorial damselfishes (and surgeonfishes as well) on these
communities should be expanded to encompass larger spatial scales on the reef than has heretofore been
done.
(8) Why are herbivorous fishes more diverse in tropical waters than in temperate waters? Several
hypotheses have been proposed to explain this latitudinal pattern, but few are testable. The hypothesis that
food processing rates are constrained at low temperatures so that energy demands are not met at the low end
of the environmental temperature range seems testable and may help explain the rarity of strictly
herbivorous fishes in temperate latitudes.
(9) Phylogenetic analysis of related fish groups that contain both herbivorous and carnivorous species and
span both temperate and tropical latitudes. A hypothesis of relationships using cladistic techniques and a
data set comprising of digestive tract characters could be developed. This approach might help elucidate the
evolution of herbivory in different monophyltic groups and help explain the distributional patterns of
herbivorous fishes. Candidates for this type of analysis include groups of apparently related taxa such as (1)
girellids, kyphosids and scorpidids, and (2) labrids, scarids and odacids.
ACKNOWLEDGEMENTS
Numerous colleagues aided in the preparation of this review by providing theses, articles in press, and
published papers. In this regard, I particularly wish to thank T.A.Anderson, J.H.Burk, J.H.Choat,
W.H.Fenical, M.E.Hay, M.A.Hixon, M.J.Kingsford, M.G.Meekan, W.L.Montgomery, S.N.Murray, V.J.Paul,
D.W.Rimmer, P.D.Steinberg, T.E.Targett, and D.A.Thomson. Thanks are also due to D.N.Waugh who
compiled some of the data, N.E.Caudill who obtained many articles on short notice through interlibrary loan
and M.B.Fris who delivered an important fish specimen on even shorter notice. I am especially grateful to
C.D.Irelan who gave indispensable help in preparing the figures, compiling the tables and assembling the
manuscript. M.B.Fris, C.D.Irelan, S.N.Murray, and M.A. Neighbors offered constructive comments on the
manuscript in its various stages. My research on herbivorous fishes has been supported by the National
Science Foundation (currently by grant OCE-8716368).
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221

THE BENGUELA ECOSYSTEM PART VI SEABIRDS

A.BERRUTI*
Sea Fisheries Research Institute, Private Bag X2, Rogge Bay 8012, Cape Town, South
Africa
N.J.ADAMS and S.JACKSON
Percy FitzPatrick Institute of African Ornithology, University of Cape Town, Rondebosch
7700, Cape Town, South Africa
ABSTRACT The ecology of seabirds in the Benguela upwelling system off western southern
Africa is reviewed. The marine avifauna comprises a distinctive assemblage of 12 breeding
seabirds (including nine endemic taxa) and 36 species which are regular non-breeding visitors.
Research has concentrated on the resident seabirds, particularly on the interaction between the
three most abundant species, the Cape gannet oM rus ac nep sis,
aj ckass penguin nehpS i
scus
ed rem sus,
and Cape cormorant ahP
al rc ocorax ac ep
nsis, and their commercially-exploited fish
prey, notably the pilchard aS rdinop
s oce al t us and anchovy nE rg aul is aj op nicus ac nep sis .
Changes in the population sizes and th e diets of these three species are consistent with changes
in the catches of the purse-seine fisheries. The pelagic ecology of the non-breeding seabirds and
the responses of seabirds to small-scale and mesoscale variability are poorly known. Bottomtrawling activities appear, however, to be an important determinant of the distribution of the larger
non-breeding species. At present population levels, seabirds probably play a relatively minor role
in energy and nutrient cycling in the Benguela ecosystem. Although the processes regulating
primary production in the Benguela ecosystem appear to be intact, man has brought about major
transformations. Seabird numbers have been reduced in the past by the collection of eggs, chicks,
adults, and guano and by the over-exploitation of epipelagic fish prey. aM n has also reduced the
numbers of predators thought to make prey available to seabirds in mixed-species feeding
assemblages.
INTRODUCTION
The Benguela ecosystem is one of the worlds four major eastern-boundary current regions (Wooster &
Reid, 1963), where primary production is enhanced by wind-driven upwelling (Cushing, 1969) and which
are dominated by similar fish assemblages (Parrish, Bakun, Husby & Nelson, 1983; Crawford, 1987).
223
Various aspects of the Benguela ecosystem have been reviewed: physical features and processes (Shannon,
1985), chemical processes (Chapman & Shannon, 1985), plankton (Shannon & Pillar, 1986), important fish
invertebrate resources (Crawford, Shannon & Pollock, 1987), and coastal zone ecology (Branch &
Griffiths, 1988). This paper reviews the literature on the ecology of seabirds in the Benguela ecosystem and
attempts to identify key ecological processes which affect seabird populations. A full bibliography of all
ornithological literature referring to the seabirds of southern Africa up to 1980 is contained in Cooper &
Brooke (1981) and is partly updated by Brown (1985). Aspects of the interaction between the Cape gannet
Morus capensis, jackass penguin Spheniscus demersus, and Cape cormorant Phalacrocorax capensis and
their commercially valuable fish prey are discussed by Crawford et al. (1987).
SEABIRD RESEARCH IN THE BENGUELA ECOSYSTEM
Seabirds are conspicuous top predators in marine ecosystems, often competing directly with man for food
(Furness, 1982). The interaction between large populations of resident seabirds and their commercially
important fish prey has provided the impetus for much of the seabird research in the Benguela ecosystem
(Frost, 1981; Hockey, Cooper & Duffy, 1983). This topic was the subject of intensive research in the 1950s
(e.g. Davies, 1955; Rand, 1959, 1960a,b, 1963a,b; Matthews, 1961) and again from the late 1970s (e.g.
Crawford & Shelton, 1978, 1981). Changes in the diet and population dynamics of the abundant resident
seabirds relative to changes in fish resources over a period of 30 years (e.g. Crawford & Shelton, 1978,
1981) are probably better known in the Benguela system than for any other large marine ecosystem over a
similar length of time. Since the 1970s, the scope of marine ornithological research has broadened and the
biology of most species breeding in southern Africa has been studied at the nest (Hockey et al. 1983). The
pelagic ecology of only the jackass penguin and Cape gannet are, however, well known (Wilson, 1985a;
Berruti, 1987; Heath & Randall, in press; Wilson, Wilson & Duffy, 1988). Comparatively little is known of
the ecology of the non-breeding seabirds which seasonally visit the Benguela ecosystem (Cooper, 1981a). This
imbalance is reflected in the unequal coverage given to these two groups in this review.
Seabirds are defined as birds which obtain all or much of their food from the open ocean. Birds which
feed in the exposed intertidal region or on the shoreline, or which seldom occur at sea, are excluded.
THE OCEANOGRAPHY OF THE BENGUELA ECOSYSTEM AND AGULHAS
BANK
Seabird assemblages are influenced at different spatial and temporal scales by dynamic oceanographic
processes which affect the availability, distribution and abundance of their marine prey (Schneider & Piatt,
1986; Hunt & Schneider, 1987). The reviews of these processes and their effects (Chapman & Shannon,
1985; Shannon, 1985; Shannon & Pillar, 1986) are used to describe briefly salient features of the Benguela
ecosystem which may affect seabirds.
We define the northern boundary of the Benguela System as the Angola- Benguela front, situated
between 15c and 17S (Shannon, Agenbag & Buys, 1987). The 1000-m depth contour is taken as the
offshore boundary, and includes the entire continental shelf and trawling grounds for bottom-fish (Fig 1)
(Shannon, 1985). Cape Point does not constitute a biological boundary (Duffy, Siegfried & Jackson, 1987b)
and extensive migrations of epipelagic fish occur between the west coast and Agulhas Bank (Crawford et
*Present address: Durban Natural History Museum, PO Box 4085, Durban 4000, South Africa
224
A.BERRUTI, N.J.ADAMS AND S.JACKSON
Fig 1.The Benguela Ecosystem, Agulhas Bank and the continental shelf of southern Africa as defined by the 1000 mdepth contour. Place names mentioned in the text are given.
al. 1987). In the area east of Cape Agulhas, several resident seabirds of the Benguela ecosystem breed in
greatly reduced numbers, or not at all. We consider the western Agulhas Bank as part of the Benguela
ecosystem. The latitude of the mouth of the Orange River is arbitrarily used to divide the Benguela
ecosystem into northern and southern sectors. Differing marine water masses, which may constitute distinct
habitats for seabirds, are temporally and spatially mobile (Shannon, 1985).
The Benguela ecosystem is characterised by upwelling and equatorward surface flow (Fig 1). The area
influenced by upwelling is 150200 km wide. The frontal region between this zone and warmer oceanic
waters is dynamic and is characterised by plumes, filaments, eddies, and the advection of filaments of warm
Agulhas Current water into the southern Benguela ecosystem (Lutjeharms & Stockton, 1987). Plumes of
upwelled waters are separated from oceanic waters by sharp thermosaline gradients and are most marked
during active upwelling. Upwelling occurs at different temporal and spatial scales. Eight upwelling cells
exist between 15c and 35S, including the Cape Peninsula and Cape Columbine (Lutjeharms & Meeuwis,
1987). In the southern Benguela off the Cape Peninsula, upwelling is pulsed with a periodicity of 36 days
but is less variable and slower north of Cape Columbine. In the northern Benguela north of Lderitz,
upwelling is most intense in winter and spring, but is perennial at Lderitz. In the southern Benguela,
upwelling is most intense in summer, but advection of warmer offshore waters may restrict the surface area
of upwelling, and the thermal front may lie close inshore when active upwelling relaxes (Shelton, Boyd &
Armstrong, 1985). In winter, the water column is well mixed and the zone of cool water along the coast is
broad. During the process of upwelling and subsequent warming of waters transported away from the coast,
the nutrient levels become depleted as phytoplankton biomasses increase, lagged by zooplankton blooms.
Secondary plankton blooms may occur. There are interannual differences in the intensity of upwelling.
The spatial distribution of phytoplankton is highly variable in the southern Benguela, but dense
concentrations of phytoplankton are often located offshore in aged, upwelled waters. Nutrient levels and
plankton production are consistently high in the southern Benguela north of Cape Columbine. Zooplankton
levels are highest but most variable inshore, but are higher in St Helena Bay than on the Agulhas Bank. The
extensive upwelling area at Lderitz (Lutjeharms & Meeuwis, 1987) apparently acts as a barrier to
epipelagic, neritic fish, separating stocks of the same fish species (Crawford et al., 1987; Agenbag &
Shannon, 1988).
The Agulhas Bank is a wide bulge of the continental shelf off the southern tip of Africa east of the Benguela
system (see Fig 1), which deflects the Agulhas Current farther south. Upwelling occurs along the eastern
edge of the Agulhas Bank. In summer and late autumn, waters of the Agulhas Bank are characterised by
thermoclines and sub-surface phytoplankton maxima, but in winter, waters are well-mixed (Boyd, Tromp &
Horstman, 1985; Carter, McMurray & Largier, 1987). Nutrient upwelling is limited. Moderate levels of
nutrients occur only in spring; levels in summer are lower because of nutrient depletion in strongly stratified
waters (Brown & Hutchings, 1985).
The structural features of the southern Benguela system proposed by Bang (1971) are variable spatially
(both longshore and offshore) and temporally, and this variability should be recognised in investigations of
the structure and role of seabird assemblages, communities or habitats (cf Abrams, 1985a).
225
THE SEABIRD ASSEMBLAGE OF THE BENGUELA ECOSYSTEM

Seabirds are the most mobile and conspicuous of marine organisms and a large proportion of the seabird
species recorded in southern African waters are vagrants or very rare (Brooke & Sinclair, 1978; Clancey,
Brooke, Irwin & Markus, 1980; Clancey, Brooke, Crowe & Mendelsohn, 1987; Ryan & Rose, 1989). An
assessment of the regularity of occurrence and abundance of seabird species recorded in the Benguela
ecosystem is therefore necessary. Breeding seabirds are defined as those species which breed in the
Benguela ecosystem; non-breeding species are usually seasonal visitors.
THE BREEDING SEABIRDS
Of the 14 species of birds usually regarded as the breeding seabirds of southern Africa (Brooke, 1981a;
Cooper, Williams & Britton, 1984; Berruti, 1989), 12 breed within the Benguela ecosystem, the greyheaded
gull Lams cirrocephalus and roseate tern Sterna dougallii being excluded (Table I). Although the
greyheaded gull occurs at the Cunene estuary, along the central Namibian coast and very sparsely along the
coastline of the southern Benguela (Whitelaw, Underbill, Cooper & Clinning, 1978; Cooper, Robertson &
Shaughnessy, 1980; Ryan, Cooper, Stutterheim & Loutit, 1984b; Cooper, Hockey & Ryan, in prep.), it
mainly inhabits freshwater and estuarine habitats and scavenges along the shoreline (Whitfield, 1977; De
Kock & Randall, 1984). Only one reference to feeding at sea in southern Africa was locatedMiller (1951)
stated that the greyheaded gull occasionally feeds on pilchards Sardinops ocellatus off Natal during the
sardine run. This species should not be regarded as a seabird until it is shown that it regularly feeds at sea.
At present, the roseate tern breeds only in Algoa Bay in southern Africa (Randall &
TABLE I
The breeding seabird species of the Benguela ecosystem
Species
Sphenisciformes
jackass penguin, Spheniscus demersus
Pelecaniformes
white pelican, Pelecanus onocrotalus
Cape gannet, Morus capensis
Cape cormorant, Phalacrocorax capensis
bank cormorant, P.neglectus
crowned cormorant, P.coronatus
whitebreasted cormorant, P.carbo lucidus
Charadriiformes
kelp gull, Larus dominicanus
Hartlaubs gull, L.hartlaubii
Damara tern, Sterna balaenarum
swift tern, S.bergii bergii
Caspian tern, Hydroprogne caspia
Status
endemic
widespread
endemic
endemic
endemic
endemic
widespread
endemic subspecies
endemic
endemic
endemic subspecies
widespread
Randall, 1980). Although it has previously bred in very small numbers at Dyer Island in the Benguela
ecosystem, the bulk of the small southern African population has always bred at localities in the Algoa Bay
226
region (Randall & Randall, 1980). Roseate terns occur rarely in the Benguela ecosystem (e.g. Cooper et al.,
in prep.) and this species is therefore regarded as a rare vagrant. Two breeding species with a tenuous claim
as seabirds are the white pelican Pelecanus onocrotalus and Caspian tern Hydroprogne caspia. White
pelicans rarely feed at sea in the southern Benguela (Guillet & Crowe, 1981; Brooke, 198la) but in the
northern Benguela they occur regularly in the Walvis Bay lagoon, in Sandwich Harbour (40 km south of
Walvis Bay), and along the central Namibian coast (Berry & Berry, 1975; Whitelaw et al., 1978; Cooper et
al., 1980), where they presumably feed on marine prey. Although the Caspian tern mainly occurs in
freshwater and estuarine habitats, it feeds regularly in calm marine bays. The degree to which the two
species rely, however, on marine prey requires further study.
NON-BREEDING SEABIRDS
A total of 77 non-breeding seabird species has been recorded in southern Africa (Ryan & Rose, 1989)
(Table II). We exclude six of these species, the lesser blackbacked gull Larus fuscus, herring gull LOTUS
argentatus, Franklins gull Larus pipixcan, blackheaded gull Larus ridibundus, gullbilled tern Gelochelidon
nilotica, and whitewinged tern Chlidonias leucoptera, because they are vagrants or only occasionally
marine in the Benguela system.
TABLE II
Seabird species which visit but do not breed in the Benguela ecosystem, divided into species which occur regularly and
species which are vagrant, irruptive or very rare
Regular species
Podicipediformes
blacknecked grebe
Procellariiformes
wandering albatross
shy albatross
blackbrowed albatross
greyheaded albatross
yellownosed albatross
northern giant petrel
southern giant petrel
Antarctic fulmar
pintado petrel
greatwinged petrel
softplumaged petrel
broadbilled prion
whitechinned petrel
Corys shearwater
great shearwater
sooty shearwater
Manx shearwater
Podiceps nigricollis
Diomedea exulans
D. cauta
D. melanophris
D. chrysostoma
D. chlororhynchos
Macronectes halli
M. giganteus
Fulmarus glacialoides
Daption capense
Pterodroma macroptera
P. mollis
Pachyptila vittata
Procellaria aequinoctialis
Calonectris diomedea
Puffinus gravis
P. griseus
P. puffinus
little shearwater
European storm petrel
Leachs storm petrel
Wilsons storm petrel
blackbellied storm petrel
Phalacrocoracidae
reed cormorant
Charadriiformes
grey phalarope
Arctic skua
longtailed skua
pomarine skua
Subantarctic skua
Sabines gull
Sandwich tern
common tern
Arctic tern
Antarctic tern
little tern
black tern
Vagrant or very rare species
Sphenisciformes
king penguin
macaroni penguin
rockhopper penguin
Procellariiformes
royal albatross
sooty albatross
lightmantled sooty albatross
Antarctic petrel
Bulwers petrel
whiteheaded petrel
Atlantic petrel
Kerguelen petrel
blue petrel
slenderbilled prion
fairy prion
grey petrel
fleshfooted shearwater
whitebellied storm petrel
Pelecaniformes
P. assimilis
Hydrobates pelagicus
Oceanodroma leucorhoa
Oceanites oceanicus
Fregetta tropica
Phalacrocorax africanus
Phalaropus fulicarius
Stercorarius parasiticus
S. longicaudus
S. pomarinus
Catharacta antarctica
Larus sabini
Sterna sandvicensis
S. hirundo
S. paradisaea
S. vittata
S. albifrons
Chlidonias niger
Aptenodytes patagonicus
Eudyptes chrysolophus
E. chrysocome
Diomedea epomophora
Phoebetria fusca
P. palpebrata
Thalassoica antarctica
Bulweria bulwerii
Pterodroma lessonii
P. incerta
P. brevirostris
Halobaena caerulea
Pachyptila belcheri
P. turtur
Procellaria cinerea
Puffinus carneipes
Fregetta grallaria
227
228
greater frigatebird
redbilled tropic bird
whitetailed tropic bird
redtailed tropic bird
Australian gannet
Charadriiformes
south polar skua
blacklegged kittiwake
roseate tern
royal tern
sooty tern
bridled tern
common noddy
Fregata minor
Phaethon aethereus
P. lepturus
P. rubricauda
Morus serrator
Catharacta maccormicki
Rissa tridactyla
Sterna dougallii
S. maxima
S. fuscata
S. anaethetus
Anous stolidus
Another seven species are not known to have occurred in the Benguela system or Agulhas Bank: Laysan
albatross Diomedea immutabilis, Audubons shearwater Puffinus lherminieri, wedgetailed shearwater
P.pacificus, brown booby Sula leucogaster, blacknaped tern Sterna anaethetus, whitecheeked tern
S.repressa, and lesser noddy Anous tenuirostris. The reed cormorant Phalacrocorax africanus is added to
the list because it has been recorded as a non-breeding bird on the northern Namibian coast south of the
Cunene river and in Algoa Bay (Crawford, Shelton, Brooke & Cooper, 1982b; Every & Spearpoint, 1984;
Ryan, Cooper & Stutterheim, 1984a; Ryan et al, 1984b). The non-breeding seabird fauna of the Benguela
system consists of 65 species: 36 occur regularly while 29 are regarded as vagrants, very rare or irruptive
(Table II) and are not considered as regular members of the marine avifauna of the area. They are ignored in
the following discussion.
BIOGEOGRAPHY
The breeding avifauna of the Benguela System, Agulhas Bank, and southern Agulhas Current (Algoa Bay)
is highly distinctive, and is bounded in the north on both the east and west coasts by tropical marine
avifaunas (Harrison, 1983; Cooper et al., 1984). No seabirds have been known to breed in Angola (Brooke,
1981b), or in southern Moambique in this century (Brooke & Cooper, 1982). Of the 12 seabird species of
the Benguela ecosystem, nine taxa (seven species and two subspecies) are restricted to southern Africa as
breed ing species (see Table I). The specific status of the Cape gannet, Hartlaubs gull Larus hartlaubii, and
crowned cormorant Phalacrocorax coronatus has been debated, but they are at present regarded as full species
(Clancey et al., 1980; Crawford et al., 1982b; Clancey et al, 1987). Subspecific status has been accorded to
the kelp gull Larus dominicanus vetula and swift tern Sterna bergii bergii which breed in southern Africa
(Brooke & Cooper, 1979a; Clancey et al., 1980; Clancey et al, 1987). Freshwater and marine populations of
the whitebreasted cormorant Phalacrocorax carbo lucidus in southern Africa are assigned to the same
subspecies although the marine population is apparently discrete (Brooke, Cooper, Shelton & Crawford,
1982; Jarvis, 1970).
The breeding distribution of seabirds is constrained by the availability of breeding sites free of terrestrial
mammalian predators. Offshore islands and guano platforms provide the safest and most important breeding
sites in southern Africa (Cooper & Berruti, in press). There are four important groups of islands (including
artificial sites) off southern Africa; the guano platforms off central and northern Namibia at Walvis Bay,
229
Swakopmund and Cape Cross, the group of islands off southern Namibia (both northern Benguela System),
the islands off the southwestern Cape between Dyer Island and Lamberts Bay (southern Benguela System)
and the Algoa Bay islands (Agulhas Current) (see Fig 1).
Four species, the whitebreasted cormorant, Damara tern, kelp gull, and Cape cormorant, breed north of
Swakopmund in the northern Benguela, and their breeding distributions extend to Algoa Bay on the east
coast (Clinning, 1978a; Randall, Randall, Batchelor & Ross, 1981a; Brooke et al., 1982; Cooper, Brooke,
Shelton & Crawford, 1982; Crawford, Cooper & Shelton, 1982a). The relatively small number of breeding
species off northern Namibia may be a result of the lack of natural breeding sites in this area. The only
marine population of the white pelican in southern Africa breeds on a guano platform at Walvis Bay, central
Namibia, having bred previously at Sandwich harbour (Crawford et al., 1981). Three species, the bank
Phalacrocorax neglectus and crowned cormorants and Hartlaubs gull breed from central Namibia to the
western Agulhas area (Cooper, 1981b; Crawford et al. 1982a; Williams, 1988; Berruti, 1989). Another four
species (jackass penguin, swift and Caspian terns, and Cape gannet) breed from central or southern Namibia
to Algoa Bay (Clinning, 1978b; Randall et al., 1981a; Crawford et al., 1983b; Shelton, Crawford, Cooper &
Brooke, 1984; Williams, 1988). There are relatively large breeding populations of only two (jackass
penguin and Cape gannet) of the eight species that occur east of Cape Agulhas (Crawford et al., 1983b;
Shelton et al., 1984). The breeding seabird assemblage of Algoa Bay is an extension of the Benguela
avifauna.
The breeding seabirds of the Benguela ecosystem are mainly derived from tropical orders: the
Pelecaniformes and Charadriiformes (Brooke, 1981a). The jackass penguin is the only representative of
Sphenisciformes, an order with its origins in the southern cold regions, although at least four fossil penguins
are known from southern Africa (Brooke, 19811a). The lack of breeding Procellariiformes is surprising as
they breed in other major eastern-boundary upwelling zones. The Benguela System had more breeding
seabirds in the geological past. In the late Miocene and early Pliocene, the breeding fauna included
penguins and petrels, as well as gannets and cormorants (Rich, 1980). Olson (1985a,b) suggested that the
climate and waters of the southeastern Atlantic Ocean were colder at that time. The Benguela upwelling
system is thought, however, to have evolved as an eastern-boundary upwelling system in the late Miocene
(610 Myr ago), while persistent upwelling is thought to have become established in the late Pliocene (about
2 Myr ago) (Shannon, 1985). It is unlikely that the lack of breeding procellariiforms is a result of warmer
conditions as suggested by Olson (1983, 1985a,b), because the Benguela ecosystem supports at least 22
procellariiform species as regular visitors and is no warmer than other eastern-boundary currents which
support breeding procellariiforms. Changes in the availability of suitable nest sites and competition with
abundant breeding seabirds and Cape fur seals Arctocephalus pusillus pusillus may, however, have caused
the displacement of procellariiforms from the few flat islands remaining when water levels changed. The
present assemblage of breeding seabirds has existed for at least 100 000 years, although the relative
proportions of the species appear to have altered (Siegfried, Cooper & Avery, 1982).
On a global scale, three major marine faunal zones have been defined: northern cold, tropical, and
southern cold (Briggs, 1974). These may be subdivided into the Arctic and boreal zones; southern and northern
subtropical and tropical zones; and subantarctic and Antarctic (Ashmole, 1971; Brooke, 19811a).
Geographically, southern Africa falls within the southern subtropical zone (Ashmole, 1971; Brooke,
1981a). Of the 36 regular non-breeding seabirds, 22 are procellariiforms, and 18 of these breed in the
subantarctic and Antarctic regions (Table III). There are 17 charadriiform visitors which, with two
exceptions, breed in the Arctic and boreal regions. Only the Laridae and Phalacrocoracidae have both
breeding and non-breed-
230
TABLE III
The taxonomic grouping of breeding seabirds and taxonomic grouping and breeding grounds of seabirds which are
regular, non-breeding visitors to the Benguela ecosystem Breeding
Breeding
species
Non-breeding species
All species
Taxon
Total
Arctic and
boreal
N. and S.
Subtropics
and Tropics
Antarctic
and
Subantarctic
Total number Resident % Non-resident

%
Podicipedida
e
Pelecanidae
Spheniscidae
Diomedeidae
Procellaridae
Hydrobatida
e
Sulidae
Phalacrocora
cidae
Charadriidae
Laridae
Stercoraridae
Total
100
1
1
0
0
0
0
0
0
1
2
0
0
0
1
0
0
0
5
11
2
1
1
5
13
4
100
100
0
0
0
0
0
100
100
100
1
4
0
0
0
1
0
0
1
5
100
80
0
20
0
5
0
12
1
5
3
12
0
1
0
4
0
1
1
20
1
12
4
48
0
41
0
25
100
59
100
75
ing representatives. The non-breeding seabirds are dominated by the Procellaridae (13 species) and the
Laridae (12 species).
The zoogeography of southern African seabirds has been discussed by various workers (Liversidge,
1959; Winterbottom, 1972, 1974; Brooke, 1981a). Liversidge (1959) and Winterbottom (1972, 1974)
divided the marine area of southern Africa into eastern and western regions based on the distribution of
breeding seabirds and in accordance with major differences in the sea surface temperatures of the warm
Agulhas and cold Benguela systems. Winterbottom (1974) regarded Cape Agulhas as a convenient dividing
point. Neither author commented on the high degree of endemism in southern Africa, partly because
taxonomic changes have resulted in the recognition of subsequent endemic taxa. Both authors regarded the
oceanic birds (defined by Winterbottom, 1974, as farther than 5 km offshore) as being part of the Southern
Oceanic avifauna, although their analyses were based on inadequate lists of non-breeding seabirds.
Brooke (19811a) considered both non-breeding and breeding seabirds in dividing the southern African
marine area into three zoogeographical divisions: west (Cape Cross to Cape Agulhas), south (a transitional
zone from Cape Agulhas to Kei mouth), and east (Kei mouth to Maputo) and suggested that the Moamedes
province of Angola be included as part of the Benguela seabird assemblage. The seabird assemblages show
changes from north to south in the Benguela System. Six seabirds reach their northernmost breeding limits
at Walvis Bay or between Walvis Bay and Lderitz. Most of the marine populations in the Benguela
ecosystem of the blacknecked grebe Podiceps nigricollis, white pelican, Damara and black Chlidonias niger
terns and pomarine Stercorarius pomarinus and longtailed S. longicaudus skuas occur in the northern
Benguela (Jensen & Berry, 1972; Clinning, 1978a; Lambert, 1980; Ryan, 1980; Ryan & Rose, 1989). The
number of procellariform species and their abundance decreases from Walvis Bay northwards while several
231
southern species e.g. Antarctic fulmar Fulmarus glacialoides, greyheaded albatross Diomedea chrysostoma,
and Antarctic tern Sterna vittata are very rare north of the Orange River (Cooper, 1976; Ryan & Rose, 1989).
Even if the short-term and seasonal variations in abundance of seabirds are taken into account, strict
adherence to geographical boundaries in the context of highly mobile seabirds and their habitats, may be
biologically meaningless because such boundaries are unlikely to define accurately seabird habitats or even
zoogeographic regions.
SPECIES RICHNESS
The Benguela ecosystem has fewer breeding species than three other eastern-boundary upwelling systems,
the California, Canary, and Humboldt Currents (Table IV). The Canary Current is lacking in seabirds which
pursue prey underwater, notably cormorants (Le Grand, Emmerson & Martin, 1984). The California
Current, with most breeding species, supports eight alcids (Jehl, 1984), which do not breed in any of the
other systems. The seabird assemblages of both the Humboldt and Benguela systems have an abundant sulid
and a flock-feeding cormorant. Both have a pelican and a penguin. The brown pelican Pelecanus thagus and
white pelican are, however, not ecological equivalents. The brown pelican is an abundant plunge-diving
marine species,
TABLE IV
The number of seabird species in each family and order which breed in the Benguela, California, Canary, and Humboldt
systems, based on this paper; Duffy, Hays & Plenge (1984b); Jehl (1984); Le Grand, Emmerson & Martin (1984) and
Schlatter (1984)
Taxon
Current systems
Order Family
Benguela
California
Canary
Humboldt
0
0
0
2
5
0
5
3
0
0
4
1
0
1
1
4
0
0
1
0
3
0
1
0
1
0
1
0
1
2
3
0
5
0
0
12
7
1
8
27
4
0
0
15
5
0
0
18
Sphenisciformes
Spheniscidae
Procellariiformes
Procellaridae
Hydrobatidae
Pelecanoididae
Pelecaniformes
Phaethontidae
Pelecanidae
Sulidae
Phalacrocoracidae
Fregatidae
Charadriiformes
Laridae
Rhynchopidae
Alcidae
Total
232
whereas the white pelican is essentially a freshwater species which has colonised calm marine waters where
it feeds from the surface.
Despite the low number of breeding seabirds, the assemblage of seabird species in the Benguela system is
rich. The 48 species, which occur regularly, comprise 15% and 17% of the total number of seabird species
listed by Harrison (1983) and Croxall, Evans & Schreiber (1984), respectively.
The abundance and species richness of seabirds is dependent on the scale of time and distance over which
these parameters are measured (Schneider & Duffy, 1985), particularly in the case of non-breeding seabirds
which are not constrained by the distribution of breeding sites. In the southern Benguela, the species
richness of seabirds offshore of the 200 m depth contour increases because of the presence of many nonbreeding species (Duffy, Siegfried & Jackson, 1987b), The fishing activities of bottom-trawlers in waters
deeper than 200 m affect the distribution of some seabird species (Jackson, 1988; Ryan & Moloney, 1988)
and may locally enhance seabird abundance and species richness (Abrams, 1983, 1985a). Fourteen species
of Northern Hemisphere seabirds occur in the Benguela ecosystem in the summer with the Arctic tern
Sterna paradisaea common as a passage migrant only (Ryan & Rose, 1989). With the exception of the
winter-breeding greatwinged petrel Pterodroma macroptera, another 19 species of non-breeding seabirds
from the Southern Hemisphere occur in the Benguela ecosystem mainly in winter (Cooper & Dowle, 1976;
Ryan & Rose, 1989), resulting in an increase in species richness (Summerhayes, Hofmeyr & Rioux, 1974;
Abrams & Griffiths, 1981; Abrams, 1983). The great shearwater Puffinus gravis and blackbellied storm
petrel Fregetta tropica are common on passage only, being abundant in September-October and April-May
(Ryan & Rose, 1989). Immature and non-breeding individuals of many of the abundant procellariiform species
are present in summer in small numbers when the bulk of the populations are present on the breeding
grounds (Ryan & Rose, 1989).
Changes in the structure of seabird assemblages associated with evolving and decaying upwelling events
have not been described in the Benguela System. Detailed surveys of seabird distribution off California
(Briggs & Chu, 1987) have demonstrated high densities of planktivores around the edges of upwelling plumes
with piscivorous seabirds concentrated downstream of major upwellings in less turbulent waters. The
persistence and seasonal predictability of upwelling in the Benguela System may play an important role in
the timing and success of seabird breeding (Duffy, Berruti, Randall & Cooper, 1984a).
FEEDING ECOLOGY
FORAGING GUILDS
Foraging guilds provide a useful framework to summarise the known feeding ecology of seabirds (Tables V
and VI). The breeding seabirds are classified by prey type, feeding zone, and foraging technique (Table V).
The least well known breeding seabirds are the Damara tern, white pelican, Caspian tern, and whitebreasted
cormorant. Because the diets of the non-breeding seabirds are so poorly known and because many species
now rely on trawler offal as a primary food source, evolutionarily selected foraging differences may be
difficult to detect, and the classification of non-breeding species into guilds based on diet and foraging
technique (Abrams & Griffiths, 1981; Abrams, 1983, 1985a) is less useful. Duffy et al. (1987b) categorised
seabirds into three broad guilds (inshore and benthic, epipelagic, trawler offal) according to major prey
types in order to estimate seabird consumption of different food types in the Benguela ecosystem. We have
categorised non-breeding seabirds by foraging zone, feeding techniques, geographical area, and seasonal
occurrence (Table VI).
233
DIET
Breeding seabirds
The diet of most breeding Benguela seabirds, with the exception of the Caspian tern and white pelican, has
been investigated in varying detail (Tables VIIXIV, see Figs 2 and 3). The diet compositions are presented
as percentage numerical abundance, mass, and frequency of occurrence as defined by Hyslop (1980).
The only reported diet items of the marine population of white pelicans
TABLE V
Synopsis of feeding ecology of resident seabird species in the Beuguela ecosystem. Brackets indicate secondary (Cape
gannet) or unknown importance (Kelp and Hartlaubs gulls) of particular foraging technique. Foraging techniques are
defined according to Harper, Croxall & Cooper (1985). Further references are cited in feeding ecology section (pages
285303). Scientific names are given in Table I
Predominant
food type
Where prey
caught
Species
Predominant
prey
Main feeding
techniques
Feeding zone
Major
references
Invertebrates
surface
Epipelagic
fish
surface
Damara tern
small surface
fish, blennies
surface seize,
dipping, piracy
Siegfried
(1977);
Shaugnessy
(1980);
Brooke &
Cooper
(1979b)
surface/
shallow
plunging
Walter (1984);
Ryan (1987a)
bivalves,
crustaceans
small
invertebrates
nearshore and
shoreline
nearshore and
shoreline
(kelp gull)
Hartlaubs
gull
surface seize,
piracy,
dipping
sheltered bays
mainly
N.Benguela
Clinning
(1978a)
Caspian tern
fish
sheltered bays
swift tern
anchovy,
pelagic goby
(Hartlaubs
gull)
white pelican
pelagic goby
surface/
shallow
plunging
surface/
shallow
plunging,
dipping
surface seize,
dipping
surface
seizing
neritic waters
Rand (1959);
Crawford &
Shelton
(1981);
Davies (1955,
1956, 1958);
Matthews
(1961);
Matthews &
fish
near surface
Cape gannet
inner neritic
waters
nearshore in
N.Benguela
sheltered bays
in N.Benguela
pilchard,
anchovy,
saury
Walter (1984);
Walter,
Cooper &
Suter (1987)
Walter (1984)
Berry & Berry
(1975)
deep plunging
234
Berruti
(1983);
Cooper
(1984);
Batchelor &
Ross (1984);
Crawford et
al. (1985);
Berruti (1987)
sub-surface
Cape
cormorant
pilchard,
anchovy,
pelagic goby,
Cape horse
mackerel
pursuit diving
inner neritic
waters
jackass
penguin
anchovy,
pilchard
pursuit diving
inner neritic
waters
Sub-surface
fish &
Crustaceans
benthic
sub-surface/
benthic
whitebreasted
cormorant
fish
(Sparidae)
Rand (1960a);
Davies (1955,
1956, 1958);
Matthews
(1961);
Crawford &
Shelton
(1981);
Cooper
(1984);
Crawford et
al. (1985);
Wilson
(1985a);
Randall &
Randall (1986)
pursuit diving shallow
nearshore
bank
cormorant
clinids,
blennies,
crustaceans
pursuit diving
pursuit diving
crowned
cormorant
clinids
nearshore
shallows,
rocky
substrate
nearshore
coastal kelp
beds
Rand (1960b);
Williams &
Cooper (1983)
Davies (1955,
1956, 1958);
Matthews
(1961); Rand
(1960a);
Crawford &
Shelton
(1981);
Matthews &
Berruti
(1983);
Cooper (1984,
1985a);
Crawford et
al. (1985);
Duffy et al.
(1987c)
Rand (1960b);
Cooper
(1985a)
Rand (1960b)
bank
cormorant
pelagic goby
pursuit diving
Offal
surface
(kelp gull)
(Cape gannet)
hake
deep plunging
open waters
in N.
Benguela
hake
trawling
grounds
235
Crawford et
al. (1985)
surface seize,
piracy, dipping
nearshore,
shoreline,
trawling
grounds
Brooke &
Cooper
(1979b)
Rand (1959);
Crawford &
Shelton
(1981); Davies
(1955, 1956,
1958);
Matthews
(1961);
Matthews &
Berruti
(1983);
Cooper
(1984);
Batchelor &
Ross (1984);
Berruti
(1987);
Crawford et
al. (1985)
TABLE VI
Synopsis of ecological features relating to dietary differences within feeding guilds of regularly occurring non-resident
seabird species occurring in southern African waters. Foraging techniques are defined according to Harper, Croxall &
Cooper (1985). Unless otherwise indicated, the major reference for all species is Ryan & Rose 1989
Species
Where prey
caught
Feeding
technique
Feeding zone
Seasonality
Major reference
blacknecked
grebe
reed cormorant
benthos/surface
pursuit diving
pursuit diving
more numerous
in winter
present all year
Ryan (1980);
Robertson (1981)
sub-surface
sooty shearwater
sub-surface
pursuit diving,
surface diving,
surface seize
pursuit diving,
surface diving,
surface seize
pursuit diving,
surface diving,
surface seize
pursuit diving,
surface diving,
surface seize
coastal bays in
N.Benguela
nearshore,
extreme
N.Benguela
mainly inner
neritic waters
more numerous
in winter
Jackson (1988)
mainly inner
neritic waters
September
March
shelf-break,
oceanic waters
mainly winter
shelf-break,
oceanic waters
SeptemberOctober, AprilMay
Manx shearwater
little shearwater
great shearwater
236
Species
Where prey
caught
Feeding
technique
Feeding zone
Seasonality
European stormpetrel
Leachs stormpetrel
Wilsons stormpetrel
blackbellied
storm-petrel
grey phalarope
surface
pattering
shelf-break,
trawling grounds
shelf-break,
oceanic waters
shelf-break,
trawling grounds
oceanic waters
November
March
OctoberJanuary
broadbilled prion
Sabines gull
pattering
pattering
pattering
surface seize
hydroplaning,
surface seizing,
pattering
neritic and
oceanic waters,
shelf-break
mainly neritic
waters
more abundant in
winter
September
November, May
summer
MaySeptember
neritic waters
SeptemberMay
sandwich tern
pattering, surface
plunging
surface plunging
coastal waters
common tern
dipping
coastal waters
Arctic tern
little tern
dipping, surface
plunging
dipping, surface
plunging
dipping
black tern
dipping
pintado petrel
surface seize
softplumaged
petrel
surface seize
greatwinged petrel
surface seize
Corys shearwater
surface seize,
surface plunging
surface seize,
surface diving
shelf-break,
oceanic waters
southern inner
neritic waters
nearshore coastal
waters
coastal N.
Benguela
shelf-break,
trawling grounds
shelf-break,
oceanic water,
mainly S.
Benguela
shelf-break,
oceanic waters
neritic waters
more abundant in
summer
more abundant in
summer
mainly September
November
April-November
Antarctic tern
whitechinned
petrel
neritic, oceanic
waters, trawling
grounds
Major reference
Furness (1983)
summer
summer
May-October
May-October
mainly November
March
OctoberApril
more numerous in
winter
Jackson (1988)
Antarctic fulmar
surface seize
blackbrowed
albatross
surface seize
greyheaded
albatross
surface seize
yellownosed
albatross
shy albatross
surface seize
wandering
albatross
surface seize
southern giant
petrel
surface seize
northern giant
petrel
surface seize
Subantarctic skua
piracy, dipping,
surface seize
surface seize
longtailed skua
aerial/surface
piracy, dipping
Arctic skua
pomarine skua
aerial
piracy, dipping
piracy, dipping
TABLE VII
trawling grounds
in S.Benguela
shelf-break,
oceanic waters,
southern trawling
grounds
shelf-break,
trawling grounds
in S.Benguela
shelf-break,
oceanic waters
neritic waters,
shelf-break, fronts,
trawler grounds
shelf-break,
oceanic waters,
mainly S.
Benguela
neritic and oceanic
waters, trawling
grounds
neritic and oceanic
waters, off seal
colonies in N.
Benguela
mainly shelfbreak, trawling
grounds, neritic
waters
neritic waters and
trawling grounds
in N. Benguela,
oceanic in S.
Benguela
neritic waters
mainly neritic
waters in N.
Benguela
237
JuneOctober
particularly
common in winter
JuneSeptember
more abundant in
winter
more numerous in
winter
more numerous in
winter
more numerous in
winter
more numerous in
winter
more abundant in
winter
Sinclair (1980)
SeptemberMay
Lambert (1980)
mainly summer
mainly summer
238
Diet of Hartlaubs gull Larus hartlaubii, swift tern Sterna bergii, and Damara tern S.balaenarum in the Benguela
ecosystem. %N=percentage of diet by numerical abundance, %F=percent frequency of occurrence in diet
Species
Hartlaubs gull
swift tern
swift tern
Damara tern
Time period
Feb 1982
Feb 1982
19771986
19751977
Area
Possession Is., N.Benguela Possession Is., N.Benguela Saldanha Bay

Central
region, S.Benguela N.Benguela
Sampling method
otoliths, pellets
otoliths, pellets
regurgitated,
stomach contents
otoliths, pellets
Source
Walter (1984)
Walter (1984)
Walter, Cooper &

Suter (1987)
Clinning (1978a)
No. of samples
35
No. of items
85
72
1311
22
Diet measured
%N
%F
%N
%F
%N
%N
Sufflogobius
bibarbatus
Lampanyctodes
hectoris
Merluccius spp.
Engraulis
japonicus capensis
Hepsetia breviceps
Etrumeus
whiteheadii
Liza richardsonii
Trachurus
capensis
Sardinops
ocellatus
Unidentified
blenny
Other fish
Pterygosquilla
armata
Cephalopoda
Other
invertebrates
39
63
97
91
61
38
0
0
0
0
3
0
10
0
4
51
0
9
0
0
0
0
0
0
0
0
6
6
0
0
0
0
0
0
0
0
0
0
5
3
14
0
68
0
0
0
0
0
0
0
0
9
8
0
0
0
0
0
0
0
0
0
0
5
1
9
0
Sample size
are the chicks of Cape cormorants, eaten at the guano platform where both species nest (Berry, 1976).
Elsewhere, the white pelican eats fish weighing up to 500 g (Cramp & Simmons, 1977) and it is probable
that this species feeds on marine fish in central Namibia.
The gulls are generalist feeders, and much of their terrestrial food is scavenged from man. The marine
diet of the Hartlaubs gull includes amphipods, isopods and fish (Table VIII; Furness, 1983; Walter, 1984;
239
Ryan, 1987a). At Possession Island in the northern Benguela, an analysis of otoliths in regurgitated pellets
showed the diet of this gull to consist entirely of pelagic goby Sufflogobius bibarbatus and lanternfish
Lampanyctodes hectoris (Walter, 1984). In addition, Hartlaubs gulls kleptoparasitise other birds (Morant,
1987; Ryan, 1987a). Before the arrival of European man, the Hartlaubs gull may have relied mainly on
swarming crustaceans caught in the nearshore zone and invertebrates caught along the shoreline (Ryan,
1987a). Important marine food items of kelp gulls are bivalves and offal from bottom trawlers and other
human sources (Siegfried, 1977; Sinclair, 1978; Brooke & Cooper, 1979b; Ryan & Moloney, 1988).
Predation on fish has been recorded (Shelton, De Villiers & Crawford, 1978). Kelp gulls are predators of
seabirds, their eggs and young (Cooper, 1974, 1977a) and they kleptoparasitise other birds (Hockey, 1980;
Avery, 1983; Furness, 1983). Natural scavenging is frequently recorded (Shaughnessy, 1980). Before
European colonisation of southern Africa, kelp gulls may have fed along the shoreline, eating bivalves and
scavenging dead animals, as well as catching surface-living fishes and crustaceans at sea (Brooke & Cooper,
1979b).
The diet of the Damara tern is not well known, and comprises mainly unidentified juvenile blennies. It
also includes the southern mullet Liza richardsonii, anchovy Engraulis japonicus capensis and squid in its
diet (Table VII; Clinning, 1978a). The swift tern eats mainly pelagic goby in the northern Benguela and
anchovy in the southern Benguela (Walter, 1984; Walter, Cooper & Suter, 1987). The diet of the Caspian
tern in the Benguela ecosystem has not been described, but elsewhere it feeds on fish up to 250 mm in
length (Cramp & Simmons, 1985).
The diets of marine populations of the whitebreasted cormorant are poorly known (Table VIII). Rand
(1960b) showed that sparids were important in their diet in the southern Benguela. Cape horse mackerel
Trachurus capensis, musselcracker Sparodon durbanensis, crustaceans, and molluscs were also recorded as
prey in the Benguela ecosystem. De Kock & Randall (1984) noted freshwater, estuarine, and marine fishes
in the diet of whitebreasted cormorants in Algoa Bay. In two Natal estuaries, Mugilidae were the most
important prey (Whitefield, 1977; Jackson, 1984). Whitebreasted cormorants were reported to feed on the
southern mullet in St Helena Bay (Davies, 1956). In a southern Cape estuary, Whitefield (1986) found the
Cape silverside Hepsetia breviceps, a small species, to be the most important prey.
In the southern Benguela, bank and crowned cormorants feed mainly on clinids and other slow-moving
benthic prey (Table VIII; Rand, 1960b; Williams & Burger, 1978; Williams & Cooper, 1983; Cooper,
1985a). At Dassen Island, the diet of the bank cormorant also includes flat fish (Pleuronectiformes) and
platanna-klipfishes (Xenopoclininae) (Cooper, 1985a). At Mercury and Ichaboe islands, the diet consists
almost entirely of pelagic gobies (Cooper, 1984; Crawford, Cruickshank, Shelton & Kruger, 1985). A
TABLE VIII
240
Diet of the whitebreasted cormorant Phalacrocorax carbo, bank cormorant P.neglectus, and crowned cormorant
P.coronatus in the Benguela ecosystem. N and F as in Table VII
Species
whitebreasted
cormorant
bank cormorant
bank
crowned cormorant
cormoran
t
crowned crowned
cormorant cormorant
Time
period
19541956
19541956
1979
1980
May 1980 Sept-Oct

1980
Area
S.W.Cape
S.W.Cape
Ichaboe
S.W.Cape
Is.,
N.Bengue
la
Marcus
Marcus
Is.,
Is.,
S.W.Cape S.W.Cape
Sampling
method
shot, stomach
contents
shot, stomach
contents
regurgitat shot, stomach

contents
ed
stomach
contents
regurgitat
ed
stomach
contents
Source
Rand (1960b)
Rand (1960b)
Crawford Rand (1960b)

et al.
(1985)
Williams Williams
& Cooper & Cooper
(1983)
(1983)
No. of
samples
68
41
10
No. of
items
9a
470
88
143
13
Diet
measure
%N
%F
%N
%F
%N
%N
%F
%N
%N
Sparidae
Clinidae
Blennidae
Sufflogob
ius
bibarbatu
s
Syngnath
us
Ammodyt
es
Triglidae
Heteromy
cteris
Chorisoc
hismus
Merlucci
us spp.
Other fish
89
0
0
0
100
0
0
0
0
23
10
0
0
40
16
0
0
0
0
95
0
10
0
0
0
60
0
0
0
75
0
0
0
46
46
0
15
20
22
0
0
0
0
3
2
6
4
0
0
0
28
0
10
0
0
0
0
10
11
17
10
19521956
regurgitat
ed
stomach
contents
Sample size
241
Species
whitebreasted
cormorant
bank cormorant
bank
crowned cormorant
cormoran
t
crowned crowned
cormorant cormorant
Time
period
19541956
19541956
1979
1980
May 1980 Sept-Oct

1980
Area
S.W.Cape
S.W.Cape
Ichaboe
S.W.Cape
Is.,
N.Bengue
la
Marcus
Marcus
Is.,
Is.,
S.W.Cape S.W.Cape
Sampling
method
shot, stomach
contents
shot, stomach
contents
regurgitat shot, stomach

ed
contents
stomach
contents
regurgitat
ed
stomach
contents
Source
Rand (1960b)
Rand (1960b)
Crawford Rand (1960b)

et al.
(1985)
Williams Williams
& Cooper & Cooper
(1983)
(1983)
No. of
samples
68
41
10
No. of
items
9a
470
88
143
13
Diet
measure
%N
%F
%N
%F
%N
%N
%F
%N
%N
Crustacea
ns
Cephalop
oda
Other
invertebra
tes
22
53
43
30
10
41
12
19521956
regurgitat
ed
stomach
contents
Sample size
Cormorants and molluscs not included.
small but important part of the diet of bank cormorant is the rock lobster Jasus lalandii (Rand, 1960b;
Avery, 1983; Cooper, 1985a).
The diets of Cape gannets, jackass penguins, and Cape cormorants are detailed in Tables IXXIV.
Differential rates of digestion of different food types may result in a bias towards the more durable prey
items (Duffy & Laurenson, 1983; Furness, Laugksch & Duffy, 1984; Wilson, La Cock, Wilson &
Mollagee, 1985; Jackson & Ryan, 1986). Diet studies are based on stomach contents obtained by shooting
(e.g. Davies, 1955; Rand, 1959; Matthews, 1961), regurgitation (Cooper, 1984; Berruti, 1987) or stomach
pumping (Wilson, 1985b). The compositions of the diets of the Cape gannet, jackass penguin and Cape
cormorant in the 1950s (Davies, 1955, 1956; Rand, 1959, 1960a,b; Matthews, 1961) were recalculated from
original data presented in these studies (Tables IXXIV). Empty stomachs were excluded from the
calculation of percentage frequency of occurrence. Percentage mass was recalculated using stomach
contents at the time of collection and not reconstituted mass. Items which were noted as present but were not
242
enumerated, were not included in the recalculation of percent numerical abundance. Diet data presented by
Davies (1955, 1956) were confusing. There are unaccountably large differences between the recalculated
diet compositions and those presented in figures in Davies (1955, 1956). Although the percentage numerical
abundance over-emphasises the contribution of the relatively small and numerous anchovy compared to the
larger pilchard (Duffy & Jackson, 1986), it has been the most frequently used measure of diet composition
in the Benguela ecosystem. All measures of diet composition, however, demonstrate the large differences in
diet between northern and southern Benguela and within the same region over the 30-year period between
the 1950s and 1970s and 1980s (see Figs 2 and 3). In Figures 2 and 3, the numerical abundances of prey in
the diet are averaged over years at one locality or over several localities in a region.
The diets of the Cape gannet, jackass penguin and Cape cormorant tend to be dominated by the same prey
species (Tables IXXIV; Davies, 1955, 1956, 1958; Rand, 1959, 1960a,b; Matthews, 1961; Berry, 1976;
Crawford & Shelton, 1981; Matthews & Berruti, 1983; Cooper, 1984; Crawford et al., 1985; Wilson, 1985b;
Duffy, Wilson & Berruti, 1985; Berruti, 1987; Duffy, Wilson & Wilson, 1987c). These prey species are
pilchard, Cape horse mackerel and anchovy (eaten by all three seabird species), saury Scomberesox saurus
(eaten by Cape gannet) and pelagic goby (eaten by jackass penguin and Cape cormorant). Dominant prey, with
the exception of trawler offal taken by Cape gannets and cephalopods eaten by jackass penguins (Randall,
Randall & Klingelhoeffer, 1981b; Crawford et al., 1985), are epipelagic shoaling fish (Crawford, Shannon
& Pollock, 1987; Berruti, 1988). Changes in the species composition of the diets of the Cape gannet,
jackass penguin and Cape cormorant from the 1950s to the early 1970s, the late 1970s and early 1980s are
consistent with changes in fishery catches of each fish species (Crawford & Shelton, 1981; Cooper, 1984;
Randall & Randall, 1986; Berruti, 1987). There are distinct regional similarities in the diets of all three
species (Tables IXXIV), so that dietary changes are shown in relation to the composition of the purse-seine
catch off Namibia and the western Cape respectively (Figs 2 and 3).
In the 1950s, pilchard dominated the diets of the Cape gannet, jackass
TABLE IX
243
Diet of the Cape gannet Morus capensis in the northern Benguela. All localities except Walvis Bay (central Namibia)
are in southern Namibia. N and F as in Table VII. %M=percentage of diet by mass
Area
Walvis Bay
Walvis Bay
Mercury,
Mercury Is. Ichaboe Is. Possession
Ichaboe
Is.
and
Possession
Is.
Time period 19571958
19581959
19781979 Nov 1978 Nov 1978 Dec 1978

Feb 1979
Feb 1979 Feb 1982
Sampling
method
shot, stomach contents shot, stomach contents
Source
Matthews (1961)
Sample size 155
regurgitate regurgitate regurgitate regurgitate

d, stomach d, stomach d, stomach d, stomach
contents
contents
contents
contents
Matthews & Berruti (1983) Crawforda

& Shelton
(1981)
Crawforda
et al.
(1985)
Crawforda
et al.
(1985)
Crawforda
et al.
(1985)
240
256
116
967
345
Diet
measure
%M
%N
%F
%M
%N
%F
%N
%N
%N
%N
Sardinops
ocellatus
Engraulis
japonicus
capensis
Trachurus
capensis
Sufflogobi
us
bibarbatus
Merluccius
spp.
Scomberes
ox saurus
Other
93
85
81
93
99
76
85
69
36
77
10
10
28
19
22
21
11
Crawford & Shelton (1981) is a subset of Crawford et al. (1985).
244
TABLE X Diet of the jackass penguin Spheniscus demersus in the northern Benguela. All localities except Walvis Bay
(central Namibia) are in southern Namibia. N and F as in Table VII, M as in Table IX
Area
Walvis Bay
Mercury and
Ichaboe Is.
Halifax and
Possession Is.
Mercur Ichabo
y Is.
e Is.
Halifax Possess Mercur

Is.
ion Is. y,
Ichabo
e,
Halifax
and
Possess
ion Is.
Time
period
19571958
1980
1980
Feb
1980
Feb
1980
Jan
1980
Jan
1980
1980
Samplin shot, stomach contents stomach

g
pumping
method
stomach
pumping
stomac
h
pumpin
g
regurgi
tated,
stomac
h
content
s
stomac
h
pumpin
g
stomac
h
pumpin
g
stomac
h
pumpin
g
Source
Matthews (1961)
Crawford &
Shelton (1981)
Crawforda &
Shelton (1981)
Crawfo
rda et
al.
(1985)
Crawfo
rda et
al.
(1985)
Crawfo
rda et
al.
(1985)
Crawfo
rda et
al.
(1985)
Crawfo
rda et
al.
(1985)
Sample
size
19
121
83
50
43
21
45
114
Diet
%M
measure
Sardin
ops
ocellat
us
Engrau
lis
japonic
us
capensi
s
Trachu
rus
capensi
s
Sufflog
obius
bibarb
atus
Merluc
cius
spp.
%N
%F
%M
%N
%M
%N
%N
%N
%N
%N
%N
94
79
68
21
71
92
53
17
73
37
56
24
19
245
Area
Walvis Bay
Mercury and
Ichaboe Is.
Halifax and
Possession Is.
Mercur Ichabo
y Is.
e Is.
Halifax Possess Mercur

Is.
ion Is. y,
Ichabo
e,
Halifax
and
Possess
ion Is.
Time
period
19571958
1980
1980
Feb
1980
Feb
1980
Jan
1980
Jan
1980
1980
Samplin shot, stomach contents stomach

g
pumping
method
stomach
pumping
stomac
h
pumpin
g
regurgi
tated,
stomac
h
content
s
stomac
h
pumpin
g
stomac
h
pumpin
g
stomac
h
pumpin
g
Source
Matthews (1961)
Crawford &
Shelton (1981)
Crawforda &
Shelton (1981)
Crawfo
rda et
al.
(1985)
Crawfo
rda et
al.
(1985)
Crawfo
rda et
al.
(1985)
Crawfo
rda et
al.
(1985)
Crawfo
rda et
al.
(1985)
Sample
size
19
121
83
50
43
21
45
114
Diet
%M
measure
%N
%F
%M
%N
%M
%N
%N
%N
%N
%N
%N
Cephal
opoda
Other
19
12
30
11
26
44
99
93
40
10
50
Crawford & Shelton (1981) overlaps with Crawford et al. (1985).
TABLE XI
246
Diet of the Cape cormorant Phalacrocorax capensis in the Northern Benguela. All localities except Walvis Bay and
Swakopmund (both in central Namibia) are in southern Namibia. N and F as in Table VII, M as in Table IX
Area
Walvis Bay
Walvis Bay
Swakopmun Merc Merc Ichab Ichaboe Is.

d
ury, ury
oe Is.
Posse Is.
ssion
and
Ichab
oe Is.
Ichab Merc
oe Is. ury
Is.
Time 19571958
period
19581959
19731974
1978
1979
Nov
1978
Feb
1980
Nov Nov 1978

1978
Feb
1980
1982 Feb
1982
1983
Sampl shot, stomach

ing
contents
metho
d
shot, stomach
contents
shot,
stomach
contents
regur
gitate
d
stom
ach
conte
nts
regur
gitate
d
stom
ach
conte
nts
regur regurgitated
gitate stomach
contents
d
stom
ach
conte
nts
otolit
hs,
pellet
s
otolit
hs,
pellet
s
Sourc Matthews (1961)

e
Matthews & Berruti Berry (1976) Craw Craw

(1983)
forda forda
&
et al.
Shelt (1985
on
)
(1981
)
Craw Coopera
forda (1981 5b)
et al.
(198
5)
Duff
ya et
al.
(198
7c)
Duff
ya et
al.
(1987
c)
Sampl 210
e size
250
101
10
93
176
71
225
19
%M
Diet
measu
re
%N
%F
%M
%N
%F
%M
%N
%M
%N
%N
%N
%F
%Nb
%Nb
Sardi
nops
ocell
atus
Engr
aulis
japon
icus
cape
nsis
Trac
hurus
cape
nsis
Suffl
ogobi
us
87
67
87
90
76
71
84
80
15
12
28
23
16
21
14
13
65
96
72
100
95
94
100
Area
247
Walvis Bay
Walvis Bay
Swakopmun Merc Merc Ichab Ichaboe Is.

d
ury, ury
oe Is.
Posse Is.
ssion
and
Ichab
oe Is.
Ichab Merc
oe Is. ury
Is.
Time 19571958
period
19581959
19731974
1978
1979
Nov
1978
Feb
1980
Nov Nov 1978

1978
Feb
1980
1982 Feb
1982
1983
Sampl shot, stomach

ing
contents
metho
d
shot, stomach
contents
shot,
stomach
contents
regur
gitate
d
stom
ach
conte
nts
regur
gitate
d
stom
ach
conte
nts
regur regurgitated
gitate stomach
contents
d
stom
ach
conte
nts
otolit
hs,
pellet
s
otolit
hs,
pellet
s
Sourc Matthews (1961)

e
Matthews & Berruti Berry (1976) Craw Craw

(1983)
forda forda
&
et al.
Shelt (1985
on
)
(1981
)
Craw Coopera
forda (1981 5b)
et al.
(198
5)
Duff
ya et
al.
(198
7c)
Duff
ya et
al.
(1987
c)
Sampl 210
e size
250
101
10
%M
Diet
measu
re
bibar
batus
Merl 0
ucciu
s spp.
Other 4
a
b
93
71
225
19
%N
%F
%M
%N
%F
%M
%N
%M
%N
%N
%N
%F
%Nb
%Nb
<1
13
15
Crawford & Shelton (1981) is a subset of Crawford et al. (1985).

%N is estimated from histograms in Duffy el al. (1987c).
TABLE XII
176
248
Diet of the Cape gannet Morus capensis in the southern Benguela and Algoa Bay. Where %F (frequency of occurrence)
has been recalculated from original data, empty stomachs have been excluded. N and F as in Table VII, M as in
Table IX
St Helena Bay
S.W.Cap Malgas
e
Is.
La Lamberts Bay
mb
erts
Bay
&
Mal
gas
Is.
Malgas Is.
Bird Is.a Algoa

Bay
Tim 19531954
e
peri
od
19541955
1954
1956
1977
1978
197 19771986
8
197
9
19781986
19781981
Sam shot, stomach

plin contents
g
met
hod
shot, stomach
contents
shot,
stomach
contents
regurgita
ted
stomach
contents
reg regurgitated
urgi stomach
tate contents
d
sto
ma
ch
con
tent
s
regurgitated
stomach
contents
regurgitated
stomach
contents
Sour Davies (1955)

ce
Davies (1956)
Rand
(1959)
Cooper
(1984)
Cra Berruti (1987)b Berruti (1987)b Batchelor &

wfo
Ross (1984)
rd
&
She
lton
(19
81)
Are
a
Mainly St
Helena Bay
Sam 91
ple
size
Diet %
mea M
sure
Sar
din
ops
oce
llat
us
En
gra
ulic
jap
160
75 or
211c
203
122 3647
4
4818
2031
%N %F %
M
%N %F %
M
%N %N %F %N %
M
%N %F %
M
%N %F %
M
%N %F
60
27
37
83
81
60
51
19
13
18
14
48
44
58
19
67
37
14
15
20
25
39
17
78
63
81
77
32
63
44
12
34
31
249
St Helena Bay
S.W.Cap Malgas
e
Is.
La Lamberts Bay
mb
erts
Bay
&
Mal
gas
Is.
Malgas Is.
Bird Is.a Algoa

Bay
Tim 19531954
e
peri
od
19541955
1954
1956
1977
1978
197 19771986
8
197
9
19781986
19781981
Sam shot, stomach

plin contents
g
met
hod
shot, stomach
contents
shot,
stomach
contents
regurgita
ted
stomach
contents
reg regurgitated
urgi stomach
tate contents
d
sto
ma
ch
con
tent
s
regurgitated
stomach
contents
regurgitated
stomach
contents
Sour Davies (1955)

ce
Davies (1956)
Rand
(1959)
Cooper
(1984)

wfo
Ross (1984)
rd
&
She
lton
(19
81)
Are
a
Mainly St
Helena Bay
Sam 91
ple
size
Diet
mea
sure
oni
cus
cap
ens
is
Tra
chu
rus
cap
ens
is
Suff
log
160
75 or
211c
203
122 3647
4
4818
2031
%
M
%N %F %
M
%N %F %
M
%N %N %F %N %
M
%N %F %
M
%N %F %
M
%N %F
14
12
12
30
<1
250
St Helena Bay
S.W.Cap Malgas
e
Is.
La Lamberts Bay
mb
erts
Bay
&
Mal
gas
Is.
Malgas Is.
Bird Is.a Algoa

Bay
Tim 19531954
e
peri
od
19541955
1954
1956
1977
1978
197 19771986
8
197
9
19781986
19781981
Sam shot, stomach

plin contents
g
met
hod
shot, stomach
contents
shot,
stomach
contents
regurgita
ted
stomach
contents
reg regurgitated
urgi stomach
tate contents
d
sto
ma
ch
con
tent
s
regurgitated
stomach
contents
regurgitated
stomach
contents
Sour Davies (1955)

ce
Davies (1956)
Rand
(1959)
Cooper
(1984)

wfo
Ross (1984)
rd
&
She
lton
(19
81)
Are
a
Mainly St
Helena Bay
Sam 91
ple
size
Diet %
mea M
sure
obi
us
bib
arb
atu
s
Me 0
rlu
cci
us
spp
.
160
75 or
211c
203
122 3647
4
4818
2031
%N %F %
M
%N %F %
M
%N %N %F %N %
M
%N %F %
M
%N %F %
M
%N %F
17
32
32
29
<1
251
St Helena Bay
S.W.Cap Malgas
e
Is.
La Lamberts Bay
mb
erts
Bay
&
Mal
gas
Is.
Malgas Is.
Bird Is.a Algoa

Bay
Tim 19531954
e
peri
od
19541955
1954
1956
1977
1978
197 19771986
8
197
9
19781986
19781981
Sam shot, stomach

plin contents
g
met
hod
shot, stomach
contents
shot,
stomach
contents
regurgita
ted
stomach
contents
reg regurgitated
urgi stomach
tate contents
d
sto
ma
ch
con
tent
s
regurgitated
stomach
contents
regurgitated
stomach
contents
Sour Davies (1955)

ce
Davies (1956)
Rand
(1959)
Cooper
(1984)

wfo
Ross (1984)
rd
&
She
lton
(19
81)
Are
a
Mainly St
Helena Bay
Sam 91
ple
size
Diet %
mea M
sure
Sco
mb
ere
sox
sau
rus
Oth
er
a
160
75 or
211c
203
122 3647
4
4818
2031
%N %F %
M
%N %F %
M
%N %N %F %N %
M
%N %F %
M
%N %F %
M
%N %F
26
39
10
22
17
24
29
14
30
12
25
11
15
10
Arithmetic means of annual means from 19781981.

Crawford & Shelton (1981) are a subset of Berruti (1987).
c Original sample of 257 birds included either 36 or 85 empty stomachs (Rand 1959: Tables 9 and 14).
b
252
Fig 2.Diet compositions (prey species by percentage numerical abundance) of the Cape gannet Morus capensis in
19571958 (Matthews, 1961), 19581959 (Matthews & Berruti, 1983), 19781982 (Crawford et al., 1985; mean of
Ichaboe, Mercury and Possession islands); of the jackass penguin Spheniscus demersus in 19571958 (Matthews,
1961), 1980 (Crawford et al., 1985; mean of Ichaboe, Mercury and Possession islands) and of the Cape cormorant
Phalacrocorax capensis in 19571958 (Matthews, 1961), 1958 1959 (Matthews & Berruti, 1983), 19731974 (Berry,
1976), 19781980 (Crawford et al., 1985; mean of Ichaboe, Mercury and Possession islands) and in 19821983 (Duffy,
Wilson & Wilson, 1987c; mean of Ichaboe and Mercury islands), in the northern Benguela ecosystem in relation to the
total catch of each prey species by the purse-seine fishery off Namibia after Crawford, Shannon & Pollock (1987).
penguin and Cape cormorant in central Namibia in the northern Benguela (Tables IXXI), There were no
diet studies off southern Namibia at this time, but it is likely that pilchard was the dominant prey. A major
pilchard fishery was based in Lderitz between 1964 and 1974. By 1974, the pilchard had become scarce
and purse-seiners were forced to search farther north (Cram, 1977; Crawford et al., 1987). Pilchard catches
decreased greatly in the northern Benguela in 1968 and even further in 1974 (Fig 2). The diet of Cape
cormorants off northern Namibia comprised mainly pilchard before and after the 1968 decrease in commercial
pilchard catches, but consisted mainly of pelagic goby in southern Namibia in the late 1970s (Fig 2;
Table XI). There have been no subsequent diet studies of any of the three species off central Namibia. In the
late 1970s off southern Namibia, the main diet item of jackass penguins was pelagic goby (Fig 2; Table X),
while that of Cape gannets was anchovy (Fig 2; Table IX). Pelagic goby was a major food item of many
predatory fishes and Cape fur seals in this region in the late 1970s and early 1980s (Crawford et al., 1987,
and references therein).
The jackass penguins, Cape gannets and Cape cormorants in the southern Benguela were not as dependent
on pilchard as those in the northern Benguela (Fig 3; Tables VIIXIV). The occurrence of other species,
mainly Cape horse mackerel and anchovy, is reflected in the multi-species nature of the catches of the purseseine fishery of the western Cape (Fig 3; Tables XIIXIV). Following the crash of the pilchard stocks in the
1960s, Cape gannets were able to exploit anchovy, saury, and trawler offal, whereas penguins switched to a
diet consisting almost entirely of anchovy. The Cape cormorant diet was dominated by anchovy and Cape
horse mackerel. Berruti (1987) and Wilson, Wilson & Duffy (1988) caution that the different methods of
diet study in the 1950s (shooting at sea) and post-1978 (sampling at breeding colonies) may invalidate some
of these comparisons.
Outside the Benguela System, the diet of the Cape gannet and the jackass penguin has been studied in
Algoa Bay in the late 1970s (Batchelor, 1982; Randall, 1983; Batchelor & Ross, 1984; Randall & Randall,
1986). Dominant prey items of Cape gannets were pilchard, anchovy and saury (Batchelor, 1982; Batchelor
& Ross, 1984). Anchovy and round herring Etrumeus
TABLE XIII
253
Diet of the jackass penguin Spheniscus demersus in the southern Benguela and Algoa Bay. Where %F (frequency of
occurrence) has been recalculated from original data, empty stomachs have been excluded. N and F as in Table VII, M
as in Table IX
Area Mainly St Helena St Helena Bay
Bay
S.W.Cape
Saldanha
Marcus Island
Bay region
St Croix Is.,
Algoa Bay
Time 19531954
perio
d
19541955
19541956
19771978 19801981
19791981
Sam shot, stomach

pling contents
meth
od
shot, stomach
contents
shot, stomach
contents
stomach
contents
stomach pumping stomach pumping
Sour Davies (1955)

ce
Davies (1956)
Rand (1960a)
Cooper
(1984)
Wilson (1985b)
Randall (1986)
Randall &
Sam
ple
size
92
236
30
556
240
16
Diet %M %N
meas
ure
%F
%M %N
%F
%Ma %N
%F
%N
%F
%M %N
%F
%M %N
%F
77
72
63
54
26
40
33
21
23
20
35
71
32
21
18
24
84
60
80
60
85
56
32
62
13
18
11
26
21
11
14
27
20
54
26
Sar
dino
ps
ocel
latu
s
Eng
raul
is
japo
nicu
s
cap
ensi
s
Tra
chur
us
cap
ensi
s
Etru
meu
s
whit
ehe
adii
Suffl
ogo
254
Area Mainly St Helena St Helena Bay

Bay
S.W.Cape
Saldanha
Marcus Island
Bay region
St Croix Is.,
Algoa Bay
Time 19531954
perio
d
19541955
19541956
19771978 19801981
19791981
Sam shot, stomach

pling contents
meth
od
shot, stomach
contents
shot, stomach
contents
stomach
contents
stomach pumping stomach pumping
Sour Davies (1955)

ce
Davies (1956)
Rand (1960a)
Cooper
(1984)
Wilson (1985b)
Randall (1986)
Randall &
Sam
ple
size
92
236
30
556
240
16
Diet %M %N
meas
ure
bius
biba
rbat
us
Cep 0
0
halo
pod
a
Oth 17
21
er
a
%F
%M %N
%F
%Ma %N
%F
%N
%F
%M %N
%F
%M %N
%F
10
53
23
13
21
47
12
21
Mass of invertebrates not given in this study.
TABLE XIV
255
Diet of the Cape cormorant Phalacrocorax capensis in the southern Benguela. Where %F (frequency of abundance) has
been recalculated from original data, empty stomachs have been excluded. N and F as in Table VII, M as in Table IX
Area
Mainly St Helena St Helena Bay

Bay
S.W.Cape
Saldanha
Bay
Lam Mar
berts cus
Bay Is.
Mal
gas
Is.
Dass Stra Dye

en
ndfo r Is.
Is.
ntei
n
Time 19531954
perio
d
19541955
19541956
19771978 198
2
198
5
1982 1982 198
4
1985 1983 198
5
Samp shot, stomach

ling contents
meth
od
shot, stomach
contents
shot, stomach
contents
stomach
contents
otoli
ths,
pelle
ts
otoli
ths,
pelle
ts
otoli
ths,
pelle
ts
Sour
ce
Davies (1956)
Rand (1960b)
Cooper
(1984)
Duff
y el
al.
(198
7c)
Duff
y et
al.
(198
7c)
57
175
119
286
277
Davies (1955)
Samp 35
le
size
198
4
198
1
198
5
otoli
ths,
pelle
ts
otoli
ths,
pelle
ts
otoli
ths,
pelle
ts
Duff
y et
al.
(198
7c)
Duff
y et
al.
(198
7c)
Duff
y et
al.
(198
7c)
Duff
y et
al.
(198
7c)
44
58
130
202
Diet %M %N
meas
ure
%F
%M %N
%F
%M %N
%F
%N
%F
%Na %Na %Na %Na %Na %Na
34
34
37
68
30
58
12
15
10
24
21
30
20
15
52
23
15
12
18
50
76
64
58
75
89
62
85
31
30
23
19
21
16
26
21
17
20
35
15
25
45
Sard
inop
s
ocell
atus
Eng
rauli
s
japo
nicu
s
cape
nsis
Trac
huru
s
cape
nsis
Etru
meu
s
whit
ehea
dii
256
Area
Mainly St Helena St Helena Bay

Bay
S.W.Cape
Saldanha
Bay
Lam Mar
berts cus
Bay Is.
Mal
gas
Is.
Dass Stra Dye

en
ndfo r Is.
Is.
ntei
n
Time 19531954
perio
d
19541955
19541956
19771978 198
2
198
5
1982 1982 198
4
1985 1983 198
5
Samp shot, stomach

ling contents
meth
od
shot, stomach
contents
shot, stomach
contents
stomach
contents
otoli
ths,
pelle
ts
otoli
ths,
pelle
ts
otoli
ths,
pelle
ts
Sour
ce
Davies (1956)
Rand (1960b)
Cooper
(1984)
Duff
y el
al.
(198
7c)
Duff
y et
al.
(198
7c)
57
175
119
286
277
Davies (1955)
Samp 35
le
size
198
4
198
1
198
5
otoli
ths,
pelle
ts
otoli
ths,
pelle
ts
otoli
ths,
pelle
ts
Duff
y et
al.
(198
7c)
Duff
y et
al.
(198
7c)
Duff
y et
al.
(198
7c)
Duff
y et
al.
(198
7c)
44
58
130
202
Diet %M %N
meas
ure
%F
%M %N
%F
%M %N
%F
%N
%F
%Na %Na %Na %Na %Na %Na
Am
mod
ytes
cape
nsis
Pter
osm
aris
axill
aris
Suff
ogo
bius
biba
rbat
us
Merl
ucci
us
spp.
Othe
r
a
24
21
18
17
14
12
15
17
16
20
11
%N is estimated from histograms in Duffy et al. (1987e).
whiteheadii dominated the diet of jackass penguins (Randall, 1983; Randall & Randall, 1986).
257
Fig 3.Diet compositions (prey species by percentage numerical abundance) of the Cape gannet Morus capensis in
19531954 (Davies, 1955, 1956), 19541956 (Rand, 1959), 19771978 (Cooper, 1984) and 19781986 (Berruti, 1987;
mean of Lamberts Bay and Malgas Island); of the jackass penguin Spheniscus demersus in 19531954 (Davies, 1955,
1956), 19541956 (Rand, 1960a), 19771978 (Cooper, 1984) and 19801981 (Wilson, 1985b) and of the Cape
cormorant Phalacrocorax capensis in 19531954 (Davies, 1955, 1956), 19541956 (Rand, 1960b), 19771978
(Cooper, 1984) and 1982 1985 (Duffy et al., 1987c; mean of Marcus, Malgas and Dassen islands and Lamberts Bay) in
the southern Benguela ecosystem in relation to the total catch of each prey species by the purse-seine fishery off the
western Cape after Crawford et al. (1987). Maasbanker=Cape horse mackerel.
Anchovy and pelagic goby may be ecological replacements of the pilchard (Crawford et al., 1987). The
changes in the diets of jackass penguins and Cape cormorants were accompanied by a decrease in mean
prey size (Crawford & Shelton, 1981; Cooper, 1984). Whereas the mean prey size of Cape gannets
decreased, gannets also increased the size range of prey taken by catching saury and juvenile snoek
Thyrsites atun and scavenging hake Merluccius spp. from trawlers (Crawford & Shelton, 1981; Cooper,
1984; Berruti, 1987). The change from pilchard to alternative prey has usually meant a slight decrease in
prey quality, because pilchard have a higher energy density than anchovy or hake (Batchelor & Ross, 1984;
Heath & Randall, 1985). The high quality of epipelagic shoaling fish has been demonstrated
experimentally. Cape gannet chicks fed ad lib. on pilchard grew faster and attained higher mass asymptotes
than chicks reared on hake (Batchelor & Ross, 1984). Similarly, jackass penguin chicks raised on fish
(including anchovy) grew faster and reached higher mass asymptotes than those fed squid. In addition,
assimilation efficiencies were higher for fish than squid (Heath & Randall, 1985).
Non-breeding seabirds
The diets of non-breeding visitors are poorly known and have been studied only in the southern Benguela
(Furness, 1983; Duffy, Siegfried & Jackson, 1987b; Jackson, 1988). The food of such seabirds may be
divided into three main types: offal provided by the bottom trawlers, surface-shoaling fishes (pilchard and
anchovy), and smaller, surface-living crustaceans and zooplankton. Nearly all the larger and some of the
smaller procellariiforms, classed as cephalopod eaters by Abrams & Griffiths (1981), appear to rely
largely on offal from the fishing industry (Duffy et al., 1987b; Jackson, 1988; Ryan & Moloney, 1988).
Although a few species e.g. yellownosed albatross Diomedea chlororhyncos, are known to catch fish (Ryan
& Rose, 1989), the composition of their diet prior to the advent of bottom trawling is not known. An
example of the changes which may have taken place is the statement by Davies (1955) that blackbrowed
albatrosses Diomedea melanophris regularly fed on pilchard in St Helena Bay. It is possible that the species
of albatross was mis-identified because the yellownosed albatross is known to catch epipelagic fish in the
Benguela ecosystem whereas the blackbrowed albatross is not (Ryan & Rose, 1989). During several cruises
in the 1980s, very few albatrosses of any species were, however, seen in St Helena Bay, and none was seen
feeding on epipelagic fish (A.Berruti, unpubl. data). Among the non-breeding species, the diets of the sooty
shearwater Puffinus griseus and Corys shearwater Calonectris diomedea comprise mainly the adults of
surface-shoaling fishes such as pilchard, anchovy, and saury, and the whitechinned petrel procellaria
aequinoctialis eats a small amount of anchovy (Berruti, 1988; Jackson, 1988). The little shearwater Puffinus
assimilis, Manx shearwater P. puffinus, and great shearwater presumably feed on epipelagic shoaling fish in
the Benguela ecosystem. The smaller species, including terns and Sabines gull Larus sabini (Furness,
1983), storm petrels, and prions feed on small surface-dwelling prey (Ashmole, 1971). In Algoa Bay, the
roseate tern eats ratfish Gonorhyncus gonorhyncus and other small surface-dwelling fishes (Randall &
Randall, 1978). The skuas kleptoparasitise seabirds, mainly the terns, small gulls, and Cape cormorants,
258
although they may also catch prey and take offal from trawlers (Sinclair, 1980; Duffy, 1982; Furness, 1983;
Harrison, 1983). In contrast to the situation in the northern Benguela (Lambert, 1980), the longtailed skua
mainly catches its own prey in the southern Benguela (Ryan & Rose, 1989). The diets of the blacknecked
grebe, which feeds in sheltered nearshore waters (Robertson, 1981; Ryan, 1980; Shaughnessy, 1983), and
marine reed cormorants in northern Namibia are unknown.
FORAGING TECHNIQUES
Feeding techniques described below are defined by Harper, Croxall & Cooper (1985). Breeding seabirds
apparently use a wider range of techniques to catch prey than do non-breeders, although this may partly
reflect the lack of observation of non-breeding seabirds. The four cormorant species and jackass penguins
catch prey by pursuit diving. Burger (1978) compared the functional anatomy of the feeding apparatus of
the four resident species of cormorants and suggested that the beak and jaws of Cape cormorants are
adapted for rapid movement and seizing of fast-moving prey. The Caspian, Damara, and swift terns catch
prey by surface or shallow plunging and dipping. Cape gannets are the only seabird to feed by deep
plunging in the Benguela ecosystem. White pelicans probably catch small fish by surface filtering, usually
feeding in large groups. The kelp and Hartlaubs gulls display a wide range of techniques, feeding while
flying, on the water surface, and on land. Hartlaubs gulls are more agile than kelp gulls and when both
species are present, usually are first to reach prey items (Duffy, Heseltine & La Cock, 1987a).
The feeding techniques of jackass penguins have been investigated in detail, indicating that foraging
groups rarely number more than 17 individuals (Wilson, Wilson & McQuaid, 1986; Ryan, Wilson &
Cooper, 1987). Small groups facilitate synchronised diving and hence effective foraging. In spite of this,
most birds forage alone (Broni, 1985; Wilson et al., 1986). Jackass penguins feed by circling small schools
of fish and then capturing them (Wilson, 1986). Countershading of penguins and some cormorants generally
has been regarded as hunting camouflage (Siegfried, Williams, Frost & Kinahan, 1975). Conspicuous flank
coloration of jackass penguins may, however, increase the efficiency of prey capture by depolarising fish
schools (Wilson, 1986; Ryan et al., 1987). Penguins catch fish from below, seizing fish on or near the
opercula with the tip of the beak (Wilson, 1986).
The larger, non-breeding species mainly seize prey at the surface, although they may occasionally surface
dive to catch prey (Sinclair, 1978; Nicholls, 1979; Voisin & Shaughnesy, 1980; Voisin, 1981). The Puffinus
shearwaters catch prey by pursuit diving. The smaller forms use a variety of techniques to feed at the
surface. Storm petrels catch prey by pattering, and the terns by dipping and surface or shallow plunging.
The European storm petrel Hydrobates pelagicus has been recorded surface-diving for offal (Griffiths, 1981).
The roseate tern catches prey by dipping (Randall & Randall, 1978). Both Sabines gull and broadbilled
prion use a range of techniques, whereas the grey phalarope Phalaropus fulicarius picks up small prey by
surface seizing. Most skuas obtain food by piracy (Furness, 1983). Duffy (1982) suggested that
kleptoparasitic seabirds were in nearly all cases shallower foragers than their hosts, thus obtaining food
otherwise unavailable to them. Arctic skuas Stercorarius parasiticus kleptoparasitise small gulls and terns,
presumably eating the variety of small surface-living prey regurgitated by these species (Furness, 1983). In
the northern Benguela, longtailed skuas kleptoparasitise a similar suite of species, in particular comic terns
Sterna hirundo/paradisaea and Sabines gulls (Lambert, 1980). Natural prey is caught by dipping (Ryan &
Rose, 1989). Subantarctic skuas Catharacta subantarctica, in addition to piracy, eat offal (Sinclair, 1980).
Blacknecked grebes mainly forage in groups and exhibit synchronised surface diving (Robertson, 1981).
The provision of food by trawlers allows observation of the intensely competitive interactions between
feeding seabirds (Sinclair, 1978; Ryan & Rose, 1989). The albatrosses and gannets usually monopolise the
259
source of food at the net or close to the ship, albatrosses seizing prey at the surface while the gannets plunge
dive. Whitechinned and pintado petrels usually feed farther away, while the more agile terns, skuas and
gulls swoop in to seize prey. Sooty shearwaters dive at the edges of the assemblages to seize items that are
slowly sinking. Prions and storm petrels feed away from the larger species on small items.
SPATIO-TEMPORAL ASPECTS OF FORAGING
The foraging of seabirds, and therefore their partitioning of food resources, is geared to processes which
occur at spatial and temporal scales varying from the megascale to the microscale (Schneider & Piatt, 1986;
Hunt & Schneider, 1987). Within the Benguela ecosystem, processes relevant to the foraging of seabirds
take place at scales from metres to hundreds of kilometres and from seconds to years. There have been no
studies in the Benguela ecosystem of seabird distribution and foraging in relation to mesoscale and
microscale oceanographic features, such as thermo-saline fronts, upwelled water masses, and slick lines.
Smaller species, notably the terns and Sabines gulls and also Corys shearwaters often feed at fronts
(Haney & McGillivary, 1985a,b; Ryan & Rose, in press), and along slick lines, which are a surface feature
of internal waves (Haney, 1987). Off California, grey phalaropes feed at localised areas where prey is
concentrated by converging waters (Briggs, Dettman, Lewis & Tyler, 1984). Because seabird foraging in
relation to these processes is poorly documented in the Benguela ecosystem, this section will consider only
the following aspects of spatial divisions in seabird foraging: habitat, depth at which seabirds feed in the
water column, and distance from the breeding colony or shore. The temporal scales that will be considered
are daily and seasonal changes. Feeding associations which are relatively brief in duration and occur over
relatively short spatial scales are dealt with separately. In summer, cyclonic frontal systems move eastwards
to the south of South Africa unimpeded, producing strong southeasterly winds (Shannon, 1985). In winter,
the fronts follow more northerly paths, producing storms and strong north-westerly winds (Shannon, 1985).
There have been, however, no studies in the Benguela ecosystem of the responses of foraging in seabirds to
these changes in weather patterns (Manikowski, 1971; Mendelsohn, 1981).
Habitats
Seabird habitats in the nearshore zone may be characterised by readily recognisable and spatially fixed
biotic and physical correlates such as the presence of kelp beds, type of substratum and depth of water. In
the oceanographically dynamic pelagic environment, marine water masses in the same geographical area
may, however, have very different biotic and physical characteristics over time (Armstrong et al., 1987a).
Seabird foraging zones off southern Africa have been defined in terms of water depth by Duffy et al.
(1987b), presumably because of the distinction between nearshore and inshore-offshore feeding species.
The a priori classification of seabird habitats according to water depth (e.g. Ashmole, 1971) assumes that
water depth is the primary determinant of seabird habitats. Although there may be general correlations
between water depth and other parameters of the habitat, e.g. temperature and distance from shore (Ryan &
Moloney, 1988), these are not necessarily the primary characteristics of the foraging habitats of individual
species or assemblages.
Sheltered bays are the main feeding areas of at least three breeding seabirds, the white pelican, Damara
and Caspian terns (Berry & Berry, 1975; Frost & Shaughnessy, 1976; Clinning, 1978a). The crowned
cormorant feeds inter-and infratidally on rocky shores (Williams & Cooper, 1983). The bank cormorant
usually feeds in Ecklonia and Laminaria kelp beds, but feeds in the open ocean off Mercury and Ichaboe
islands and over shingle and coarse sand at Dassen Island (Cooper, 1985a). The whitebreasted cormorant
260
has been recorded feeding in open water over sand and reefs, near islands, and in estuaries. In estuaries,
whitebreasted cormorants may feed from the near-surface to the bottom (Whitfield, 1977, 1986; Jackson,
1984).
Sheltered bays or calm waters may be important to terns in general. Large numbers of migrant terns,
particularly the common Sterna hirundo and sandwich S.sandvicensis terns feed and roost in sheltered areas
such as St Helena Bay (Cooper, in prep.; A.Berruti, unpubl. data).
At present, there are no published studies correlating the pelagic distribution of a seabird species or
assemblages of species with oceanographic data from spatially dynamic habitats (e.g. matured upwelled
waters) in the Benguela ecosystem. Data which may yield such correlations exist for oceanographic water
masses in the Agulhas retroflection area south of the Agulhas Bank (P.G.Ryan, unpubl. data).
Depth of foraging
Most seabirds in southern Africa feed within the uppermost few metres of ocean. Even the jackass penguin
which is capable of diving to 130 m, usually forages within 30 m of the surface (Wilson, 1985a). There is a
far higher proportion of benthic and sub-surface feeding species amongst breeding that non-breeding
species. Birds feeding in shallow waters may, of course, feed close to the bottom. Crowned, bank, and
whitebreasted cormorants apparently dive to the bottom to feed when foraging close inshore (Wilson &
Wilson, 1988). In contrast, Cape cormorants forage primarily in midwater regions (Wilson & Wilson,
1988). The whitebreasted and bank cormorants remain submerged for longer periods than the crowned or
Cape cormorants (Cooper, 1986). The larger, non-breeding species mainly seize prey at the surface,
although they may dive occasionally from the surface to catch prey (Sinclair, 1978; Nicholls, 1979; Voisin
& Shaughnessy, 1980). One case of plunge diving has been recorded (Voisin, 1981). Amongst the nonbreeding species, only five species of shearwaters may be regarded as sub-surface feeders and only the reed
cormorant and blacknecked grebe as sub-surface or benthic feeders.
Distance of foraging from the shore
Breeding seabirds may be divided into species that feed on prey caught in the nearshore zone (within 1 km
of the shore) or farther offshore (Duffy, Siegfried & Jackson, 1987b). Species feeding offshore may forage
in the inner (within 1015 km of the shoreline) or entire neritic zone (over the continental shelf). Seabirds
feeding on nearshore prey are the bank, crowned, and whitebreasted cormorants, white pelican, and Damara
and Caspian terns. Species feeding farther offshore are the Cape gannet, Cape cormorant, jackass penguin,
and swift tern (Walter, 1984; Wilson, 1985a; Berruti, 1987). The Hartlaubs and kelp gulls feed on land, in
estuaries, and in the nearshore environment (Brooke & Cooper, 1979b; Ryan, 1987a), the kelp gull also
regularly feeds at trawlers over the shelf-break (Ryan & Moloney, 1988), at other fishing boats and natural
feeding associations throughout the neritic zone (pers. obs.).
The larger, non-breeding, mainly offal-eating species are concentrated on the bottom-trawling grounds at
water depths of 4001000 m on the edge of the continental shelf. Non-breeding terns typically roost ashore,
so limiting their offshore foraging range (Ryan & Rose, 1989). A few species, notably Corys and sooty
shearwaters, Sabines gull, and broadbilled prion, Pachyptila vittata are widely distributed over the neritic
zone.
261
Distance of foraging from the breeding colony

Foraging ranges of breeding birds are constrained by the need for adult birds to return to the nest site to feed
chicks. Data have been collected by direct observations of birds (Berruti, 1987), use of remote sensing
devices (Wilson, 1985a), and radiotelemetry (Heath & Randall, in press). Birds dependent on large but
presumably spatially unpredictable shoals forage farther from the colony than those dependent on slowmoving benthic organisms. Bank commorants usually feed in shallow water immediately offshore but up to
9 km from the nest site (Cooper, 1985a). Within the guild feeding on epipelagic shoaling fish, flying
proficiency and ability to ingest food which can be regurgitated back to the chick at the nest also influence
foraging range. The theoretical maximum foraging range of jackass penguins feeding small chicks at
Marcus Island, Saldanha Bay, and at sea for approximately 11 hours, was 24 km, although the actual range
was 20 km (Wilson, 1985a) with most birds seen between 4 and 12 km from the centre of the bay (Broni,
1985; Wilson, Wilson & Duffy, 1988). Jackass penguins tend to move up and down the coast rather than
out to sea and 80% occurred within 3 km of the coast. Jackass penguins from St Croix Island in Algoa Bay
demonstrated a different feeding pattern (Heath & Randall, in press). Breeding birds were absent for a mean
period of 45 hours, with a minimum mean foraging range of about 55 km (Heath & Randall, in press).
Devices used to determine the speed, depth, and foraging range of penguins (Wilson & Bain, 1984a,b) may
affect foraging performance (Wilson, Grant & Duffy, 1986; Heath & Randall, in press). Swift terns, by
comparison, are proficient flyers but are restricted in foraging range, seldom occurring farther than 10 km
offshore, because they usually carry single fish prey to the chicks in their bills (Walter, Cooper & Suter,
1987; Duffy, 1987). Breeding Cape gannets are capable of regurgitating large meals and may travel 200 km
or more in a longshore direction and up to 90 km offshore from the colony (Berruti, 1987).
Activities of bottom-trawlers
Ryan & Moloney (1988) examined attendance patterns of seabirds at trawlers in the southern Benguela to
investigate the effects of the availability of offal from bottom-trawlers on the distribution of seabirds.
Jackass penguins, softplumaged petrels Pterodroma mollis and Cape cormorants avoided feeding
assemblages at trawlers, whereas blackbrowed and shy Diomedea cauta albatrosses, pintado Daption
capensis, and whitechinned petrels were attracted. Cape gannets and kelp gulls only foraged at trawlers in
deeper waters. An analysis of the seabird assemblages revealed deep and shallow water faunal zones.
Temporal differences in foraging
The only breeding seabird which may feed at night regularly is the Hartlaubs gull (Walter, 1984; Ryan,
1987a) although the kelp gull has been reported to feed at night at sea in the lights of a ship (Berruti, 1988).
Most breeding seabirds forage all the year in the Benguela ecosystem with some exceptions. The Damara
tern migrates to the Gulf of Guinea in winter (Collar & Stuart, 1985). Juvenile Cape gannets migrate to the
Gulf of Guinea and farther west in winter (Broekhuysen, Liversidge & Rand, 1961; Crawford et al., 1983b).
Swift terns and kelp gulls disperse along the east coast of southern Africa (Cooper et al., in prep.) and Cape
cormorants occasionally move up the east coast to Natal (La Cock, 1986).
Little is known of diurnal feeding patterns of non-breeding seabirds. The bottom-trawlers fish mainly
during daylight hours so that daytime feeding at trawlers is expected. There is distinct seasonality in the
occurrence of species of non-breeding seabirds (see Table VI, p. 288).
Populations of epipelagic shoaling fish are characterised by predictable seasonal migrations of different
portions of the population (Crawford, 1981; Crawford, Shannon & Pollock, 1987), with concomitant
262
changes in shoaling behaviour, which presumably affect their availability to seabirds. Consequently,
seabirds depending on epipelagic shoaling fish tend to be seasonal breeders, raising chicks during periods of
high availability of fish. During the non-breeding season, these birds may disperse away from breeding
sites. Seabirds dependent on more sedentary benthic prey breed successfully throughout the year and
consequently are restricted to foraging in close vicinity to breeding sites in all months.
FEEDING ASSOCIATIONS
Feeding associations between seabirds, cetaceans, and fishes, notably tunas, are important in tropical oceans
(Harrison, Hida & Seki, 1983; Au & Pitman, 1986). The importance of feeding associations to seabirds is
not well documented in temperate regions, although such associations are frequent (e.g. Evans, 1982).
Feeding associations are important in the feeding ecology of many seabirds in southern Africa (Furness,
1983; Batchelor & Ross, 1984; Randall & Randall, 1984; Berruti, 1987, 1988; Ryan & Rose, 1989). Natural
feeding associations appear to be particularly important to terns and Cape gannets, which catch fish by
plunging or dipping (Jensen & Berry, 1972; Randall & Randall, 1984; Berruti, 1987, 1988). Corys
shearwaters, sooty shearwaters, and whitechinned petrels are known to feed with tuna or cetaceans in the
southern Benguela (Berruti, 1988; Jackson, 1988; Ryan & Rose, 1989) and are used by fishermen to locate
feeding tuna (B.Rose, pers. comm.). Feeding associations generally include one or more species which
catch prey by underwater pursuit. These may be seabirds, either jackass penguins or Cape cormorants,
predatory fish such as yellowfin tuna Thunnus albacares, Cape fur seals or cetaceans, usually the common
dolphin Delphinus delphis or Brydes whale Balaenoptera edeni (Randall & Randall, 1984; Smale, 1986;
Berruti, 1987, 1988). Cape gannets have been recorded feeding in association with dusky dolphins
Lagenorhyncus obscurus, longfin tuna Thunnus alalunga, skipjack Katsuwonus pelamis, yellowtail Seriola
lalandii, snoek, and the shark Carcharinus brachyurus (Smale, 1986; Berruti, 1987, unpubl. data). In Algoa
Bay, Randall & Randall (1984) distinguished between feeding aggregations preying on small and large fish.
Smaller predators such as penguins and terns fed on smaller prey, while larger species such as gannets and
common dolphins fed on larger prey. Seabirds which catch prey by dipping or diving would appear to be
commensal with predators feeding underwater (Au & Pitman, 1986). It is possible that these associations
are, however, mutualistic because diving or dipping seabirds may further disorientate fish trapped at the
surface by predators attacking from below (Colblentz, 1985; Smale, 1986).
A functionally different association occurs when seabirds scavenge scraps from other predators feeding
on larger prey, e.g. petrels scavenging from feeding Cape fur seals. This type of feeding association may
have predisposed some species to become commensals with bottom-trawlers (e.g. Jackson, 1988). The
whitechinned petrel regularly accompanies cetaceans in the Southern Ocean (Enticott, 1986) and its diet off
the western Cape contains a high proportion of trawler offal (Jackson, 1988).
POPULATION DYNAMICS
Seabirds generally are long-lived birds with low adult mortality rates (Croxall, 1987). Factors which are
important in regulating seabird populations are the availability of food in the vicinity of seabird breeding
colonies (Ashmole, 1971; Furness & Birkhead, 1984; Hunt, Eppley & Schneider, 1986; Birt et al., 1987)
and the availability of breeding space (Duffy, 1983a). Populations may also be regulated by food
availability in the non-breeding season, particularly through juvenile survival (Ashmole, 1971; Furness &
Birkhead, 1984). Catastrophic mass mortalities, apparently due to short-term food shortages, periodically
263
may reduce seabird populations (Ashmole, 1971; Duffy, 1983a; La Cock, 1986). Disease or heavy
infestations of endo- or ectoparasites may cause mass mortality or desertion of seabird colonies (Feare,
1976; Duffy, 1983b). Man has directly affected seabird abundance by the harvesting of eggs and birds and
by the destruction of breeding habitats, and indirectly through the introduction of predators and pollutants
(Croxall, Evans & Schreiber, 1984). Because of the lack of information on the population dynamics of nonbreeding seabirds in the Benguela system, this section is largely confined to a review of the productivity and
mortality of breeding seabirds, mainly the abundant species.
NON-BREEDING SEABIRDS
Episodic mortalities of non-breeding seabirds resulting from natural phenomena occur in southern African
waters (Batchelor, 1981; Ryan & Avery, 1987; Ryan, Connell & Gardner, 1988; Ryan & Rose, 1989). It is,
however, not known whether the mortality rates or sizes of populations of non-breeding seabirds in the
Benguela system have changed although human-induced mortality does occur (Ryan & Rose, 1989). It is
likely that the population sizes of non-breeding seabirds in the Benguela system are controlled by processes
acting at or near the distant breeding sites. The assertion that the abundance of non-breeding seabirds in
southern African waters has increased in response to increased amounts of trawler offal (Abrams, 1983)
requires validation (Ryan & Moloney, 1988). There are estimates in South Africa (including the southern
Benguela and Walvis Bay) of the population sizes of non-breeding tern species which roost ashore (Cooper,
1976; Cooper et al., in prep.).
BREEDING SEABIRDS
In the Benguela ecosystem, seabird species feeding on restricted nearshore prey have smaller total
populations and tend to occur in smaller colonies than those feeding on the abundant shoaling fishes
(Table XV). Although 28 and 63 breeding localities have been recorded for jackass penguins and Cape
cormorants, respectively (Cooper & Berruti, in press), 87% of the breeding birds in the two species were
concentrated in six and nine colonies, respectively in 19781981 (Cooper et al., 1982; Shelton et al., 1984).
Over most of their range, bank cormorants feed on benthic prey and occur in small colonies (Cooper, 1981
1b). Concomitant with the change in diet to the abundant pelagic goby in the northern Benguela (Crawford
et al., 1985), the numbers of nests at Mercury and Ichaboe islands, however, increased from 50 and 1302 in
1956 to 2305 and 4102 in 1978, respectively (Cooper, 1981b; Crawford et al., 1985). These increases
strongly suggest the bank cormorant populations are limited by food. The Mercury Island population
collapsed subsequently because of competition with Cape fur seals for breeding space (Crawford, David,
Williams & Dyer, in press). The generalist species, the Hartlaubs and kelp gulls have adapted to human
activities and populations are thought to be increasing (Ryan, 1987a; R.J.M.Crawford, pers. comm.). There
is little information on population trends in breeding seabirds which feed on localised
TABLE XV
The total population size (number of individuals), number of colonies and range in size of colonies (number of
individuals) of breeding seabird species feeding on restricted nearshore resources, abundant pelagic shoaling fishes, and
general foods, in the Benguela ecosystem
Total population Colonies
Major prey type
Pelagic shoaling fish
No
Size References
264
Total population Colonies

Major prey type
No
Size References
Cape gannet
jackass penguin
Cape cormorant
bank cormorantb
swift ternc
Restricted inshore prey bank
cormorantd
whitebreasted cormorante
crowned cormorant
white pelicane
Caspian ternc,e
Damara ternf
Generalists
Hartlaubs gullc
kelp gull
106 306
267 228
277 032
12 814
9 830
5 230
6
29
63a
2
21a
45
2 770194 478
2290 000
2100 000
4 6108 204
2003 308
14520
Crawford et al. (1983b)

Shelton et al. (1984)
Cooper et al. (1982)
Cooper (1981b)
Cooper et al. (in prep.)
Cooper (1981b)
5 048
5 330
250 304
280
?
70a
43
1
20a
30
21 508
2560
250
1247
526
Brooke et al. (1982)

Crawford, Cooper & Shelton (1981)
Cooper, Williams & Britton (1984)
33 000+
22 398
65a
41
21 446

Not all colonies used as breeding sites every year.

Mercury and Ichaboe Island populations only.
c Does not include entire northern Benguela population.
d All colonies except Mercury and Ichaboe.
e Marine population only.
f Semi-colonial.
b
prey resources and it is likely that the overall trends in population size are a consequence of various colonyspecific factors. Since the 1950s, whitebreasted cormorants, Caspian and roeate terns in Algoa Bay are
thought to have decreased whereas numbers of kelp gulls have remained stable (Randall et al., 1981a).
POPULATION FLUCTUATIONS OF CAPE GANNETS, JACKASS PENGUINS AND
CAPE CORMORANTS
Changes in the population sizes of the Cape gannet, jackass penguin, and Cape cormorant are better
documented than such changes for other seabird species in the Benguela ecosystem. Their guano has been
harvested since the 1840s (Shaughnessy, 1984), and guano harvests have provided an index of the
abundance of these three seabirds since the late nineteenth century (Crawford & Shelton, 1978; Duffy &
Siegfried, 1987). The sizes of seabird populations in the Benguela ecosystem were highly variable before
commercial fishing by man began (Crawford & Shelton, 1978; Duffy & Siegfried, 1987), presumably
because of the high natural variation in the biomass of shoaling fish, which are the principal prey of the
abundant seabirds (Crawford, 1987; Crawford, Shannon & Pollock, 1987; Shackleton, 1987). Details of
population changes of the three species are most conveniently discussed in terms of three regions: northern
Benguela, southern Benguela, and east of Cape Point to Algoa Bay, because of regional differences in their
diet (see pages 293303). Changes in the populations at Algoa Bay are considered because all colonies east
of Cape Point follow the same trends.
265
Fig 4.Population estimates of the Cape gannet, jackass penguin and Cape cormorant in the southern Benguela, 1956
1987 (Cooper et al., 1982; Crawford et al., 1983b; Shelton et al., 1984; Berruti, 1987) in relation to the total catch of the
purse-seine fishery off the western Cape after Crawford et al. (1987).
Gannet populations at all islands have been counted from aerial photographs (Shelton, Crawford, Kriel &
Cooper, 1982) but estimates of the proportion of non-breeders present and the rate of breeding failure at the
time of photographing are necessary to obtain accurate estimates of the absolute size of the breeding
population. The size of the breeding colony on Bird Island, Algoa Bay, has been estimated from colony area
(Randall & Ross, 1979; Batchelor & Ross, 1984) but simultaneous determination of nest density is
necessary to obtain accurate estimates of the size of the breeding population because nest density is
apparently variable (Crawford et al., 1983b). None of these three values were measured directly in 1956 and
1969 at Algoa Bay. The area of the nests, which were removed annually for use as fertiliser, indicated a
large increase in the colony area between 1956 and 1967 (Randall & Ross, 1979) but the direct counts from
aerial photographs showed no increase (Crawford et al., 1983b), possibly because of desertion through
breeding failures. If censuses are intermittent, interannual variations in the proportion of non-breeding
adults in the population may bias estimates of rates of population change. Changes in counts from 1982
1984 at Malgas Island are an example (Fig 4). Previous population estimates are, however, adequate to
determine population trends (Shelton et al., 1982). Approximate trends of population size at Algoa Bay
were made from egg harvests in the eighteenth and nineteenth centuries (Ross, 1978).
Three colonies of gannets exist in the northern Benguela (Crawford et al., 1983b). At Mercury Island, the
population decreased between 1956 and 1969 and has since fluctuated at slightly higher levels (Crawford et
al., 1983b; Crawford et al., in press). At Ichaboe Island, numbers diminished greatly from 1956 until 1980,
and increased again until 19851986 (Crawford et al., 1983b; Berruti, 1987). At Possession Island, the
decrease from 1956 has continued unchecked until the most recent census in 1986 (Crawford et al., 1983b;
Berruti, 1987). In the southern Benguela, colonies at Malgas Island and Bird Island, Lamberts Bay,
decreased in size between 1956 and the late 1960s, thereafter increased until 1987 (Crawford et al., 1983b;
Berruti, 1987, unpubl. data). There is one gannet colony east of Cape Point, in Algoa Bay, whose numbers
have increased between 1956 (Randall & Ross, 1979; Batchelor & Ross, 1984) and 1985 (Berruti, 1987).
Ross (1978) suggested that the size of this colony was relatively constant from the eighteenth century to the
mid-twentieth century, after which it began to increase.
Decreases in the pilchard stocks are regarded as the cause for decrease in gannet numbers off southern
Namibia in the northern Benguela (Crawford & Shelton, 1978, 1981), as this fish is the preferred prey of
Cape gannets (Davies, 1956; Batchelor & Ross, 1984; Berruti, 1987; Berruti & Colclough, 1987). Cape
gannets appeared unable to exploit fully the abundant pelagic goby (Crawford et al., 1985) and anchovy
does not seem to have been abundant in this region (Crawford, Shannon & Pollock, 1987). Most of the
anchovy caught in the northern Benguela between 1971 and 1978 were caught north of 25S (Crawford et
al., 1987). The severity of the decrease in gannet numbers in this region increases from north to south, being
apparently related to a shrinkage of the range of the pilchard and anchovy to the north (Cram, 1977;
Crawford et al., 1987). In the southern Benguela, anchovy, hake, and saury have provided alternative prey
resources after the collapse of the pilchard, and gannet populations increased after 1969. Two indices of the
survival of first-year birds from Malgas Island in the 1950s were found to be significantly related to
estimates of pilchard biomass (Crawford et al., 1987). The large increase in 1987 may be associated with an
increase in pilchard stocks (Berruti & Colclough, 1987; Berruti, 1987). There is little information on fish
stocks in the Algoa Bay area where the increase in gannet numbers has been relatively greatest. The
increase may be a recovery from population levels far below those determined by food availability, perhaps
266
because of poor management of guano-scraping (Randall & Ross, 1979). Pilchard have been more important
in the gannet diet at Algoa Bay since 1978, indicating a greater availability on the south coast (Batchelor &
Ross, 1984; Berruti, 1987). Most of the pilchard present in Algoa Bay recruits on the west coast (Armstrong,
Berruti & Colclough, 1987b), and its availability in Algoa Bay should have been affected by decreases in
pilchard stocks off the western Cape. Decreases in pilchard availability to gannets in Algoa Bay may,
however, have been offset by the presence of a large stock of adult anchovy off the south and east coasts
(Hampton, 1987).
Crawford et al., (1983b) argued that inter-colony emigration was necessary to maintain the higher rates
of population growth of the southern gannet colonies observed within the period 1969 to 1981, but this
presupposes accurate population estimates. Variability in the number of non-breeding adults (see Fig 4) and
in the high juvenile mortality (Jarvis, 1974; Duffy et al., 1984a) may account for observed population
changes. Nevertheless, inter-island migration was demonstrated by the attempted colonisation of Dyer
Island by up to 1000 birds, mostly immatures including three ringed two- and three-year old birds from
Malgas Island and Lamberts Bay (Berruti, 1985). The hypothesis that emigration accounts for regional
shifts in population requires that the rate of emigration from declining colonies is greater than that from stable
or increasing colonies. This has not been demonstrated. There are isolated records of disease and
endoparasites in Cape gannets (Uys, Don, Marshall & Wells, 1966; Appleton, 1982). Fledgling Cape
gannets are occasionally killed by Cape fur seals as they swim away from the breeding colony
(Shaughnessy, 1978). Cape gannets have a slow rate of potential increase because the maximum chick
production is one per year and first-year mortality is high (Jarvis, 1974), but adult survival appears to be
high (Furness & Cooper, 1982).
Population trends of Cape cormorants are not easily determined because the species breeds over an
extended period (Rand, 1960b), moves readily between breeding areas (Berry, 1976; Crawford & Shelton,
1981) and frequently deserts nests (Randall et al., 19811a; Duffy et al., 1984a; Crawford, Williams &
Crawford, 1986). There is, however, at least partial fidelity to the nest site (Berry, 1977), presumably related
to predictable feeding conditions. Estimates of the overall population size have been influenced by the
potentially large number of cormorants breeding on artificial platforms in the northern Benguela, and the
accuracy of these counts is unknown (Cooper et al., 1982). The estimate of numbers of Cape cormorants in
1956 by Crawford & Shelton (1981) may considerably under-estimate the overall population at that time
because it did not include non-breeding birds (cf. Rand, 1963b; Berry, 1976). Crawford & Shelton (1981)
suggested an enormous increase in the numbers of Cape cormorants breeding on platforms between 1956
and 1973. In 1973, Berry (1976) estimated that the total populations of Cape cormorants on the platforms
varied between 450 000 and 1 050 000 individuals. Evidence which supports a population increase between
1956 and 1973 is the increase in guano harvests from the platforms over this period (Cooper et al., 1982).
Cape cormorants decreased in numbers between 1973 and 1985 (Crawford & Shelton, 1981; Cooper et al.,
1982; Crawford et al., 1987). Cape cormorants breeding at the islands off southern Namibia increased
between 1956 and 1978, but decreased between 1978 and 1985, although at a slower rate than off northern
Namibia (Crawford et al., 1987). In the southern Benguela, Cape cormorant populations remained relatively
stable between 1956 and 1978 (Crawford & Shelton, 1981; Cooper et al., 1982). There have, however, been
successive years of breeding failure in the 1980s (Duffy et al., 1984a; La Cock, 1986; Crawford et al.,
1986). The only large colony of Cape cormorants east of Cape Point, at Dyer Island, has increased greatly
between 1956 and 1978 (Crawford & Shelton, 1981; Cooper et al., 1982).
The increase in Cape cormorant populations at the guano platforms may have resulted from the
appearance of strong pilchard year-classes in the late 1960s (Crawford et al., 1987). These cormorants
continued to eat mainly pilchard (Berry, 1976) after the decrease in catches in 1970 (Crawford et al., 1987).
267
Fig 5.Population estimates of the Cape gannet, jackass penguin, and Cape cormorant in the northern Benguela, 1956
1982 (Berry, 1976; Cooper et al., 1982; Crawford et al., 1983b; Shelton et al., 1984; Berruti, 1987), in relation to the
total catch of the purse-seine fishery off Namibia (after Crawford et al., 1987). Guano platform refers to the guano
platform off Walvis Bay.
After the second decrease in pilchard catches in 1974, Cape cormorants decreased in numbers (Fig 5).
Crawford et al. (1987) suggested a positive correlation between the numbers of breeding Cape cormorants
and anchovy catches off Namibia. This correlation may be misleading as it ignores the 1973 estimates of the
total, as opposed to the breeding Cape cormorant populations. In 1973 and earlier, Cape cormorants were
eating mainly pilchard (Matthews, 1961; Berry, 1976; Matthews & Berruti, 1983) so comparisons with
pilchard catches (Figs 2 and 5) are appropriate. Off southern Namibia, the Cape cormorants switched to
pelagic goby (Crawford & Shelton, 1981; Cooper, 1985b; Crawford et al., 1985). In the southern Benguela,
Cape cormorants appear to have successfully switched to anchovy after the collapse of the pilchard catches
in 1966 (Crawford et al., 1987). Recent cormorant breeding failures, however, suggest that the anchovy is
not a predictable resource for Cape cormorants, despite estimates of adult anchovy biomass in excess of one
million metric tons (Hampton, 1987). The great increase in Cape cormorant populations at Dyer Island since
1956 may be related to the presence of a large adult anchovy stock on the Agulhas Bank (Hampton, 1987).
Because Cape cormorants are mobile and have a high rate of potential increase (Berry, 1976), they can
take advantage of short-term regional increases in prey abundance (Crawford, Shelton & Berruti, 1983a).
Conversely, the species appears to be vulnerable to temporary food shortages, leading to mass desertion of
nests and death of adults (Rand, 1960b; Crawford, Shelton, Batchelor & Clinning, 1980; Duffy et al., 1984a;
La Cock, 1986). In 19851986, desertions occurred at all major colonies between Lderitz and Cape
Agulhas (Crawford et al., 1986). These events are likely to be important in regulating the population size of
Cape cormorants.
Counting of jackass penguin populations is difficult because of variability in the level of adult
absenteeism at colonies, principally because of interannual variation in the timing and success of breeding,
the proportion of breeders and the prolonged breeding season (Randall, Randall, Cooper & Frost, 1986a).
Counts of moulting birds (Randall et al., 1986a) suggest previous under-estimation of total penguin
population size. Counts of breeding birds repeated over a number of years using consistent methods should,
however, allow population trends to be determined (Shelton et al., 1982).
The population size of jackass penguins breeding at islands (mainly Ichaboe and Mercury islands) north
of Lderitz in the northern Benguela showed little change between 1956 and 1967, but had increased greatly
by 1978 (Crawford & Shelton, 1981). Small mainland colonies found in this area during the 1980s may
have been established during this period (Loutit & Boyer, 1985). Crawford et al. (1987) showed a
northward shift in the bulk of the breeding population of jackass penguins after 1967, although overall
populations off Namibia in 1985 had decreased to 17% of the 1956 population. The population at Mercury
Island has decreased between 1978 and 1985 because of displacement by an expanding Cape fur seal
population (Crawford et al., in press). Other penguin colonies have been displaced by Cape fur seals
(Shaughnessy, 1980; Crawford et al., 1985). The sizes of jackass penguin colonies between Lderitz and the
Orange River have decreased rapidly and continuously since 1956. Colonies in the southern Benguela north
of Cape Point have similarly decreased in size (Crawford & Shelton, 1981; Shelton et al., 1984; Crawford,
et al., 1987) with the exception of the recolonisation of Robben Island discovered in 1983 (Shelton et al.,
1984). This colony has continued to grow in numbers by immigration (R.J.M.Crawford, unpubl. data).
Colonies east of Cape Point have increased greatly since 1956 (Crawford & Shelton, 1981; Shelton et al.,
1984; Cooper, in press). In addition, two mainland colonies have become established in the 1980s (Cooper,
268
in press; A.Berruti, unpubl. data) and a single mainland breeding attempt was noted in the eastern Cape
(Every, 1983).
The general decrease in total penguin numbers has been attributed to egg-harvesting, guano-collecting
and competition with fisheries (Frost, Siegfried & Cooper, 1976). This decrease has continued despite the
cessation of egg-collecting in 1965 and of guano-scraping on many islands since the 1960s (Shelton et al,
1984; La Cock, Duffy & Cooper, 1987; A.Berruti, unpubl. data). The collapse of the pilchard stocks is
thought to be the reason for the continued penguin population decrease between Lderitz and Robben Island
(Crawford & Shelton, 1978, 1981; Crawford et al., 1987). The islands south of Lderitz were particularly
severely hit by a decline in prey availability. North of Lderitz, jackass penguins switched successfully to
pelagic gobies after the pilchard decreased (Crawford et al., 1985). In Algoa Bay, penguin chick mortality has
resulted from heat stress (Randall, 1983), although jackass penguins show some behavioural adaptations to
nesting in a hot, arid environment (Frost, Siegfried & Burger, 1976). Mortality as a result of rainfall and
trematode infestations has been recorded at Algoa Bay (Randall & Bray, 1983; Randall, Randall & Erasmus,
1986b). Tick infestations do not, however, appear to affect penguin breeding success at Marcus Island
(Daturi, 1986).
Off South Africa, life-table parameters have been determined at the stable St Croix colony at Algoa Bay
(Randall, 1983) and at the declining Marcus Island colony in the Saldanha Bay region off the west coast (La
Cock et al., 1987). Breeding success was higher in the declining Marcus Island colony, but juvenile survival
was far lower. Duffy et al. (1987d) suggested that greater juvenile mortality off the west coast may be a
result of direct competition with commercial purse-seiners in the offshore region. Randall et al., (1987)
showed that fledgling penguins disperse in a clockwise direction from southern African colonies. For
penguins from Marcus Island, it is proposed that competition between juveniles and the commercial fishery
takes place in St Helena Bay (Duffy et al., 1987d). Fledgling jackass penguins, however, disperse rapidly
(Randall et al., 1987) and Marcus Island fledglings may travel farther than St Helena Bay. Rand (1960a)
recorded that the diet of eight immature penguins contained a greater proportion of slow-moving prey such
as stomatopods and polychaetes than the diet of adults. These prey species are not commercially exploited,
suggesting limited competition between juvenile penguins and purse-seiners. The hypothesis that juvenile
penguins eat more larval epipelagic fish than do adults (Wilson, 1985a) is unsupported by direct evidence.
Adult survival at the declining Marcus Island colony (La Cock et al., 1987) was lower than at two south
coast islands: St Croix (Randall, 1983) and Dyer Island (La Cock & Hanel, 1987). Based on the observation
that the foraging range of breeding penguins and fishing area of the purse-seiners are largely separate
(Wilson, 1985a; Broni, 1985; Wilson, Wilson & Duffy, 1988), Duffy et al. (1987d) suggested that there was
no direct competition between breeding penguins and purse-seiners. This presupposes the unlikely situation
of no interchange of anchovy shoals between inshore and offshore areas. The lack of any significant
negative correlation between fishery catches and growth rates of penguin chicks (Duffy et al., 1987d) is
more convincing proof of little or no direct competition. There is no specific explanation for low adult
survival in the Benguela ecosystem although competition with the purse-seiners in the non-breeding season
is implied (Duffy et al., 1987d). Adult penguins have a number of predators (Cooper, 1974; Shaughnessy,
1978; Randall, Randall & Compagno, 1988). Many studies of the population dynamics of jackass penguins
(e.g. Randall, 1983; La Cock et al., 1987; La Cock & Hanel, 1987) may be subject to many sources of bias
(Aebischer & Coulson, 1987).
An alternative hypothesis is that the survival of adult and juvenile penguins may be reduced in the nonbreeding season because anchovy distribution off the west coast is unpredictable as a result of the southward
migration of anchovy. Current estimates of anchovy spawner biomass have been in the region of a million
metric tons (Hampton, 1987), suggesting an abundant resource despite commercial fishing. The bulk of the
269
anchovy population recruit on the west coast from March onwards and migrate southwards to the Agulhas
Bank (Crawford, 1981), where most are located by November (Hampton, 1987). The anchovy resource may
be more predictable from Robben Island south and eastwards (Hampton, 1987). In addition, penguins may also
prey on local populations of anchovy recruited away from the main west coast recruitment area (Duffy,
Wilson & Berruti, 1985).
Over the last 30 years, evidence has accumulated that the populations of the Cape gannet, jackass
penguin, and Cape cormorant have been limited by food (see pages 311318). It appears that episodic
reductions in fish availability preceding or associated with global weather changes may result in the
widespread failure of the breeding of seabirds (Duffy et al., 1984a; La Cock, 1986). The El Nio
phenomenon has been linked to massive mortality and breeding failure of seabirds in the Pacific Ocean
(Ainley & Lewis, 1974; Duffy, 1983b; Schreiber & Schreiber, 1984). El Nio is a local expression of
changes in the Southern Oscillation which is a major feature of the atmospheric and hydrospheric
circulations over the Pacific Ocean (Barber & Chavez, 1983). Mass mortalities of breeding seabirds in the
Benguela system tended to occur in the same year as anomalous worldwide climatic events, but often
preceded warm-water events (La Cock, 1986). The relationship between the Southern Oscillation and
environmental anomalies in the Benguela ecosystem, and its effects on fish populations, are not well
understood (Shannon, Crawford & Duffy, 1984; La Cock, 1986).
The lack of breeding space may have limited seabird populations before the settlement of Europeans in
southern Africa (Burger & Cooper, 1984). Interspecific competition for breeding space is, however, minimal
in the Benguela ecosystem at present (Duffy & La Cock, 1985), although Cape fur seals have displaced
seabirds from breeding colonies at some islands (Crawford et al., in press). Lack of absolute breeding space
may not be limiting the size of Benguela seabird populations, but the distribution of breeding space is not
optimal (Burger & Cooper, 1984). There is very little available breeding space off northern Namibia and on
the Agulhas Bank, where there are large stocks of epipelagic fish and other food resources (Crawford et al.,
1987). The limited number of breeding sites is demonstrated by the frequent use of artificial structures,
notably wrecked and floating ships, by cormorants (Cooper, 1981b; Brooke et al., 1982; Cooper et al., 1982;
Crawford et al., 1982b; Brooke & Loutit, 1984). In addition, the colonisation of a new mainland colony at
Bettys Bay, western Agulhas Bank, by whitebreasted, bank, and crowned cormorants took place within a
few months of its permanent protection from distrubance (Cooper, 1988). Whilst ticks have been recorded
from the nests of several seabirds (Williams, 1978; Daturi, 1986), it has yet to be shown that parasite
infestations and diseases are important in controlling seabird populations in the Benguela system.
Direct human interference as a factor in the regulation of breeding seabird populations is now relatively
unimportant (Cooper & Berruti, in press), although local populations of the jackass penguin have suffered
heavy mortality from oil spills (Morant, Cooper & Randall, 1981). Excluding the impact of commercial fishing
activities, the most important indirect effects appear to be the impact of introduced predators (Berruti, 1986)
and pollution. The accumulation of organochlorine pesticide residues, polychlorinated biphenyls and heavy
metals in seabird eggs apparently has not reached levels where they may cause mortality (De Kock &
Randall, 1984; Gardner, Siegfried & Connell, 1985). The extent and potential effects of ingestion of plastic
pellets on seabirds occurring off southern Africa have been examined (Ryan, 1987b; Ryan, Connell &
Gardner, 1988). Plastic pellets occurred most frequently in procellariiforms, particularly blue petrels
Halobaena caerulea, great shearwaters and pintado petrels and are probably ingested as a result of
misdirected feeding attempts. Evidence for detrimental effects on adult seabirds are equivocal but there is
some evidence that seabirds may assimilate toxic chemicals from ingested plastic pellets (Ryan et al.,
1988).
270
ENERGY FLOW AND NUTRIENT CYCLING

On a regional scale and at present population sizes seabirds may play only a relatively minor role in energy
and nutrient cycling compared with the large populations of predatory fish and marine mammals (Bergh,
Field & Shannon, 1985; David, 1987). The amount of food consumed by seabirds is considered below.
ENERGY FLOW
Attempts to quantify the role of seabirds as consumers in southern African marine ecosystems have
concentrated on the southern Benguela (Duffy, Siegfried & Jackson, 1987b). The first models of seabird
consumption were proposed in the 1950s and resulted from complaints by the fishing industry of excessive
seabird predation on commercially valuable fish (Davies, 1955), a perception that still exists in some
quarters today (Anonymous, 1983). These estimates of food consumption by the three most abundant
seabirds, jackass penguin, Cape gannet, and Cape cormorant in the southern (Davies, 1955, 1956, 1958;
Rand, 1959, 1960a,b) and northern Benguela (Matthews, 1961) were determined by multiplying the
numbers of seabirds by daily food consumption estimated from stomach contents. High initial estimates of
food consumption (Davies, 1955) were reduced as more realistic census data and feeding rates were used
(Davies, 1958; Rand, 1959, 1960a,b). Jarvis (1971) used the same methods to estimate the food
consumption of Cape gannets in the southern Benguela.
The objectives of such studies then changed from merely determining the food consumption to
understanding the flow of energy through the marine system. The energetic requirements for chick growth of
the jackass penguin and Cape gannet were estimated empirically (Cooper, 1977b, 1978). Cooper (1981a)
produced a preliminary model of energy flow through seabirds and seals in the southern Benguela without
describing methods. Furness & Cooper (1982) used a bioenergetic model to estimate energy flow to jackass
penguins, Cape cormorants, and Cape gannets in the Saldanha Bay region, incorporating the costs of egg
production, chick-rearing and moulting. The assimilation efficiency, population dynamics, and time budgets
of each species were also included but the sources of some of these data are unclear. The model was based
on Furness (1978). Energy consumption was converted to weight of fish consumed. This model, the most
detailed for a seabird community in southern Africa, showed that seabirds consumed an amount of fish
equal to 30% of the fishery catches in this area, and estimated that seabirds were consuming 23% of
anchovy production. This model, however, used Virtual Population Analysis (VPA) to estimate fish stock
sizes. This technique, which estimated the anchovy biomass as 300 000400 000 metric tons, has since been
discarded (Armstrong, Shelton & Prosch, 1985) in favour of direct acoustic surveys which show an anchovy
biomass of about one million metric tons (Hampton, 1987). Most of the stocks of epipelagic fish species
eaten by seabirds migrate through the Saldanha Bay region (Crawford, et al., 1987), where seabird densities
are high, to the Agulhas Bank, where seabird densities are low (Duffy, Siegfried & Jackson, 1987b).
Accordingly, the estimate of seabird predation in the Saldanha Bay area by Furness & Cooper (1982) as a
proportion of the anchovy stock is too high.
Nagy, Siegfried & Wilson (1984) estimated annual food consumption, mainly anchovy, of jackass
penguins from the Saldanha Bay fishing grounds by combining field metabolic rates, measured using
doubly labelled water, and time budgets. Annual fish consumption was estimated at 16 800 metric tons.
This is considerably higher than the approximately 10 500 metric tons estimated by Furness & Cooper
(1982), a difference largely attributed to the lower value of metabolisable energy content accorded to their
anchovy prey by Nagy et al. (1984). Total food consumption over the entire South African fishing grounds
was estimated at 22 100 metric tons.
271
The most comprehensive account of the role of seabirds as predators (Duffy et al., 1987b), estimated the
consumption of all seabirds from the Agulhas Bank to Lderitz, using bioenergetic equations and
abundance data from censuses from ground, ship, and aerial surveys. The abundance and energy
consumption of seabirds varied seasonally and regionally, and non-breeding seabirds consumed more than
breeding seabirds. Total consumption of all seabirds was estimated 150 000 metric tons and of breeding
seabirds in the southern Benguela at 50 000 metric tons. Although the authors recognised the low accuracy
of census at sea, the study is a useful first attempt at quantifying the role of the seabird community as a
whole.
Duffy & Siegfried (1987) used estimates of the guano produced by an average seabird in the southern
Benguela to convert the guano harvests from this region into seabird abundance for the period 19051974.
Energy consumption of this average seabird was then converted to fish mass, and suggested that the
consumption of fish varied between 10 000 and 50 000 metric tons in this time period. Their abundance
estimates are low compared with actual census figures (Crawford & Shelton, 1978; Cooper, Williams &
Britton, 1984). Nevertheless, their conclusion that the breeding seabirds did not take more than 5% of fish
biomass remains true because of the substantial margin of error allowed.
Three major problems face the determination of seabird food consumption. The first of these is estimation
of abundance of both breeding seabirds at colonies (Shelton et al., 1982; Duffy & Siegfried, 1987) and nonbreeding seabirds at roosts or at sea (Briggs, Tyler & Lewis, 1985a,b). In particular, penguin populations
may have been greatly under-estimated in the past (Randall et al., 1986a). Secondly, the diet of the most
important seabirds has changed in time (Crawford & Shelton, 1981; Cooper, 1984; Berruti, 1987) which can
lead to misleading estimates of consumption of particular fish species if diet and census estimates are not
contemporaneous. Thirdly, the estimation of energy consumed can vary greatly (Duffy & Siegfried, 1987)
depending on the choice of energetic equation (Laugksch & Duffy, 1984), bird weight, and parameters used
for assimilation efficiency and energy density of prey (Heath & Randall, 1985; Jackson, 1986), time and
activity budgets (Furness, 1982) and the energy costs of incubation and moulting (Furness & Cooper,
1982).
Given these constraints, it may be suggested that assessment of the food consumption of seabirds is
unlikely to be accurate or precise. The wide range of methods used to estimate the biomass of fish
consumed in the southern Benguela, however, yielded results of a similar order of magnitude varying
TABLE XVI
Estimates of food consumption by Cape gannet Morus capensis, jackass penguin Spheniscus demersus and Cape
cormorant Phalacrocrax capensis (19051978), and all seabirds (19831984) in the Benguela ecosystem, South Africa,
modified from Duffy, Siegfried & Jackson (1987b). Details of methods given in the text (pages 320321) and by Duffy
et al. (1987b) and by Duffy & Siegfried (1987). ND=no data available
Total consumption
103t
Population (individuals103)
Period
Approximate area
penguin
gannet cormorant References
19051974
1050
Southwestern
Benguela
Southwestern Cape
Walvis Bay area
Entire Benguela
West Coast
Entire Benguela
ND
ND
ND
103
+
130
ND
50
50
61
50
ND
120
200
80
ND
19541955 18
19571958 37.5
1958
45
1970
5
1977
250
Duffy & Siegfried

(1987)
Rand (1959, 1960a,b)
Matthews (1961)
Davies (1958)
Jarvis (1971)
Cooper (1981b)
272
Total consumption
103t
Population (individuals103)
Period
Approximate area
penguin
gannet cormorant References
1978
16.4
Southwestern Cape
724
174
37.5
1978
6372
Entire Benguela
104.3
185.7
372
Post 1964
50
Southern Benguela
ND
ND
167
1978
1978
56.2
16.8
Southern Benguela
Southwestern Cape
107
122
84
432
1978
22.1
Entire Benguela
160
19831984
156.5a
Southern Benguela
19831984
115.8b
Southern Benguela
a
b
Furness & Cooper

(1982)
Laugksch & Duffy
(1984)
Bergh, Field &
Shannon (1985)
This study
Nagy, Siegfried &
Wilson (1984)
Nagy, Siegfried &
Wilson (1984)
Duffy, Siegfried &
Jackson (1987b)
Duffy, Siegfried &
Jackson (1987b)
All food types.

Pelagic fish only.
from 10 00090 000 metric tons (Table XVI). There are no estimates of seabird consumption in Algoa Bay
where population sizes are well known. Seabirds eat a small part of primary production, estimated at 0.02%
by Duffy et al. (1987b), and do not compete to any marked extent with the commercial fishery. Food
consumption has been estimated at 0.82.8 g.m2.yr1 by Duffy et al. (1987b) and 1.82.1 g.m2.yr1 by
Abrams (1985b).
The level of trophic impact of breeding seabirds depends on the trophic level of their most important prey
species, anchovy and pilchard. Both these species eat mainly zooplankton which are primary or secondary
consumers (James, 1987; unpubl. data). Seabird predators in the Benguela feed at several trophic levels, and
are most likely to be tertiary or quaternary consumers. Over the last 3040 years, much of the energy
flowing to non-breeding seabirds has been in the form of offal or discarded mid-water or benthic fish from
the bottom fishery (Stanford, 1953; Grindley, 1967; Sinclair, 1978; Abrams & Griffiths, 1981).
NUTRIENT CYCLING
Colonially-nesting seabirds concentrate at islands to breed and roost, usually in large numbers. Guano
deposition is considerable. Under natural circumstances, some of the guano finds its way into the nearshore
marine environment where it causes nutrient enrichment and consequently may locally enhance marine
phytoplankton production. Bosman & Hockey (1986) have demonstrated nutrient enrichment in intertidal
and nearshore waters in Saldanha Bay. These nutrients are potentially available to enhance primary
production in the waters (Bosman, Du Toit, Hockey & Branch, 1986) and hence ultimately food supply to
benthic and demersal prey in this region. These effects around seabird colonies are probably highly
significant locally, but are not so relative to the large amounts of nutrients in the surrounding upwelled waters
at the scale of the ecosystem.
273
THE USE OF SEABIRDS IN FISHERY MANAGEMENT IN SOUTHERN AFRICA

Information on the interaction between seabirds and their commercially important prey may be used directly
in the assessment of the status of these stocks, or indirectly to test the assumptions on which other estimates
of stock size are based (Berruti, 1987). In the southern Benguela system, the direct use of information from
seabirds has been proposed for the assessment of pilchard stocks. Information from seabirds may be
generally useful for short-lived epipelagic shoaling organisms which show large interannual variations in
biomass (Berruti, 1987).
Estimation (notably VPA) of the size of the pilchard and anchovy stocks depended on catch-based
information (e.g. Armstrong, Shelton, Prosch & Grant, 1983) until direct survey techniques were introduced
(Hampton, Shelton & Armstrong, 1985). Because the use of catch-based information generally is unable to
provide timely warning of fluctuations in recruitment, attention turned to the possible use of seabirds as a catchindependent means of assessing the state of epipelagic fish populations (Newman & Crawford, 1980). Timeseries of guano yields were used by Crawford & Shelton (1978) to demonstrate significant correlations
between guano yields at several localities and catch-based parameters of pilchard abundance, and between
guano yields and catches and catch rates of snoek (a predator of pilchard). Because pilchard was the major
prey of the three guano-producing seabirds (Rand, 1959, 1960a,b), it was assumed that pilchard abundance
controlled guano production and it was suggested that guano harvests could be used as an index of the state
of fish resources. Guano is, however, deposited up to 12 months before collection, and so cannot provide a
timely warning of poor fish recruitment for a recruit-based fishery. Siegfried & Crawford (1978) found
significant correlations between the guano yield and the number of jackass penguin eggs collected at Dassen
Island. Assuming that food supply controlled guano yields, Siegfried & Crawford (1978) suggested that
guano yields may be correlated with environmental factors, so providing a forecast of fish abundance.
Bergh (1986) analysed guano harvests at islands in the Benguela system and Algoa Bay, and suggested that
fluctuations in the pilchard recruitment explained the short-term component in variability of guano harvests.
The guano harvest at Lamberts Bay was proposed as an index of pilchard recruitment. The diet of guanoproducing seabirds at Lamberts Bay has, however, contained very little pilchard in recent years (see
Tables XIIXIV). Furthermore, the three-year lag in correlation between the guano harvests at Lamberts
Bay and Algoa Bay (Bergh, 1986) is not in accordance with evidence that the pilchard migrates from the
west coast to Algoa Bay within the first year of their lives (Armstrong, Berruti & Colclough, 1987b).
Attempts were made to correlate the size of breeding seabird populations with estimates of the abundance
of epipelagic fish stocks. Crawford & Shelton (1981) showed similar changes in seabird numbers and fish
catches or estimates of fish populations. The time-series of population counts were, however, inadequate for
statistical tests and there is doubt about the accuracy of some population estimates (see pages 312315).
Furthermore, estimates of fish biomass by VPA have been criticised (Butterworth, 1983; Armstrong et al.,
1985; Hampton, 1987).
It is necessary to demonstrate whether the parameter of seabird biology measured as an index of fish
abundance, is related to the absolute or relative abundance of the prey. Also, the degree to which this
relationship is affected by the abundance of alternative prey must be determined. There is evidence that the
Cape gannet prefers pilchard (Batchelor & Ross, 1984; Berruti, 1987) and responds to the absolute biomass
of pilchard at low total pilchard biomasses rather than that of alternative prey (Berruti & Colclough, 1987).
The composition of gannet diet was proposed as a measure of the trend in the absolute abundance of
pilchard (Berruti, 1987; Berruti & Colclough, 1987). The contribution of pilchard to gannet diet at Lamberts
Bay and at Malgas Island has increased from 1982 to 1987 (Fig 6) (Berruti, 1987; Berruti & Colclough,
1987), indicating an increase in pilchard biomass.
274
Fig 6.The annual percentage (by mass) of pilchard Sardinops ocellatus in the diet of the Cape gannet Morus capensis
at Lamberts Bay (19781987) and Malgas Island (19791987) (Berruti, 1987, unpubl. data).
The first direct surveys of the biomass of anchovy stocks using acoustics and mid-water trawls became
available in 1984 (Hampton et al., 1985). This technique produced consistent results for anchovy showing a
far larger stock than previously estimated (Hampton, 1987). Its appropriateness for estimating pilchard
biomass has, however, yet to be properly assessed. Pilchard occur in surface layers not sampled by
acoustics (Hampton, Agenbag & Cram, 1979). Acoustic surveys have not always covered the full
distributional range of the pilchard (Hampton et al., 1985; Hampton, 1987; Armstrong et al., 1987b). Given
these problems, the reliability of direct survey of pilchard when this species is at low overall biomasses
needs further validation and it is under these conditions that gannets may provide the most reliable index of
trends in pilchard abundance (Berruti & Colclough, 1987). Current management of pilchard and anchovy
stocks in the southern Benguela relies on estimates of their absolute biomass to establish quotas. It is
doubtful whether absolute estimates can ever be derived from seabird data. Seabird indices will, however,
provide important complementary data if the biomass estimate provided by catch-based or direct survey
techniques have very wide confidence limits or large biases.
SEABIRDS AS BIOLOGICAL SAMPLERS
Seabirds feed mainly during the day, catching prey in the surface layers of the ocean. Therefore, they
provide a means of sampling even the relatively large and mobile fishes such as juvenile snoek (Dudley,
1987) and saury (Berruti, 1988). There is little information on the movements and availability of epipelagic
fishes in the Benguela ecosystem particularly during the day. In particular, nearly all of the estimated 150
000 metric tons of fish eaten by seabirds in the southern Benguela (Duffy et al., 1987b) is caught in the
surface layers during the day, contrary to current perceptions of the spatio-temporal distributions of these
fish species (e.g. Shelton & Hutchings, 1981; Hampton, 1987).
The distribution and movements of fish species in the Benguela ecosystem have mainly been investigated
over long temporal (greater than months) and spatial (greater than hundreds of kilometres) scales (cf.
Crawford, Shannon & Pollock, 1987; Hampton, 1987). Seabird data series have been used to investigate the
regional distribution patterns of pilchard (Armstrong et al., 1987b), snoek (Dudley, 1987), and saury
(Berruti, 1988). The year-round occurrence of anchovy and pilchard as far east as Algoa Bay was
demonstrated by studies of the diet of the Cape gannet by Batchelor (1982) and Batchelor & Ross (1984).
Duffy, Wilson & Berruti (1985) have proposed an alternative hypothesis for the process of anchovy
recruitment based partly on penguin diet data. At shorter time scales, the occurrence of commercially
important fish prey in several studies of the diet of seabirds have produced new information on fish
distribution or have contradicted previously known patterns of occurrence (Duffy et al., 1984a; Walter,
1984; Crawford et al., 1985; Duffy, Wilson & Berruti, 1985; Wilson, 1985a,b; Walter, Cooper & Suter,
1987; Jackson, 1988).
CONCLUSIONS
The Benguela ecosystem is a complex and highly variable ecosystem, and it cannot be assumed that the
processes which operate in the southern Benguela where most seabird research has taken place, are the same
as those operating in the northern Benguela. Man has greatly altered the abundance of many species
275
occupying the upper levels of the trophic web (Crawford, Shannon & Pollock, 1987), but the basic
processes regulating primary productivity do not appear to have been affected.
Man has brought about four major transformations of the Benguela ecosystem, which have affected
seabird populations. Seabirds have not been as severely harvested as other top predators, but have been
indirectly affected (Cooper & Berruti, in press). Initially, breeding seabirds must have been greatly
disturbed by the rush to exploit the accumulated guano deposits in the 1840s. Alterations to the breeding
islands must have been extensive and are not documented. For example, it is suggested that the Cape gannet
colonies at Halifax and Possession islands were founded after gannets were displaced from Ichaboe island
during the initial guano rush (Crawford et al., 1983b). After the initial rush to scrape the accumulated guano,
the islands were subsequently protected to allow annual exploitation of fresh guano deposits (Shaughnessy,
1984). Not one major breeding island has been permanently lost as a potential breeding station and nearly
all are now protected by conservation agencies (Cooper & Berruti, in press).
Man has altered the abundance of fish species available to birds by direct exploitation (Crawford et al.,
1987). This exploitation is known to have affected three seabird species, the Cape gannet, jackass penguin,
and Cape cormorant, which feed mainly on epipelagic shoaling fishes. It is, however, not certain whether
other migrant seabirds preyed on pilchard before the stocks collapsed.
Man has greatly altered the abundance of large cetaceans and predatory fishes such as tuna and snoek,
which are important key species in feeding associations (see page 309). If such associations were an
important source of food to certain species of seabirds, the depletion of such predators may have greatly
reduced food naturally available to seabirds.
Man has, however, made an alternative food supply in the form of trawler offal available to seabirds. The
supply of trawler offal is temporarily and spatially constant, and may have offset depletions of natural food
resources. The change from natural prey to trawler offal would, however, tend to hide any evolutionarily
selected diet differentiation. Adaptations allowing seabirds to feed in association with other predators may
enable seabird species to switch readily to food supplied by trawlers. This applies particularly to the larger
procellariiforms which apparently now obtain nearly all their food from trawlers. Observation of natural
feeding associations and foraging may allow the determination of evolutionarily determined patterns of
feeding.
Seabirds are generally the most mobile of marine consumers. This mobility allows seabirds to overcome
problems of patchy and unpredictable distribution of prey, despite their generally limited penetration of the
water column. The seabird populations of the Benguela form a continuum between the relatively sedentary,
small and scattered populations of breeding species which feed on nearshore prey, and the highly mobile
non-breeding species, which may sometimes occur in vast aggregations. In between these two extremes are
the breeding seabirds which range over much of the neritic zone to feed on the highly abundant epipelagic
fishes of the Benguela system, but which are still tied to a colony when breeding.
Most research on the response of seabirds to variability in the Benguela ecosystem has concentrated on
the response of three or four species of breeding seabirds to changes in the epipelagic fish resources. Thus,
the diet of these species was the basis for the suggestion that many species of seabirds in the Benguela
ecosystem are non-selective or opportunistic feeders (Crawford, 1987). It can be expected that predators
feeding on a single prey type may change to other prey species of similar ecological and morphological
characteristics (Duffy, Siegfried & Jackson, 1987b). The change in the prey species of the bank cormorant
from slow-moving benthic species caught in kelp beds to the pelagic goby caught in the sub-surface area in
open water (Crawford et al., 1985) is more compelling evidence for opportunism. Nevertheless, there are
differences in the foraging of the species feeding on epipelagic shoaling fish. Cape gannets prefer pilchard
to anchovy and hake (Davies, 1956; Batchelor & Ross, 1984; Berruti, 1987; Berruti & Colclough, 1987), but
276
are unable to exploit successfully pelagic goby which is readily available to seabirds which catch prey by
pursuit diving (Crawford et al., 1985). The Cape gannet and swift tern are able to catch saury by plunging,
whereas the seabird species which feed while swimming underwater or on the water surface appear unable
to do so (Berruti, 1988). Even within a feeding guild, the changes in the population sizes of the Cape gannet,
jackass penguin, and Cape cormorant in response to the differential abundance of different prey species
have differed greatly and show that change of prey species does not guarantee continued survival or
evolutionary stability.
The contention that seabirds are opportunistic feeders is also apparently supported by the mixed-species
assemblages feeding at a single food source, trawler offal, where they are separated by body size (Ryan &
Rose, in press). Some species, however, actively avoid trawler assemblages (Ryan & Moloney, 1988) and
the existence of mixed-species assemblages in no way disproves the hypothesis that seabirds show speciesspecific differences in natural foraging behaviour determined by natural selection pressures.
Comparatively little is known of the ecology of other more sedentary breeding seabirds and how these
species have responded to change in the Benguela ecosystem. Even less is known of the non-breeding
seabirds, even common shore-roosting species. The foraging patterns of all seabird species should be
defined at shorter time and distance scales, in relation to the physical and biotic mechanisms which make
food available to seabirds (e.g. Briggs et al., 1984). These changes take place at distances scales of 10107m
and of minutes to months (Schneider & Duffy, 1985; Schneider & Piatt, 1986; Hunt & Schneider, 1987).
Such research must be undertaken if an understanding of the evolutionarily significant processes which
have shaped the present community is to be achieved.
ACKNOWLEDGEMENTS
We thank our colleagues who have read and criticised earlier drafts of this manuscript, particularly
R.J.M.Crawford, R.M.Randall, G.J.B.Ross, and P.G.Ryan. We thank R.J.M.Crawford, R.James, B.Rose,
and P.G. Ryan for unpublished information. The figures were drawn by A.van Dalsen and his assistants.
N.Adams is funded by the South African National Council for Oceanographic Research through the Benguela
Ecology Programme. S. Jackson is the recipient of a doctoral bursary from the South African Council for
Scientific and Industrial Research.
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REVIEW OF RESEARCH RELEVANT TO THE

CONSERVATION OF SHALLOW TROPICAL MARINE
ECOSYSTEMS*
B.G.HATCHER
Marine Biological Laboratory, Zoology Department, The University of Western
Australia, P.O.Box 20, North Beach, W.A., 6020 Australia.
R.E.JOHANNES
CSIRO Marine Laboratories, P.O.Box 1538, Hobart, Tasmania, 7001 Australia.
and
A.I.ROBERTSON
Australian Institute of Marine Sciences, PMB No. 3, Townsville, MC., Qld., 4810
Australia.
ABSTRACT eH re we introduce the recent literature dealing with the assessment, interpretation,
and management of anthropogenic impacts on shallow tropical marine ecosystems. A definitive
treatment in 1975 is used as the starting point for a review of subsequ ent extensive research
conducted into these topics. A table of comparisons between tropical and temperate ecosystems
is updated and discussed in terms of its implications for tropical conservation practice. The major
ecosystems of the shallow marine tropics are treated separately. Coral reefs receive the most
attention; more a reflection of their attractiveness to scientists perhaps, than of the extent of their
degradation relative to mangrove or seagrass ecosystems. oD cument ation of the degradation of
these ecosystems has improved greatly over the past decade. U nderstanding of the mechanisms
of impact and interactions between effects, ecosystems and their components is increasing
incrementally. Research into the prediction and control of man s interaction with the marine
environments of the tropics has, however, done little to slow the seemingly inexorable acceleration
of their degradation.
INTRODUCTION
In a recent review Janzen (1986) states that time is rapidly running out for the terrestrial ecosystems of the
tropics. At the present rate of degradation, there will be little of the natural environment remaining for
scientists to study ten years from now. By citing none of the extensive literature concerning terrestrial
ecology and management in the tropics, Janzen (1986) underlines the possibility that the scientific method
will not avert tragedy.
CONSERVATION OF TROPICAL MARINE ECOSYSTEMS
285
Can the same conclusions be drawn about the future of tropical marine ecosystems?
Over the last decade a rapid increase in obvious examples of the degradation of tropical marine
communities and environments has led many scientists to sound alarms (e.g. Antonius, 1977; Wood, 1977;
Salvat, 1978; Bennell, 1979; Linden & Jernelov, 1980; McManus, 1980; Rodriquez, 1981; Falanruw, 1982;
Pathmarajah, 1982; Schroeder, 1982; Stoddart, 1982; Poli et al., 1983; Salm, 1983; Dahl, 1985a; De Silva,
1985; Endean & Cameron, 1985; Muzik, 1985; Rogers, 1985; Wells, 1986). The vastness and relative
inaccessibility of many tropical marine ecosystems has served to attenuate the impact of human activities,
including scientific research. Evidence for increases in the frequency and intensity of anthropogenic damage
to tropical marine ecosystems is confounded by concurrent increases in knowledge of those effects.
Assessment of the urgency of conservation problems is further complicated by our profound ignorance of
the basic principles of operation applying to the complex ecological systems which characterise the marine
tropics. Our knowledge of many tropical marine communities will always be inadequate for complete
understanding (Bradbury & Reichelt, 1982; Bradbury, Reichelt & Green, 1985). Some of the best
documented cases of major alterations in tropical marine communities, such as the Crown-of-Thorns
outbreaks on coral reefs (Endean, 1977; reviewed by Moran, 1986), or massive mortalities of benthic
organisms (Mitchell & Ducklow, 1976; Gladfelter, 1982; Lamberts, 1983; Lessios, Glynn & Robertson,
1983; Oliver, 1985; Brown, 1987a; Williams, Goenaga & Vicente, 1987; Carpenter, 1988) cannot yet be
adequately explained in terms of anthropogenic or natural causes (Brown, in press; Dahl & Salvat, in press).
Although no rigorous balance sheet of degradation rate relative to documentation rate exists, there has
been enough damage in well-monitored areas of the shallow marine tropics over the past decade to
demonstrate that environmental destruction due to pollution and over-exploitation is proceeding at an
accelerating rate. The degradation in the Philippines, Southeast Asia, Oceania, and parts of Africa has
increased markedly since monitoring began (e.g. Dahl & Baumgart, 1983; UNEP, 1984c, 1985g,h; Dahl,
1987; Gomez, 1988). In southeast India virtually the entire reef in the area of Mandapam Camp has been
literally carted away to provide construction materials, and similar things are happening on the east coast of
Malaysia. Siltation problems due to deforestation and agriculture are increasing in many areas. Dynamite
fishing has caused widespread damage to the coral reefs of the Phillipines. There has been a precipitous
decline in mangrove forest area in a number of Caribbean and Indo-Pacific countries in recent decades.
Certainly more cases of degradation are coming to light because of increasing research; but extreme
examples are becoming much easier to find.
We suggest that the scenario projected by Janzen (1986) for the terrestrial systems of the tropics also
applies to tropical marine ecosystems, but that the time scale of the processes of destruction on a global
scale is somewhat longer. This does not justify complacency. If they are to remain employed, scientists
studying the marine ecosystems of the tropics must take a more active role in contributing to the
formulation of conservation policy. But perhaps they have the luxury of not being faced with the need for
immediate radicalisation. We believe that it is not too late for a traditional review of the scientific literature
to contribute usefully to the conservation of the marine tropics.
Rather than attempting to provide a comprehensive review of research relevant to conservation in tropical
waters, we focus on those aspects for which temperate zone experience offers little guidance. To keep the
references within bounds we refer, where possible, to reviews rather than original research papers. Coral
reefs receive the bulk of our attention. This is a reflection of the concentration of human usage of and
knowledge about reef ecosystems, but not of their abundance, which is relatively small on an areal basis
* Contribution No. 75 from University of Western Australias Marine Biological Laboratory; Contribution No. 480 from
the Australian Institute of Marine Science.
286
(Smith, 1978). Little reference will be made to unvegetated soft-bottom communities; although they are
ubiquitous in the tropics, research on them lags far behind that on coral reef, mangrove, and seagrass
communities.
The marine climate and the inapplicability of single-species models to the complex communities of the
tropical ocean mean that their resources must often be conserved in the context of the ecosystems in which
they are embedded (e.g. Ray, 1976, 1986; Bright, Jaap & Cashman, 1981; Salm & Clark, 1984). For this
reason we have subdivided the review on the basis of the major types of tropical marine ecosystems. The
format is not meant to imply independence of ecological processes or methods of conservation. Much of the
extensive research on human impacts and management in coral reefs is relevant to other tropical marine
ecosystems. Hydrodynamic and trophic fluxes connect all of the marine and coastal ecosystems of the
tropics to varying degrees (Ogden & Gladfelter, 1983; Birkeland, 1985), a fact of great relevance to the
study and management of tropical marine resources.
THE LITERATURE
Since the major treatment of tropical marine pollution by Wood & Johannes (1975) there has been an
explosion of published research on both the ecological and management aspects of the topic which is
relevant to conservation. Much of it is reported in the proceedings of multidisciplinary symposia and
conferences organised on the theme of the coral reef ecosystem (e.g. Taylor, 1977; Gomez et al., 1982;
Baker, Carter, Sammarco & Stark, 1983; Reaka, 1983, 1985; Delesalle et al., 1985; Jokiel, Richmond &
Rogers, 1986; Devaney, Reese, Burch & Helfrich, 1987; Choat et al., in press) and, occasionally, other
ecosystems (e.g. mangals: Soepadmo, Rao & Macintosh, 1984; Field & Dartnall, 1987), resources (e.g. reef
fisheries: Pauly & Murphy, 1982) and their management (e.g. Anonymous, 1985a,b). Particularly
encouraging are those workshops which focus on interactions between ecosystems of the tropics (e.g.
Ogden & Gladfelter, 1983; UNESCO, 1984; Birkeland, 1985, 1987a).
This broad-based literature is augmented by a number of books which provide overviews of tropical
marine ecosystems or communities, and often include chapters on anthropogenic effects and management
(e.g. Cronin, 1975; Golley & Medina, 1975; Chapman, 1976, 1977; McRoy & Helfferich, 1977; Livingston,
1979; Phillips & McRoy, 1980; Clough, 1982; Kennedy, 1982; Barnes, 1983; Long & Mason, 1983; Mann,
1983; Por & Dor, 1984; Teas, 1984; Ward & Saenger, 1984; Ruddle & Johannes, 1985; Hutchings &
Saenger, 1987; Longhurst & Pauly, 1987; Dubinsky, in press).
The literature dealing with the application of ecological knowledge to conservation practice in the marine
tropics is strongly supported by international organisations monographs and edited reference works,
symposia and workshops. These include methodological texts and management manuals (e.g. Stoddart &
Johannes, 1978; Dahl, 1981a; Huntsman, Nicholson & Fox, 1982; Saenger, Hegerl & Davie, 1983;
Geoghegan, Jackson, Putney & Renard, 1984; Kenchington & Hudson, 1984; Salm & Clark, 1984; Snedaker
& Snedaker, 1984), tropical marine resource inventories published by the IUCN Conservation Monitoring
Centre (e.g. Crossland, 1986; Dahl, 1987; UNEP-IUCN, 1988), and local, specific case studies in the UNEP
Regional Seas Reports and Studies Series (e.g. Pathmarajah, 1982; UNEP, 1982, 1984a,b,c,
1985a,b,c,d,e,f,g,h; Dahl & Baumgart, 1983; Eldredge, 1987a), and in the UNESCO Reports in Marine
Science (e.g. UNESCO, 1981a,b, 1983; Ogden & Gladfelter, 1983, 1986). These organisations have also
published in the wider field of conservation science (e.g. IUCN, 1976, 1980; UNESCO-UNEP, 1984);
which is also addressed in several books (e.g. Soule & Wilcox, 1980; Soule, 1986; Chia, Soysa, Lockwood
& Collier, in press), and topical compendia concerning pollution management and conservation aspects
(e.g. Johnson, 1976; Librero & Collier, 1977; Chua & Mathias, 1978; Barrett & Rosenberg, 1981; Morauta,
287
Pernetta & Heaney, 1982; Cairns & Buikema, 1984; Chua & Charles, 1984; Lai & Feng, 1984; Brown,
1986; Salvat, 1987a).
Reviews of the literature dealing with the ecology of coral reef organisms and communities, and their
responses to stress and perturbation, are abundant. Coral growth was reviewed by Buddemeier & Kinzie
(1976) and more recently by Gladfelter (1985). Davies & Montaggioni (1985) review reef growth in the
geological context, and Hutchings (1986) reviews reef destruction through bioerosion. The diversity of reef
corals has most recently been reviewed by Huston (1985); Lewiss (1977) review of production processes
on reefs has been updated by Kinseys (1985). Sale (1980) considered the ecology of coral reef fish
communities, and Russ (1984) and Munro & Williams (1985) have focused on their fisheries. The recovery
of reef corals after major disturbance was reviewed by Pearson (1981), and Highsmith (1982) considered an
important aspect of such recovery: reproduction by fragmentation. The phenomenon of Acanthaster
population fluctuations, and their effects on reef communities was reviewed by Moran (1986). Antonius
(1982) reviewed the pathology of reef corals.
Literature documenting the effects of human activities on coral reef ecosystems has also received
considerable attention in reviews. Johannes (1975) considered most forms of anthropogenic degradation of
reef communities, and several chapters in Salvat (1987a) provide updates. Other authors have focused on
specific impacts, usually in terms of their effects on corals or coral-dominated communities (e.g. oil: Loya &
Rinkevich, 1980; Knap et al., 1983; heavy metals: Howard & Brown, 1984; drilling muds: Dodge &
Szmant-Froelich, 1985; sewage: Pastorok & Bilyard, 1985). Brown & Howard (1985) provide a recent
review of literature based on laboratory and field studies of the effects of both natural and human-induced
stress on reef corals. Glynn (1982) considered the response of coral community structure to man-made links
between the Atlantic and Pacific oceans.
Reviews dealing with the ecology or deterioration of other tropical marine ecosystems are scarce in
comparison. Lugo & Snedaker (1974) and Walsh (1974) reviewed the published information on mangroves.
Rollet (1981) provides a bibliography of research to 1975. Saenger et al. (1983) reviewed the global status
of mangrove ecosystems. Hamilton & Snedaker (1984) edited an excellent volume on mangrove uses and
management. Recent reviews of mans impact on southeast Asian and Pacific mangrove ecosystems have
been made in a series of publications (UNDP-UNESCO, 1986a,b, 1987a,b,c; Field & Dartnall, 1987). We
could not find a comprehensive review of research or conservation of tropical seagrass communities.
Polunin (1983) provides an excellent example of a review which is useful to ecologists and managers
alike in his documentation of the marine resources of Indonesia. Byrne (1979) undertook a similar task for
the island ecosystems of the tropical Pacific, as did Chua & Charles (1984) for the east coast of Malaysia. Dahl
(1987) provides a comprehensive review of the natural resources and human activities on an island-byisland basis for Oceania, and Eldredge (1987a) has compiled a bibliography of information on Pacific island
ecosystems.
Management and conservation theory and practice in the marine tropics have received little attention in
the form of literature reviews. Lewis (1976) provides useful insights from other fields of research in his
review of long-term ecological monitoring of shallow marine communities. Johannes (1978a) surveyed the
literature on traditional marine conservation methods in Oceania, Dahl (1985b) reviewed similar topics for
New Caledonia, while Grigg (1979) compiled published information on issues and problems of managing
coral reef ecosystems on the Pacific Islands. Munro & Williams (1985) have reviewed the literature
relevant to the assessment and management of coral reef fisheries. A recent book produced by the US
Congress, Office of Technology Assessment (Anonymous, 1987) for resource management on islands
under US jurisdiction in the Caribbean and tropical Pacific, devotes considerable space to coastal marine
resources.
288
In the present review we build on those which preceeded it, and consider recent sources of information
which may provide fresh insight into the conservation of tropical marine ecosystems.
THE DISTINCTIVENESS OF SHALLOW TROPICAL MARINE ECOSYSTEMS
Tropical shallow water communities are subject to many of the same anthropogenic stresses as communities
at higher latitudes. But the relative importance of these stresses differs. Excessive nearshore sedimentation
due to bad land management, for example, is a bigger problem in the tropics, whereas industrial pollution is
more widespread in the temperate zone. In addition, the unique structures and functions of some tropical
marine communities result in different responses to a given stress. For example, the aerial roots of
mangrove trees render them sensitive to certain stresses which have comparatively little impact on saltmarsh grasses, their closest ecological counterparts at higher latitudes (Chapman, 1977).
Man also uses tropical marine resources in a number of distinctive ways, which often dictate methods of
resource management differing from those developed for temperate marine resources. For example,
tropical, low technology fishing involves methods and customary resource use patterns very different from
those of industrial fisheries (Johannes, 1978a). This creates some unique problems for tropical fisheries
managers (e.g. Haines, 1982; Munro & Smith, 1984). Ways in which tropical marine ecosystems and
organisms differ from their temperate zone counterparts were summarised by Johannes & Betzer (1975) and
are updated here in Table I. A number of inferences concerning the impacts of stress in tropical waters can
be drawn from this Table. Unfortunately few of them have been adequately tested.
The release of heated wastewater has the potential to be more stressful in the tropics because many
tropical marine organisms live at environmental temperatures closer to their upper thermal limits than
organisms at higher latitudes (Moore, 1972; Vernberg, 1981). Temperature increases of only a few degrees
(often associated with El Nio events) have been implicated in widespread mortalities of reef corals (e.g.
Fankboner & Reid, 1981; Faure et al., 1984; Glynn, 1984; Suharsono & Kiswara, 1984; Burns, 1985;
Harriot, 1985).
It is less widely recognised that tropical organisms must also live closer to their lower oxygen limits. Not
only are metabolic rates generally higher, but dissolved oxygen concentrations are lower; sea water
saturated with air contains 35% less oxygen at 30C than at 8C. Thus, any environmental perturbation
which lowers the oxygen concentration (such as thermal pollution or increased biological oxygen demand)
should exert a greater effect on tropical biota. For example, Fitzhardinge & Tyler (in press) document coral
mortality as a result of accumulations of macroalgal detritus around patch reefs, and nominate oxygen
depletion by decomposition processes as the causative agent. Mass mortalities of marine organisms due to
thermal and pollution-induced hypoxia is becoming a significant problem in the Gulf of Mexico (Renaud,
1985).
Kinsey (1973, pers. comm.) has shown that the respiratory requirement for oxygen in a natural coral reef
community was just balanced at night by available oxygen. Thus, further reduction in oxygen (brought about
by an
TABLE I
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Ways in which shallow tropical marine ecosystems differ from their temperate counterparts at comparable depths.
References are not intended to be exhaustive
PHYSICAL AND CHEMICAL CHARACTERISTICS
Temperature
Higher mean: by definition (see text). Much lower annual range

(Sverdrup, Johnson & Fleming, 1942). Thermal maximum closer to
ambient temperature (Mayer, 1914).
Light
Higher total received annually: (Stehli, 1968). Lower annual range of
input (Sverdrup et al., 1942). Lower annual range in day length
(MacArthur, 1972).
Dissolved oxygen
Lower: (Riley & Chester, 1971).
Total dissolved carbon dioxide
Lower: (Revelle & Fairbridge, 1957).
Dissolved phosphorus and fixed nitrogen
Lower: (Sverdrup et al., 1942).
Water clarity
Higher: (Jerlov, 1968), except in many mangrove communities (Wilber,
1971) and estuaries.
Rainfall (and consequently coastal run-off) More variable seasonally: (MacArthur, 1972).
Tides
Sediments
Seasons
Incidence of storms (cyclones, hurricanes, typhoons)

COMMUNITY STRUCTURE
Species diversity
Diversity within genera

Mean size
Biomass
Distribution
Population density of individual species
Lower mean amplitude, although small increase near Equator

(Moore, 1972).
Calcareous sediments, more characteristic of tropical waters,
have lower adsorption capacities than clay sediments: (e.g.
Segar & Pellenbarg, 1973).
Typically two monsoonal or trade wind seasons rather than
four, distinguished more on the basis of wind, rainfall, and
current patterns than temperature.
Greater: (Nieuwolt, 1977).
Higher: benthic macrophytes (Gessner, 1970); benthic
invertebrates (Sanders, 1968; Stehli, 1968; Bakus, 1969;
Wade, 1972; Grassle, 1973; Golikov & Scarlatto, 1973; Abele,
1974; but see Dexter, 1972); fishes (Lindsey, 1966; Goldman
& Talbot, 1973); phytoplankton (Wood, 1965).
Higher: (Kohn, 1971).
Smaller: benthic invertebrates (although broader size range in
some taxa) (Bakus, 1969; Moore, 1972; Goreau, 1966); fishes
(although most really large species are tropical) (Lindsey,
1966); zooplankton (Bogorov, 1960; Russell, 1934; Heinrich,
1962a) ; benthic macrophytes (Bakus, 1969) ; phytoplankton
(Odum, Beyers & Armstrong, 1963; Tundisi, 1971).
Lower: zooplankton (Bogorov, 1960; Heinrich, 1962b);
benthic macrophytes (Bakus, 1969); phytoplankton (Hulburt,
1966); benthic invertebrates (Wade, 1972). Similar: fish
(Goldman & Talbot, 1973).
Patchier: benthic invertebrates (Bakus, 1969; Golikov &
Scarlatto, 1973; Grassle, 1973).
Lower: benthic invertebrates (Bakus, 1969; Golikov &
Scarlatto, 1973); phytoplankton (Ryther, 1963). Less seasonal
variation, zooplankton (Russell, 1934; Heinrich, 1962a).
290
Population size
Predators
Colonial life forms

Zooplankton/phytoplankton ratio
Abundance of herbivorous fishes
Eggs
Larvae
Meristic counts
Benthic macrophyte taxa
Phytoplankton taxa
Zooplankton taxa
Lipids
Chromosome number Hirota, 1973).
External anatomy
Colour polymorphism
Genetic variability
BIOLOGICAL FUNCTIONS
Metabolic rates
Gross primary productivity
Growth rates
Thermal tolerance
Frequency of reproduction
Reproduction potential
Breeding seasons
Smaller: (Grassle, 1973).

Higher percentage: zooplankton (Heinrich, 1962a,b); softbottom benthos (Day, 1963); fishes (Goldman & Talbot,
1973).
Greater incidence.
Greater: (Russell, 1934; Rutman & Fishelson, 1969).
Greater: (Bakus, 1969).
Smaller, less yolk: benthic invertebrates (Thorson, 1950;
Mileikovsky, 1972); fishes, demersal (Thresher, in press).
Higher percentage planktonic: benthic invertebrates (Thorson,
1950; Giese, 1959; Mileikovsky, 1971); fishes (Sale, 1980).
Generally lower: fishes (Barlow, 1961; Garside, 1970;
Lindsey, 1975).
Greater proportion of chlorophytes and rhodophytes:
(Feldman, 1938; Bakus, 1969; Gessner, 1970).
Greater proportion of flagellates: (Hulburt, 1966).
Greater proportion of copepods?: (Russell, 1934).
Lower concentrations: plankton (Wimpenny, 1941; Lee &
Lower: fishes (Nikolsky & Vesilev, 1973).
More adaptions for predation defence: gastropods and
bivalves (Vermeij, 1974, 1978).
More conspicuous: (Grassle, 1973).
Higher: (Cameron, 1977).
Higher at ambient temperatures (Vernberg, 1962): benthic
invertebrates (Scholander, Flagg, Walters & Irving, 1953);
fishes (Wohlschlag, 1964); zooplankton (Ikeda, 1970);
phytoplankton (Eppley, 1972); benthic macrophytes
(Gessner, 1970).
Higher: coral reefs (Bunt, 1975; Kinsey, 1982); mangroves
(Bunt, 1975); seagrass communities (Larkum, 1981). Lower:
phytoplankton (except in regions of upwelling) (KoblentzMischke et al., 1970).
Higher: fishes (Pauly, 1984but see Edwards, 1984, for
dissenting view); phytoplankton (Sheldon, 1984); bivalves
(Parulekar, 1984).
Smaller range: fishes (Bakus, 1969; Brett, 1970); molluscs
(Moore, 1972).
Greater: fishes (Nikolsky, 1970).
Higher: invertebrates (Valentine & Ayala, 1978).
Longer: fishes (Dutt, 1969; Munro, Gaut, Thompson &
Reeson, 1973); zooplankton (Heinrich, 1962a). Those of
different species spread more evenly through the year:
zoobenthos (Moore, 1972); fishes (Qasim, 1955; Goodbody,
Asexual reproduction
Larval development
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1962; Munro et al., 1973); zooplankton (Heinrich, 1962a).

Unrelated to temperature: fishes (Johannes, 1978b).
Higher incidence: invertebrates (Grassle, 1973).
Faster: fishes (Delsman, 1926; Blaxter, 1969); zooplankton
(Heinrich, 1962a).
Slower: benthic invertebrates (Thorson, 1950, 1961).

Feeding habits
More specialised: fishes (Bakus, 1969); gastropods (Kohn,

1971).
Natural mortality rate
Higher: fishes (Pauly, 1979b, 1980; Pauly & Ingles, 1982).
Niche width
Smaller: (Bakus, 1969; Sanders, 1968; MacArthur, 1972).
Larvae
Higher percentage with specialised pelagic stage: fishes
(Gosline, 1971); invertebrates (Giese, 1959).
Lower oxygen limit
Closer to ambient levels: (Johannes & Betzer, 1975).
Toxicity
Greater incidence: fishes (Halstead, 1965); invertebrates
(Halstead, 1965; Bakus & Green, 1974).
Venom
Greater incidence: (Halstead, 1965).
Symbiosis and parasitism
Greater incidence: (Grassle, 1973).
Life span
Shorter: fishes (Gunter, 1957; Munro, 1975); bivalves
(Parulekar, 1984).
Degree of calcification of skeletons and invertebrates Greater: (Vermeij, 1978).
Gaping of bivalve shells
Reduced: (Vermeij & Veil, 1978).
Nutritional value of seagrasses
Lower: (Drew, 1980).
Endemism
Lower: algae (Womersley, 1959; van den Hoek, 1984).
Higher: invertebrates (Bakus, 1969).
Hermaphroditism
Greater incidence: fishes (Robertson & Choat, 1974).
Much greater: (Revelle & Fairbridge, 1957).
Biological precipitation of CaCO3
Higher: (Stehli, Douglas & Newell, 1969; Stehli & Wells,
Rates of evolution
1971).
experimental reduction in water circulation and gas exchange across the water surface) caused virtually
total destruction, by asphyxiation of all fish and crustaceans in one and a half tidal cycles. No one seems to
have examined further the possibility that oxygen may be an important limiting factor in tropical
communities in which water circulation is restricted.
Because solid and liquid pollutants are more soluble and metabolic rates are faster at higher temperatures,
rates of biological uptake of pollutants are likely to be higher in warm tropical waters but so, also, are rates
of excretion and biological and physico-chemical degradation (Johannes & Betzer, 1975). Information on
the relative effects of common pollutants in tropical systems is scarce. The few documented cases where
pollution has produced no significant degradation of corals in reef communities (reviewed by Brown &
Howard, 1985) involve sedimentation associated with extractive activities, and do not allow comparison
with examples in the temperate zone.
The results of experimental studies do little to foster generalisations about the impact of pollutants in the
marine tropics. For example, Marsh, Pendleton, Wilkins & Hillmann-Kitalong (1985) examined the effects
of dissolved sulphur dioxide from a power station scrubber on a variety of marine organisms. Responses in
terms of mortality or reduced growth varied with species from insignificant to moderate, a common finding
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in studies of toxic effects in temperate communities. At present there are insufficient comparative data on
the metabolism and toxicity of most pollutants to draw useful conclusions about their consequences in
tropical versus temperate marine ecosystems (Table I).
Incident ultraviolet radiation increases with decreasing latitude. It has been found recently that UV
radiation is harmful to many shallow marine organisms even at subtropical latitudes (e.g. Jokiel, 1980;
Jokiel & York, 1982, 1984; Wood, 1987). The deleterious environmental effects of reductions in the
atmospheric ozone layer would thus apparently not be limited to the terrestrial environment.
Dissolved nutrient concentrations are usually much lower in tropical surface waters than in temperate
waters. The elevation of phosphate concentrations by 0.75 M in New England waters, for example, would
result on the average, in doubling of phosphate concentration, whereas in the eastern Caribbean it would
constitute an approximately 40-fold increase. The implications of this for tropical community structure and
function are not clear, but the possibility exists that the impact of a given increase in nutrient concentrations
on a nutrient-poor tropical marine community might be much greater than that on a typical temperate
marine community. Birkeland (1987a) postulates that the pattern of nutrient availability is a major
determinant of large scale differences in benthic community structure in the coastal environments of the
tropics. Nutrient loading of tropical lagoons from sewage discharges favours primary productivity in the
water column, often resulting in eutrophication of water bodies having restricted exchange circulation. This
produces both direct and indirect effects on biota which may lead to major alterations in community
structure and function (reviewed by Pastorok & Bilyard, 1985).
Such effects, however, are not inevitable. Kimmerer & Walsh (1981) and Le Gall & Fesquet (1985)
found that inputs of organic waste to partially enclosed coral reef lagoons had no measurable influence on
nutrient dynamics. Tomascik & Sander (1985) found that coral growth rates varied in a non-linear fashion
along a gradient of eutrophication towards an island in the Caribbean: increasing to a threshold, then
decreasing at higher levels of pollution. Again, the comparative studies required to ascertain the relative
susceptibility of tropical marine ecosystems to eutrophication are lacking.
The diversity of edible fishes and invertebrates is much higher in the tropics than at higher latitudes, and
no one or few species dominate the catch. This is just one of the reasons why tropical nearshore fisheries
present the most complex fisheries management problems in the world (Pauly, 1979a; Munro, 1982; Munro
& Smith, 1984; Usher, 1984). A large proportion of tropical organisms have an extended pelagic stage in
their life histories. Consequently, the maintenance of their populations depends to a large degree on the
survival of larval organisms in the oceanic environment independent of their adult, benthic or epibenthic
habitats. Alterations to the circulation patterns or quality of this water, whether associated with changes in
the adult habitat or not, may have profound effects on recruitment, and hence on the resulting adult
populations (e.g. Scheltema, 1986; Tegner, 1986; reviewed for coral reef fish in Munro & Williams, 1985;
Parrish, 1987).
In recent years the notion that tropical marine communities exist in temporally stable, physically benign
environments has lost favour, and is being supplanted by a quite different picture. Lugo (1980), for example,
states that the natural periodic stresses to which mangrove communities are subject (large temperature and
salinity excursions, storm-generated winds and waves, and excessive sedimentation) are often sufficient to
slow down, set back, or reverse succession, or actually destroy portions of the mangal. Cyclical mortality
and expansion of mangroves in response to natural periodic disturbances appears to be a common
occurrence, especially along arid coastlines (Cintron, Lugo, Pooland & Morris, 1978).
Similar natural, periodic perturbations have repeatedly been shown to exert strong controls on the
structure of coral reef communities (e.g. Smith, 1975; Glynn, 1976; Woodley et al., 1981; Dollar, 1982;
Walker, Roberts, Rouse & Huh, 1982; Walsh, 1983; Eldredge & Kropp, 1985), as well as other shallow
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tropical marine areas (e.g. Bortone, 1976; Salomon & Naughton, 1977; Ogg & Koslow, 1978; Birch &
Birch, 1984; Burch, Burch & Thorsson, 1985). When natural stresses are intense and/or frequent, the
affected communities may be hypersensitive to additional stresses imposed by mans activities. For this and
other reasons Moore (1972) and Johannes & Betzer (1975) have suggested that shallow tropical marine
communities may be less resistant to anthropogenic stresses than those in shallow temperate waters.
Alternatively, it has been argued that frequent disturbances allow adaptation to occur at both the organism
and community level (e.g. a community dominated by opportunists), resulting in a higher degree of
resistance to additional stress (e.g. Holling, 1978). At present there is insufficient information to resolve the
issue (Dahl & Salvat, in press). It is that the form of the stress is at least as important as the intensity or
frequency in both temperate and tropical ecosystems (Brown & Howard, 1985; Rapport, Regier &
Hutchinson, 1985).
CORAL REEFS
For the purposes of this review, coral reefs are defined as carbonate structures at or near sea level which
support viable populations of scleractinian corals, although this definition is by no means universal
(Preobrozhensky, 1977). Confined (with few exceptions) between 30N and 30S of the Equator, coral reef
ecosystems are arguably the oldest, and certainly the most diverse and complex ecosystems on earth.
Their complexity is manifest on all conceptual dimensions: geological history, growth, and structure (e.g.
Adey, 1978; Hopley, 1982; reviewed by Davies & Montaggioni, 1985), biological adaptation, evolution,
and biogeography (e.g. Shaklee, Tamaru & Waples, 1982; Kohn, 1983; Jackson & Hughes, 1985),
community structure (e.g. Connell, 1978; Rosen, 1981; reviewed by Huston, 1985), organism and ecosystem
metabolism (reviewed by Gladfelter, 1985; Kinsey, 1985), physical regimes (e.g. Roberts, Murray &
Suhayda, 1975; Pickard, 1983; Dustan, 1985), and anthropogenic interactions (e.g. Johannes, 1982;
Chesher, 1985; Conte, 1985).
The challenge of comprehending this complexity has attracted a great deal of scientific attention during
the last 15 years as geologists, ecologists, and anthropologists develop and test paradigms in this, the
ultimate ecosystem. These efforts have demonstrated in a most convincing fashion the inadequacy of
current scientific theory and expertise to provide prediction and control in these ecosystems (Bradbury &
Reichelt, 1982; Bradbury, Hammond, Reichelt & Young, 1984) in the face of rapidly escalating human
pressure (Salvat, 1978; Gomez, 1982/83, 1988; Wells, 1986).
FUNDAMENTAL RESEARCH
While descriptions of pattern play a major role in coral reef science (e.g. Battistini et al., 1975; Done, 1982;
Rogers, Gilnak & Fitz, 1983; White & Porter, 1985), particularly as applied to conservation and
management (Dahl, 1981a; Kelleher, 1982; Venkataramanujam, Santhanam & Sukumaran, 1982; Maragos
& Elliot, 1985), it is the elucidation of processes controlling structure and pattern in reef communities, and
the quantification of ecosystem function which have developed markedly. Here we attempt to summarise
those aspects of coral reef research which relate indirectly through theoretical paradigms and explanatory
models, or directly by design, to conservation issues.
The growth of reefs in terms of net accretion is a fundamental process controlling their ability to rebuild
themselves after destructive events, and determining the time scales at which they must be managed for
conservation purposes. The upper and lower limits of Holocene growth rates have been established, and
locally applicable mean values identified (reviewed by Davies & Montaggioni, 1985). The major control on
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vertical reef growth rate is variation in sea level relative to the reef top during the Holocene transgression
(Chappell, 1983; Davies, Marshall & Hopley, 1985).
The perceived discrepancy between the growth of reefs in the Atlantic versus the Pacific Oceans can be
resolved upon consideration of relative sea-level history, and spatial scales of examination (Kinsey, 1982).
Vertical growth rate and reef morphology change markedly as the reef top approaches sea level; factors
which have significant influence on productivity (e.g. Adey & Steneck, 1985) and implications for
conservation. For example, the submerged bank barrier reefs of the eastern Caribbean are less susceptible to
many of the common human impacts on reefs because of their depth below the sea surface and consequent
isolation (Bright, Jaap & Cashman, 1981).
Studies of reef growth continue in terms of coral growth and calcification (reviewed by Buddemeier &
Kinzie, 1976; Gladfelter, 1985), sedimentation and infilling (e.g. Shinn et al., 1982; Ginsburg, 1983), while
attention has recently been directed to bioerosion as it influences net accretion rates (e.g. Scoffin et al.,
1980; Kiene, 1985; Hutchings, 1986). These studies demonstrate that turnover times for corals and coral
communities span years to decades, while those of whole reefs are of the order of tens of thousands of years
(Hatcher, Imberger & Smith, 1987). Of particular interest are the recent findings concerning the relative
youth of the Great Barrier Reef (Symonds & Davies, 1985), and controls on the latitudinal limits of coral
reef development (Grigg, 1982), which are probably more complex than simple temperature effects
(Johannes et al., 1983b).
Much effort has been made in the last five years to identify determinants of reef community structure.
Structure is usually defined in the rather narrow terms of local species diversity, or distribution and
abundance, as ecologists grapple with the bewildering array of reef organisms. In most instances taxonomic
groupings of corals or fish are studied with a view to testing hypotheses (usually developed in simpler
systems) which explain observed patterns within and between habitats in terms of ecological succession,
resource partitioning, competition, predation, and the intensity and frequency of disturbance. There is a
massive literature on these topics, and no comprehensive review or synthesis has been undertaken. The
underlying paradigms have historical basis in stability-complexity theory developed in population dynamics
(e.g. Goodman, 1975) and a more recent basis in succession and disturbance theory (e.g. Connell & Slatyer,
1977).
The original model of the coral reef as the ultimate expression of stability, physical constancy, and
biological accommodation has received a severe battering from ecologists working on algal, coral, and
demersal reef fish communities. This resulted in a polarisation of viewpoints along two conceptual axes.
The bases of controversy lie in: (1) the relative importance of pre- and post-recruitment processes in
controlling the populations of reef organisms along dimensions of distribution and abundance, and (2) in the
degree to which biotic interactions (as opposed to physical controls and disturbance regimes) structure
biological communities along a diversity dimension. Introductory discussions of these concepts as they
pertain to reef communities can be found in Bradbury (1977), Cameron (1977), Sale (1977), Connell (1978)
and Richards & Kindeman (1987).
One set of models suggests that the community patterns observed on reefs are the result of the order and
densities in which organisms reach the benthos from an unpredictable planktonic milieu (e.g. Sale &
Williams, 1982). Another set assumes there is a relatively consistent supply of recruits to the benthos, and
that the patterns observed result from the interaction between competitive processes which drive the
community towards a climax state and disturbance factors which interfere with this succession (e.g.
Connell, 1983).
Fortunately, current views transcend these pseudo-dichotomies. It is now generally accepted that in
complex ecosystems (such as coral reefs) both of these processes are likely to operate contemporaneously at
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different spatial scales, and contiguously at different temporal scales. The challenge now for reef ecologists
is to combine assessments of the relative importance of various processes at a given set of time and space
scales into heuristic models which acknowledge interactions between scales (e.g. Bradbury, 1977; Reichelt,
Green & Bradbury, 1983; Hatcher et al., 1987).
These essentially theoretical deliberations have yet to prove of great practical value to resource
managers. They have, however, changed the way scientists perceive reef systems. For example, we now
recognise the importance of pelagic life stages and recruitment-controlling processes in the population and
community dynamics of fish (reviewed by Sale, 1980; Munro & Williams, 1985; Richards & Kindeman,
1987) and corals (e.g. Birkeland, Rowley & Randall, 1982; Rogers et al., 1984; Wallace, 1985). The recent
discovery that the majority of corals reproduce by releasing gametes into the water column and thence
produce small, long-lived larvae (Harrison et al., 1984; Babcock et al., 1986) re-emphasises the need for
research on physical processes affecting the transport and dispersion of planktonic stages (e.g. Johannes,
1978b; Lobel & Robinson, 1983; Navaluna & Pauly, 1984; Williams, Wolanski & Andrews, 1984; Oliver &
Willis, 1987).
There is an increased appreciation of the role of local disturbance regimes (e.g. Bradbury & Young,
1981; Dollar, 1982; Porter, Battey & Smith, 1982; Connell, 1983; Hixon, 1983; Walsh, 1983), as well as
major natural disasters and catastrophes in the control of coral reef community structure. The catastrophes
include anomalous sea-level fluctuations (e.g. Yamaguchi, 1975; Loya, 1976), large temperature and
salinity excursions (e.g. Walker et al., 1982; Bohnsack, 1983; Glynn, 1984, 1985; Burns, 1985; Holthus,
Evans & Maragos, 1986), volcanic eruptions (e.g. Grigg & Maragos, 1974; Eldredge & Kropp, 1985) and,
most extensively, storms (e.g. Randall & Eldredge, 1977; Salomon & Naughton, 1977; Ogg & Koslow,
1978; Woodley et al., 1981; Rogers, Suchanek & Pecora, 1982; Kaufman, 1983; Lassig, 1983; Rogers et
al., 1983; Walsh, 1983; Laboute, 1985; Reichelt, Green & Bradbury, 1985; Kjerfve, Magill, Porter &
Woodley, 1986).
Major biological disturbances involving large fluctuations of echinoderm populations including Crownof-Thorns starfish (reviewed by Moran, 1986) and sea urchins (e.g. Lessios, Glynn & Robertson, 1983;
Downing & El-Zahr, 1987) continue to produce extensive and poorly understood changes in reef
community structure (e.g. Done, 1985) and metabolism (e.g. Carpenter, 1988). It is that the reef
environment is far from constant. Physical disturbance is a major structuring force at several spatial and
temporal scales, and reef communities are highly variable in their responses and resilience. Unfortunately,
improved understanding of these processes has contributed little to the assessment and control of
anthropogenic disturbances to coral reef communities.
More promising has been the development of a better appreciation of the nature of complexity in reef
ecosystems, and its implications for explanation, prediction, and control. The key is scale. Processes which
are important at one scale are not necessarily so at another. For instance, observed differences in the
patterns of reef-fish recruitment are largely a function of the spatial scale (e.g. coral head, patch reef, reef
platform, reef province) at which they are measured (Sale et al., 1984; Doherty, 1987). Community stability
may (in terms of species biomass) be high as a function of trophic complexity at the ecosystem level, but
low as a function of species diversity at the habitat level (King & Pimm, 1983).
Considerations of spatial scales appropriate to reef processes, and the degree of connection and
interaction between spatial units (habitats, wholereefs, etc.) are essential to the management of human
impacts on reef systems. Consideration of time scales is of even greater importance, given the great
temporal range of reef processes (Hatcher et al., 1987). Observation and management timetables must
account for the extreme variability in rate constants applicable to organism and system function (Bunt, 1983).
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Recently, the need for long term data records (Younge, 1973) has been receiving well-deserved attention
(e.g. Shinn, 1976; Dahl & Lamberts, 1978; Armstrong, 1982; Davis, 1982; Boulon, 1986; Dustan & Halas,
1987). Reefs must be viewed as dynamic structures which undergo large changes in their physical and biotic
components at highly variable rates. Stability is a relative condition, which must be related to both the
nature and scales of perturbations (e.g. Bradbury, Hammond, Moran & Reichelt, 1985b; Brown, 1987a;
Dahl & Salvat, in press).
In most cases where ecological theory has been applied to specific management or conservation problems
in complex systems it has, however, proved inappropriate or, at best, inadequate, such as in the application
of island biogeography to nature preserves (Simberloff & Abele, 1976), population models to multispecies
fisheries (May et al., 1979), and predation models to starfish infestations (Yamaguchi, 1986). The reasons
for these failures of translation reside in the nature of complex systems (Bradbury & Reichelt, 1982;
Prigogine & Allen, 1982; Anonymous, 1986a). It is through the characterisation of this complexity and the
development of appropriate models for predicting system and component responses to perturbations, that
ecological theory can contribute usefully to coral reef conservation and management.
Some current approaches include equilibrium biomass modelling (Polovina, 1984), probabilistic and
stochastic simulation (James & Stark, 1983), self-learning polynomial models (Green, Bradbury & Reichelt,
1983), and dimensional analysis (Hatcher et al., 1987).
It is crucial to recognise that different models are required for management than for scientific
understanding, and that the one does not necessarily follow from the other (Bradbury, Reichelt & Green,
1985a; Putney, 1986). In short, one important message for reef conservation arising over the past 15 years
of scientific research is that many established ecological models do not work on coral reef systems, and few
of those which do form a basis for management; a separate class of management models is required.
ANTHROPOGENIC EFFECTS
From a conservation standpoint, empirical data on the effects of human activities on coral reef communities
is a major requirement. Reefs provide a broad range of benefits to humans including: food, protection from
the elements, raw materials for construction, clothing etc., ornamental and decorative goods, medicinal and
industrial chemicals, waste disposal sites, equipment and weapons testing grounds, diverse genetic
configurations, recreational, aesthetic and educational experience. The exploitation of these resources
inevitably results in impacts to the reef ecosystem, including: water pollution in the form of sewage,
industrial waste, agricultural chemicals, fossil fuels, thermal effluent and freshwater run-off; turbidity and
sedimentation due to generation, resuspension, and transport of sediment from land clearing, dredging,
construction, and mining activities; wholesale removal of reef structure due to mining, dredging, and
blasting for navigation, construction, and military purposes; destruction of reef structure due to ship
groundings, trampling, anchoring, trawling, and explosive detonations; removal of living organisms targeted
in fishing and collecting activities; and the inadvertent destruction of non-target organisms as a result of all
of these activities. Documentation of these anthropogenic impacts on reefs has increased substantially
during the past decade. Advancement in our understanding of the mechanisms of effect, and their
consequences has been much less substantial.
Sedimentation
Increased sediment load in waters surrounding coral reefs resulting from land clearing, construction, mining,
dredging, and drilling activities has continued to be the major threat to their conservation in many regions
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(e.g. Weiss & Goddard, 1977; Rodriquez, 1981; Tsuda, 1981; Chansang, Boonyanate & Charuchinda, 1982;
Falanruw, 1982; Pathmarajah, 1982; Dahl & Baumgart, 1983; Gourlay, 1983; Hoffman, 1983; Polunin,
1983; Bird, Dubois & Iltis, 1984; UNEP, 1984a, c, 1985g; Frazier et al., 1985; Gabrie, Porcher & Masson,
1985; Guilcher, 1985; Head & Hendry, 1985; Rogers, 1985; Brown, 1986; Salvat, 1987b). On a global
scale, other impacts seem insignificant by contrast.
An important consideration is whether sediment is delivered to the substratum or is simply advected
through the system. In the latter case, effects are mainly a result of light reduction due to increased turbidity
(e.g. Bak, 1978; Salvat et al., 1979; Ricard, 1980). When sedimentation occurs, adverse effects on sessile
benthic organisms are strongly species-specific; ranging from minimal to catastrophic (e.g. Eldredge &
Kropp, 1985; reviewed by Brown & Howard, 1985; Pastorok & Bilyard, 1985; Hubbard, 1986).
Laboratory and field studies have demonstrated decreased calcification, photosynthetic and nutrient
uptake rates, and increased production of mucus, zooanthellae expulsion and pathology in corals subjected
to sediment loading (reviewed by Brown & Howard, 1985). Adaptive responses by many corals (e.g.
sediment shedding) often, however, restrict mortality to the treatments receiving the highest concentrations
in short-term experiments (e.g. Coffroth, 1985; reviewed by Brown & Howard, 1985).
In situ studies have shown that the localised effects of sedimentation on reef communities can be severe.
They include reduced algal and coral diversity, smothering of crustose floral and faunal assemblages, and
reductions in epifaunal densities (e.g. Salvat et al., 1979; Galzin, 1982; Marszalek, 1982; reviewed by Brown
& Howard, 1985; Gabrie et al., 1985; Pastorok & Bilyard, 1985; Peyrot-Clausade, 1985; Yamazato, 1987).
Much of the impact may be due to the infilling of the complex topography of the reef surface (Choi, 1982),
which is positively correlated with community structure (e.g. fish diversity: Luckhurst & Luckhurst, 1978)
and function (e.g. nutrient regeneration: Andrews & Mller, 1983). Conversely, some reef communities have
been found to exhibit little or no obvious response to increased sediment loading (e.g. Sheppard, 1980;
Dollar & Grigg, 1981; Hudson, Shinn & Robbin, 1982). Certain fleshy algae, gastropods, and suspended
bacteria have been found to increase in areas near dredging operations (e.g. Galzin, 1982; Naim, 1981),
although it is not whether these changes in density were direct (or indirect) effects of sedimentation.
Generalisation about the effects of sediment loading on reef-fish communities is even more difficult.
Responses range from the disappearance of most large species (e.g. Galzin, 1982) to no detectable effects (e.g.
Dollar & Grigg, 1981). Reef fish do not appear to be useful indicators of habitat degradation due to sediment
loading (e.g. Amesbury, 1982), except perhaps in extreme circumstances.
It is that high rates of sedimentation are detrimental to reef growth and maintenance. It is equally that the
problem is usually the indirect result of terrestrial activities, and is often difficult to control (e.g. Chansang
et al., 1982; Falanruw, 1982; Polunin, 1983; Guilcher, 1985; Head & Hendry, 1985; White, 1987c). Reef
managers in most cases are restricted to simple monitoring of obvious effects such as turbidity and
mortality. Often these signs appear too late for remedial action.
Identification and observation of the species and symptoms most sensitive to sediment loading (i.e.
indicator species) is one approach which could provide early indications of degradation. The great
variability in the form and magnitude of response by reef organisms (especially corals: e.g. Yamazato, 1987;
reviewed by Brown & Howard, 1985) to sedimentation precludes universal indicators; these must be
determined on a local case-by-case, or at best regional, basis.
Recent advances in the analysis of density bands in coral skeletons (e.g. Hudson, 1981; Isdale, 1984;
Boto & Isdale, 1985) may allow compilation of long-term records of sediment loading for baseline and
comparative purposes. Short-term measurements of coral growth rates have the potential to indicate recent
sedimentation stress (e.g. Brown & Scoffin, 1986), but many other factors such as light (itself influenced by
suspended sediment), temperature, and salinity stress also affect growth, thereby confounding
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determinations of cause (e.g. Highsmith, 1979; reviewed by Brown & Howard, 1985; Tomascik & Sander,
1985; Yap & Gomez, 1985a).
Chemical Pollution
Chemical pollution on reefs often accompanies sediment loading, and the effects may be difficult to
separate (e.g. Carey, 1982; Walker & Ormond, 1982; Brown, 1987b). Some chemicals have unequivocably
negative effects. For example, chlorine is highly toxic to many reef organisms, particularly planktonic
forms including phytoplankton and invertebrate larvae (Campbell, 1977; Best, Bailey, Marsh & Matlock,
1982). The disposal and clean-up of such substances on and around coral reefs should be regulated using
established protocols (e.g. Cairns & Buikema, 1984). Other elements such as the heavy metals have rarely been
found in naturally occurring reef organisms at concentrations which pose a threat to their survival (Windom
et al., 1984; Denton, 1986; Denton & Burdon-Jones, 1986a, b; but see Brown, 1987b). Variable metal
concentrations observed in the flesh and skeletons accumulating organisms such as giant clams and corals
are generally attributable to the geochemical properties of their environments (Stebbing,
1976; Khristoforova & Bogdanova, 1982; Dodge et al., 1984a; Martin, 1984; Denton & Burdon-Jones,
1986e); thus their occurrence may be used as a tracer of previous inputs (e.g. Shen, Boyle & Lea, 1987).
Most experimental studies of the effects of metals have focused on corals (reviewed by Howard & Brown,
1984). Many coral species appear to be resistant to a broad range of toxic elements (e.g. Marsh et al., 1985;
Howard, Crosby & Alino, 1986), although the mechanisms remain unclear. Again, interspecific variation is
high, and larval life stages may be better able to cope with some toxins than coral colonies. This conclusion
cannot be extended to some other toxic chemicals such as herbicides and pesticides. Chlorinated
hydrocarbons are rapidly concentrated through reefal food webs and may have serious long term
consequences for consumers even at relatively low concentrations (Lamberts, 1977; Olafson, 1978;
Solbakken et al., 1984; Glynn, Howard, Corcoran & Freay, 1986).
Understanding the effect of oil on coral reef communities is important because of the geographic
association between reefs and both the extraction and transport of petroleum. Extensive physiological data
from laboratory experiments with corals demonstrate the generally harmful effects of both crude oil and
dissolved fractions, but responses are species specific (e.g. Elgershuizen & DeKruijf, 1976; Dodge et al.,
1984b; Mitchell & Fitt, 1984; reviewed by: Roy, 1981; Knap et al., 1983; Brown & Howard, 1985; Loya &
Rinkevich, 1987). Far less information is available on the toxicity of hydrocarbons to other reef organisms
(e.g. Eisler, 1975).
There is no consensus on the nature of whole-community response to oil pollution on reefs, nor on the
differential effects attributable to the various hydrocarbon compounds and their decomposition products
(reviewed by Loya & Rinkevich, 1980, 1987). The impact of acute applications (i.e. large spills) will be
minimised if direct contact with organisms is avoided (i.e. if the pollutant forms a film on the sea surface).
The buoyancy and vertical mixing characteristics of oil are functions of its composition and age, as well as
environmental factors such as temperature, solar radiation, and hydrodynamics. Hence, the restriction of oil
to the sea surface cannot be confidently predicted, particularly in the tropics. Prolonged occurrence of
surface films over reef communities will produce indirect negative effects in the forms of reduced light
penetration and gas flux (e.g. Kinsey, 1973; Mathias & Langham, 1978), as well as direct effects such as
leaching of soluble fractions into the mixed layer of the water column, deposition of surface films on
shallow benthos by wave and tide. The use of chemical dispersants, which mix the pollutant into the water
column, is generally inappropriate in shallow water over reefs because it brings the most toxic volatile
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components (including the dispersant itself) into direct contact with reef organisms (Lewis, 1971; Loya &
Rinkevich, 1980; Neff & Anderson, 1981).
Chronic, low-level applications of hydrocarbons have been implicated in the degradation of reef
communities in Malaysia (Mathias & Langham, 1978), Panama (Birkeland, Reimer & Young, 1976), the
Red Sea (e.g. Rinkevich & Loya, 1977; Hanna, 1983; Dicks, 1984), and Indonesia (Seng et al., 1987).
Several other potentially negative factors such as low tides, sewage imputs and sedimentation in some of
these areas (e.g. the Red Sea) confound conclusions about specific effects of oil pollution (Loya, 1976;
Fishelson, 1977; Mergner, 1982).
The picture emerging is that petroleum hydrocarbons pose a variable, but significant threat to coral reefs
communities. At present, the main source of damage is chronic, low-level leakage of oil and related
products near production, loading and transport facilities, rather than massive spills. Extensive research and
practical experience has produced a reasonably good understanding of the behaviour and effects of
petroleum hydrocarbons in temperate marine environments. The applicability of this work to tropical
marine ecosystems is limited by differences in both physical and biotic variables. The specific responses of
reef organisms have proved to be highly variable (e.g. corals: Neff& Anderson, 1981; reviewed by: Brown
& Howard, 1985; Loya & Rinkevich, 1987). There is great need for comprehensive and well-designed
research into the effects of oil pollution on whole reef communities.
Sewage Pollution
Sewage inputs to coral reef areas can take the form of dissolved inorganic nutrients, dissolved organic
material and/or particulate organic material (reviewed by: Pastorok & Bilyard, 1985; Marszalek, 1987).
Long standing assumptions about nutrient limitations to coral reef production (Smith, 1984) might lead one
to predict strong community responses to sewage inputs. The sign and magnitude of effects in natural reef
communities exhibit, however, no simple (predictable) pattern. For example, Tomascik & Sander (1985,
1987a, b) examined coral growth rate, reproduction, and community structure along a gradient of increasing
nutrient enrichment, turbidity, sedimentation, toxicity, and bacterial production (eutrophication). Small
increases in these variates above oligotrophic levels enhanced coral growth rates; but at higher levels coral
growth and diversity declined, and asexual reproduction became more common. Johannes, Wiebe &
Grassland (1983a) describe three distinct patterns of nutrient flux in a patch reef, which they relate to the
concentration of inorganic nutrients in the surrounding water.
On larger scales, the nutrient regime of the waters surrounding and within coral reefs plays a major role
in determining their structure and function. Geographical and temporal variation in the mechanism, such as
upwelling (Andrews & Gentien, 1982), ground water (Lewis, 1987; Rougerie & Waulthy, in press), and
pattern (i.e. pulsed or steady) of nutrient inputs, produce major differences in coral reefs through both direct
and indirect (e.g. algal competition, recruitment success) effects (Johannes et al., 1983b; Hallock & Schlager,
1986; Birkeland, 1987b; Wiebe, 1987). Whether human activities significantly influence these large-scale
effects is unclear.
Experimental additions of nitrogen and phosphorus to reef communities on a small scale have increased
rates of primary production, but produced little change in the benthic algal standing crop or community
composition (Kinsey & Davies, 1979; Hatcher & Larkum, 1983). High phosphate concentrations have been
shown to inhibit skeletal growth in corals, but the levels required to produce an effect are far in excess of
those occurring in all but the most polluted reefs (Kinsey & Davies, 1979; El-Rayis, Abbas & Qurashi,
1982; Dodge et al., 1984a; Tomascik & Sander, 1985). Larger inputs of several nutrient species in sewage
can produce blooms of both planktonic and benthic algae which may grow to dominate the reef community
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at the expense of other benthic organisms, including corals (e.g. Banner, 1974; Smith et al., 1981; Walker
&Ormond, 1982; reviewed by Pastorok & Bilyard, 1985). Smith et al. (1981) concluded that the original
source of nitrogen supporting an extensive macroalgal bloom in Kaneohe Bay was in the form of particulate
organics, rather than in dissolved forms (which were taken up rapidly by the planktonic community).
The studies in Kaneohe Bay provide the most comprehensive case history of sewage effects on reef
communities available. There the effects of pollution on corals, and on benthic community structure and
function appear to be no more predictable from models based on energy or nutrient fluxes than have those
on the water column community (Maragos, Evans & Holthus, 1985; Evans, Maragos & Holthus, 1986).
Another conclusion of major importance is that many of the changes in response to sewage input were
reversed very slowly, or not all, after the sewage outfall was diverted offshore (Smith et al., 1981; Russo,
1982; Evans et al., 1986).
Evidence is accumulating that coral reef benthic community structure can assume at least two stable forms:
one coral-dominated, and one macroalgae-dominated (Lighty, 1982; Hatcher, 1984, 1985). The factors
which control shifts between stable states on coral reef communities are poorly understood (e.g. Bradbury
et al., 1985b) but anthropogenic effects may be implicated (e.g. Hatcher, 1984).
Thermal Pollution
Sea temperature has a pervasive influence on most aspects of coral reefs (Potts & Swart, 1984). As
Johannes (1975) pointed out, thermal pollution such as the discharge of heated water from a power plant has
potentially greater impact on tropical communities than on temperate ones. In the last ten years there have
been a large number of studies of both organism and community responses to thermal stress on coral reefs
(reviewed by Brown & Howard, 1985), particularly that caused by power plants (Neudecker, 1987). The
findings of research on corals concur on three general points: temperature increases of 46C are sufficient
to cause reduced growth or death in most coral species; sensitivity to thermal stress is inversely proportional
to metabolic and growth rates; and there is a large degree of both genotypic and phenotypic plasticity in the
response of coral species to thermal stress (e.g. Coles, Jokiel & Lewis, 1976; Marsh, Chernin & Doty, 1977;
Coles & Jokiel, 1978; Jokiel & Guinther, 1978; Marcus & Thorhaug, 1982; Yap & Gomez, 1984). Brown &
Howard (1985) point out however, that simple extrapolations of temperature effects on corals to coral
communities are inappropriate because of the great variability in responses among species and habitats.
Coles et al. (1976) and Coles & Jokiel (1977) found that corals from a high-latitude coral reef in Hawaii had
upper thermal tolerance levels which were about 2C lower than those of the same species on the tropical
reef at Enewetak. Marcus & Thorhaug (1982) report similar differences between Atlantic and Pacific
species of Parites.
The effects of thermal pollution on reef biota other than corals have received scant attention.
Susceptibility may be lower in motile species or those with temperate affinities (e.g. Marsh et al., 1977). As
in temperate regions, where heated effluent can sometimes be used to advantage, thermal energy inputs to
coral reefs need not always be regarded as pollution. The magnitude of their impact will be strongly
dependent on the dissipative qualities of the receiving water body. For example, Coles (1984, 1985)
discovered that thermal effluent from a power station in Hawaii enhanced the local recruitment of corals by
up to ten times the recruitment to control areas. In some cases the chemicals used to clean and maintain power
plant plumbing may pose a greater threat to reef communities than elevated sea-water temperature.
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Radioactive pollution
Documentation of the long-term effects of nuclear weapons tests conducted in the Marshall Islands in the
1940s and 1950s continues at a low, but steady rate (e.g. Noshkin, Wong & Eagle, 1979; Spies, Marsh &
Kercher, 1981; Hudson, 1985). Johannes conclusion (1975) that the accumulation and concentration of
long-lived, highly radioactive isotopes in inorganic materials and organisms on reefs is the sole, but
unacceptably pernicious impact of any global significance, remains fundamentally valid in light of recent
studies. But Hudsons (1985) suggestion that nuclear testing may have sterilised long-lived corals, if true,
has ominous implications. At present, nuclear detonations on reefs are restricted to a single atoll in French
Polynesia. Preliminary reports on the less controversial impacts of these weapons tests on reef organisms
and structure have only recently begun to emerge (e.g. Bablet & Perrault, 1987a, b).
A more common source of radioactive pollution is waste released from nuclear power plants, hospitals,
and industry. While such discharges are usually regulated so as not to exceed safe background levels in
receiving water bodies, biotic concentration processes may confound this simple management practice.
Fortunately such sources are rarely located in proximity to reefs.
Hydrodynamic influences
Several other anthropogenic impacts can be grouped with those discussed above on the basis of their
delivery to reef communities via the water column. Freshwater run-off due to coastal land clearing or large
scale desalination may alter the salinity of water bathing reef organisms, causing osmotic stress. Reduced
salinity has been shown to produce negative effects on corals in isolated experiments (e.g. Coles & Jokiel,
1978; Marcus & Thorhaug, 1982; Coffroth, 1985) but community level effects have received little attention.
Similarly, the suggestion that reduced oxygen tension in reef waters (due to inhibition of gas flux or
increased biological and chemical oxygen demand) may be a significant stress on coral reef biota (Johannes
& Betzer, 1975) has not been tested convincingly. The fact that anoxic conditions did not develop over
significant areas in Kaneohe Bay as a result of massive inputs of organic matter (Smith et al., 1981)
suggests that such effects are minimised in well-flushed environments, but not eliminated altogether (e.g.
Fitzhardinge & Tyler, in press).
The oceans surface is littered with junk; a problem of global significance (Laist, 1987). Because coral
reefs form structures at or near the sea surface (often in areas of strong currents), they accumulate flotsam.
The abundance of man-made refuse (especially plastic items) is becoming significant not only near
population centres (e.g. McManus & Wenno, 1981; Willoughby, 1985) but in more remote areas (often near
shipping lanes) as well (e.g. Rashid, 1980). In addition to being unsightly, many items of flotsam are
demonstrably dangerous to large animals including sharks, turtles, and marine mammals.
That all pollutants depend on the hydrodynamic environment for delivery to reef communities explains to
a large degree the variability observed in their effects through space and time. Every impact so far discussed
must be qualified with information on the role that water movement plays in dispersing, diluting,
concentrating, and delivering a given material or energy in the proximity of its source and the various reef
habitats. Water circulation in and around coral reefs is notoriously complex (e.g. Roberts & Suhayda, 1983;
Andrews & Furnas, 1986). This complexity makes the prediction of pollutant trajectories and
concentrations very difficult. In addition, transformations may take place in the advecting water mass which
amplify, attenuate or alter qualitatively the form of the effects of pollutants on reef communities. For example,
Smith et al. (1981) found that the bulk of dissolved nutrients released in sewage to Kaneohe Bay were
incorporated in particulate matter in the water column before delivery to the benthos.
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The relationship between hydrodynamics and non-conservative materials (i.e. those which cannot be
modelled in the same way as the water mass) is a developing area of research. Application of the associated
theory to coral reef dynamics is still, however, at a rudimentary stage, (e.g. Smith & Jokiel, 1978; Williams,
Wolanski & Andrews, 1984; Oliver & Willis, 1987).
It is becoming increasingly apparent that hydrodynamic processes exert overriding controls on many
ecological processes and patterns, from organism morphology to community structure (e.g. Jokiel, 1978;
Bradbury & Young, 1981; Navaluna & Pauly, 1984; Foster, 1987). It follows that alterations to the
hydrodynamic regime in reef areas by human activities (e.g. harbour construction, channel dredging, coral
rock mining) may produce far-reaching biological effects, especially downstream of the alterations.
Improvements in our understanding of both the physical oceanography of reefs and the relationship between
hydrodynamics and ecology will be expensive, but the potential benefits from this line of scientific enquiry
in terms of conservation of coral reefs are likely to be great.
Physical disturbance
Closely related to hydrodynamic processes are physical disturbances which form a major class of impacts
on coral reefs. As complete structures, coral reefs are exceptionally robust. They dissipate prodigious
amounts of kinetic energy in breaking waves and deflecting currents. They have the capacity for self-repair.
As a result, structural insults to reefs in the form of point source impacts such as ship groundings (e.g.
Dollar & Grigg, 1981; Hatcher, 1984; Curtis, 1985; Smith, 1985), trampling (e.g. Woodland & Hooper,
1977; Liddle & Kay, 1987), boat anchor and diver damage (e.g. Davis, 1977; Tilmant & Schmahl, 1982;
Lund, Anderson, Gladfelter & Davis, 1986) rarely produce widespread or long term structural damage to
coral reefs (but see Tilmant, 1987, and Gittings & Bright, 1988, for examples of exceptions to this
generalisation).
A major reason for this is the ability of most corals to regrow from colony fragments (Highsmith, 1982;
Mitchel-Tapping, 1983). As the frequency of these impacts, however, increases, so will the potential for
serious damage to coral reef structure and thence community function (Grigg, 1983). For example, coral reef
communities decimated by continuous dynamite fishing demonstrate the cumulative effect of small physical
disturbances recurring in periods much shorter than the regrowth time of the biota (Alcala & Gomez, 1979;
De Silva, Betterton & Smith, 1984; Ongkosongo, 1981; Chesher, 1985). Chronic, low level physical
disturbance such as occurs in popular marine parks may have worse implications for reef conservation than
rare, highly destructive events because it does not allow adequate time for community recovery (e.g. Davis,
1977; Dustan & Halas, 1987; Tilmant, 1987). This point is of particular significance for high-latitude coral
reefs, where coral growth rates are slow (Crossland, 1984) and macroalgal competition intense (Johannes et
al., 1983b); recovery times may be of the order of decades (e.g. Grigg & Maragos, 1974; Evans et al.,
1986).
Most forms of physical disturbance listed above simulate natural disturbances to which reef ecosystems
have adapted through evolutionary time. Natural physical disturbance regimes (waves, tides, storms) are
potent forces structuring and maintaining diversity in coral reef communities (e.g. Dollar, 1982; Rogers et
al., 1982; Connell, 1983; Grigg, 1983; Lassig, 1983; Walsh, 1983). In so far as anthropogenic physical
disturbances emulate natural intensities and frequencies, they are, at most, of local significance. Most
human activities are relatively puny physical events compared with a tropical cyclone or submarine
earthquake.
Other forms of physical disturbance are more insidious because they do not mimic natural disturbances
and produce secondary effects which are difficult to predict. The best examples of these sorts of
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perturbations are mining and dredging activities which remove huge sections of the reef structure, thereby
altering the hydrodynamic regime (e.g. Gabrie, Porcher & Masson, 1985; Head & Hendry, 1985; UNEP,
1985, a, b; Salvat, 1987b). Altered circulation may in turn produce conditions unsuitable for the regrowth of
reef-building biota (Birkeland, 1984; Wolanski, Pickard & Jupp, 1984). Such effects are particularly serious
in the case of platform reefs enclosed by intertidal reef crests, where the opening of navigation channels
allows the lagoon to drain with the falling tide (e.g. Gourlay, 1983).
Extractive activities
The final set of anthropogenic impacts on reefs considered here are those which involve the extraction of
reef resources. In addition to secondary effects discussed previously (e.g. increased sedimentation as a
result of trawling, dredging or coral mining), harvesting has direct, and often immediately detrimental
effects on the biological communities of the reef.
Reef communities have high trophic complexity, and consist of many species with generally small
populations and individual sizes (Sale, 1980; Huston, 1985). For these reasons as well as the small size of
the ecosystem unit (the reef) local populations are easily depleted (Grigg, 1979), although coral reefs
commonly support high secondary productivity (Lewis, 1977; Marshall, 1985). The implications of these
characteristics for yields from reef fisheries have been discussed recently by Marten & Polovina (1982) and
Russ (1984), and the conservation of tropical fisheries is reviewed in a separate section of this paper.
Intensive, non-selective fisheries, in which virtually everything edible or saleable is harvested reflect the
high productivity of the reef ecosystem in yields of as much as 20 tonnes.km2yr1 (e.g. Alcala, 1981).
Yields from monospecific fisheries on reefs are generally unstable and low relative to their temperate
counterparts, and hence they are easily overfished. For example, Joannot & Bour (1988) concluded the
modest harvest rate of a favid coral on a New Caledonian reef was ten times the maximum sustainable yield,
and predicted a rapid collapse of the fishery. For reasons which are not yet , yields from certain
monospecific fisheries on high-latitude coral reefs appear to contradict this generalisation (e.g. Hatcher,
1985).
A common pattern of exploitation of living reef resources for human consumption begins with targeting
the largest and most abundant species of acceptable quality. Criteria are then progressively relaxed as
exploitation proceeds until virtually every catchable individual is taken, using progressively less selective
(and often more destructive) fishing methods such as dynamite or poisons (Gomez & Alcala, 1979; Polunin,
1983; Chesher, 1985; Alcala & Gomez, 1987; Eldredge, 1987b; Gomez, Alcala & Yap, 1987).
In developed countries reef fisheries have a higher recreational component, and have not generally
reached such levels of overall depletion. Stocks of particularly desirable species of large predators may,
however, become seriously reduced by highly selective fishing methods such as spearing (e.g. Craik, 1982).
The effects of over-fishing on the structure and function of reefs as systems has received little attention
(Munro, Parrish & Talbot, 1987). We do not know to what extent species are functionally interchangeable
in a reef community such that when some are over-fished, others can take on their ecological roles in the
community. Given the great range of specialisation in reef organisms, the likely effects of over-fishing will
depend strongly on the species and community involved. For example, the removal of all cleaner wrasses
from a reef might cause a decline in the populations of large fish which they service, due to parasite-induced
mortality. But there is no evidence that reefs fished free of large herbivorous fish have become algaedominated.
Collection of reef organisms for sale is a form of fishing which is highly selective, and often intensive on
a local scale. The primary organisms harvested include ornamental shells (Glucksman & Lindholm, 1982;
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Wells, 1982; Sims, 1985; Yen, 1985; Wells & Alcala, 1987), semi-precious and common corals (Grigg,
1977; McManus, 1980; Oliver & McGinnity, 1985; Wells & Alcala, 1987), and aquarium fish (Lubbock &
Polunin, 1975; Albaladejo & Corpuz, 1982; Wood, 1985; Randall, 1987). When collection is for markets
demanding live specimens, such as the marine aquarium trade, the wastage through mortality in transit can
be very high (Wells, 1986), but need not be (e.g. Lewis, 1988). In some areas collecting has resulted in large
areas of reef becoming depleted of many originally common, as well as rare, species (e.g. Gomez, 1982/83;
Yen, 1985). As with other forms of fishing, it is not yet possible to predict the impact of collecting activities
on a reef ecosystem as a whole. But effects on non-target species can be significant when poisons are used
(e.g. Rubec, 1986).
Direct effects of harvesting, such as the virtual disappearance of giant clams from some Pacific Island
countries (e.g. Bryan & McConnell, 1976), are obviously serious in view of the major conservation goal of
maintaining diversity. Our lack of knowledge about the long-term effects of depletion of target species on
the function of coral reef communities means that these effects are less obvious, but not necessarily less
serious. Given our limited understanding of interactions between organisms of reef communities, such
impacts must be examined on a case-by-case basis for the foreseeable future.
Introductions
The introduction of new species to coral reef communities, whether deliberate or accidental, is an
increasingly serious threat to their integrity as aquaculture programmes and rapid transport develop
(Eldredge, 1987c). The containment of alien species and unwanted contaminants in culture systems can
never be guaranteed, and the behaviour of the organism in the complex communities of coral reefs is
impossible to predict. The introduction of the red alga Eucheuma to various Pacific islands (e.g. Russell,
1982, 1983) provides a good example of these points.
Tourism
The attractions of tropical seas, convenient transportation and the popularity of SCUBA diving bring
increasing numbers of tourists in close proximity to coral reef ecosystems (e.g. Rogers, 1988). In developed
countries such as Australia tourism represents a significant threat to reef conservation (e.g. McCabe, 1981),
but one which they can afford to control (e.g. Kelleher & Dutton, 1985) using income from the industry to
ensure its continued profitability.
Tourism is also growing rapidly in developing countries, where the capacity to control its impacts is often
inadequate (Gomez, 1982/83; Goodwin, 1986; Tilmant, 1987; Vant Hof, in press). The effects of tourism
include those associated with construction and land development (discussed previously), as well as direct
human interference with sensitive biota. Tourism has been implicated in the degradation of many reef areas,
particularly in southeast Asia (e.g. Rashid, 1980; Chansang, Boonyanate & Charuchinda, 1982; Srithanya,
Muchacheep, Srirattanachai & Harden, 1982; Tsuda, 1981; Wijsman-Best, Moll & De Klerk, 1982). Often
the income from tourism enterprise must be used for more immediate purposes than reef conservation in these
regions.
Synergism
The threats to the conservation of coral reefs posed by any one of the impacts discussed above cannot be
considered or managed in isolation because they rarely occur in isolation. Coral mining is accompanied by
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sediment suspension and altered water circulation. Coastal land clearing alters salinity, turbidity, nutrient
loading, and mixing in adjacent water bodies. Secondary and synergistic effects are inevitable. For example,
reductions of live coral cover, whether as a result of destructive fishing practice or not, lead to reduced
abundances of demersal fish (Carpenter, Miclat, Albaladejo & Corpuz, 1982; Bell & Galzin, 1984; Sano,
Shimizu & Nose, 1984; Galzin, 1987).
The complexity of biological and physical interactions in reef ecosystems means that fairly simple
phenomena can produce manifold or hierarchial patterns of effect. Often these involve changes in
competitive networks or predator selectivity. For example, disturbances may enhance the growth of
macroalgae, which subsequently outcompete corals for space and light (Banner, 1974; Marszalek, 1982;
Hatcher, 1984; Dustan, 1987). Destructive behaviour and population outbreaks of coral predators such as
muricid snails (e.g. Moyer, Emerson & Ross, 1982; Boucher, 1986) or Crown-of-Thorns starfish (reviewed
by Moran, 1986) have been indirectly linked to human activities as they affect terrestrial inputs to reef
communities (Birkeland, 1982, 1985; Muzik, 1985; Glynn et al., 1986; Yamaguchi, 1986; Nishihira, 1987);
but the causal mechanisms remain obscure. The incidence of the toxic dinoflagellate responsible for
ciquatera poisoning has been shown to increase as a result of human-induced disturbance (particularly
sewage pollution) in reef communities where fish are regularly eaten (e.g. Yasumoto et al., 1980; Bagnis,
1987).
Anthropogenic disturbance may also serve to amplify the impact of natural stresses such as dessication or
UV radiation (e.g. Yamaguchi, 1975; Loya, 1976; Mergner, 1982; Faure et al., 1984; Howard, Crosby &
Alino, 1986; Khlmann, 1988). Individual perturbations may not be of sufficient magnitude to damage
directly reef components, but in combination may produce dramatic effects such as zooxanthellae expulsion
(e.g. Jaap, 1979) or the coral shut-down syndrome (e.g. Chesher, 1985), because of synergism amongst
factors (e.g. Coles & Jokiel, 1978). Sublethal impacts, either individual or multiple, may allow naturally
destructive processes such as bacterial infections to gain the upper hand (e.g. Mitchell & Chet, 1975;
Antonius, 1977, 1982; Galzin, 1982; Segel & Ducklow, 1982). The combined effects of domestic sewage
and industrial chemical pollution near population centres often reduce water quality to the point where
overall fishery production is reduced (e.g. Rau, 1979).
The number of permutations of effect can be expected to increase roughly as a power function of the number
of factors, making prediction of a net effect difficult in all but the simplest situations. The complexity of
community response even to simple perturbations on reefs means that impacts which are apparently neutral
(e.g. Dollar & Grigg, 1981) may produce significant changes in community structure over the long term due
to secondary effects which are difficult to predict (e.g. Hatcher, 1984).
Fishelson (1977) suggests that the net effect of all impacts on a reef system may be greater than the sum
of its component disturbances due to cumulative effects on the development of the ecosystem through time,
resulting in large scale instability of system structure. Convincing evidence for, or against, this hypothesis is
lacking, but the apparent sensitivity of coral reefs to environmental pollution (Khlmann, 1988) supports it.
Because of synergistic effects, prediction of the impact of anthropogenic stresses based on single-factor
experiments, often conducted in laboratory conditions with organisms isolated from the community, are of
limited value. On the other hand, inadequately controlled field experiments may also obfuscate because the
measurement of all relevant variables is unlikely, and the identification of the important ones is difficult.
Large scale, in situ experiments using intact ecosystems, such as the diversion of sewage from Kaneohe Bay
(Smith et al., 1981), can be very revealing but are decidedly difficult to arrange to accommodate the
researcher. Experiments using microcosms as analog models of coral reef communities are increasingly
employed to examine their integrated responses to perturbation (e.g. Smith, Jokiel, Key & Guinther, 1979;
Adey, 1983) but the practical value of this approach has barely been explored.
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RESEARCH FOR MANAGEMENT

The difficulty of separating natural from anthropogenic impacts poses serious problems for management
decision makers (Anonymous, 1986a). The widespread death of corals in tropical seas around the world
cannot be attributed solely to natural or anthropogenic causes, but rather a site and time varying mix of both
(e.g. Glynn, 1983; Brown, 1987a; Nishihira, 1987). The Crown-of-Thorns starfish phenomenon (reviewed
by Moran, 1986) provides an example of our inability to resolve causes and mechanisms in a scientifically
or politically satisfactory fashion, due to the lack of management-orientated research (James, 1976; Rowe &
Vail, 1984; Raymond, 1986). Measuring degradation of the reef environment, whether due to anthropogenic
activities, natural perturbations or both, is still largely a subjective exercise, subject to the serious
constraints on experimentation and interpretation which plague all environmental impact assessments
(Stewart-Oaten, Murdoch & Parker, 1986). Brown (in press) evaluates the usefulness of various techniques
for assessing impacts on reefs.
Methods for conserving coral reefs should reflect the fact that they differ from other marine ecosystems
in important respects. The problems of monitoring and predicting change in an environment dominated by
the physics of the fluid medium are common to all marine ecosystems (e.g. Ray & Norris, 1972; Ray, 1986).
The functional complexity of the physical and biotic sub-systems in reef ecosystems and their interactions
are, however, poorly understood. The non-equilibrial nature of coral reef communities makes it difficult to
determine standard reef conditions against which to evaluate impacts, although reef community
metabolism is a potentially useful exception to this generalisation. The extreme between-habitat variability
of many reef processes (e.g. nutrient supply, Birkeland, 1987b; productivity, Hatcher, 1988; grazing,
Sammarco, 1987; recruitment, Doherty, 1987; mortality, Walhe, 1985) means that experiments must be
replicated extensively in space before generalisations are attempted. These factors, plus the isolation and
exposure of coral reefs, make research for management difficult and expensive in comparison with that on
other heavily used marine ecosystems such as estuaries.
Bradbury & Reichelt (1982) and Bradbury, Reichelt & Green (1985a) use the term holding strategy to
describe the tactic of protecting reef communities until information required for sound management
decisions is collected. Most commonly this involves the creation of marine nature reserves around reefs,
which are subsequently studied. There now exist more than 200 such reserves in at least 50 countries
(Salvat, 1982a, b; Wells, 1986; Dahl, 1987). Until recently much of the research conducted in these areas
has been of little immediate value to managers because it has focused on fundamental rather than applied
aspects of marine science. Several avenues of research are, however, developing which are of direct
relevance to the management of coral reef areas.
Monitoring the regrowth of coral reef communities following substantial anthropogenic degradation
indicates that recovery is typically slow (of the order of decades) and often incomplete (e.g. Alcala &
Gomez, 1979; Bouchon, Jaubert & Bouchon-Navaro, 1981; Sakai & Yamazato, 1984; Yap & Gomez, 1984,
1985a; Alino et al., 1985; Curtis, 1985; Holthus, Evans & Maragos, 1986). This contrasts with the quite
rapid recovery rates following many natural disturbances discussed previously, and reviewed by Brown &
Howard (1985) and Pastorok & Bilyard (1985). One explanation for this is that anthropogenic perturbations
tend to be chronic, while natural perturbations are usually infrequent (albeit sometimes severe) thereby
allowing reef communities opportunity for recovery (Wells, 1986). Estimations of recovery patterns and times
is further complicated by geographic differences which limit the generality of lessons learned in case
studies. For example, Sammarco (1987) suggests that differences in grazer populations, and sexual versus
asexual coral reproductive methods make the time scale of community recovery from major perturbations
longer for Caribbean than for Indo-Pacific reefs.
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Restoration of reef habitat following anthropogenic degradation is expensive and often ineffective. For
example, transplantation of living corals into damaged areas has achieved only limited success (i.e. high
mortality and slow growth) at great expense (e.g. Maragos, 1974; Bouchon et al., 1981; Yap & Gomez,
1984; Gabrie, Porcher & Masson, 1985). The countries where reef restoration is most needed can least
afford such programmes.
Areas of technological research relevant to management of coral reef ecosystems include remote sensing
(discussed on pp. 383384); inventions which reduce human-induced damage such as mooring systems
(Salm & Robinson, 1982; Halas, 1985) or sediment-control curtains (Gabrie et al., 1985); automated
ecological measurement (e.g. Barnes & Devereux, 1984; Griffith, Cubit, Adey & Norris, 1987); and
computer simulation of community response to perturbation (e.g. Gaus, Macintyre & Herchenroder, 1984;
Reichelt, Green & Bradbury, 1985; Kjerfve et al., 1986).
Relevant biological research includes that on population genetics of reef organisms, which has great
potential to determine the origins and spatial boundaries of both natural and commercially exploited stocks
(e.g. Shaklee, Tamaru & Waples, 1982; Nergel & Avise, 1983; Stoddart, 1983, 1986), and the identification
of easily monitored organisms which provide early indications of system degradation, such as specialist
consumers (Reese, 1981; UNESCO, 1986), and corals (Hudson, 1981, 1985; Dodge et al., 1984a; Peters,
1984; Tomascik & Sander, 1985, 1987b).
The usefulness of indicator species in assessing degradation of coral reefs (e.g. Reese, 1981) depends on
the existence of common, highly sensitive organisms within their diverse communities (OConnor &
Dewling, 1986). As yet no reef species has been identified as a universal indicator of system condition
which can be used in the way mussels have in shallow temperate ecosystems (Goldberg, 1986). As
discussed previously, the responses of the most likely candidates (corals) to stresses are highly variable
amongst species (reviewed by Brown & Howard, 1985).
In developing the concepts of stress ecology at the level of ecosystems Barrett, Van Dyne & Odum (1976),
Odum, Finn & Franz (1979), and Rapport, Regier & Hutchinson (1985) argue that anthropogenic
perturbations create predictable changes in productivity, nutrient cycling, species diversity and dominance.
Methods for rapidly measuring these system-level variables on coral reefs (e.g. community structure:
Tomascik & Sander, 1987a; Harger, 1986; community productivity: Barnes & Devereaux, 1984) have the
potential to provide useful indicators of ecosystem health without detailed examination of large numbers of
component species.
Conservation requires the balance of often mutually exclusive human activities against the intrinsic
conservation value of the resource. In addition to the essentially fundamental research discussed above,
management-orientated research is required to develop: (1) criteria for multiple use of coral reef
environments (Kelleher, 1982; Zell, 1982; Soegiarto, 1986; Tisdell, 1986; White, 1986, 1987a;
Anonymous, 1987); (2) simple procedures for monitoring resource use (Dahl 1981a, b; Bakus, 1982/83;
Kenchington & Hudson, 1984); and (3) effective tactics for public education and enforcement (Cabanban &
White, 1982; Geoghegan et al., 1984; Holthus, 1985; Miller, 1986; White, 1987b). Common currencies and
economic models which allow the conservation value of reefs to be compared directly with their commercial
value (e.g. Bakus, 1982/83; Blanchet, 1985; Pfeffer & Tribble, 1985; Vant Hof, 1985) have proved useful
in the development of multiple use methods of management.
Note that most of these research priorities are essentially sociological, rather than ecological. Where
ecological research is required it must be conducted with a perception of its end-use, and the results
provided in language comprehensible to non-scientists (e.g. Hatcher, Hatcher & Wright, 1988).
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MANGROVE COMMUNITIES
Mangrove communities are marine tidal forests. The constituent trees and shrubs are a taxonomically
diverse group of more than 50 species characterised by adaptations to loose, wet soils, saline habitats, and
periodic tidal submergence. Mangrove communities are best developed in the tropics, where they fringe
about 25% of the coastline. Although the trees do not tolerate temperatures below freezing, they extend well
into the temperate zone in Japan, Florida, and Australia. Mangrove communities have no structural
analogues at higher latitudes, where salt marshes commonly occupy similar habitats (see Chapman, 1977).
Process-orientated research on mangroves has lagged behind that on coral reefs, and did not really get
underway until the late 1960s. Until this time mangroves were viewed as wastelands in most developed
countries, in spite of the fact that mangrove forests were being successfully managed for timber and
charcoal production in Malaya (Watson, 1928), and had long been an important source of a variety of
products for traditional societies (e.g. Meehan, 1982; Saenger, Hegerl & Davie, 1983; Lu Chang & Lin
Peng, 1987). Recently, however, there has been a surge of interest in the factors that control the structure
and functions of mangrove ecosystems, and here we provide a brief review of several key areas of research
most relevant to the conservation of mangroves.
FUNDAMENTAL RESEARCH
Although the areal extent and composition of mangrove forests in many tropical regions remain to be
documented, there has been some progress in determining the factors responsible for the distribution patterns
of trees on several scales. Temperature is the most important determinant of a species range on a global scale
(Markly, McMillan & Thompson, 1982; Blasco, 1984; Saenger & Moverley, 1985), with the severity and
duration of minimum temperatures being the controlling influence on seedling establishment (Lugo &
Patterson-Zucca, 1977). Of greater interest for this review are, however, the factors which contribute to the
great variation in mangrove community structure and function among sites (estuaries, bays) within
geographic regions. Differences in soil salinity, the frequency of tidal inundation, sedimentation, soil
chemistry, degree and frequency of freshwater flow and ground-water availability have all been cited as having
an influence on diversity patterns (Macnae, 1968; Clarke & Hannon, 1970; For, Dor & Amir, 1977;
Semeniuk, 1983; Wells, 1983, 1985). A recent examination of forest composition patterns in 92 estuaries in
tropical Australia has revealed that maximum and minimum air temperature, tidal amplitude, estuary length,
catchment size, rainfall variation, and the frequency of tropical cyclones all contribute significantly to the
variance in tree species richness (Smith & Duke, 1987). In regions of the world with much more frequent
cyclones than tropical Australia, for instance the Sunderbans (Mulcherjee & Tiwari, 1984), it is likely that
such natural disturbances have a major impact on forest species richness.
Zonation patterns within mangrove forests have traditionally been viewed as resulting from adaptive
responses of individual species to intertidal gradients in factors such as the frequency of tidal inundation and
pore-water salinity (e.g. Watson, 1928; Macnae, 1968; Lugo, 1980). Disjunct species distribution patterns
(Johnstone, 1983), and experimental tests which have shown that seedlings of mangroves often have their
highest growth rates and best survival where adult conspecifics are absent (Rabinowitz, 1978) or in one
particular zone of the intertidal (Smith, 1987a), suggest, however, that factors such as propagule dispersal,
competition (for light and nutrients: Janzen, 1985; Lugo, 1986) and predation on propagules are also
important in determining zonation patterns.
Experimental tests of the importance of competition are few (e.g. Smith, 1987b) but recent work on weed
predation (mainly by intertidal crabs) has shown that this may be a major factor in determining tree species
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distribution patterns in Australia (Smith, 1987b,c), southeast Asia as well as in the New World (Smith,
Chan, Mclvor & Robblee, 1988).
Although it was once suggested that mangrove zonation recapitulated successional sequences in coastal
regions of Florida (Davies, 1940) and that mangrove forests were thus active land-builders, this appears to
be true only for locations where sediment is accumulating rapidly, or in areas of recent colonisation, where
rates of seaward growth of up to 200 m per year have been reported (Macnae, 1968). The role of mangroves
appears, however, more passive than active, and geomorphological and hydrological processes (Spackman,
Dolsen & Riegel, 1966; Thorn, 1975) appear to be dominant forces in determining whether mangrove
shorelines are accreting or eroding. The role of mangroves therefore appears to be the stabilisation of
sediments which have been deposited by physical forces.
Mangrove forest succession involves four phases: colonisation, early development, maturity, and
senscence; but massive natural mortality (due to hurricanes, sea-level rises, fire, hypersalinity) usually
prevents stands from reaching the final stage. Analysis of 28 worldwide reports of massive mangrove tree
mortality led Jimenez, Lugo & Cintron (1985) to conclude that: (1) mangrove environments are dynamic
and cyclical; massive die-offs are often associated with, (a) drastic reductions in intensity and/or frequency
of run-off and flushing of mangrove stand or, (b) chronic flooding and/or massive sedimentation; (2) the
development of even-aged stands following extensive disturbance enhances the opportunity for subsequent
massive tree mortalities; and (3) disease and other biotic factors do not appear to be the main, direct causes
of massive die-backs, but may seriously affect forests weakened by changes in the physical environments.
The primary productivity of mangrove forests varies enormously at both the local and regional scale.
Recent reviews of the ecophysiology of mangroves (Clough, Andrews & Cowans, 1982; Clough, 1984)
suggest that salinity and climatic factors (solar irradiance, cloudiness and the ratio of precipitation to evapotranspiration), together with nutrient availability (see p. 367) are key factors regulating mangrove growth
and productivity.
Maintaining an optimal salt balance is a major requirement for maximising metabolic rates in mangroves.
Although mangroves exclude a high proportion of salt at the roots, the small proportion that is not excluded
is concentrated in leaves by upward movement in the transpiration stream (Clough et al., 1982). Species
may differ in their capacity to exclude salt and thus in their ability to cope with changes in pore-water
salinity. Most of the mechanisms involved in maintaining a salt balance in leaves, apart from exclusion of
salt by roots which seems to be a passive process (Scholander, 1968), require an expenditure of metabolic
energy. The respiratory losses during periods of high substratum salinity and high evapo-transpiration may
be considerable. They are likely to be higher in areas of the tropics with long dry seasons, where the leaf to
air vapour pressure deficit is high, than in areas where high humidities prevail during the year and where
soil salinities remain low (Ball & Farquhar, 1984; Andrews & Muller, 1985).
Laboratory studies have shown that mangroves attain optimum growth at intermediate salinities (e.g.
Downton, 1982; Clough, 1984), and in the field, canopy height and net productivity both increase with
decreasing salinity (Cintron & Schaeffer-Novelli, 1983). A recent field survey of gas exchange properties of
19 species of mangroves in tropical Australia and Papua New Guinea has shown that for all species
stomatal conductance (a measure of the degree of stomatal opening) and carbon dioxide assimilation rate both
decreased with increasing salinity and with increasing leaf to air vapour pressure deficit (Clough & Sim,
pers. comm.). High salinity conditions for mangroves are thus analogous to drought stress in terrestrial
plants because the upper limit to diurnal fluctuations in leaf water potential (which determines stomatal
conductance) is set largely by the salinity of the soil porewater. During drought years when interstitial
salinities are high, die-backs are common in inner swamps and shallow lagoons and may effect large tracts
of forest (e.g. Jimenez et al., 1985).
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Because the gas exchange properties of mangrove leaves react rapidly to changes in soil salinity as well
as to other environmental changes (Ball, 1986) studies of photosynthesis in mangroves not only form the
basis for measuring primary production (Clough, 1987) but are a potentially valuable tool for rapid
monitoring of mangrove health in the face of environmental changes.
The nutrient status of mangrove soils, nutrient requirements for primary production, and the ability of
mangrove forests to act as a source of dissolved nutrients for adjacent habitats have all received attention
recently. In tropical Australia, Boto & Wellington (1984) have shown that soil inorganic nitrogen and
soluble reactive phosphorus levels in non-vegetated areas in close proximity to forests were an order of
magnitude greater than within the forest. Fertilisation experiments in the same forest (Boto & Wellington,
1983) showed that tree growth was nitrogen-limited in the low to mid-intertidal zone, while in the mid-to
high intertidal, which experienced little fresh sedimentation, soil mineral deficiencies (e.g. phosphorus)
were also apparent. Similarly, mangrove forests in Florida responded positively to nutrient (as guano)
additions (Onuf, Teal & Valiela, 1977). In temperate salt marshes, Mendelssohn (1979) has suggested that
apparent nitrogen limitation may be related to the anaerobic nature of most marsh soils. Significantly Boto
& Wellington (1983, 1984) found that above ground plant biomass in an Australian mangrove forest was
correlated with the soil redox potential, as was the nitrogen content of new leaves.
Based on rates of primary production and tissue nutrient concentrations it has been estimated that plant
uptake could account for rates of nitrogen and phosphorus transfer from the sediments of 250 kg N.ha1.yr1
and 20 kg Pha1yr1 (Boto & Wellington, 1983; Clough, Boto & Attiwill, 1984; Boto, Bunt & Wellington,
1984). Plant uptake from soils in forests is therefore a significant sink for nutrients (see also Walsh, 1967;
Nedwell, 1974, 1975; Odum & Johannes, 1975).
Two studies in mangrove waterways have shown that the long held belief that mangrove systems are
important sources of outwelled dissolved nutrients is unlikely to be true. In a mangrove system almost
entirely influenced by tidal action Boto & Wellington (1988) have shown that there was no net annual
exchange of dissolved organic or inorganic nutrients, and that there was a significant import of dissolved
phosphorus amounting to 24% of the requirement for primary production. In a comparison of two river
systems in Malaysia, one with and one without mangrove vegetation, Nixon et al. (1984) have suggested
that mangroves were not a significant source of dissolved nutrients; most nutrients were derived from
terrestrial systems higher in the watersheds they studied.
Two other pieces of dogma about the role of mangrove swampstheir global importance as nursery
grounds and their role in outwelling of particulate detritushave also recently been critically appraised.
Despite the quantity of research on mangroves as nursery grounds in Florida (e.g. Odum, 1971; Lindall,
Hall, Fable & Collins, 1973; Odum & Heald, 1975; Odum, Mclvor & Smith, 1982; Lewis, Gilmore, Crewz
& Odum, 1985; Thayer, Colby & Hettler, 1987) there have been few quantitative tests of the nursery ground
hypothesis at low latitudes. Yanez-Arancibia, Linares & Day (1980) have shown that a mangrove-fringed
lagoon in Mexico had greater densities offish and different fish communities than adjacent habitats. In
northern Australia Staples, Vance & Heales (1985) have clearly shown that the prawn Penaeus merguiensis
is found only in mangrove-lined creeks during the juvenile phase of its life-cycle.
The most comprehensive comparison of tropical inshore habitats as nursery grounds is provided by
Robertson & Duke (1987a), who sampled juvenile fish communities in mangrove, seagrass, and mudflat
habitats in northeastern tropical Australia. They showed that the densities of fish and prawns in mangrove
habitats of four different estuaries were up to an order of magnitude greater than in the adjacent nearshore
habitats. While many of the small fish species captured are not commercial species in Australia, they are
important in the trawl fisheries of serveral nearby southeast Asian countries and are important forage fish for
large predators such as the barramundi, or sea bass, Lates calcarifer (Robertson & Duke, 1987a). Given
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some of the similarities in the fish faunas of mangrove habitats in Australia and Papua New Guinea (Liem &
Haines, 1977; Collette, 1983; Quinn & Kojis, 1985) it is likely that the findings of Robertson & Duke
(1987a) also apply to much of the coastline of Papua New Guinea.
Boto & Bunt (1981) and Robertson (1986) have recently estimated tidal export of particulate organic
matter (POM) of 7 kg Cha1day1 from a mangrove forest in tropical Australia. Most particulate organic
carbon (POC) was in the form of intact leaves and reproductive parts of mangrove trees. Such export
represents 15000 tonnes Cyr1 from the 60 km2 of mangrove forests in their study site. At first glance this
would appear to provide a massive subsidy to adjacent coastal habitats. The POC is, however, widely
dispersed once it leaves the point of origin, and would contribute, at most, 16% of the carbon required for
sediment bacterial production in the nearby Great Barrier Reef lagoon (Robertson, Alongi, Daniel & Boto,
in press). This indicates that the correlations between offshore prawn catches and the areal extent of tropical
mangrove swamps that have been documented by several authors (Martosubroto & Naamin, 1977; Nair,
Omar & Rahman, 1977; Turner, 1977, 1986; Gedney, Kapetsky & Kuhnhold, 1982; Staples et al., 1985;
Pauly & Ingles, 1986; Soepadmo, 1987) are probably not due to a food chain link with mangroves provided
by outwelled mangrove detritus, as is often suggested (e.g. Snedaker, 1978). This view is supported by
the analysis of Rodelli et al. (1984) who showed that mangrove-derived carbon is a small component of the
somatic carbon of consumers captured offshore from mangrove forests in Malaysia.
It is more likely that the connection between offshore catches and mangroves derives from the estuarine
and/or mangrove dependence of juvenile penaeid prawns (e.g. Staples et al., 1985; Pauly & Ingles, 1986;
Turner, 1986; Robertson & Duke, 1987a), or that the correlations derive in part from factors related more to
freshwater outflow than to the presence of mangroves. Positive correlations between freshwater run-off and
fisheries yields are well established in the temperate zone (e.g. Sutcliffe, 1973; Dame et al., 1986) and are
beginning to receive attention in the tropics (Browder, 1985; Staples, 1985; Soberon-Chavez et al., 1986;
Pinto, 1987).
Evidence that removal of an area of wetland habitat will result in a fall in prawn catches in adjacent inshore
regions is difficult to find. Turner (1986) has recently discussed the situation in Ecuador, where removal of
large areas of mangroves for shrimp ponds has resulted in a decline in offshore harvests of penaeids. A
similar result was observed after the large-scale reclamation of intertidal (non-mangrove) wetlands in Japan
(Doi, Okada & Isibashi, 1973). Catches of prawns on the west coast of India, however, remained high
despite the removal of large tracts of mangroves (Macnae, 1974).
A requirement for the estimates of POC flux made by Boto & Bunt (1981) was the development of a
hydrological model for mangrove forests subject only to tidal influence (Wolanski, Jones & Bunt, 1980).
The model revealed that flow rates are much greater on ebb versus flood tides. This occurs because the
complex matrix of mangrove trunks and prop roots acts as a barrier to water flow during the early phase of
the ebb tide. When water does flow out of the forest, it does so at an increased velocity because of the
gradient that has been set up between forest and channel. A major effect of greater ebbtide currents is
scouring of the channels within forest, and the deposition of sediment seaward of the mangrove fringe
(Wolanski et al., 1980).
In areas of the tropics with long dry seasons, water exchange between mangrove estuaries and the open
ocean is greatly curtailed. Lateral trapping of water in mangroves (e.g. Wolanski et al., 1980) is a dominant
process controlling longitudinal mixing in mangrove-fringed tidal rivers. In the dry season in such systems
Wolanski & Ridd (1986) have shown that longitudinal diflusivity is typically two orders of magnitude
higher than it would be in the absence of the mangrove forests. In addition, a salinity maximum zone can
develop near the mouths of such estuaries due to evaporation in shallow coastal waters. The resultant high
salinity plug may completely block mixing of estuarine and oceanic waters (Wolanski, 1986). Even during
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short-lived flood events in these seasonal estuaries, rapid flushing may not occur because fresh water may
remain within the mangrove swamp for several days owing to the lateral trapping of water (Wolanski &
Ridd, 1986).
Although there are few data, several recent papers suggest that the supply of ground water to mangroves
may contribute significantly to forest structure and productivity. Johannes (1980a) suggests that in some
cases the supply of nitrogen to mangrove forests from the submarine discharge of ground water may be of
greater importance than that provided by other processes. In addition, in non-estuarine conditions, low
salinity ground water may provide the mechanism for the flushing of salt from mangrove forests (Wolanski
& Gardiner, 1981). Finally, the zonation patterns of mangroves in tropical Western Australia have been
shown to be controlled to a large degree by ground water discharge (Semeniuk, 1983).
There are many similarities in the fate of mangrove primary production in most mangrove systems,
including low levels of herbivory (Heald, 1971; Johnstone, 1981; Robertson & Duke, 1987b), and large
proportions of weight loss during decomposition of leaves in the form of dissolved organics (Fell, Master &
Newell, 1980; Robertson, 1988). Research on trophodynamics in Old World mangrove forests indicates,
however, that the food chain models developed for Florida swamps (e.g. Odum & Heald, 1975; Odum,
Mclvor & Smith, 1982) are not wholly applicable to the more species-rich mangrove forests of the Indowest Pacific region (Robertson, 1987).
Crabs of the subfamily Sesarminae are dominant members of the macrofauna in mangrove forests of the
Indo-west Pacific (Macnae, 1968) and are known consumers of leaf litter (e.g. Malley, 1978). These crabs
can remove up to 30% of the annual leaf fall (Robertson, 1986) and a substantial proportion of reproductive
propagules (Smith, 1987c) in low to mid-intertidal Rhizophora forests, and up to 80% of all litter fall in high
intertidal forests which are rarely flushed by tides (Robertson & Daniel, 1989). This gradient of increasing
litter turnover by shredders with tidal height is the reverse of that observed in Florida (Odum & Heald, 1975;
Twilley, 1985; Twilley, Lugo & Patterson-Zucca, 1986) where shredders are important in subtidal regions
and microbial decay of litter is the major process in the high intertidal of basin forests.
Rapid turnover of litter by shredders in Indo-west Pacific mangrove forests is just one of the mechanisms
which facilitates the high bacterial production measured in the sediments of these forests (Alongi, 1988).
There is also a close coupling between bacterial production and dissolved organic carbon (DOC) pools in
the sediments of tropical Australian mangrove forests (Stanley, Boto, Alongi & Gillan, 1987), and there
may be a large amount of recycling between DOC and bacteria (Alongi, in press), implying that bacteria are
an important sink for carbon in this system. Meiofauna and protozoan densities are low and do not correlate
with bacterial standing stocks, which suggests that a relatively small proportion of bacterial production is
consumed directly (Alongi, 1987a,b). The contribution to detrital pools from decay of trunks and branches
of trees may be equal to the amount of litter turned over by sesarmid crabs (Robertson & Daniel, in press).
The Florida food chain model (Odum & Heald, 1975; Odum et al., 1982) also indicates that the trophic
links between mangrove primary production and higher consumers are indirect, depending on microbially
mediated decay of mangrove litter fall and consumption of a variety of small detritivores before energy and
carbon are available to higher trophic levels. During the wet season in tropical Australian mangrove forests,
the larval stages of crabs are, however, a dominant component of the zooplankton and are the major prey of
the juvenile fish community (Robertson, Dixon & Daniel, 1988). Given that most of the larvae are
sesarmids, there exists a direct trophic pathway (leaf litter to crabs to larvae to fish) linking juvenile fish to
mangrove tissue in this region.
Despite such direct connections, it seems unlikely that trophic links alone can explain the higher densities
of fish in mangroves versus other inshore habitats (Robertson & Duke, 1987a). Other factors include the
exclusion of marine predators due to freshwater inflow to mangroves (Blaber, Young & Dunning, 1985),
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the physical barrier to predators provided by mangrove roots (Robertson, 1988) and reduced effectiveness
of predators due to high turbidity in estuaries (Blaber & Blaber, 1980).
ANTHROPOGENIC EFFECTS
The single biggest threat to mangrove forests is their extirpation by man. Throughout the tropics vast areas
of mangrove forest have been clear-felled for woodchip production or to accommodate farming,
aquaculture, salt mining, tin mining, housing, port and airport facilities and industrial sites (e.g. Walsh,
1977; Saenger, Hegerl & Davie, 1983; Hegerl, 1984a; Kongsangchai, 1984; Phillips, 1985; Singh, Garge,
Pathak & Mall, 1986; Comacho & Bagarinao, 1987; Rao, 1987; Untawale, 1987). In Viet Nam spraying
with defoliants during the war in the 1960s and 1970s killed most of the mangroves in the Mekong Delta
(Kempf, 1988). Mangrove forests have been reduced in extent by 75% in Puerto Rico (Martinez, Cintron &
Encarnacion, 1979) and by 20% in peninsular Malaysia (Ong, 1982). Between 1967 and 1976, mangrove
areas in the Philippines declined by almost 50%at a rate of almost 17000 ha annually (Librero, 1984). In
Sabah 40% of the total mangrove areas was the subject of woodchipping licences with interest being shown
in exploiting the remaining 60% (Saenger et al., 1983). There are similarly depressing statistics in
connection with a variety of other countries, including Malaysia, Indonesia, Venezuela, India, Bangladesh,
Benin, and Gambia.
Ironically reclamation of mangroves for agriculture or aquaculture often fails due to the oxidation of the
pyrites (FeS2) usually present in anaerobic mangrove soils, when it is exposed to oxygen. This can result in:
(1) the release of sulphuric acid with the consequent acidification of soil and water, (2) the associated
inhibition of phosphorus uptake by algae, (3) high aluminium concentrations which can be toxic to fish and,
(4) the production of ferric hydroxide floes which may clog the gills of fish (e.g. Saenger et al., 1983;
UNDP-UNESCO, 1987b). Yields from such aquaculture or agriculture ventures are usually much lower
than originally projected (Saenger et al., 1983; New & Rabanal, 1985; Kapetsky, 1987).
Efforts to increase fish-pond production in the tropics are often based on creating more ponds by
reclaiming additional mangrove areas (e.g. Polunin, 1983) and vast areas of mangroves have been
earmarked for such development in the near future (New & Rabanal, 1985). A practical alternative is to
encourage more intensive production in already existing ponds (New & Rabanal, 1985; Kapetsky, 1987); by
so doing, it is possible to increase yields per unit area by up to an order of magnitude without building more
ponds (Hamilton & Snedaker, 1984). Unfortunately, government fish production incentives have often
encouraged more extensive rather than more intensive fish-pond farming in tropical coastal regions (e.g.
Chong, 1984; Naamin, 1987). Current rapid advances in high-intensity prawn culture (e.g. New & Rabanal,
1985; Lawrence, 1985) may help reverse this trend.
Harvesting of mangrove forests for timber and charcoal production can be managed on a sustained yield
basis. In Malaysia the 40 000 ha Matang forest has been harvested successfully on a 3040 yr rotational
basis since early this century (Watson, 1928; Ng, 1987) Similar sustained-yield forestry projects operate in
Thailand (Aksornkoae, 1987), Burma (Hla, 1987), and Venezuela (Pannier, 1979). In comparison, largescale clear-felling of forests for woodchip industries is a major threat to forests in southeast Asia because
there is little natural regeneration of trees in logged areas, which also become dominated by fast-growing
undesirable mangrove species such as Acrostichum (Chan, 1987).
Sustained-yield timber harvesting in mangroves appears to have comparatively little impact on adjacent
fisheries. Studies in the Matang forest have shown that the combination of natural litter fall in the
developing forest and slash remaining from the previous harvest contribute detritus to food chains at a rate
similar to that observed in pristine forest (Wong, Ong & Gong, 1982; Gong, Ong, Wong & Dhanarajan,
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1984). Small-scale fisheries continue to operate in the mangrove waterways in the Matang reserve
(Ong, 1982), and commercial trawling remains successful in adjacent inshore waters (Soepadmo, 1987).
Large artisanal and commercial fisheries are associated with mangrove forests (e.g. Macnae, 1974; Pauly
& Ingles, 1986). Kapetsky (1985) has estimated that the median yield of finfish, shrimps, and crabs from
mangrove-associated lagoons and estuaries is about 9 tonnes-km2yr1. Much of this catch is taken by
people resident in or close to mangrove forests, and worldwide there are about such people directly
dependent on such smallscale fisheries within mangroves (Kapetsky, 1985). In developed countries, large
numbers of amateur fishermen also use mangrove-lined regions as their major fishing sites. For instance
about man-days of fishing per year were spent in sheltered inshore waters (mostly mangrove estuaries and
bays) in the state of Queensland in Australia in 1985 (Anonymous, 1986b).
Commercial fisheries, mainly for penaeid prawns, are generally concentrated immediately adjacent to
mangrove areas. Assuming there is a causal relationship between mangrove areal extent and inshore prawn
catches (Pauly & Ingles, 1986; Turner, 1986; and see pp. 367370 for full discussion of this issue), the most
recent analysis suggests that worldwide a mean of 14.0 (range 1.375.6) tonnes of prawns are captured per
square kilometre of mangrove forest each year (Pauly & Ingles, 1986).
Although mangrove communities develop best in the absence of strong currents or wave action, they do
mitigate coastal erosion. Fosberg (1971) has suggested that the 1970 hurricane and tidal wave which
claimed several hundred thousand lives in Bangladesh might not have been so destructive if thousands of
hectares of mangrove forests in the area had not been replaced with rice paddies. Bangladesh has since
undertaken a large scale mangrove planting programme to protect the coastline (Saenger et al., 1983).
In China, establishment of mangrove forests on previously eroding shorelines, that were subject to
flooding at spring tides and during typhoons, has allowed the transformation of previously poor land to
productive rice-growing areas (Lu Chang & Lin Peng, 1987). The restoration of damaged mangrove
communities by replanting, and factors affecting such efforts have received considerable attention and
success in recent years (e.g. De 1a Cruz, 1984; Hamilton & Snedaker, 1984; Jara, 1987; Kempf, 1988).
Where some mangroves must be sacrificed, it is desirable to leave a belt of uncleared mangrove between the
cleared area and the coast or waterway as a buffer (e.g. Soegiarto, 1984).
Changes to the hydrological regime are the second biggest cause of death of trees in mangrove forests.
Such changes may occur through: (1) the construction of dams or barrages in river systems e.g. in
Venezuela (Pannier, 1979) and Gambia (Saenger et al., 1983); (2) the diversion of fresh water for irrigation,
e.g. in Bangladesh (Saenger et al., 1983) and Trinidad (Bacon, 1970); (3) the pumping of ground water
(Saenger et al., 1983); or (4) impoundment due to the construction of level banks and roads e.g. in Malaysia,
Puerto Rico, Surinam, and Australia (Watson, 1928; Patterson-Zucca, 1982; Jimenez, Lugo & Cintron,
1985; Gordon, 1987).
In cases where freshwater flow is reduced, the subsequent increase in soil salinity favours more salttolerant mangrove species, resulting in a shift in forest species composition. In Bangladesh, there has been a
rapid loss of forest areas dominated by Heritiera fames, a favoured timber tree, due to freshwater diversion
practices further inland (Saenger et al., 1983). Increases in soil salinity probably result in greater salt
concentrations in the leaves of trees, and hence influence the gas exchange capabilities of trees (see pp.
366 367). Death will result when stomatal conductance is so low that carbon dioxide assimilation rates do
not balance the trees metabolic requirements. When forests are impounded, gas exchange through the
extensive aerial root systems of mangroves is prevented and trees die, probably through a combination of
factors.
In addition to the usually irreversible loss of habitat associated with tin mining, salt pan development,
clear-felling and infilling of mangrove forests, these practices also result in greater sediment loads (and
315
heavy metal loads in the case of tin mining) within mangrove waterways. Decreased ebb-flow current speeds
due to clear-felling of extensive mangrove forests bordering tidal waterways will result in high
sedimentation rates and infilling of these creeks (see Wolanski, Jones & Bunt, 1981). Although mangroves
commonly occur in sediment-laden water, they cannot tolerate sediment deposition which results in burial
of the aerial roots. Conversely, when rivers are dammed, or barrages are built, sediment supply to mangrove
areas decreases and there may be significant loss of mangrove habitat (Pannier, 1979; Saenger et al., 1983;
Krishnamurthy & Jeyaseelan, 1984). Unfortunately, because the geomorphology of mangrove forests often
undergoes great natural changes (Thorn, 1975; Pannier, 1979) separating natural and man-induced changes
is often difficult.
Nedwell (1974, 1975), Odum & Johannes (1975), and Clough, Boto & Attiwill (1984) have all discussed
why mangrove communities may serve as useful natural treatment plants for sewage and some other
potential pollutants. The addition of nutrients in sewage to mangroves may even be beneficial in some
instances, since tree growth has been shown to be nutrient-limited in a number of mangrove communities
(see p. 367). The disposal of excessive organic wastes into mangroves, however, can lead to defoliation and
death of trees or may be deleterious to associated flora and fauna (Saenger et al., 1983). In Malaysia, release
of effluent from oil-palm processing factories directly into mangrove-lined rivers has not killed trees, but has
decreased phytoplankton and fish abundance near the outfall (Hegerl, 1984a; Lee, Kaur & Broom, 1984;
Seow & Broom, 1984). Such effects are likely to be exacerbated where riverine flushing is not as
pronounced, for instance in regions with long dry seasons (Wolanski, 1986; Wolanski & Ridd, 1986).
Clough et al. (1984) argue that the discharge of waste directly into mangrove forests may sometimes be
preferable to discharge into drainage channels running through such communities. Much further research is,
however, required on the cycling and impact of pollutants in mangrove ecosystems before the optimal
conditions for waste discharge are adequately understood. In particular, little is known of the influence of
pollutants on mangrove rhizophore dynamics.
Large oil spills have occurred in the vicinity of mangrove forests in Puerto Rico, the US Virgin Islands,
Saudi Arabia, Florida, Ecuador, Nigeria, and Australia (Lai, 1984). Immediate effects of these spills varied
from acute, resulting in defoliation and death of trees, saplings and fauna to intermediate with death of
invertebrates, but no effect on trees (Dicks, 1984; Lai, 1984; Getter, Ballou & Koons, 1985). A set of field
experiments designed to investigate the effects of oil spills in Malaysian mangroves demonstrated that
susceptibility to oil and chemically dispersed oils varied among species, while saplings of all species 180 cm
in height were more susceptible than large trees (Lai & Feng, 1984). The same authors provide a guide to
the use of chemical dispersants when dealing with an oil spill.
Oil spills may have long term effects on mangroves. A mangrove forest that received litres of crude oil in
St Croix showed little regeneration after seven years (Lewis, 1979). In Australia, Allaway (1987) has shown
that the extent of mortality of mature Avicennia marina trees is correlated with the amount of oil residue in
the sediment; most mangroves in sediment with 2.4% crude oil by weight died within two months. The
cause of mortality appeared to involve interruption to the water supply to the leaves (Allaway, 1987).
Mangrove forests are often used as sites for solid waste disposal, especially near centres of human
population (e.g. Saenger et al., 1983; Lai, 1985). Such dumping may kill the mangroves in the immediate
area and can also cause major health hazards through the release into mangrove waterways of toxic
substances which are incorporated directly or indirectly (via the sediments) into mangrove-associated food
chains (Harbison, 1986).
Kolehmainen, Morgan & Castro (1974) described the effects of heated sea water on mangrove plants and
animals in Puerto Rico. Banus (1983) reports that the re-establishment of communities of red mangrove,
316
Rhizophora mangle, in areas in which it has been partly or completely destroyed by thermal pollution, could
only be accomplished if water temperatures were kept at or below 37C for most of the time.
MANAGEMENT
Following this brief review of major anthropogenic effects of mangrove systems, it is worthwhile
considering several further conclusions made by Jimenez et al. (1985) in their review of massive die-offs of
mangroves. These authors state that: (1) humans may tilt the balance towards higher mortality rates (of
trees) by introducing chronic stresses that inhibit regeneration mechanisms, and (2) that recovery after
natural perturbation is generally faster than after human-induced perturbations because the latter are usually
chronic or create new ecological conditions inimical to regeneration. They conclude (Jimenez et al., 1985, p.
183), neither massive die-offs nor parasitic infections are catastrophic in the sense that mangroves are
unable to cope with these conditions. The real catastrophes occur when human misunderstandings of how
these systems work allow irreversible environmental changes from which no. recovery is possible.
Perhaps the major question facing managers of mangrove forests at the present time is how to balance the
demands for land for aquacultural developments against the natural fisheries based on mangrove swamps
and sustained-yield forestry production of mangroves. Arguments for mangrove conservation would carry
more weight with some influential segments of the public if they could be couched in terms of cost benefit
analysis. As yet, there are few areas of the world where biologists can show persuasively, for example, that
mangrove communities will yield more to man when conserved than when reclaimed for other uses. In part
this is due to the problems of comparing incommensurablese.g. the aesthetic value of mangroves as
wildlife sanctuaries versus the cash value of real estate development (Mercer & Hamilton, 1984). Recent
research has, however, shown clearly that mangroves are important nursery areas for a variety of valuable,
commercially harvested marine animals such as penaeid prawns (see pp. 367369), and recent analyses of
the monetary value of mangrove-associated fisheries, sustained-yield wood products and aquaculture
ventures in mangroves (Table II) make some comparisons possible. In compiling these figures we have tried
to obtain data for the 19841985 period, have used figures for aquaculture of shrimp only, and tried where
possible to use data on artisanal fisheries catches in or near mangroves so that the still questionable
relationship between mangroves and inshore commercial shrimp catches need not be assumed. In addition
the data on forest products refer mainly to charcoal production (Table II).
Although there may be some argument about the value per kg we have assigned to shrimp, the data in
Table II clearly indicate that in Malaysia and Thailand, sustained-yield management of forests for capture
fisheries and charcoal produced similar revenue to that achieved by aquaculture ventures in or near
mangroves. In Bangladesh, the figures suggest a much greater (about5) value for aquaculture. In both the
Philippines and Burma, one of either the capture fishery or charcoal production had a similar value to
aquaculture. The major implication from the data is that with the current state of aquaculture technology in
most of these countries, there is no net gain in removing mangroves for aquaculture pond construction. A
more profitable line for managers of these areas would be to push for more profit
TABLE II
Relative monetary value ($USha1yr1) of capture fisheries, aquaculture, and sustained-yield forest products (mainly
charcoal) in mangrove systems in the mid-1980s. NA=no data available
Country
Capture fisheries
Aquacultureb
Forest products
Bangladesh
Brazil
21a
346
NA
55d
NA
769a
Country
Capture fisheries
Aquacultureb
Forest products
Burma
Indonesia
Malaysia
Philippines
Thailand
NA
NA
1375c2773a
561h
100a1623f
320640
684
32001
800
1600
236g
NA
203290c
NA
227e
317
Kapetsky (1985).
Based on shrimp yields (kg-ha1yr1) in New & Rabanal (1985) and assuming US$4 per kg for shrimp.
c Ng (1987) figures for west coast of Malaysia.
d From figures in Choudhury (1987).
e From Aksornkoae (1987), assuming value of charcoal similar to that in Malaysia (Ng, 1987), i.e. US$152 per tonne.
f From Aksornkoae (1987), assuming 22% of shrimp catch from small scale fisheries close to mangroves (see
Aksornkoae, 1987) and sale price of shrimps at US$4 per kg.
g Charcoal production in Irrawaddy Delta (Hla, 1987), and assuming price of charcoal at US$1 50 per tonne.
h From Pauly & Ingles (1986), using data for artisinal shrimp catch and assuming US$4 per kg for shrimp.
i Probably an over-estimate, see New & Rabanal (1985).
b
able use of already existing ponds (Hamilton & Snedaker, 1984; New & Rabanal, 1985).
We would like to caution here that on its own the monetary value of the three uses of mangroves
discussed above (Table II) provide only a partial (and probably poor) assessment of the complete
management options. This is because the socio-economic value of each option also needs to be evaluated
(see pp. 380386).
Finally, we wish to draw the readers attention to two important recommendations for combating
mangrove degradation made by the IUCN Working Group on Mangrove Ecosystems (Saenger et al., 1983).
The recommendations are especially worth noting because they are all too often ignored by biologists
hesitant to move beyond artificial disciplinary boundaries. First, the Working Group discusses the need for
socio-economic studies of mangrove users. One cannot set policies for the management of a natural
resource responsibly without understanding the needs and perceptions of people whose livelihoods or lifestyles depend upon it (e.g. Jhamtani & Djaja, 1985; Reeves, 1985; Smith, 1985a,b). Secondly, they urge
developing National Mangrove Plans, and discuss the design of such programmes. In this connection they
describe legislation and administration relevant to mangrove management in Australia, the Philippines, and
Fiji, and discuss their respective strengths and weaknesses.
TROPICAL SEAGRASS COMMUNITIES
Seagrass communities extend from the Equator into subpolar waters. The gross primary productivity of
tropical seagrass beds, in common with that of mangrove and coral reef communities, ranks among the
highest recorded for natural communities anywhere, and is often higher than that of seagrass beds at higher
latitudes (McRoy & McMillan, 1977; Virnstein, Nelson, Lewis & Howard, 1984). Until comparatively
recently, most seagrass research has been undertaken in the Caribbean (e.g. see Ogden & Gladfelter, 1983,
1986). This short review of the literature will summarise the emerging paradigms which have developed
from work in the Caribbean, and reference work from the Indo-west Pacific and elsewhere, where appropriate.
Diversity of seagrasses in the Caribbean is low when compared with several regions in the Indo-west
Pacific region and elsewhere (Lipkin, 1975; Johnstone, 1978; Bridges, Phillips & Young, 1982; Ogden &
Ogden, 1982; Lanyon, 1986; Zieman, 1986; Poiner, Staples & Kenyon, 1987). Seagrass meadows extend to
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20 m depth in the Caribbean, and even deeper in the Red Sea (Aleem, 1979; Wahbeh, 1982). In contrast,
most seagrass beds in the tropical regions of Indo-west Pacific occur in more shallow water (Johnstone,
1978; Bridges et al., 1982; Ogden & Ogden, 1982; Coles et al., 1987). The major factor influencing the
depth distribution of seagrasses is light penetration (Wahbeh, 1982; Dennison, 1987). In places such as the
Torres Strait and the Gulf of Carpentaria in tropical Australia, seagrasses are often restricted to shallow
regions by the turbid water (Bridges et al., 1982; Poiner et al., 1987).
Seagrasses stabilise sediments because leaves slow current flow, thus increasing sedimentation of
particles (Fonseca & Fisher, 1986). The roots and rhizomes form a complex matrix which binds sediments
and stops erosion. The ratio of below-ground to above-ground biomass of seagrasses increases with
increasing sediment particle size, presumably due to the need for a greater root mass for nutrient absorption
in coarse sediments, which have lower nutrient concentrations (Zieman, 1986).
Seagrasses with dense root masses may create and stabilise near-vertical sediment walls (Davies, 1970),
greatly reduce the height of storm surges (Whitaker, Reid & Vastano, 1973), and in some instances seem
hardly affected by hurricanes which severely damage nearby mangroves and coral reefs (Zieman, 1975; den
Hartog, 1977; but see Birch & Birch, 1984). Besides stability, seagrasses impart a chemical environment to
the sediments (the rhizosphere) which allows them to support a much greater biomass of aerobic micro-and
macrofauna than areas of unconsolidated sediment. Seagrasses also provide a physical baffle to hydrodynamic
flows which encourage the settlement of the larvae of benthic animals (e.g. Eckman, 1983). Finally, where
calcareous algal epiphytes are common on seagrasses, meadows of seagrass contribute significantly to local
sedimentation (Zieman, 1983; Walker & Woelkerling, 1988).
McRoy (1983) and Wiebe (1987) have recently reviewed nutrient dynamics in tropical seagrass beds.
Although both reviews reveal that we know little about this important subject, several interesting facts
emerge. First, nitrogen fixation associated with the roots and shoots of Thalassia varies from negligible to
100% of the nitrogen required for production. The variation in nitrogen fixation rates may arise through
differences in the ambient inorganic nitrogen concentrations or advection of particulate detritus among
sites. Secondly, there is a definite relationship between the depth of the organic sediment layer and the type
of vegetation present in the Caribbean. Increased sediment depth allows greater root development and in
situ recycling of nutrients within the seagrass bed. Ammonium concentrations in the sediment may be
reduced in areas subject to heavy grazing by sea urchins and turtles.
Like mangroves, tropical seagrasses provide important shelter sites for small fish (e.g. Hutomo &
Martosewojo, 1977) and the juveniles of commercially harvested shrimp (e.g. Young, 1978). In the
Caribbean shelter provided by seagrass is limited mainly to fish less than about 15 cm long (Ogden, 1980;
Robblee & Zieman, 1984). Much of the predation in these communities occurs at night when large schools
of snapper, grunts, squirrel-fishes, and other predators leave the shelter of nearby coral reefs to forage over
seagrass beds (e.g. Ogden & Zieman, 1977; Birkeland, 1985). In tropical Australia, several recent papers
have shown that the thin ribbon of patchy seagrass meadows dominated by species of Halophila and
Halodule are the primary nursery site of several species of juvenile penaeid prawns which are the basis of
the major fishery in this region (Coles & Lee Long, 1985; Staples; Vance & Heales, 1985; Coles et al.,
1987; Poiner et al., 1987). These seagrass communities are subject to widespread mortality from cyclones
(Birch & Birch, 1984), and recruitment to the prawn fishery may be influenced by such changes in habitat
availability (Poiner, pers. comm.).
Comparatively few tropical animals consume seagrasses directly. Noteworthy among them are green
turtles (Bjorndal, 1980), dugong (Heinsohn, Wake, Marsh & Spain, 1977), and (especially in the Caribbean)
certain sea urchins, acanthurids (surgeonfishes) and scarids (parrotfishes) (Ogden, 1980; Kirkman &
Young, 1981; Zieman, 1983; Thayer et al., 1984).
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Herbivory usually accounts for 1015% of tropical seagrass production (e.g. Greenway, 1976; Zieman,
Thayer, Robblee & Zieman, 1979; Zieman, 1983; Ogden, 1987); the rest, as with mangrove leaves, supports
a detritus food chain, either in situ, or after being transported elsewhere by currents or as dissolved organic
matter (Zieman et al., 1979; Klug, 1980; Zieman, 1983; Moriarty et al., 1985). Locally, however, grazers
which move out from coral reefs and graze on seagrass beds consume a much higher proportion of primary
production and are responsible for halos around patch reefs (Ogden, Brown & Salesky, 1973).
Seagrass blades also serve as substratum for a variety of epiphytic algae. Recent analysis of the food
webs associated with seagrass meadows indicate that the highly productive epiphytic communities of
tropical seagrasses (e.g. Heij, 1987) may be more important in the supporting secondary production than
seagrass detritus itself (e.g. Fry, 1984; Klumpp, Howard & Pollard, in press). A variety of epifaunal taxa are
associated with tropical seagrass beds (e.g. Heck & Wetstone, 1977; Virnstein et al., 1984; Bauer, 1985)
and there are often complex trophic interactions among the eipfauna before energy and materials in seagrass
food chains become available to fish predators (Young & Young, 1977; Heck & Thoman, 1981; Heck &
Wilson, 1987). The epifauna of tropical seagrass beds may also control the growth of epiphytic algae (Van
Montfrans, Wetzel & Orth, 1984) and thus exert an indirect control on seagrass productivity (Howard &
Short, 1986).
Dredging and filling appear to have caused the destruction of more tropical seagrass habitats than any other
human activity (Thayer, Wolfe & Williams, 1975; Queen, 1977; UNESCO, 1979; Thorhaug, 1981). Both
dredging and filling result in. direct loss of seagrasses, but increased turbidity adjacent to dredging
operations, and changes to the current patterns after dredging also have major negative effects on seagrass
depth distribution, production, and biomass (Thorhaug, 1981; Ogden & Gladfelter, 1983). Denuded areas
may not recover for many decades (Thorhaug & Austin, 1976) because of chronic turbidity due to the
continual resuspension of unconsolidated sediments.
Other impacts, such as damage from fishing activities (e.g. Zieman, 1976), boating (e.g. Williams, 1988),
and changes to run-off patterns from adjacent land masses caused by mining and logging activities also
decrease seagrass habitat in the tropics (e.g. Fonseca, 1987). The best way to halt the destruction of seagrass
meadows is the education of those directly involved, such as developers and fisherman (Fonseca, 1987).
Increases in the nutrient load of waters bathing seagrass beds also lead to widespread mortality and loss
of habitat (e.g. Cambridge et al., 1986). Epiphytic algae on seagrasses derive most of their nutrients from
the water column (Zieman, 1983) and increased growth of the algae due to increased nutrient loading leads
to seagrass death (Silberstein, Chirrings & McComb, 1986).
Seagrass growth can be affected not only by oil pollution, but also by the dispersants used to treat oil
spills (Hatcher & Larkum, 1982; Zieman et al., 1984; Thorhaug, Marcus & Booker, 1986). Zieman (1975)
discusses these problems in more detail, as well as the impacts of other forms of pollution on tropical
seagrass. There is little that is new to add to this earlier review of the topic.
The synergistic effects of increased turbidity and oil pollution may have disastrous effects on seagrass
meadows. Fonseca (1987) describes how increased sediment load in the coastal waters near Phuket in
Thailand, as a result of tin mining, has caused a shift in the species composition of the local seagrass
meadows, favouring mainly intertidal species. Because oil pollution has its major influence on seagrass in
shallow water (Thorhaug, 1981), an oil spill in this region could destroy completely the seagrass meadows.
Thorhaug (1981) and Zieman (1982) have reviewed the impact of increased water temperatures (from
power generator cooling systems) on tropical seagrass communities. Because the upper lethal limit of
tropical seagrasses is just above their summer ambient temperature, small shifts in water temperature result
in widespread mortality.
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Recent years have witnessed expanding efforts, with varied success, to stabilise sediments and/or reestablish destroyed tropical seagrass communities by replanting (e.g. Thorhaug, 1983, 1985, 1986;
Thorhaug, Miller, Jupp & Booker, 1985, and references therein). Thorhaug et al. (1985) demonstrate that
the species of seagrass chosen for rehabilitation should be determined on the basis of the type of
environmental stress existing in the area. The re-establishment of seagrass beds in developing nations may
not, however, be possible given the extremely high costs associated with transplants (Fonseca, Kenworthy &
Phillips, 1982; Fonseca, 1987).
COMMUNITY INTERACTIONS
Interactions occur between reef, mangrove, and seagrass communities (Ogden & Gladfelter, 1983;
Birkeland, 1985; Wiebe, 1987). Coral reefs function as self-repairing breakwaters, creating the low energy
conditions which favour mangrove development along thousands of miles of coastline. Large quantities of
calcareous sediments produced by erosion of reef skeletal material create substrata for the establishment of
seagrass and mangrove communities. Both mangrove and seagrass communities reduce the offshore transport
of terrigenous sediments, thus reducing their impact on adjacent reef communities. The export of mangrove
and seagrass detritus may serve as energy and nutrient subsidies to reef communities, although the
quantitative significance of this export is not well established.
All three communities exhibit faunal overlap. The presence of seagrass beds enhances nearby reef fish
biomass in the Caribbean, apparently because of the forage ground these communities provide (Ogden &
Zieman, 1977; Birkeland, 1985). Seagrass beds provide nurseries for coral reef fishes (Ogden & Zieman,
1977). The use of mangroves as nurseries by coral reef fishes may not, however, be as substantial as is
commonly believed (Parrish, 1987). Quinn & Kojis (1985) examined the composition of the fish fauna in
two mangrove communities in Papua New Guinea, only one of which was close to a coral reef community.
There was little difference in species composition between the two communities. While these authors
observations sustain .the view that mangroves serve as important nursery areas for many fish species, they
do not support the notion that these communities function as important nurseries for coral reef fishes
specifically.
Some coral reef, mangrove or seagrass communities exist in isolation. Here the interactions described
above may be of minor importance or absent. But where such connections are important, and such areas are
widespread throughout the tropics, conservation efforts focused on only one or two of these communities in
isolation may prove inadequate. Anything that affects one of these communities may ultimately affect the
others.
Coral reefs, no matter how rigorously managed internally, will decline if, when adjacent mangroves are
cleared or seagrass beds dredged, the resulting increase in sediment-transport envelopes the reefs.
Productivity of food fishes and lobsters feeding in seagrass beds may suffer if adjacent coral reefs, where
many of these species shelter, are degraded. Mangrove communities will be threatened where the reefs
which protect them from high wave energies are removed to create channels or anchorages.
Birkeland (1985, p. 12) has argued that although such intercommunity interactions are significant,
factors that are more important when attempting to make practical decisions for coastal zone management
are the characteristics of coastal terrain, topography, substratum, water current patterns and rivers.
Much of what we understand at present to be the principles underlying the functioning of tropical marine
ecosystems is based on information derived from studies carried out in limited geographic areas. Until
recently, pioneering studies in Florida dominated our knowledge of mangrove communities, despite the fact
that Florida mangroves are species-poor. Similarly, a disproportionate fraction of our knowledge concerning
321
tropical seagrass ecology derives from studies of the comparatively species-poor Caribbean. Expanded
studies in the Indo-Pacific have revealed that some of the generalisations accepted today concerning the
functioning of these communities should, in fact, be restricted to certain geographic areas (e.g. Robertson,
1986, 1987; Robertson & Daniel, 1989). A comprehensive review of similarities and differences in the
structure and function of Atlantic versus Pacific tropical ecosystems (and the implications for management)
has recently been edited by Birkeland (1987a).
The vast majority of sea bottom in shallow tropical waters consists of unconsolidated sediment. This
habitat has received very little serious investigation until recently in studies of inter-reefal habitats (e.g.
Birtles & , Arnold, 1983; Drew & Abel, 1985; Alongi, in press). Here the sediments appear to support
substantial communities of infauna and epiflora. The degree to which these areas interact with neighbouring
reef, seagrass, and mangrove communities, or are impacted by human activities is almost unknown
(Robertson et al., in press).
The impacts of accelerated sedimentation due to mans terrestrial activities on nearshore tropical
communities, discussed above, emphasises the importance of maintaining the integrity of watersheds and
coastlines adjacent to protected marine areas, and including adjoining terrestrial habitats in marine reserves
(e.g. Rogers, 1985).
FISHERIES CONSERVATION
During the past few years there has been a rapidly expanding awareness of the importance of traditional,
artisanal or small-scale fisheries which characterise many nearshore tropical waters (e.g. Smith, 1979;
Emmerson, 1980; Johannes, 19811a; Panayotou, 1982; Johnson & Stein, 1986). Although the catch-perunit-effort of artisanal fishermen is very low, their numbers are very highover eight million throughout
the tropicsand their total catch amounts to almost one-half of the worlds food fish. Only about oneeighth as much fossil fuel energy is expended on capturing this portion of the catch as on the remainder
caught by industrial fishermen (Thompson, 1980).
Artisanal fisheries possess a number of features which dictate a rather different approach to research and
to conservation of stocks than that taken in typical industrial fisheries. Artisanal fisheries usually involve,
per-unit-of-catch, far more fishermen, boats, methods used, habitats fished, species caught, landing sites,
and distribution channels than industrial fisheries. The cost of gaining the information necessary for
conventional management of such complex fisheries would often exceed the economic benefits by a great
margin. What is needed, therefore, are research short-cutsquick and dirty methods of applying theory
for management purposes, methods which do not require the kinds and amounts of data we cannot
realistically expect to obtain (Marr, 1981).
One simplifying approach is to treat groups of species as single management units, and various theoretical
multi-species fisheries models have been proposed. But because of a poor understanding of stock
boundaries and the unavailability of other model parameters, these models appear to have relatively little to
offer at present in the way of paradigms for tropical multispecies fisheries (Kirkwood, 1982, p. 83).
The development of simplified methods for estimating mortality rates and catch curves from catch lengthfrequency distributions, and new techniques for daily aging of tropical fishes using otolith structure has
useful applications in important single-species tropical fisheries (e.g. Munro, 1982; Pauly, 1982).
Tropical fishermen themselves can sometimes provide much valuable information on local fish behaviour
and the timing and location of spawning and migration pathways of various species. For example, the
number of species throughout the tropics known by biologists to form lunar spawning aggregations has
more than doubled in the past few years as a consequence of information provided by tropical artisanal
322
fishermen (Johannes, 1978b). These aggregations provide biologists with excellent opportunities to monitor
stocks because they occur at predictable times and location. They also provide a useful focus for
management (Johannes, 1980b).
In order to manage artisanal fisheries it is necessary to study not only the biological resources, but also
the methods and relevant customs and values of the people who use them. It was for this reason that
Emmerson (1980), in a wide-ranging analysis of tropical artisanal fisheries, concluded that anthropologists
and biologists working together offer the best hope for improving management.
Some tropical fishermen recognised the need for conservation offish stocks centuries before westerners.
Such awareness was widespread in Micronesia and Polynesia where seafood was the main source of animal
protein and accessible marine resources were limited largely to narrow fringes of reef and lagoon. Here for
centuries islanders employed size restrictions, closed seasons, closed areas, taboos on exploiting spawning
aggregations, limited entryin fact every basic marine conservation measure used in the West only since
about 1900 (Johannes, 1978b). Similar customs have been found in Africa, South America, and elsewhere.
But their practice is weakening in the face of westernisation, political upheavals and, until recently, wellmeaning but uncomprehending expatriate fisheries managers. Research is urgently needed to document such
practices. Modern management regimes which recognise and incorporate, where practical, local
management systems and customs, are likely to gain greater local support and thus be easier to enforce.
Traditional authority and indigenous environmental regulations often carry considerably more weight in the
thousands of isolated fishing villages in the tropics than do government edicts. In some tropical regions such
traditional practices have, however, lapsed. In other cases they may never have existed. In such places other
approaches to conservation must be sought. Whatever they are, it is becoming increasingly that they must
be culturally as well as environmentally sensitive (e.g. Smith, 1979; Emmerson, 1980; Johannes, 1981b;
Marr, 1981; Panayotou, 1982; Wright, Hatcher & Hatcher, in press).
METHODS OF MANAGEMENT: POLICY AND PRACTICE
The truism that environmental management involves the control of human behaviour rather than of
environmental processes is particularly valid in the societies and marine ecosystems of the tropics because
our capacity for prediction and control of processes in their complex communities is so poor.
Sound conservation ethics have evolved both in simple island societies where the limitations of natural
resources are especially obvious (Johannes, 1978a, 1982), and in developed nations which can afford to
apply substantial human and economic resource to the task (e.g. Woodley, 1985; Putney, 1986). There
exists a large middle ground in developing countries where uncontrolled development in response to socioeconomic pressures has produced the worst cases of environmental degradation (e.g. Yap & Gomez, 1985b;
Soegiarto, 1986; Tisdell, 1986; White, 1986; Sorenson & Brandani, 1987). In many tropical countries these
effects can be directly related to the rapid increase in human population (Grigg, 1979; Wijsman-Best, Moll
& De Klerk, 1982; Gomez, 1982/83).
Several environmental measures correlate with this population growth. In Indonesia, for example, coastal
land (including much mangal) has been cleared and excavated for Tamback mariculture since the 1400s.
There are now about ha devoted to this subsistence activity, indicating the redisposition of about of sediment
and substantial alterations to patterns of terrestrial run-off (Polunin, 1983). Similarly, between 1958 and
1980 the proportion of terrigenous material in lagoonal sediments adjacent to Mayotte Island in the Indian
Ocean increased from about 20 to 40%, while the human population density of Mayotte Island increased
from about 60 to 140km2 (Guilcher, 1985).
323
It appears that the demands made by human populations on the marine resources of developing countries
are greater than those in developed countries with similar population densities. Gomez (1982/83, p. 282)
suggests that this may be due in part to the lack (or loss) of a conservation ethic: Apparently deep-seated in
the social fabric is the inability to reconcile drive for economic gain with the obvious wisdom of long-term
planning and conservation. If true (and we feel it is for many developed nations as well) it follows that
scientific understanding of the effects of human activities is of secondary importance in many cases. Of
primary importance is altering the perception and ethics of those who utilise the resources.
The best available recommendations for management in the marine tropics are of a common-sense
nature, requiring little in the way of detailed scientific knowledge (e.g. Geoghegan et al., 1984;
Kenchington & Hudson, 1984; Librero, 1984; UNEP, 1985af). Effort may sometimes be better spent on
culture-specific public awareness and education programmes than on scientific research (e.g. Grigg, 1977;
White, 1981, 1987b; Cabanban & White, 1982; Maragos, Soegiarto, Gomez & Dow, 1983; De Silva, 1985;
Nasr, 1985; Miller, 1986). The value of self-regulation through public education cannot be over-emphasised
given the immense cultural and economic impediments to adequate enforcement of conservation rules in
many countries (e.g. Burbridge & Koesoebiono, 1980; Robinson, Polunin, Kvalvagnaes & Halim, 1981;
Huffman, 1983; Conte, 1985; Dahl, 1985b; Nasr, 1985). Chesher (1985, p. 216) states: Discovering the
extent and causes of the inability of island governments to react to the coral reef problems is probably a
more difficult research problem, and a more important one, than discovering the extent and causes of the
coral reef damage itself. Human nature and the scientific establishment being what they are, research is
likely to remain firmly focused on understanding nature rather than controlling mans avarice or improving
his environmental awareness.
Modern conservation employs several methods, including the establishment of nature reserves or
multiple-use zoning plans which delimit reserves (e.g. Gomez & Yap, 1982; Soegiarto, 1982; Morris 1983;
Broadus & Gaines, 1987; White, 1987a); the collection of data in conservation-orientated research and
monitoring programmes (e.g. Dahl, 1981b; Grigg, 1982; Kelleher, 1982; Koechlin & Boye, 1984; Gilmour
& Craik, 1985); and the implementation of management policy through public education and enforcement
(e.g. Burbridge & Koesoebiono, 1980; Robinson et al., 1981; Gawel, 1982; Kelleher & Kenchington, 1982;
Bakus, 1982/83; Maragos et al., 1983; Holthus, 1985; Miller, 1986).
Basic to conservation practice in the poorly known areas of the tropics is an inventory of resources and
human activities. This has been widely recognised during the past decade, and increasing numbers of useful
and relevant documents are available for several regions of the tropics, e.g. Africa (UNESCO, 1981b;
UNEP, 1984b,c), the Caribbean (UNESCO, 1983; UNEP, 1984a), India (Venkataramanujam, Santhanam &
Sukumaran, 1982), southeast Asia (Polunin, 1983; Chua & Charles, 1984), and Pacific islands (UNESCO,
1981a, Dahl & Baumgart, 1983; Maragos & Elliot, 1985; UNEP, 1985h).
Recent advances in remote sensing technology are revolutionising the mapping of shallow tropical waters
(e.g. UNESCO, 1986). The tools allow inventory and monitoring of specific habitats (e.g. Warne, 1978;
Pirazzoli, 1984), resources (e.g. Bour, Loubersac & Rual, 1985), and dynamic processes (e.g. Praseno &
Sukarno, 1977; Quinn & Kojis, 1984). The development in Australia of an inexpensive image analysis tool
called MicroBRIAN brings remote sensing within reach of those who cannot spend large amounts of time
and money on development work (Jupp et al., 1985; Mayo, 1986). The system can analyse either satellite or
airborne scanner images or aerial photography, using a microcomputer. The Great Barrier Reef Marine Park
Authority and the Australian Survey and Land Information Group are using the system for mapping the
Great Barrier Reef at a cost far below that of ground surveys. The system is at present being used to map
coral reef, mangrove, and seagrass communities in the southeast Asian region. The Australian Institute of
324
Marine Science is at present investigating the potential of the system for delineating Crown-of-Thorns
starfish outbreaks (Reichelt, 1987).
Policy for the management of natural resources should be based on ecological and socio-economic
principles tailored to fit local conditions (e.g. Maragos et al., 1983; Olsen, 1987). Thus, models for resource
use in areas of relatively low exploitation may focus most strongly on natural processes (e.g. Bradbury &
Reichelt, 1982; Grigg, 1982), while those developed for areas where usage is intense (and ecological data
usually scarce) tend to concentrate on socio-economic processes (e.g. Burbridge & Koesoebiono, 1980;
Gawel, 1982; Blanchet, 1985; Holthus, 1985). Recent approaches to integrated management policy include
systems-analysis models which incorporate and formalise interactions between cultural, economic and
natural processes (e.g. Bakus, 1982/83; Bradbury, Reichelt & Green, 1983; James & Stark, 1983; Stark,
1984; Berwick & Chamberlin, 1985; Loomis & Walsh, 1986; Schonewald-Cox & Bayless, 1986). In their
present state of development, however, the principal value of such models lies much more in the
educational aspects of their construction than in the management value of their predictions.
MARINE CONSERVATION AREAS
Marine reserves, parks, and other conservation areas are being designated with increasing frequency in the
tropics (e.g. Bjorkland, 1974; Ormond, 1978; Davis, 1981; Salvat, 1982a,b; White, 1981, 1987a; Weyer,
1982; Chavan, 1983; Nasr, 1985; Dahl, 1987). Unfortunately many are conservation areas in name only,
with little effort devoted to their management. Ray & Norris (1972) and Ray (1976, 1986) review the
general concepts of marine park formation, and Gomez & Yap (1982) outline their application in the
Philippines.
Criteria for selection and delineation of such areas are not well developed, although Abelson (1978),
Bakus (1982/83), and Salm (1984) make some useful suggestions. White (1981, 1986) found that marine
reserves in the Philippines, Indonesia, and Malaysia showed the greatest potential for maintenance and
improvement of environmental quality when the active participation of local people in management
activities was encouraged. Public involvement forms a fundamental part of the planning, zoning and day-today management of the worlds largest (and wealthiest) marine park, the Great Barrier Reef of Australia
(e.g. Anonymous, 1982; Morris, 1983; Woodley, 1985).
Marine protected areas have been justified on the basis that they maintain a range of representative habitats
and biota for study and recreation, and for the replenishment of adjacent sites of extractive exploitation
(Bjorkland, 1974; IUCN, 1980; Davis, 1981; Salvat, 1982a,b; Gomez & Yap, 1982; Randall, 1982;
McNeely & Miller, 1984). While these justifications are intuitively valid to conservation-orientated
scientists, little scientific or economic research has been done to test them. Russ (1985) found that the
available evidence supported the contentions that marine reserves amidst intensely exploited sections of
coral reef maintained fish species abundance and richness, provided undisturbed breeding grounds, and
exported biomass via emigrating adults. It was not whether these areas also exported large numbers of
larval recruits to surrounding reefs. Sound research, using the opportunities for manipulative
experimentation provided by reserve creation (e.g. Sainsbury, 1982), is urgently required to help to define
and measure the value of marine protected areas in the tropics.
Island biogeographic theory (e.g. MacArthur & Wilson, 1967; Diamond, 1975; Boecklen, 1986) has
formalised the recognition of the importance of setting aside natural reserves of sufficient size and number
so that a balance between local extinction and immigration of species is maintained (Goeden, 1979).
Sullivan & Shaffer (1975) have noted that the constriction of terrestrial habitats has resulted in habitat
islands with accelerated extinction rates and decreased species numbers. It is not yet whether this conclusion
325
can be extended to the tropical marine ecosystems considered here, but it seems likely (Davis, 1981; Salvat,
1982a; Bakus, 1982/83; Russ, 1985). An important question is that of the spatial scale of such reserves (e.g.
Dwyer & Harris, 1973; Kelleher, 1982; Hegerl 1984b), and whether the principles used to determine the
size of terrestrial reserves can be applied to marine environments.
Two estimates of critical minimum core areas for coral reef reserves have been made. Goeden (1979)
recommends 3470 ha, based on studies of Great Barrier Reef fish populations, where as Salm (1984)
suggests 300 ha, based on studies of Chagos Archipelago corals. It is not known to what degree this order of
magnitude difference is due to: ecological differences between the two areas, differences in the distribution
of reef fish and coral populations or methodological differences between the two studies. Much more
research is needed to determine the utility of ecological theory in delineating marine protected areas.
Economics are more important to some segments of the public in justifying tropical marine reserves than
ecology. Again, the long-term benefits to society in terms of maintained harvests, employment, and
recreation are obvious (e.g. Salvat, 1982a; McNeely & Miller, 1984), but few studies have calculated these
in economic terms (e.g. Loomis & Walsh, 1986) which can be directly compared with the value of shortterm over-exploitation (Vant Hof, 1985).
The immediate price of zoning and enforcing management plans in marine reserves and parks is high,
both in terms of the direct costs and the losses of income from extractive activities. These costs can be a
significant problem for all but the wealthiest societies (Grigg, 1977; UNEP, 1985b). Several authors have
argued that the creation of large reserves, isolated from human use, is economically unrealistic and socially
inappropriate in most tropical countries (e.g. Ray & Norris, 1972; Huffman, 1983; Holthus, 1985; UNEP,
1985h). Reconciliation of the conservation value of reserves with the economic value of harvesting their
resource is as thorny a problem in the shallow marine ecosystems of the tropics as elsewhere in the world.
The Bali Action Plan, arising from the 1982 World National Parks Congress (Anonymous, 1983)
contains a recommendation to investigate and utilize the traditional wisdom of communities affected by
conservation measures, including implementation of joint management arrangements between protected
area authorities and societies which have traditionally managed resources. This marks a substantial, if
belated, shift in the perception by marine and terrestrial park planners of traditional users of protected areas.
Seen less now as intruders in their own lands and waters, they are becoming accepted as integral parts of the
ecosystems. This is particularly important in tropical regions where the dominant cultural groups using
marine resources often differ greatly from those of the central government which control them.
CONCLUSION
The conservation of coral reefs and other shallow tropical marine ecosystems depends upon the outcome of
a race between the accelerating degradation of these ecosystems and two related areas of human endeavour:
the development of ecologically and sociologically sound models for management, and the effective
education of people to the value of biological conservation. As scientists we can only contribute to these
objectives. As human beings we face a more difficult task in achieving them.
ACKNOWLEDGEMENTS
B.G.Hatcher was supported during this work by a grant from the Australian Marine Sciences and
Technologies Grant Scheme. We thank K. Boto, B. Clough, C.Crossland, A.Hatcher, S.Wells, and two
anonymous reviewers for helpful comments on versions of the manuscript. J.Banning, F.Conn, C.Crossley,
326
M.Flower, J.Thomas, and W.Sharkey undertook the extensive task of typing the text, and Y.Paterson
provided valuable assistance in the library. We are grateful to Margaret Barnes for editorial assistance.
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Zieman, J.C., 1975. In, Tropical Marine Pollution, edited by E.J.F.Wood & R.E. Johannes, Elsevier, Amsterdam,
pp. 6374.
Zieman, J.C., 1976. Aquat. Bot., 2, 127139.
Zieman, J.C., 1982. The Ecology of the Seagrasses of South Florida: a Community Profile. U.S. Fish Wildl. Serv.,
Washington, D.C., FWS/OBS-82/25, 158 pp.
Zieman, J.C., 1983. In, UNESCO Rep. Mar. Sci., No. 23, UNESCO, Montevideo, pp. 8086.
Zieman, J.C., 1986. In, UNESCO Rep. Mar. Sci., No. 41, UNESCO, Paris, pp. 25 29.
Zieman, J.C., Orth, R., Phillips, R.C., Thayer, G., Thorhaug, A., 1984. In, Restoration and Management Ecosystems
Impacted by Oil, edited by J.Cairns & A.L.Buikema, Butterworth Press, Boston, pp. 108126.
Zieman, J.C., Thayer, G.W., Robblee, M.B. & Zieman, R.T., 1979. In, Ecological Processes in Coastal and Marine
Systems, edited by R.J.Livingston, Plenum Press, New York, pp. 2134.
AUTHOR INDEX
References to complete articles are given in heavy type; references to pages are given in normal type;
references to bibliographical lists are given in italics.
Abbas, M.M. See El-Rayis, O.A., 354; 393
Abbott, D.P., 55, 67, 69; 86
See Lambert, G., 47, 55; 88
Abel, K.M. See Drew, E.A., 380; 393
Abele, L.G., 343; 386
See Simberloff, D.S., 350; 408
Abelson, P., 384; 386
Abrams, R.W., 276, 284, 285, 303, 310, 323; 328
Achituv, Y., 110, 126, 128, 129, 130, 131, 132, 146, 150,
154, 155; 156
See Barnes, M., 130, 131, 154, 155; 157
See Gilboa-Garber, N., 150; 159
Adachi, R. See Yasumoto, T., 413
Adams, N.J. See Berruti, A., 273335
Adams, S.M., 187; 262
Adey, W.H., 347, 348, 362; 386
See Brawley, S.H., 247; 263
See Griffith, P.C., 363; 395
Aebischer, N.J., 318; 328
Agenbag, J.J., 276; 328
See Hampton, I., 325; 332
See Shannon, L.V., 275; 334
Ahearn, G.A. See Ferraris, R.P., 229; 264
Ahmed, S.I. See Kenner, R.A., 37; 41
Ainley, D.G., 319; 328
Aizawa, K., 26, 27; 39
Akagawa, H., 28; 39
Aksornkoae, S., 371, 375; 386

Al-Hasan, R.H., 34; 39
Al-Hussaini, A.H., 169, 183, 199, 206, 207, 208, 211,
212, 223, 231; 262
Albaladejo, V.D., 359; 386
See Carpenter, K.E., 360; 390
Alberte, R.S. See Barlow, R.G., 14, 18; 39
See Prezelin, B.B., 14, 18; 43
Alcala, A.C., 358, 359, 363; 386
See Wells, S.M., 359; 412
See Gomez, E.D., 359; 395
Alden, M. See Thomas, W.H., 44
Aleem, A.A., 376; 386
Alevizon, W.S., 179; 262
See Ebeling, A.W., 264
Alino, P. See Howard, L.S., 353, 361; 397
Alino, P.M., 363; 387
Allakhverdiev, S.I., 34; 39
Allaway, W.G., 374; 387
Allen, M.M. See Evans, E.L., 18; 40
Allen, P.M. See Prigogine, I., 350; 405
Alongi, D.M., 370; 387
See Moriarty, D.J.W., 268
See Robertson, A.L., 368; 406
See Stanley, S.O., 370; 409
Amesbury, S.S., 352; 387
Amir, A. See For, F.D., 365; 405
353
354
Anderson, D.T., 110, 111, 130, 154, 155; 156

See Egan, E.A., 130, 132, 133, 134, 136,141, 144; 159
Anderson, J.M. See Chow, W.S., 13, 21; 40
Anderson, J.W. See Neff, J.M., 353, 354; 403
Anderson, M. See Lund, H., 357; 400
Anderson, T.A., 169, 188, 199, 200, 201, 204, 211, 223,
231; 262
Andre, M. See Brechignac, F., 26; 39
Andrews, J.C., 351, 354, 357; 387
See Williams, D.M., 349, 357 ; 413
Andrews, T.J., 366; 387
See Badger, M.R., 27; 39
See Clough, B.F., 366; 391
Ankel, W.E. See Thorner, E., 113, 115; 164
Anonymous, 320, 339, 341, 350, 362, 364, 372, 384, 385;
328, 387
Ansari, Z.A. See Harkantra, S.N., 160
Antia, N.J. See Stockner, J.G., 19; 43
Antonius, A., 338, 340, 361; 387
Appleby, G., 29; 39
Appleton, C.C., 314; 328
Arenas, J.N., 133; 156
Armstrong, D.A., 306; 328
Armstrong, M.J., 314, 320, 323, 324, 325, 326; 328, 329
See Hampton, L, 323; 332
See Shelton, P.A., 276; 334
Armstrong, N.E. See Odum, H.T., 343; 403
Armstrong, R.A., 350; 387
Arnold, D.C., 137, 146, 152; 156
Arnold, P. See Birtles, A., 380; 388
Ashmole, N.P., 281, 303, 306, 309, 310; 329
Astier, C. See Kirilovsky, D., 34; 41
Atkinson, J.L., 204; 262
Attiwill, P.M. See Clough, B.F., 367, 373; 391
Au, D.W.K., 309; 329
Aurivillius, C.W.S., 119; 156
Austin, C.B. See Thorhaug, A., 378; 410
Avery, G., 291, 293; 329
See Ryan, P.G., 310; 334
See Siegfried, W.R., 281; 334
Avila, E.A., 184; 262
Avise, J.C. See Nergel, J.E., 363; 403
Avron, M., 22; 39
See Ben-Amotz, A., 34; 39
Ayala, F.J. See Valentine, J.W., 344; 411
Ayling, A.M. See Choat, J.H., 179, 180, 253, 255, 259;
263
Ayling, T., 189, 233, 235, 253; 262
Babcock, R.C., 349; 387

See Harrison, P.L., 396
Bablet, J.-P., 356; 387
Bacon, P.R., 147, 372; 156, 387
Badger, M.R., 27; 39
Bagarinao, T. See Comacho, A.S., 370; 391
Bagnis, R., 361; 387
See Yasumoto, T., 413
Bailey, R.D. See Best, B.R., 352; 388
Bain, C.A.R. See Wilson, R.P., 308; 335
Bainbridge, V., 113, 115; 156
Bak, R.P.M., 351; 387
See Dodge, R.E., 392
See Duyl, F.C.van, 55, 68, 77; 87
See Van den Hoek, C., 243; 271
Baker, J.T., 339; 387
Bakun, A. See Parrish, R.H., 273; 333
Bakus, G.J., 168, 170, 234, 239, 251, 254, 256, 258, 259,
260, 343, 344, 364, 383, 384, 385; 262, 388
Balch, W.M., 15; 39
Baldia, J.P. See Pantastico, J.B., 205; 269
Ball, M.C., 366, 367; 388
Ballantine, D.L. See Hinds, P.A., 247, 249; 266
Ballou, T.G. See Getter, C.D., 373;394
Bang, N.D., 276; 329
Banner, A.H., 354, 361; 388
Banus, M.D., 374; 388
Banzon, P.V. See Alino, P.M., 387
Barber, J. See Gounaris, K., 23; 41
Barber, R.T., 319; 329
Bardach, J.E., 237, 259; 262
Barker, M.F., 129, 130, 131, 133, 140; 156
Barlow, G.W., 179, 238, 241, 259, 343; 262, 388
Barlow, R.G., 14, 18; 39
Barnard, K.H., 116, 117, 118, 119, 120; 156
Barnes, D.J., 339, 363, 364; 388
Barnes, H., 93, 94, 95, 122, 123, 124, 125, 126, 127, 128,
133, 134, 135, 137, 138, 139, 142, 143, 144, 145, 146,
148, 149, 150, 151, 152, 153; 156, 157
See Achituv, Y., 128, 132, 146, 150, 154, 155; 156
See Dawson, R.M.C., 150; 159
See Heath, J.R., 100, 101; 160
See Klepal, W., 93, 94, 95; 161
See Munn, E.A., 94; 162
See Stone, R.L., 123, 124, 125, 143; 164
Barnes, M., 91166; 130, 131, 154, 155; 157
See Barnes, H., 93, 94, 95, 122, 123, 124, 125, 126,
127, 128, 133, 134, 135, 137, 138, 139, 142, 143, 144,
145, 146, 149, 150, 151, 152, 153; 157
AUTHOR INDEX
See Klepal, W., 93, 95; 161

Barnes, S.N., 52, 54; 86
Barrett, G.W., 340, 363; 388
Barton, M.G., 182, 188, 199, 207, 208, 214, 230, 235; 262
Bassindale, R., 119, 120, 124, 127; 157
Batchelor, A.L., 287, 297, 298, 303, 309, 310, 312, 314,
324, 326, 327; 329
See Crawford, R.J.M., 315; 331
See Randall, B.M., 280, 281; 333
Bate, C.S., 92; 157
Batham, E.J., 75, 92, 102, 103, 104, 105, 107, 108, 110,
111, 122, 123, 154; 86, 157
Battershill, C.N. See Kingsford, M.J., 256; 267
Battey, J.F. See Porter, J.W., 349; 405
Battistini, R., 347; 388
Bauer, R.T., 378; 388
Baumgart, I.L. See Dahl, A.L., 338, 340, 351, 383; 392
Baxter, C. See Roughgarden, J., 81; 89
Bayless, J.W. See Schonewald-Cox, C.M., 384; 407
Beardall, J., 21, 28, 29; 39
See Burns, B.D., 26, 27, 33; 40
See Richardson, K., 21, 35; 43
Beauchamp, K.A. See Pearse, J.S., 55; 89
Beddington, J.R. See May, R.M., 401
Beer, S., 26, 33; 39
Beers, J.R. See Venrick, E.L., 14; 44
Beets, T. See Rogers, C.S., 406
Bell, J., 360; 388
Bell, J.D., 188, 211, 231, 252; 262
See Burchmore, J.J., 263
Bellwood, D.R. See Choat, J.H., 180, 239, 241, 259; 263
See Clements, K.D., 170, 180, 181, 182, 189, 194, 196,
198, 206, 208, 213, 214, 217, 218, 221, 225; 263
Ben-Amotz, A., 34; 39
Ben-Tuvia, A. See Clark, E., 259; 263
Benente, P. See Frazier, A., 394
Bennell, N., 338; 388
Bennett, I. See Dakin, W.J., 75; 87
Bennett, J. See Sukenik, A., 19, 24, 27; 43
Bergen, M., 148; 157
Bergh, M.O., 320, 322, 324; 329
Berks, R. See Kremer, B.P., 14; 42
Berndt, W., 102, 105, 106; 157
Bernstein, B.B., 252; 262
Berrill, N.J., 45, 46, 47, 48, 49, 52, 54, 55, 57, 58, 60, 62,
63, 64, 65, 66, 67, 69, 70, 75, 80; 86
Berruti, A., 273335;274, 277, 281, 287, 293, 297, 298,
302, 303, 307, 308, 309, 312, 313, 314, 317, 319, 321,
323, 324, 325, 326, 327; 329
355
See Armstrong, M.J., 314, 324; 328

See Cooper, J., 280, 310, 319, 326; 330
See Duffy, D.C., 285, 293, 314, 315, 318, 326; 331,
332
See Matthews, J.P., 287, 293, 294, 296, 298, 315; 333
Berry, C.U. See Berry, H.H., 278, 286, 306; 329
Berry, H.H., 278, 286, 291, 293, 296, 298, 306, 314, 315,
317; 329
See Jensen, R.A.C., 283, 309; 333
Berry, J.A. See Lucas, W.J., 27; 42
Berry, P.F., 174, 256; 262
Berwick, N.L., 384; 388
Best, B.R., 352; 388
Betterton, C. See De Silva, M.W.R.N., 358; 392
Betzer, S. See Johannes, R.E., 342, 344, 345, 346, 356;
398
Beyers, R.J. See Odum, H.T., 343; 403
Bibby, J.M. See Coles, R.G., 391
Bidwell, R.G.S., 26, 33, 37; 39
Bienfang, P.K., 14; 39
See Laws, E.A., 42
Bigelow, M.A., 112; 157
Biggley, W.H. See Rivkin, R.B., 38; 43
Bildstein, K. See Dame, R., 392
Bilyard, G.R. See Pastorok, R.A., 340, 345, 351, 354,
355, 363; 404
Bingham, B.L. See Young, C.M., 73; 90
Birch, D.G. See Weger, H.G., 36; 44
Birch, M. See Birch, W.R., 346, 377; 388
Birch, W.R., 346, 377; 388
Bird, E.C.F., 351; 388
Birkeland, C., 246; 262
Birkeland, C.E., 339, 345, 349, 353, 354, 358, 361, 362,
377, 379, 380; 388
See Gomez, E.D., 395
Birkhead, T.R. See Furness, R.W., 309, 310; 332
Birmingham, B.C., 33; 39
Birt, T.P. See Birt, V.L., 329
Birt, V.L., 309; 329
Birtles, A., 380; 388
Bishop, M.W.H., 132; 157
Bjorkland, M.I., 384; 388
Bjrkman, O., 13, 17, 19, 21; 39
Bjorndal, K.A., 204, 226, 233, 377; 262, 263, 388
See Thayer, G.W., 271, 409
Bjrnsen, P.K., 34; 39
Blaber, S.J.M., 370; 388
Blaber, T.G. See Blaber, S.J.M., 370; 388
356
Blackstock, J. See Barnes, H., 150; 157

Blanchet, C., 364, 384; 388
Blasco, F., 365; 388
Blaszczyk, M. See Prejs, A., 205; 269
Blaxter, J.H.S., 254, 344; 263, 389
Blick, R.A.P. See Wisely, B., 110, 111, 126, 128, 129,
130, 131, 133, 134, 135, 138, 140, 141, 144; 165
Blom, S.-E., 95, 139, 144, 146; 157
Boan, P.I. See Moriarty, D.J.W., 402
Boardman, N.K., 13, 17, 20, 21; 39
Bocquet-Vdrine, J., 91, 92, 94, 96, 98, 99; 157, 158
Bodoy, A. See Plante-Cuny, M.-R., 14; 43
Boecklen, W.S., 385; 389
Bogdanova, N.N. See Khristoforova, N. K., 353; 398
Bger, P. See Scherer, S., 37; 43
Bogorov, B.G., 343; 389
Bohnsack, J.A., 349; 389
Bokenham, N.A.H., 126, 131, 135; 158
Bolton, J. See Jupp, D.B.L., 398
Bonin, D.J. See Leftley, J.W., 17; 42
Bonner, R.R. See Johnson Jr, T.W., 148; 161
Booker, F. See Thorhaug, A., 378, 379; 410
Bookhout, C.G. See Costlow Jr, J.D., 136, 138, 144; 158
Booyanate, P. See Chansang, H., 351, 360; 390
Borowitzka, M.A., 236, 242, 244; 263
Bortone, S.A., 346; 389
Boschma, H., 97, 98, 99, 100; 158
See Van Kampen, P.N., 97; 165
Bosman, A.L., 323; 329
Boto, K.G., 352, 367, 368, 369; 389
See Clough, B.F., 367, 373; 391
See Robertson, A.I., 406
See Stanley, S.O., 370; 409
Boucher, D. See Scoffin, T.P., 270, 407
Boucher, L.M., 361; 389
Bouchon, C., 363; 389
Bouchon-Navaro, Y., 180, 238, 239, 241, 259; 263
See Bouchon, C., 363; 389
Boulon, R., 350; 389
Bour,W., 383; 389
See Joannot, P., 359; 397
Bousfield, E.L., 143; 158
Bowen, S.H., 191, 192, 218, 232; 263
Boyd, A.J., 276; 329
Boyd, S. See Dodge, R.E., 392
Boye, M. See Koechlin, J., 383; 399
Boyer, D. See Loutit, R., 317; 333
Boyle, E.A. See Shen, G.T., 353; 408
Boyle, M.-J. See Hughes, T.P., 244; 266

Boynton, W.R., 12; 39
Boyonete, R.P. See Alino, P.M., 387
Bradbury, R.H., 239, 338, 347, 348, 349, 350, 357, 362,
384; 263, 389
See Green, D.G., 350; 395
See Reichelt, R.E., 349, 363; 405
Braithwaite, L.F. See Young, C.M., 53, 57, 68, 69, 70, 75,
77; 90
Branch, G.M., 141, 274; 158, 329
See Bosman, A.L., 323; 329
Brandani, A. See Sorenson, J., 382; 409
Brander, K.M. See Walley, L.J., 94; 165
Brandt, C.L. See Lambert, C.C., 49, 57, 58; 88
Branscomb, E.S., 137, 138; 158
Brawley, S.H., 247; 263
Bray, R.A. See Randall, R.M., 317; 333
Bray, R.N., 252; 263
See Ebeling, A.W., 181; 264
Brechignac, F., 26; 39
Breeman, A.M. See Ruyter van Steveninck, E.D.de, 243;
270
See Van den Hoek, C., 243; 271
Breeman, L.van, 139, 146; 158
Brett, J.R., 170, 199, 215, 344; 263, 389
Brewin, B.I., 46, 50; 86
Bridges, K.W.; 377; 389
Briggs, J.C., 281; 329
Briggs, K.T., 285, 305, 321, 328; 329
Bright, T.J., 339, 348; 389
See Gittings, S.R., 357; 394
Brittan, C. See Cambridge, M.L., 390
Britton, P.L. See Cooper, J., 277, 311, 321; 330
Broadus, J.M., 383; 389
Broch, H., 110, 111, 113; 158
Brock, R.E., 243, 259; 263
See Smith,. S.V., 408
Broekhuysen, G.J., 308; 329
Broni, S.C., 304, 307, 318; 329
See Duffy, D.C., 332
Brooke, R.K., 277, 278, 280, 281, 283, 286, 287, 291, 307,
311, 319; 329, 330
See Clancey, P.A., 277; 330
See Cooper, J., 274, 280, 310; 330
See Crawford, R.J. M., 280; 331
Broom, M.J. See Lee, Y.S., 373; 399
See Seow, R.C.W., 373; 408
AUTHOR INDEX
Brostoff, W.N. See Hixon, M.A., 243, 246, 247, 248, 249;
265
Browder, J.A., 368; 389
Brown, A.C., 274; 330
Brown, B.E., 338, 340, 345, 346, 350, 351, 352, 353, 354,
355, 362, 363; 389
See Howard, L.S., 340; 397
Brown, J.S., 23; 39
Brown, P.C., 276; 330
Brown, R. See Ogden, J.C., 243, 378; 268, 403
Bruce, D. See Popovic, R., 23; 43
Bruck, K. See Holdsworth, E.S., 28; 41
Bryan, P.G., 184, 185, 202, 214, 216, 223, 359; 263, 389
See Tsuda, R.T., 184; 271
Buchholz, H.von, 139; 158
Buckland-Nicks, J. See Chia, F.-S., 46, 60; 86
Buckman, N.S., 171; 263
See Ogden, J.C., 171, 179, 237, 241; 268
Buddemeier, R.W., 340, 348; 390
Buddington, R.K., 204, 208, 215, 229, 230, 231, 232; 263
See Karasov, W.H., 229; 267
Buikema, A.L. See Cairns, J., 340, 352; 390
Bull, G.D. See Babcock, R.C., 387
Bunt, J.S., 12; 40
See Boto, K.G., 367, 368, 369; 389
See Wolanski, E., 369, 373; 413
Burbridge, P.R., 383, 384; 390
Burch, B.L., 346; 390
See Devaney, D.M., 339; 392
Burch, T.A. See Burch, B.L., 346; 390
Burchmore, J.J., 169, 173, 180, 252, 253, 254, 256; 263
See Bell, J.D., 188, 211, 231, 252; 262
Burdon-Jones, C. See Denton, G.R.W., 352, 353; 392
Burge, R. See Elston, R.A., 99; 159
Burger, A.E., 304, 319; 330
See Frost, P.G.H., 317; 332
See Williams, A.J., 291; 335
Burke, R.D., 46; 86
Burns, B.D., 26, 27, 33; 40
Burns, T.P., 342, 349; 390
Burris, J.E., 14, 33, 37; 40
Butler, A.J., 74; 86
See Kay, A.M., 84; 88
Butman, C.A., 75, 196; 86, 263
Butterworth, D.S., 324; 330
Buys, M.E.L. See Shannon, L.V., 275; 334
Byrne, J.E., 341; 390
Cabanban, A.S., 364, 383; 390

Cai Rusing, 140, 152; 158
Cairns, D.K. See Birt, V.L., 329
Cairns, J., 340, 352; 390
Caldwell, M.M., 35; 40
Callan, H.G., 92; 158
Calow, P. See Sibly, R.M., 208; 270
Cambridge, M.L., 378; 390
Cameron, A.M., 344, 348; 390
See Endean, R., 338; 393
Campbell, D.G., 352; 390
Campbell, L. See Przelin, B.B., 18; 43
Cancino, J.M., 234; 263
Canvin, D.T. See Lloyd, N.D.H., 33; 42
See Yokota, A., 27; 44
Carey, J., 352; 390
Carleton, J.H. See Sammarco, P.W., 237, 246; 270
Carpelan, L.H. See Linsley, R.H., 146; 162
Carpenter, K.E., 360; 390
Carpenter, R.C., 244, 245, 338, 349; 263, 390
Carter, R.A., 276; 330
Carter, R.M. See Baker, J.T., 339; 387
Cashman, C.W. See Bright, T.J., 339, 348; 389
Cassie, R.M., 14; 40
Castilla, J.C., 251; 263
See Cancino, J.M., 234; 263
Castle, W.E., 69; 86
Castro, R. See Kolehmainen, S., 374; 399
Cavey, M.J. See Cloney, R.A., 52; 86
Chamberlain, R. See Berwick, N.L., 384; 388
Chan, H.T., 371; 390
See Smith III, J.T., 365; 408
Chandler, E.R. See McMeekin, T.A., 42
Chanpongsang, C. See Windom, H.L., 413
Chansang, H., 351, 360; 390
Chapman, A.R.O., 236, 258; 263
Chapman, P., 274; 330
Chapman, V.J., 339, 341, 364; 390
Chappell, J., 347; 390
Charles, J.K. See Chua, T.E., 340, 341, 383; 391
Charnov, E.L. See Pyke, G.H., 190; 269
Chartock, M.A., 200; 263
Charuchinda, M. See Chansang, H., 351, 360; 390
Chase, J.A. See Jones, R.S., 239, 259; 267
Chavan, S.A., 384; 390
Chavez, F.P. See Barber, R.T., 319; 329
Chen, J.W. See Buddington, R.K., 215, 229; 263
Chen, X. See Yan, W., 140; 166
Chernin, M.I. See Marsh, J.A., 355; 401
357
358
Chernoff, H., 64; 86

Chesher, R., 347, 358, 359, 361, 383; 390
Chess, J.R. See Hobson, E.S., 222; 265
Cheste, R. See Riley, J.P., 342; 406
Chet, I. See Mitchell, R., 361; 402
Cheung, P.J., 94; 158
See Coln-Urban, R., 113, 116; 158
Chevalier, J.P. See Salvat, B., 407
Chia, F.-S., 46, 60, 65; 86
See Lewis, C.A., 121, 122, 123, 152; 162
See Young, C.M., 59, 67, 73, 80, 82, 83; 90
Chia, F.S., 48, 63; 86
Chia, L.S., 340; 390
Chiffings, A.W. See Cambridge, M.L., 390
See Silberstein, K., 378; 408
Child, C.M., 47, 60; 86
Choat, H., 339; 390
Choat, J.H., 169, 170, 179, 180, 239, 241, 251, 253, 254,
255, 259; 263
See Robertson, D.R., 344; 406
See Schiel, D.R., 174, 256; 270
Choi, D.R., 351; 390
Chong, E.K., 371; 390
Choudhury, R.A., 375; 390
Chow, W.S., 13, 21; 40
Christensen, M.S., 187, 207, 214; 263
Chrzanowski, T. See Dame, R., 392
Chu, E.W. See Briggs, K.T., 285; 329
Chua, T.E., 340, 341, 383; 391
Chye, H.S. See Seng, L.T., 407
Cimberg, R.L., 121, 144, 152; 158
Cintron, G., 346, 366; 391
See Jimenez, J.A., 366, 372; 397
See Martinez, P., 371; 401
Clancey, P.A., 277, 280; 330
Clark, C.W. See May, R.M., 401
Clark, E., 259; 263
Clark, J.R. See Salm, R.V., 339, 340; 407
Clarke, L.D., 265; 391
Clarke, T.A., 179; 263
Clegg, D.J. See Crisp, D.J., 134; 158
Cleland, M.G. See Robertson, D.R., 171; 270
Clements, K.D., 170, 179, 180, 181, 182, 189, 194, 196,
198, 206, 207, 208, 211, 213, 214, 217, 218, 221, 224,
225, 234; 263
Clinning, C.F., 280, 281, 283, 286, 290, 291, 306; 330
See Whitelaw, D.A., 277; 335
Cloney, R.A., 45, 46, 49, 51, 52, 53, 60, 65, 74, 78; 86
See Robinson, W.E., 52; 89

See Torrence, S.A., 52, 53, 54, 67, 78; 89
Cloud Jr, P.E., 237; 263
Clough, B.F., 339, 366, 367, 373; 391
Coats, D.W., 14, 18; 40
Codreanu, R., 95, 99; 158
Coetzee, D.J., 225; 263
Coffroth, M.A., 351, 356; 391
Coker, R.E., 116; 158
Colbeck, J. See Appleby, G., 29; 34
See Holdsworth, E.S., 29; 41
Colblentz, B.E., 309; 330
Colbow, K. See Popovic, R., 23; 43
Colburn, T. See Hay, M.E., 242; 265
Colby, D.R. See Thayer, G.W., 367; 409
Colclough, J. See Armstrong, M.J., 314, 324; 328
See Berruti, A., 312, 313, 324, 325, 327; 329
Coleman, J.R. See Birmingham, B.C., 33; 39
Coleman, N., 253; 263
Coles, R.G., 376, 377; 391
Coles, S.L., 355, 356, 361; 391
Colin, P.L. See Thresher, R.E., 239, 254; 271
Collar, N.J., 308; 330
Collette, B.B., 225, 368; 264, 391
Collier, W.L. See Chia, L.S., 340; 390
See Librero, A.R., 340; 400
Collins, L.A. See Lindall Jr, W.N., 367; 400
Collins, M.R., 182, 208, 223, 224; 264
Colman, B., 26, 27, 33; 40
See Birmingham, B.C., 33; 39
See Cook, C.M., 26, 33; 40
Coln-Urban, R., 113, 116; 158
Comacho, A.S:, 370; 391
Compagno, L.J.V. See Randall, B.M., 318; 333
Conacher, M.J., 201, 253, 259; 264
Conklin, E.G., 46, 57; 86
Connell, A.D. See Gardner, B.D., 319; 332
See Ryan, P.G., 310, 319; 334
Connell, J.H., 74, 81, 82, 146, 247, 250, 347, 348, 349,
358; 86, 158, 264, 391
Conover, R.J., 204; 264
Conte, E., 347, 383; 391
Contreras, G.T. See Stefoni, D.L., 133, 141; 164
Cook, C.M., 26, 33; 40
Cook, P.A., 145; 158
Cooper, J., 274, 277, 278, 280, 281, 283, 285, 287, 291,
293, 296, 297, 300, 301, 302, 303, 306, 307, 310, 311,
313, 314, 315, 317, 318, 319, 320, 321, 322, 326; 330
AUTHOR INDEX
See Brooke, R.K., 280, 286, 287, 291, 307, 311, 319;
329
See Burger, A.E., 319; 330
See Crawford, R.J.M., 280, 281, 311; 331
See Duffy, D.C., 285; 331
See Furness, R.W., 314, 320, 321, 322; 332
See Harper, P.C., 286, 288, 304; 332
See Hockey, P.A.R., 274; 332
See La Cock, G.D., 317; 333
See Morant, P.D., 319; 333
See Randall, R.M., 315; 334
See Ryan, P.G., 277, 280, 304; 334
See Shelton, P.A., 281, 312; 334
See Walter, C.B., 286, 290, 291, 308, 326; 335
See Whitelaw, D.A., 277; 335
See Williams, A.J., 287, 291, 292, 293, 306; 335
Corcoran, E. See Glynn, P.W., 353; 394
Comic, G. See Powles, S.B., 31; 43
Corpuz, V.T. See Albaladejo, V.D., 359; 386
See Carpenter, K.E., 360; 390
Costlow Jr, J.D., 136, 138, 148; 158
See Barnes, H., 137; 157
See Crisp, D.J., 148; 158
See Fyhn, U.E.H., 95; 159
Coulson, J.C. See Aebischer, N.J., 318; 328
Cowans, I.R. See Clough, B.F., 366; 391
Cowey, C.B., 231; 264
See Tacon, A.G.J., 231; 271
Cox, G.J. See Ayling, T., 189, 233, 235, 253; 262
Craft, L.L. See Palmisano, A.C., 42
Craigie, J.S., 193; 264
Craik, G.J.S., 359; 391
Craik, W. See Gilmour, A., 383; 394
Cram, D.L., 298, 313; 330
Cramp, S., 291; 330, 331
Crawford, C. See Grove, D.J., 215; 265
Crawford, P.B. See Crawford, R.J.M., 314; 331
Crawford, R.J.M., 273, 274, 275, 276, 280, 281, 287, 291,
292, 293, 294, 295, 296, 297, 298, 302, 303, 308, 310,
311, 312, 313, 314, 315, 317, 318, 319, 320, 321, 324,
326, 327; 331
See Brooke, R.K., 280; 329
See Cooper, J., 280, 310; 330
See Newman, G.G., 324; 333
See Shelton, P.A., 281, 291, 312; 334
359

Crawley, M.J., 168; 264
Crewz, D.W. See Lewis, R.R., 367; 400
Crisp, D.J., 54, 56, 63, 66, 67, 68, 69, 80, 81, 92, 94, 95,
127, 128, 130, 131, 132, 133, 134, 138, 139, 142, 143,
144, 145, 146, 147, 148, 149, 152, 153, 154; 86, 158
See Barnes, H., 93, 94, 124; 157
See Jones, L.W.G., 139; 161
See Lucas, M.I., 150, 153; 162
See Morris, E., 139; 162
See Patel, B., 94, 112, 113, 136, 138, 142, 145, 153;
163
Cronin, L.E., 339; 391
Crosby, D.G. See Howard, L.S., 353, 361; 397
Crossland, C.J., 340, 358; 391
See Johannes, R.E., 354; 398
Crowe, T.M. See Clancey, P.A., 277; 330
See Guillet, A., 278; 332
Croxall, J.P., 284, 309, 310; 331
See Harper, P.C., 286, 288, 304; 332
Cruickshank, R.A. See Crawford, R.J.M., 291; 331
Cubit, J.D. See Griffith, P.C., 363; 395
See Lessios, H.A., 245; 267
Cullen, J.J., 15; 40
Culver, D.A. See Lloyd, N.D.H., 33; 42
Curtis, C., 357, 363; 391
Cushing, D.H., 273; 331
Czygan, F.-C. See Demmig, B., 34; 40
DAgostina, A. See Landau, M., 138, 142; 161
Dabrowski, K., 232; 264
Dahl, A.L., 241, 243, 338, 340, 341, 346, 347, 350, 351,
362, 364, 383, 384; 264, 391, 392
Dakin, W.J., 75; 87
Dalby Jr, J. See Young, C.M., 90
Dalley, R., 116; 158
Damas, D., 52; 87
Dame, R., 368; 392
Daniel, A., 144, 147, 148; 159
Daniel, P. See Klumpp, D.W., 234, 245; 267
Daniel, P.A. See Robertson, A.I., 368, 370, 380; 406
Daniels, R.A., 257; 264
Dartnall, A.J. See Field, C.D., 339, 341; 393
Darwin, C., 92, 103, 107, 108, 109, 112, 113, 115, 122,
123, 124, 154; 159
Das, V.S.R. See Ramachandra Reddy, A., 27; 43
Daturi, A., 317, 319; 331
David, J.H.M., 320; 331
360
Davie, J.P.S. See Saenger, P., 340, 364, 370; 407

Davies, D.H., 274, 287, 291, 293, 297, 300, 301, 302,
303, 312, 320, 322, 327; 331
Davies, G.R., 377; 392
Davies Jr, J.H., 365; 392
Davies, P.A. See Crisp, D.J., 146; 158
Davies, P.J., 340, 347; 392
See Symonds, P.A., 348; 409
Davies, P.S. See Kinsey, D.W., 354; 398
Davis, A.R., 53, 58, 74, 80, 82, 83; 87
Davis, G.E., 350, 357, 358, 384, 385; 392
Davis, M. See Lund, H., 357; 400
Dawson, R.M.C., 150; 159
Day, J.H., 99, 100, 343; 159, 392
Day Jr, J.W. See Yanez-Arancibia, A., 367; 413
Day, J.W. See Soberon-Chavez, G., 408
Day, R.W., 75, 243, 244; 87, 264
Dayton, P.K., 85, 92, 132; 87, 159
De Klerk, L.G. See Wijsman-Best, M., 360, 382; 413
De Kock, A.C., 277, 291, 319; 331
De Silva, M.W.R.N., 338, 358, 383; 392
De Silva, S.S., 204; 264
De Villiers, G. See Shelton, P.A., 291; 334
De 1a Cruz, A.A., 372; 392
Debiard, J.P. See Frazier, A., 394
Deegan, L.A. See Soberon-Chavez, G., 408
DeKruijf, H. See Elgershuizen, J.H.B.W., 353; 393
Delage, Y., 96, 97, 99, 100; 159
Delaney, M.E., 15, 24, 27; 40
Delesalle, B., 339; 392
See Poli, G., 404
Delsman, H.C., 344; 392
Demers, S. See Legendre, L., 16; 42
See Rochet, M., 14; 43
See Sakshaug, E., 34; 43
Demeter, S., 34; 40
Demment, M.W., 236; 264
Demmig, B., 34; 40
Denley, E.J., 130, 131; 159
See Underwood, A.J., 81; 89
Denman, K.L. See Forbes, J.R., 14; 40
Dennett, M.R. See Gilbert, P.M., 14; 41
Dennison, W.C., 376; 392
Denton, G.R.W., 352, 353; 392
DePalma, I.P. See Lohrenz, S.E., 42
Descolas-Gros, C., 28; 40
See Mortain-Bertrand, A., 14, 31; 42
Dessenoix, C., 127, 139, 140; 159
Dettman, K.F. See Briggs, K.T., 305; 329
Devaney, D.M., 339; 392

Devereux, M.J. See Barnes, D.J., 363, 364; 388
Dewling, R.T. See OConnor, J.F., 363; 403
Dexter, D., 343; 392
Dhanarajan, G. See Gong, W.K., 371; 395
Diamond, J. See Buddington, R.K., 215, 229; 263
Diamond, J.M., 385; 392
See Karasov, W.H., 229; 267
Dicks, B., 353, 373; 392
Dietz, K.-J., 13, 21; 40
See Heber, U., 12, 21; 41
Dilly, P.N., 54, 69; 87
Dineen, J.F., 122, 123; 159
DiTullio, G.R. See Laws, E.A., 12; 42
Diviacco, G. See Relini, G., 139, 148; 163
Dixon, G.K., 26, 27; 40
Dixon, P. See Robertson, A.I., 370; 406
Djaja, B. See Jhamtani, H.P., 376; 397
Doak, W., 181, 182, 253; 264
Dodge, R.E., 340, 353, 354, 363; 392
See Knap, A.H., 399
Doe, P.E. See McMeekin, T.A., 42
Doherty, P.J., 179, 349, 362; 264, 393
See Sale, P.F., 407
Dhler, G., 35; 40
Doi, T., 369; 393
Dokemascolo, G. See Mancuso, V., 52; 88
Dollar, S.J., 346, 349, 352, 357, 358, 361; 393
Dolsen, C.P. See Spackman, W., 365; 409
Don, P.A. See Uys, C.J., 314; 335
Done, T.J., 347, 349; 393
Dor, I. See Por, F.D., 339; 405
Doty, J.E. See Marsh, J.A., 355; 401
Douglas, A.E. See Smith, D.C., 226; 270
Douglas, R.G. See Stehli, F.G., 344; 409
Douglas, W.A. See Sale, P.F., 407
Douglass, J. See Robins, C.R., 235; 270
Dow, M.A. See Maragos, J.E., 383; 401
Dowle, J.E. See Cooper, J., 285; 330
Downes, B.J. See Keough, M.J., 74, 80, 82, 83; 88
Downing, D. See Hay, M.E., 242; 265
Downing, N., 349; 393
Downton, W.J.S., 366; 393
Drew, E.A., 344, 380; 393
Dring, M.J., 12, 15, 34, 35; 40
Du Toit, J.T. See Bosman, A.L., 323; 329
Dubinsky, Z., 24, 339; 40, 393
Dudley, S.F.J., 325, 326; 331
Dubois, J.P. See Bird, E.C.F., 351; 388
AUTHOR INDEX
Ducklow, H. See Mitchell, R., 338;402

See Segel, C.A., 361; 407
Duclaux, G. See Lafargue, F., 59; 88
Duffy, D.C., 275, 284, 285, 287, 293, 296, 298, 301, 302,
303, 304, 306, 307, 308, 309, 310, 311, 312, 314, 315,
318, 319, 320, 321, 322, 323, 325, 326, 327; 331, 332
See Furness, B.L., 293; 332
See Hockey, P.A.R., 274; 332
See La Cock, G.D., 317; 333
See Laugksch, R.C., 321, 322; 333
See Schneider, D.C., 284, 328; 334
See Wilson, R.P., 274, 298, 307, 308, 318; 335
Duffy, J.E. See Hay, M.E., 188; 265
See Paul, V.J., 269
Duke, N.C. See Robertson, A.I., 368, 369, 370; 406
See Smith III, T.J., 365; 408
Dunning, M.C. See Blaber, S.J.M., 370; 388
Dustan, P., 347, 350, 358, 361; 393
Dutt, S., 344; 393
Dutton, I.M. See Kelleher, G.G., 360; 398
Duyl, F.C.van, 55, 56, 59, 64, 68, 69, 77; 87
Dwyer, P.D., 385; 393
Dybern, B.I., 69, 70, 80, 81, 83, 84; 87
Dyer, B.M. See Crawford, R.J.M., 310; 331
Eagle, R.J. See Noshkin, V.E., 356; 403
Eakin, C.M., 251; 264
Eakin, R.M., 54; 87
Earle, S.A., 171, 182, 241, 242, 243, 250, 251, 254, 260;
264
Eastman, R.C., 150; 159
Ebeling, A.W., 181, 238, 259; 264
See Bray, R.N., 252; 263
See Harris, L.G., 195; 265
Eckert, G.J. See Sale, P.F., 407
Eckman,J. E., 377; 393
Edwards, G.E. See Kobza, J., 13, 27; 41
See Usuda, H., 13, 19; 44
Edwards, R.R.C., 344; 393
Edwards, T.W., 169, 203, 204, 217, 220; 264
See Horn, M.H., 169, 182, 188, 194, 198, 230, 235,
255, 257;266
Eernisse, D.J. See Pearse, J.S., 55; 89
Egan, E.A., 130, 132, 133, 134, 136, 141, 144; 159
Eisenberg, J.F., 234; 264
Eisler, R., 353; 393
El-Rayis, O.A., 354; 393
El-Zahr, C.R. See Downing, N., 349; 393
361
Eldredge, L.G., 340, 341, 346, 349, 351, 359, 360; 393
See Randall, R.H., 349; 405
Eldridge, P. See Thomas, W.H., 44
Elgershuizen, J.H.B.W., 353; 393
Elliot, M.E. See Maragos, J.E., 347, 383; 401
Elofsson, R. See Hallberg, E., 92; 160
Elrifi, I.R. See Weger, H.G., 36; 44
Elston, R.A., 99; 159
Emanuelsson, H., 54; 87
Emerson, W.K. See Moyer, J.T., 361; 402
Emery, A.R., 185, 207, 235; 264
Emlet, R.B., 63; 87
Emmerson, D.K., 380, 381, 382; 393
Emmerson, K. See Le Grand, G., 283, 284; 333
Emson, R.H. See Strathmann, R.R., 48; 89
Encarnacion, L.A. See Martinez, P., 371; 401
Endean, R., 338; 393
Engel, W. See Schmidtke, J., 49; 89
Enticott, J., 309; 332
Eppley, R.W., 14, 18, 19, 20, 344; 40, 393
See Laws, E.A., 42
See Strickland, J.D.H., 25; 43
Eppley, Z.A. See Hunt Jr, G.L., 309; 332
Erasmus, T. See Randall, R.M., 317; 334
Eschmeyer, W.N., 188, 235, 257; 264
Eshel, A. See Beer, S., 26; 39
Estes, J.A., 193, 195, 197, 225, 227, 256, 258; 264
tienne, A.-L. See Kirilovsky, D., 34; 41
Evans, C. See Maragos, J.E., 355; 401
Evans, C.W., 355, 358; 393
See Holthus, P.F., 349, 363; 397
Evans, E.L., 18; 40
Evans, F., 112, 113, 115; 159
Evans, J.R., 19, 21; 40
See Terashima, I., 13, 27; 43
Evans, J.T. See Reinhard, E.G., 97; 163
Evans, L.V. See Kerby, N.W., 28; 41
Evans, P.G.H., 309; 332
See Croxall, J.P., 284, 310; 331
Evens, R. See Barnes, H., 150; 157
Everest, S.A., 28; 40
Every, B., 280, 317; 332
Fable, W.A. See Lindall Jr, W.N., 367; 400
Fairbridge, R. See Revelle, R., 342, 344; 406
Fairweather, P.G. See Underwood, A.J., 75; 89
Falanruw, M.V.C., 338, 351, 352; 393
Falkowski, P., 17; 40
See Sukenik, A., 19, 24, 27; 43
362
Falkowski, P.G., 14, 18, 19, 23, 24, 34, 37, 38; 40
See Boynton, W.R., 39
See Dubinsky, Z., 24; 40
Fnge, R., 170, 193, 198, 206, 215; 264
Fankboner, P.V., 342; 393
Farquhar, G.D. See Ball, M.C., 366; 388
See von Caemmerer, S., 21; 44
Fasciana, C. See Relini, G., 138, 139, 148; 163
Faulkner, D.J. See Gomez, E.D., 92; 159
Faure, G., 342, 361; 393
Feare, C.J., 310; 332
Feldman, J., 343; 393
Fell, J.W., 369; 393
Feng, M.C. See Lai, H.C., 340, 374; 399
Fenical, W. See Hay, M.E., 169, 170, 185, 188, 194, 196,
258; 265
See Paul, V.J., 194; 269
See Sun, H.H., 194; 271
Fenical, W.H. See Norris, J.N., 195; 268
Fernando, A.S., 147; 159
Ferraris, R.P., 229; 264
Ferrell, D.J. See Sale, P.F., 407
Fesquet, J.M. See Le Gall, J.Y., 345; 399
Feyling-Hanssen, R.W., 137, 143, 150; 159
Field, B., 84; 87
Field, C.D., 339, 341; 393
Field, J.G. See Bergh, M.O., 320, 322; 329
Findley, L.T. See Thomson, D.A., 188; 271
Finlayson, D.M. See Barnes, H., 95, 143, 146; 157
Finn, J.T. See Odum, E.P., 363; 403
Finney, C.M. See Landau, M., 138, 142; 161
Fish, G.R., 206, 218; 264
Fishelson, L., 171, 181, 191, 227, 353, 361; 264, 394
See Rutman, J., 343; 407
Fisher, E. See Goodbody, I., 74; 87
Fisher, J.S. See Fonseca, M.S., 376; 394
Fitt, W.K. See Mitchell, W.C., 353; 402
Fitz, H.C. See Rogers, C.S., 347; 406
Fitzhardinge, R.C., 342, 356; 394
Fitzwater, S.E. See Martin, J.H., 15; 42
Flagg, W. See Scholander, P.F., 344; 407
Fleischhacker, P., 21; 40
Fleming, R.H. See Sverdrup, H.U., 342; 409
Fletcher, E.A. See Robertson, D.R., 171; 270
Flight, W.F.G. See Jansen, W.F., 54; 88
Fogg, G.E., 33; 40
See Al-Hasan, R.H., 34; 39
Fonseca, M.S., 376, 378, 379; 394
Fontugne, M.R. See Descolas-Gros, C., 28; 40
Forbes, J.R., 14; 40

Fosberg, F.R., 372; 394
Foster, B.A., 92, 128, 129, 130, 131, 132, 133, 134, 140,
141, 143; 159
Foster, M.S., 179, 251, 252; 264
Foster, S.A., 171, 179, 244, 247, 357; 264, 394
Fowler, G.H. See Stebbing, T.R.R., 112, 115; 164
Fox, W.W. See Huntsman, G.R., 340; 397
Foxon, G.E.H., 99, 100; 159
Fraenkel, G.S., 66; 87
Franck, D. See Frazier, A., 394
Franz, E.H. See Odum, E.P., 363; 403
Frazier, A., 351; 394
Freay, A.D. See Glynn, P.W., 353; 394
Frith, H.R. See Dodge, R.E., 392
See Knap, A.H., 399
Frost, P.G.H., 274, 306, 317; 332
See Randall, R.M., 315; 334
Fry, B., 378; 394
Frydl, P., 237; 265
See Scoffin, T.P., 270, 407
Fu, C.F., 20; 40
Fujimaki, N. See Yanagimachi, R., 96, 97; 166
Fujimoto, K. See Yasumoto, T., 413
Fujita, Y. See Falkowski, P.G., 34; 40
See Mimuro, M., 18; 42
See Suzuki, R., 17; 43
Fukuyo, Y. See Yasumoto, T., 413
Furnas, B.N. See Nixon, S.W., 403
Furnas, M.J., 14; 40
See Andrews, J.C., 357; 387
Furness, B.L., 289, 291, 293, 303, 304, 305, 309; 332
Furness, R.W., 274, 309, 310, 314, 320, 321, 322; 332
Furuya, K., 14; 40
Fyhn, U.E.H., 95; 159
Gabbott, P.A. See Tooke, N.E., 145; 164
Gabrie, C., 351, 358, 363; 394
See Delesalle, B., 392
See Poli, G., 404
Gagliardi, D. See Young, C.M., 90
Gaines, A.G. See Broadus, J.M., 383; 359
Gaines, S.D., 169, 170, 196, 236, 242, 251, 257, 260; 265
See Lubchenco, J., 170, 236, 243, 244, 251; 267
See Robertson, D.R., 238; 269
Galzin, R., 259, 351, 352, 360, 361; 265, 394
See Bell, J., 360; 388
AUTHOR INDEX
See Salvat, B., 407

Ganapati, P.N., 147; 159
Ganti, S.S. See Kalyanasundaram, N., 135; 161
Gaonkar, S.N., 110, 111, 127, 128, 130, 131, 135, 136,
141; 159
Gardiner, R. See Wolanski, E., 369; 413
Gardner, B.D., 319; 332
See Ryan, P.G., 310, 319; 334
Garge, A. See Singh, V.P., 370; 408
Garland, C.D. See McMeekin, T.A., 42
Garside, C. See Balch, W.M., 15; 39
See Legendre, L., 42
Garside, E.T., 343; 394
Garstang, S.L. See Garstang, W., 54; 87
Garstang, W., 54; 87
Gates, J.E. See Weinstein, M.P., 205; 271
Gaus, R.R., 363; 394
Gaut, V.C. See Munro, J.L., 344; 402
Gawel, M., 383, 384; 394
Gearing, J.N. See Rodelli, M.R., 406
Gearing, P.J. See Rodelli, M.R., 406
Gedney, R.H., 368; 394
Geevarghese, C., 207, 211; 285
Gehl, K.A. See Colman, B., 26, 33; 40
Geider, R.J., 18, 19, 34, 37, 38; 40
See Osborne, B.A., 24; 42
See Smith, R.E.H., 37; 43
Genthe, K.W., 105; 159
Gentien, P. See Andrews, J.C., 354; 387
Geoghegan, T., 340, 364, 383; 394
George, A.I., 98; 159
George, M.J., 99; 159
Geraci, S., 135, 138, 140; 159
Gerard, V.A., 37; 40
Gerking, S.D., 187, 203, 204, 205, 214, 215, 216; 265
See Montgomery, W.L., 182, 192, 193, 194, 199, 201,
202, 204, 258; 268
Gerodette, T. See Montgomery, W.L., 243; 268
Gessner, F., 343, 344; 394
Getter, C.D., 373; 394
Gherardi, M. See Lepore, E., 95, 138, 140; 161
Ghiselin, M.T., 94; 159
Ghobashy, A.F.A.A. See Crisp, D.J., 54, 56, 63, 66, 67,
68, 69, 80, 81; 86
Gibbs, M. See Fu, C.F., 20; 40
See Kelly, G.J., 27; 41
Gibson, J. See Goodbody, I., 82; 87
Gibson, R.N., 173, 198, 256; 265
Giebel, P.E. See Weinstein, M.P., 205; 271
363
Giese, A.C., 343, 344; 394

Gieskes, W.W., 14, 15, 16; 40
Gilboa-Garber, N., 150; 159
Gillan, F.T. See Stanley, S.O., 370; 409
Gilmore, R.G. See Lewis, R.R., 367; 400
Gilmour, A., 383; 394
Gilnak, M. See Rogers, C. S:, 347; 406
Ginsburg, R.N., 348; 394
Giordano, E. See Relini, G., 135, 138, 140; 163
Gittings, S.R., 357; 394
Gladfelter, E. See Lund, H., 357; 400
Gladfelter, E.H., 340, 347, 348; 394
See Ogden, J.C., 339, 340, 376, 378, 379; 403
Gladfelter, W., 338; 394
Gilbert, P.M., 14; 41
See Kana, T.M., 14, 18, 34; 41
Glombitza, K.-W. See Ragan, M.A., 193, 194; 269
Glover, H. See Morris, I., 33; 42
Glover, H.E., 14, 19, 27, 29, 31, 33; 41
See Beardall, J., 28; 39
See Mukerji, D., 29; 42
See Przelin, B.B., 18, 34; 43
Glucksman, J., 359; 394
Glynn, P.W., 237, 340, 342, 346, 349, 353, 361, 362; 265,
394
See Lessios, H., 338, 349; 399
Goddard, D.A. See Weiss, M.P., 351; 412
Goeden, G. See Bradbury, R.H., 239; 263
Goeden, G.B., 385; 394
Goenaga, C. See Williams, E.H., 338; 413
Goertemiller, T. See Hay, M.E., 243; 265
Gohar, H.A.F., 183, 206, 208, 213, 214, 221, 225; 265
Goldberg, E.D., 363; 394
Goldman, B., 343; 394
Goldman, C.R. See Priscu, J.C., 30; 43
Goldman, J.C., 15; 41
See Glibert, P.M., 14; 41
See Li, W.K.W., 16; 42
Goldschmid, A., 199, 207, 211, 223; 265
Golikov, A.N., 343; 394
Golley, F.B., 339; 395
Gomez, E.D., 92, 138, 338, 339, 347, 359, 360, 382, 383,
384; 159, 395
See Alcala, A.C., 358, 359, 363; 386
See Alino, P.M., 387
See Maragos, J.E., 383; 401
See Molenock, J., 138; 162
See Yap, H.T., 352, 355, 363, 382; 413
Gomon, M.F., 181, 235, 255; 265
364
Gong, W.K., 371

See Nixon, S.W., 403
See Wong, C.H., 371; 413
Goodbody, I., 55, 69, 70, 74, 80, 82, 83, 84, 344; 87, 395
Goodchild, D.J. See Miller, R.G., 17, 18, 23; 41
Goodman, D., 348; 395
Good win, J.R., 360; 395
Gordon, D.M., 372; 395
Goreau, T.F., 343; 395
Gosline, W.A., 239, 344; 265, 395
Gotelli, N.J., 56, 80, 82; 87
Goulet, D. See Birt, V.L., 329
Gounaris, K., 23; 41
Gourlay, M.E., 351, 358; 395
Gowan, R.F. See Young, C.M., 90
Grant, J.J., 251; 265
See Armstrong, M.J., 323; 329
See Wilson, R.P., 308; 335
Grassle, J: F., 343, 344; 395
Grave, B.H., 138, 146; 159
Grave, C., 52, 56, 60, 65, 68, 69; 87
Grave, C.A., 51, 52, 53, 54, 55, 57, 58, 60, 63, 65, 66, 67,
68, 69, 70, 76, 77; 87
Gray, J.S. See Moriarty, D.J.W., 268
Gray, R.D., 190; 265
Green, D.G., 350; 395
See Bradbury, R.H., 338, 350, 352, 384; 389
See Reichelt, R.E., 349, 363; 405
Green, G. See Bakus, G.J., 344, 383; 388
Greenway, M., 378; 395
Greenwood, P.H. See Liem, K.F., 180, 225; 267
Gressel, J. See Ben-Amotz, A., 34; 39
Griffith, P.C., 363; 395
Griffiths, A.M., 304; 332
See Abrams, R.W., 285, 303, 323; 328
Griffiths, C.L. See Branch, G.M., 141, 274; 158, 329
Griffiths, D.J. See Thinh, L.-V., 14; 44
Griffiths, R.J.I., 131; 159
Grigg, R.W., 341, 348, 349, 358, 359, 382, 383, 384, 385;
395
See Dollar, S.J., 352, 357, 361; 393
Grindley, J., 323; 352
Groom, Th. T., 113, 152; 159
Grosberg, R.K., 64, 77; 87
Grossman, G.D., 173, 256; 265
Grove, D. See Fnge, R., 170, 193, 198, 206, 215; 264
Grove, D.J., 215; 265
Grover, A. See Grant, J.J., 251; 265
Groves, T.D.D. See Brett, J.R., 170, 199, 215; 263
Grovhoug, J.G., 259; 265

Grygier, M.J., 91, 102, 103, 105, 107; 160
See Hallberg, E., 92; 160
Guest, K.P. See Hobson, L.A., 14, 38; 41
Guilcher, A., 351, 352, 382; 395
Guillard, R.R.L. See Glover, H.E., 19; 41
Guillaume, M. See Faure, G., 393
Guillet, A., 278; 332
Guinther, E.B. See Jokiel, P.L., 355; 398
See Smith, S.V., 362; 408
Gulliksen, B., 84; 87
Gunn, D.L. See Fraenkel, G.S., 66; 87
Gunter, G., 344; 395
Gustafson, D.E. See Lohrenz, S.E., 42
Gustafson, K. See Hay, M.E., 185, 194; 265
See Paul, V.J., 269
Gustafsson, P. See Lidholm, J., 34; 42
See Samuelsson, G., 43
Gutierrez, M., 75; 87
Gygi, R.A., 237; 265
Haas, L.W. See Laws, E.A., 42
Haines, A.K., 341; 395
See Liem, D.S., 368; 400
Halas, J.C., 363; 395
See Dustan, P., 350, 358; 393
Halim, M. See Robinson, A., 383; 406
Hall, C.A. See Boynton, W.R., 39
Hall, J.R. See Lindall Jr, W.N., 367; 400
Hallacher, L.E., 199, 207, 222; 265
Hallberg, E., 92; 160
Hallegraeff, G.M. See Jeffrey, S.W., 17; 41
Halley, R.B. See Shinn, E.A., 408
Hllgren, J.-E. See Richardson, K., 16; 43
Hallock, P., 354; 396
Halstead, B.W., 344; 396
Halver, J.E. See Wilson, R.P., 231; 272
Hamilton, L.S., 340, 371, 372, 376; 396
See Mercer, D., 375; 402
Hammann, H. See Eschmeyer, W.N., 188, 235, 257; 264
Hammond, L.S. See Bradbury, R.H., 347, 350; 389
Hampton, I., 314, 315, 318, 320, 323, 324, 325, 326; 332
Hanapi, S. See Seng, L.T., 407
Hancock, A., 105; 160
Hanekom, P. See Berry, P.F., 262
Hanel, C. See La Cock, G.D., 318; 333
Haney, J.C., 305; 332
Hanna, R.G.M., 353; 396
Hannon, N.J. See Clarke, L.D., 365; 391
AUTHOR INDEX
Hansen, J.A. See Moriarty, D.J.W., 402

Hansen, V.K. See Steemann Nielsen, E., 14; 43
Hansson, L. See Stenseth, N.C., 190; 271
Harbison, P., 374; 396
Harden, V. See Srithanya, S., 360; 409
Hardin, J. See Rogers, C.S., 406
Harding, L.W. See Coats, D.W., 14, 18; 40
Harger, R., 364; 396
Harkantra, S.N., 135; 160
Harker, B.M., 94; 160
See Zann, L.P., 113, 114, 116, 132; 166
Harmelin-Vivien, M. See Delesalle, B., 392
Harmelin-Vivien, M.L. See Bouchon-Navaro, Y., 180,
238, 239, 241, 259; 263
Harms, J., 133, 134; 160
Harper, P.C., 286, 288, 304; 332
Harriot, V.J., 342; 396
Harris, G.P., 17, 21, 23, 24, 34, 35, 37; 41
Harris, J.A. See Dwyer, P.D., 385; 393
Harris, J.E. See Lindsay, G.J.H., 205; 267
Harris, L.G., 195, 252, 258; 265
Harris, R.P. See Moal, J., 42
Harrison, B.A. See Jupp, D.B.L., 398
Harrison, C.S., 309; 332
Harrison, J.C., 280, 284, 304; 332
Harrison, P.L., 349; 396
See Babcock, R.C., 387
Harrison, W.G. See Laws, E.A., 42
See Smith, J.C., 29; 43
Hartog, C.den, 377; 396
Harwood, J.L. See Gounaris, K., 23; 41
Hashimoto, K., 57; 87
Hasiak, R.J. See Sell, J.L., 232; 270
Hasumoto, H. See Furuya, K., 14; 40
Hatcher, A.I., 354, 364, 378, 382; 396
See Wright, D.G., 382; 413
Hatcher, B.G., 337414; 172, 243, 244, 348, 349, 350,
355, 357, 359, 361, 362; 265, 396
See Hatcher, A.I., 364; 396
See Wright, D.G., 382; 413
Haugen, E.M. See Legendre, L., 42
Havenhand, J.N., 75, 77, 78; 87
See Svane, I., 63, 77; 89
Hawkins, C.M. See Scoffin, T.P., 270, 407
Hay, M.E., 169, 170, 183, 184, 185, 188, 194, 195, 196,
197, 234, 241, 242, 243, 244, 245, 252, 258, 259, 260;
265
See Paul, V.J., 194, 197, 258; 269
Hays, C. See Duffy, D.C., 289; 331
365
Head, S.M., 351, 352, 358; 396

Heald, E.J., 369; 396
See Odum, W.E., 367, 369, 370; 403
Heales, D.S. See Staples, D.J., 368, 377; 409
Heaney, W. See Morauta, L., 340; 402
Heath, D.J., 48; 87
Heath, J.R., 99, 100, 101; 160
Heath, R.G.M., 274, 303, 307, 308, 321; 332
Heber, U., 12, 21; 41
See Dietz, K.-J., 13, 21; 40
Hecht, S., 74; 87
Heck Jr, K.L. See Weinstein, M.P., 205; 271;
Heck, K.L., 378; 396
Hegerl, E.J., 370, 373, 385; 396
See Saenger, P., 340, 364, 370; 407
Heggen, S.J. See Jupp, D.B.L., 398
Heij, F.M.L., 378; 396
Heinbokel, J.F. See Venrick, E.L., 14; 44
Heinemann, K.R. See Williams, P.J.le B., 14; 44
Heinrich, A.K., 343, 344; 396
Heinsohn, C.E., 377; 396
Heldt, H.W. See Krmer, S., 37; 42
Helfferich, C. See McRoy, C.P., 339; 402
Helfrich, P. See Devaney, D.M., 339; 392
Henderson, R.S. See Grovhoug, J.G., 259; 265
Hendry, M.D. See Head, S.M., 351, 352, 358; 396
Henry, D.P., 92, 148; 160
See McLaughlin, P.A., 92; 162
Herald, E.S. See Eschmeyer, W.N., 188, 235, 257; 264
Herchenroder, B.E. See Gaus, R.R., 363; 394
Herz, L.E., 108, 138; 160
Heseltine, S. See Duffy, D.C., 304; 331
Hettler, W.F. See Thayer, G.W., 367; 409
Heyward, A.K. See Babcock, R.C., 387
Hiatt, R.W., 169, 170, 176, 178, 183, 184, 185, 186, 198,
232, 237, 256; 266
Hida, T.S. See Harrison, C.S., 309; 332
Highsmith, R.C., 340, 352, 357; 396
Hilgard, G.H., 121, 122, 123, 142; 160
Hiller, R.G., 17, 18, 23; 41
Hillmann-Kitalong, A. See Marsh, J.A., 345; 401
Hilton, J.W. See Atkinson, J.L., 204; 262
Hinds, P.A., 247; 266
Hines, A.H., 126, 128, 131, 132, 138, 142, 143, 144, 145,
146, 151; 160
Hines, J.A., 127; 160
Hipkin, C.R. See Everest, S.A., 28; 40
Hirai, E., 57, 58; 87
Hiro, F., 131, 132; 160
366
Hirota, J. See Lee, R.F., 343; 399

Hitchcock, G.L., 18; 41
Hixon, M.A., 169, 170, 171, 236, 242, 243, 244, 245, 246,
247, 248, 249, 251, 349; 266, 396
Hla, U.T., 371, 375; 396
Hobson, E.S., 169, 175, 179, 183, 186, 198, 222, 241, 256,
259; 266
See Rosenblatt, R.H., 180; 270
Hobson, L.A., 14, 38; 41
Hockey, P.A.R., 274, 291; 332
See Bosman, A.L., 323; 329
Heg, J., 95; 160
Heg, J.T., 92, 93, 95, 96, 97, 98, 100, 101; 160
See Ritchie, L.E., 96, 97, 98, 100, 101; 163
Hoek, C.van den, 344; 396
Hoek, P.P.C., 99, 110, 111, 112, 113, 114, 115, 116, 118,
119, 120, 127, 134, 135, 137, 139, 140, 154; 160
Hofer, R., 215; 266
See Niederholzer, R., 205; 268
Hoffman, S.G. See Robertson, D.R., 172; 269
Hoffman, T.W., 351, 383, 385; 396
Hofmeyr, P.K. See Summerhayes, C.P., 285; 335
Holdsworth, E.S., 14, 28, 29; 41
See Appleby, G., 29; 39
Holland, D.L. See Tooke, N.E., 145; 164
Holling, C.S., 346; 396
Holm-Hansen, O., 17; 41
Holt, S.J. See May, R.M., 401
Holthus, P. See Maragos, J.E., 355; 401
Holthus, P.F., 349, 363, 364, 383, 384, 385; 397
See Evans, C.W., 355; 393
Honma, Y., 94, 138; 160
Hooper, J.N.A. See Woodland, D.J., 357; 413
Hopley, D., 347; 397
See Davies, P.J., 347; 392
Hopner Peterson, G., 137, 150; 160
Horn, M.H., 167272; 169, 182, 188, 189, 190, 191, 192,
193, 194, 198, 199, 203, 204, 217, 228, 230, 235, 255,
257; 266
See Edwards, T.W., 169, 203, 204, 217, 220; 264
See Murray, S.N., 230; 268
See Ralston, S.L., 179, 180, 217; 269
Horstman, D.A. See Boyd, A.J., 276; 329
Houghton, D.R. See Stubbings, H.G., 133; 164
Howard, L.S., 340, 353, 361; 397
See Brown, B.E., 340, 345, 346, 351, 352, 353, 354,
355, 363; 389
See Glynn, P.W., 353; 394
Howard, R.K., 378; 397

See Klumpp, D.W., 378; 399
See Virnstein, R.W., 376; 412
Howe, H.F., 170; 266
Huang Zongguo See Cai Rusing, 140, 152; 158
Huat, K.K. See Seng, L.T., 407
Hubbard, D., 351; 397
Hudinaga, M., 136, 144; 160
Hudson, B.E.T. See Kenchington, R.A., 340, 364, 383;
398
Hudson, J.H., 352, 356, 363; 397
See Shinn, E.A., 408
Hughes, D.E., 223; 266
Hughes, P.T. See Jackson, C.B.J., 347; 397
Hughes, R.N., 190; 266
See Townsend, C.R., 190; 271
Hughes, T.P., 244, 245; 266
Huh, O.K. See Walker, N.D., 346; 412
Hui, E., 92; 160
Hulburt, E.M., 343; 397
Hungspreugs, M. See Windom, H.L., 413
Hunt Jr, G.L., 274, 305, 309, 328; 332
Hunt, W.G. See Moriarty, D.J.W., 402
Hunter, I.G. See Scoffin, T.P., 270, 407
Hunter, J.R. See Blaxter, J.H.S., 254; 263
Huntsman, G.R., 340; 397
Hurley, A.C., 139, 146, 152; 160
Hurley, D.E. See Ralph, P.M., 134; 163
Husby, D.M. See Parrish, R.H., 273; 333
Husic, D.W., 36; 41
Huston, M.A., 340, 347, 358; 397
Hutchings, L. See Armstrong, D.A., 328
See Brown, P.C., 276; 330
Hutchings, P.A., 237, 339, 340, 348; 266, 397
Hutchinson, T.C. See Rapport, D.J., 346, 363; 405
Hutomo, M., 377; 397
Huus, J., 55, 57, 58; 88
Hyatt, K.D., 170; 266
Hyslop, E.J., 285; 332
Ichikawa, A., 92, 96, 97, 100; 160
Ichimura, S. See Kishino, M., 25; 41
Ikawa, T. See Akagawa, H., 28; 39
Ikeda, T., 344; 397
Iltis, J.A. See Bird, E.C.F., 351; 388
Imberger, J. See Hatcher, B.G., 348; 396
Ingles, J. See Pauly, D., 344, 368, 372, 375; 406
Inoue, A. See Yasumoto, T., 413
AUTHOR INDEX
Inoue, Y. See Ohad, I., 34; 42

Ireland, C. See Gomez, E.D., 92; 159
Irvine, G.V., 246, 249, 250; 266
Irving, L. See Scholander, P.F., 344; 407
Irwin, B. See Platt, T., 19; 43
Irwin, M.P.S. See Clancey, P.A., 277; 330
Isdale, P., 352; 397
See Boto, K.G., 352; 389
Ishibashi, I. See Kosaka, M., 130, 131, 132; 161
Ishida, J., 224; 266
Ishida, S., 108, 135; 160
Isibashi, K. See Doi, T., 369; 393
Israel, A. See Beer, S., 33; 39
Iturriaga, R., 19; 41
IUCN, 340, 384; 397
Iwaki, T., 126, 128, 149; 160
See Yokota, A., 44
Iwasa, J. See Roughgarden, J., 81; 89
Jaap, W.C., 361; 397
See Bright, T.J., 339, 348; 389
Jackson, C.B.J., 347; 397
Jackson, G.A., 63, 64, 74; 88
Jackson, I. See Geoghegan, T., 340; 394
Jackson, J.B.C., 64, 84; 88
Jackson, S., 284, 288, 289, 291, 293, 303, 306, 309, 321,
326; 332
See Berruti, A., 273335
See Duffy, D.C., 275, 284, 293, 303, 307, 320, 322,
327; 331
James, A.G., 323; 332
James, M., 350, 384; 397
James, P., 362; 397
Jansen, W.F., 54; 88
Janzen, D.H., 337, 338, 365; 397
Jara, H.F. See Moreno, C.A., 169, 256, 257; 268
Jara, R.S., 372; 397
Jarvis, M.J.F., 280, 314, 320, 322; 332, 333
Jaubert, J. See Bouchon, C., 363; 389
Jeffrey, S.W., 17;41
See Vesk, M., 17, 18; 44
Jeffries, W.B., 116, 117; 160
Jehl Jr, J.R., 283, 284; 333
Jenkins, W.J., 15; 41
Jensen, A., 34; 41
Jensen, R.A.C., 283, 309; 333
Jerlov, N.G., 342; 397
Jernakoff, P., 147; 160
Jernelov, A. See Linden, O., 338; 400
367
Jewson, D.H. See Dring, M.J., 35; 40

Jeyaseelan, M.J. See Krishnamurthy, K., 373; 399
Jhamtani, H.P., 376; 397
Jickells, T.D. See Dodge, R.E., 392
Jimenez, J.A., 366, 372; 397
Joannot, P., 359; 397
Jobling, M., 217; 266
Johannes, R.E., 340, 341, 342, 344, 345, 346, 347, 348,
349, 354, 355, 356, 358, 369, 381, 382; 397, 398
See Hatcher, B.G., 337414
See Odum, W.E., 367, 373; 403
See Ruddle, K., 339; 406
See Stoddart, D: R., 340; 409
See Wood, E.J.F., 339; 413
John, D.M., 243; 266
John, P.A., 147; 161
Johnson, B.L., 381; 398
Johnson, G.D., 254, 257; 266
Johnson, K.S. See Lohrenz, S.E., 42
Johnson, M.W., 138; 161
See Sverdrup, H.U., 342; 409
Johnson, R., 340; 398
Johnson Jr, T.W., 148; 161
Johnston, A.M., 33; 41
Johnstone, I.M., 365, 369, 376; 398
Joint, I.R., 14; 41
Joins, C., 15; 41
Jokiel, P.L., 35, 339, 345, 355, 357; 41, 398
See Coles, S.L., 355, 356, 361; 391
See Smith, S.V., 357, 362; 408
Jones, J.A., 259; 266
Jones, L.W.G., 139; 161
Jones, M. See Wolanski, E., 369, 373; 413
Jones, R.S., 170, 172, 175, 183, 194, 198, 209, 210, 218,
221, 223, 224, 237, 238, 239, 256, 259; 266, 267
Jrgensen, A.J. See Svane, I., 63, 77; 89
Jrgensen, E.G., 14, 18; 41
Joshi, G.V. See Karekar, M.D., 28; 41
Joshi, S.S. See Rege, M.S., 135, 148; 163
Joubert, C.S.W. See Berry, P.F., 262
Jouen, R. See Frazier, A., 394
Jumars, P.A. See Penry, D.L., 228, 229, 231, 236; 269
Jung, N. See Bernstein, B.B., 252; 262
Jupin, H. See Mortain-Bertrand, A., 14, 31; 42
Jupp, B. See Thorhaug, A., 379; 410
Jupp, D.B.L., 383; 398
Jupp, D.L.D. See Wolanski, E., 358; 413
368
Kabanova, J.G. See Koblentz-Mishke, O.J., 399

Kajiwara, S., 70, 72; 88
Kalyanasundaram, N., 135; 161
Kamens, T.C., 102; 161
Kamermans, P. See Ruyter van Steveninck, E.D.de, 243;
270
Kana, T.M., 14, 18, 34; 41
Kapetsky, J.M., 371, 372, 375; 398
See Gedney, R.H., 368; 394
Kaplan, A. See Zenvirth, D., 26; 44
Kapoor, B.G., 169, 170, 198, 199, 206, 222; 267
Karande, A.A., 111, 127, 128, 131, 135, 136, 139, 141,
147, 148, 154; 161
See Gaonkar, S.N., 110, 111, 127, 128, 130, 131, 135,
136, 141; 159
See Rege, M.S., 135, 148; 163
Karasov, W.H., 229; 267
Karekar, M.D., 28; 41
Karl, D.M. See Laws, E.A., 42
Kasahara, H. See Hudinaga, M., 136, 144; 160
Katz, M.J., 49, 51, 52, 54, 65; 88
Kaufman, L.S., 223, 225, 349; 267, 398
Kaufmann, R., 117, 119, 120; 161
Kaur, B. See Lee, Y.S., 373; 399
Kay, A.M., 84, 85; 88
See Liddle, M.J., 357; 400
Keefe, C.W. See Boynton, W.R., 39
Kelleher, G.G., 347, 360, 364, 383, 385; 398
Keller, A.A., 17; 41
Keller, M.D. See Glover, H.E., 19; 41
Kelly, G.J., 1144; 27, 31, 35; 41
Kemp, W.M. See Boynton, W.R., 39
Kempf, E., 371, 372; 398
Kenchington, R.A., 340, 364, 383; 398
See Kelleher, G.G., 383; 398
Kendall, S.W. See Jupp, D.B.L., 398
Kennedy, V.S., 339; 398
Kennelly, S.J., 252; 267
Kenner, R.A., 37; 41
Kenworthy, W.T. See Fonseca, M.S., 379; 394
Kenyon, R. See Poiner, I.R., 376;404
Keough, M.J., 74, 80, 82, 83, 85;88
See Kay, A.M., 85;88
Kerby, N.W., 28;41
Kerchr, J.R. See Spies, R.B., 356;409
Kerstitch, A.N. See Thomson, D.A., 188; 271
Key, G.S. See Smith, S.V., 362; 408
Khristoforova, N.K., 353; 398
Kiefer, D.A. See Falkowski, P.G., 17; 40
Kiene, W.E., 348; 398

Kimmerer, W.J., 345; 398
See Smith, S.V., 408
Kinahan, J.B. See Siegfried, W.R., 304; 335
Kindeman, K.C. See Richards, W.J., 348, 349; 406
King, A.W., 350; 398
King, F.D., 14; 41
Kingsford, M.J., 256; 267
See Schiel, D.R., 174, 256; 270
Kingsley, J.S., 53; 88
Kinsey, D.W., 340, 342, 344, 347, 353, 354; 398
Kinzie III, R.A. See Buddemeier, R.W., 340, 348; 390
Kirilovsky, D., 34; 41
Kirk, J.T.O., 15, 18, 21, 24, 25, 38; 41
Kirkman, H., 377; 399
Kirkwood, G.P., 381; 399
Kishino, M., 25; 41
Kiswara, W. See Suharsono, W., 342; 409
Kitaoka, S. See Yokota, A., 33; 44
Kjerfve, B., 349, 363; 399
See Dame, R., 392
Klepal, W., 92, 93, 94, 95, 110, 111, 117, 154; 161
See Achituv, Y., 110; 156
See Barnes, H., 93, 94, 95; 157
Klimov, V.V. See Allakhverdiev, S.I., 34; 39
Klingelhoeffer, E.W. See Randall, R.M., 293; 334
Klug, M.J., 378; 399
Klumpp, D.W., 201, 204, 205, 206, 208, 216, 217, 221,
225, 234, 245, 247, 250, 378; 267, 399
See Robertson, A.I., 208, 212, 217, 225; 269
Knaben, N., 60; 88
Knap, A.H., 340, 353; 399
See Solbakken, J.E., 409
Knight-Jones, E.W., 133, 134; 161
See Moyse, J., 153; 162
Knights, B., 199; 267
Koblentz-Mishke, O.J., 344; 399
Kobza, J., 13, 27; 41
Koechlin, J., 383; 399
Koehl, M.A.R. See Sebens, K.P., 73; 89
Koesoebiono, See Burbridge, P.R., 383, 384; 390
Kohn, A.J., 343, 344, 347; 399
Koike, H. See Ohad, I., 34; 42
Koike, I. See Polunin, N.V.C., 216, 234, 250; 269
Kojis, B.L. See Quinn, N.J., 368, 379, 383; 405
Kolber, Z. See Falkowski, P.G., 34; 40
Kolehmainen, S., 374; 399
AUTHOR INDEX
Kolosvry, G.von, 124, 125, 127, 132, 134, 136, 138, 140;
161
Kolotukhina, N.K. See Korn, O.M., 125, 126; 161
Kongsangchai, J., 370; 399
Koon, C.B. See Getter, C.D., 373; 394
Korn, O.M., 95, 125, 126, 127, 140, 141, 146, 149, 153;
161
See Ovsyannikova, I.I., 137; 162, 163
Kosaka, M., 130, 131, 132; 161
Koslow, J.A. See Ogg, J.G., 346, 349; 403
Kotrschal, K., 207, 211, 215; 267
See Goldschmid, A., 199, 207, 211, 223; 265
Kott, P., 59; 88
Kottmeier, S.T. See Palmisano, A.C., 42
Kowalevsky, A.O., 49;88
Kraay, G.W. See Gieskes, W.W., 14, 15, 16;40
Krebs, J.R. See Stephens, D.W., 190; 271
Kremer, B.P., 14, 26, 31; 41, 42
Kriel, F. See Shelton, P.A., 312; 334
Krishnamurthy, K., 373; 399
Krmer, S., 37; 42
Kropp, R.K. See Eldredge, L.G., 346, 349, 351; 393
Krger, A. See Demmig, B., 34; 40
Kruger, I. See Crawford, R.J.M., 291; 331
Krger, P., 98, 99, 106, 111, 112, 113, 114, 115, 116, 118,
119, 120, 122, 124, 139, 141, 154;161
Ku, M.S.B. See Usuda, H., 13, 19; 44
Kuda, A. See Eakin, R.M., 54; 87
Khl, H., 148; 161
Khlmann, D.H.H., 361; 399
Khnert, L., 92, 104, 105, 106, 108; 161
Kuhnhold, W.W. See Gedney, R.H., 368; 394
Kunz, B. See Schmidtke, J., 49; 89
Kusten, K. See Robinson, W.E., 52; 89
Kvalvagnaes, K. See Robinson, A., 383; 406
Kwang, L.Y. See Seng, L.T., 407
La Cock, G.D., 308, 310, 315, 317, 318, 319; 333
See Duffy, D.C., 304, 319; 331
See Randall, R.M., 334
See Wilson, R.P., 293; 335
Laboute, P., 349; 399
Lafargue, F., 59; 88
Lai, H.C., 340, 373, 374; 399
Laist, D.W., 356; 399
Lakshmano Rao, M.V. See Ganapati, P. N., 147; 159
Lal, P.N., 374; 399
Lambers, H., 36; 42
Lambert, C. See Lambert, G., 47, 55; 88
369
Lambert, C.C., 46, 48, 49, 57, 58, 60; 88

See Watanabe, H., 56, 57, 58, 59; 90
See West, A.B., 57, 58, 59; 90
Lambert, G., 47, 49, 55, 56, 57, 58, 64, 75, 82, 84; 88
See Lambert, C.C., 49, 60; 88
Lambert, K., 283, 289, 304, 305; 333
Lamberts, A.E., 338, 353; 399
See Dahl, A.L., 350; 392
Lanaras, T. See Cook, C.M., 26; 40
Landau, M., 94, 138, 142; 161
Lang, W.H., 116, 117; 161
Langdon, C., 19, 38; 42
Langham, N.P.E. See Mathais, J.A., 353; 401
Lanyon, J., 376; 399
Lanzing, W.J.R., 54; 88
See Conacher, M.J., 201, 253, 259; 264
Largier, J.L. See Carter, R.A., 276; 330
Larkum, A.W.D., 344; 399
See Conacher, M.J., 201, 253, 259; 264
See Hatcher, B.G., 243, 354; 265, 396
See Hiller, R.G., 23; 41
Larson, R.J. See Ebeling, A.W., 264
Lassig, B.R., 349, 358; 399
Lassuy, D.R., 186, 199, 202, 204, 207, 213, 216, 247,
249, 250; 267
Latif, A.F.A. See Gohar, H.A.F., 183, 206, 208, 213, 214,
221, 225; 265
Latzko, E. See Kelly, G.J., 27; 41
Lauder, G.V., 254, 257; 267
Laugksch, R.C., 321, 322; 333
See Furness, B.L., 293; 332
Laur, D.R. See Harris, L.G., 195; 265
Laurenson, L.J.B. See Duffy, D.C., 293; 331
Lawrence, A.L., 371; 399
Laws, E.A., 12, 14; 42
Laws, R.M. See May, R.M., 401
Lay, S. See Gutierrez, M., 75; 87
Le Gall, J.Y., 345; 399
Le Grand, G., 283, 284; 333
Le Reste, L., 114, 115, 116, 119, 124, 126, 127, 135, 140;
161
Lea, D.W. See Shen, G.T., 353; 408
Lee, D.J., 217; 267
Lee Long, W.J. See Coles, R.G., 377; 391
Lee, R.F., 343; 339
Lee, V. See Nixon, S.W., 403
Lee, Y.S., 373; 399
370
Leftley, J.W., 17; 42

Legendre, L., 14, 16; 42
See Rochet, M., 14; 43
Legore, R.S. See Seng, L.T., 407
Lehner, C.A. See Thomson, D.A., 174, 256; 271
Leighton, D.L., 251; 267
Leighton, K. See Robertson, D.R., 172, 259; 269
Leis, J.M. See Richards, W.J., 225; 269
Lennep van, E.W. See Lanzing, W.J.R., 54; 88
Lepore, E., 95, 138, 140; 161
Lessios, H., 338, 349; 399
Lessios, H.A., 245; 267
Leuckart, R., 97; 161
Levin, V.S. See Ovsyannikova, I.I., 141; 163
Levine, E.P., 55, 60; 88
Levings, C.D. See Wu, R.S.S., 138, 145, 147; 165
Levinton, J.S. See Sammarco, P.W., 244; 270
Levitan, D.R., 244, 245; 267
Lewis, A.D., 359; 399
Lewis, A.H. See Cook, P.A., 145; 158
See Crisp, D.J., 145; 158
Lewis, C.A., 121, 122, 123, 152; 162
Lewis, C.R. See Coles, S.L., 355; 391
Lewis, D.B. See Briggs, K.T. 305, 321; 329
Lewis III, F.G. See Virnstein, R.W., 376; 412
Lewis, J.B., 122, 123, 130, 131, 340, 341, 353, 354, 358;
162, 400
Lewis, R.R., 367, 374; 400
Lewis, S.M., 183, 184, 194, 197, 239, 243, 244, 258, 259;
267
See Hay, M.E., 265
Lewis, T.J. See Ainley, D.G., 319; 328
Lewis, V.P., 169, 205; 267
Li, W.K.W., 16, 20; 42
Librero, A.R., 340, 371, 383; 400
Liddle, M.J., 357; 400
Lidholm, J., 34; 42
Lidz, B. See Shinn, E.A., 408
Liem, D.S., 368; 400
Liem, K.F., 180, 225; 267
See Kaufman, L.S., 223, 225; 267
See Lauder, G.V., 254, 257; 267
Lieth, H., 25; 42
Lighty, R.G., 355; 400
Ligny, W.de See Seng, L.T., 407
Likens, G.E. See Whittaker, R.H., 12, 13, 17, 23; 44
Lilley, R. McM., 27; 42
Limbaugh, C., 251; 267
Limberger, D. See Taborsky, M., 179, 182; 271
Lin Peng See Lu Chang, 364, 372; 400

Linares, F.A. See Yanez-Arancibia, A., 367; 413
Lindall Jr, W.N., 367; 400
Linden, O., 338; 400
Lindholm, R. See Glucksman, J., 359; 394
Lindley, J.E. See Chapman, A.R.O., 258; 263
Lindsay, G.J.H., 205; 267
Lindsey, C.C., 343; 400
Linsley, R.H., 146; 162
Lipkin, Y., 376; 400
See Lundberg, B., 184, 185, 194; 267
Littler, D.S. See Littler, M.M., 186, 194, 197, 227, 243,
244, 258; 267
Littler, M.M., 186, 194, 195, 197, 227, 243, 244, 258; 267
Liversidge, R., 283; 333
See Broekhuysen, G.J., 308; 329
Livingston, R.J., 187, 339; 267, 400
See Stoner, A.W., 187, 207; 271
Lloyd, D. See Hughes, D.E., 223; 266
Lloyd, N.D.H., 33; 42
Lobel, P.S., 169, 170, 184, 196, 202, 205, 206, 207, 218,
220, 221, 222, 223, 224, 225, 226, 227, 233, 246, 247,
251, 349; 267, 400
See Ogden, J.C., 170, 171, 179, 180, 182, 185, 215,
242, 254, 260; 268
Lockwood, B. See Chia, L.S., 340; 390
Lohrenz, S.E., 14; 42
Long, S.P., 339; 400
Longhurst, A.R., 339; 400
Lnneborg, A. See Samuelsson, G., 43
Loomis, J.B., 384, 385; 400
Lopez, G. See Yamamoto, N., 238; 272
Lorenzen, C.J., 15, 24; 42
Louason, G. See Powles, S.B., 31; 43
Loubersac, L. See Bour, W., 383; 389
Loutit, R., 317; 333
See Ryan, P.G., 273; 334
Loya, Y., 340, 349, 353, 354, 361; 400
See Rinkevich, B., 353; 406
Lu Chang, 364, 372; 400
Lubbock, H.R., 359; 400
Lubchenco, J., 170, 236, 243, 244, 251; 267
See Gaines, S.D., 169, 170, 236, 242, 251, 254, 257,
260; 265
See Menge, B.A., 242, 251; 267
Lucas, M.I., 150, 153; 162
Lucas, W.J., 27; 42
Luckens, P.A., 126, 128, 129, 133, 134, 144, 149; 162
AUTHOR INDEX
Luckhurst, B.F., 351; 400

Luckhurst, K. See Luckhurst, B.F., 351; 400
Lugo, A.E., 340, 346, 365; 400
See Cintron, G., 346; 391
See Jimenez, J.A., 366, 372; 397
See Twilley, R.R., 370; 410
Lund, H., 357: 400
Lundlv, T. See Svane, I., 55, 82, 83; 89
Lundberg, B., 184, 185, 194; 267
Lutjeharms, J.R.E., 276; 333
Ltzen, J., 96, 97, 99, 100, 101; 162
See Heg, J., 95; 160
Lyerla, J.H. See Lyerla, T.A., 49; 88
Lyerla, T.A., 49; 88
Lynch, W.F., 63; 88
MacArthur, R.H., 342, 344, 385; 400, 401
MacGeachy, J.K. See Scoffin, T.P., 270, 407
Macintosh, D.J. See Soepadma, E., 339; 408
Macintyre, I.C. See Gaus, R.R., 363; 394
Mackas, D.L. See Forbes, J.R., 14; 40
Mackie, W., 193, 205; 267
Macnae, W., 365, 369, 372; 401
Mae, T, See Makino, A., 19; 42
Maestrini, S.Y. See Leftley, J.W., 17; 42
Magill, E.K. See Kjerfve, B., 349; 399
Makino, A., 19; 42
Malakhov, V.V. See Vorontsova, M.N., 54; 90
Mall, L.P. See Singh, V.P., 370; 408
Malley, D.F., 369; 401
Malone, T.C., 12; 42
Malusa, J.R., 126, 131, 143, 146; 162
Mancuso, V., 52; 88
Manikowski, S:, 305; 333
Mann, K.H., 258, 339; 267, 401
Maragos, J.E., 347, 355, 363, 383; 401
See Evans, C.W., 355; 393
See Grigg, R.W., 349, 358; 395
See Holthus, P.F., 349, 363; 397
Marais, J.F.K., 213, 238; 267
Marcus, J., 355, 356; 401
See Thorhaug, A., 378; 410
Markly, J.L., 365; 401
Markus, M.B. See Clancey, P.A., 277; 330
Marliave, J.B., 196; 267
Marr, J.C., 381, 382; 401
Marra, J. See Laws, E.A., 42
See Williams, P.J.le B., 14; 44
371
Marsh, H. See Heinsohn, C.E., 377; 396

Marsh, J.A., 345, 353, 355; 401
See Best, B.R., 352; 388
Marsh, K.V. See Spies, R.B., 356; 409
Marshall, J.F. See Davies, P.J., 347; 392
Marshall, L.D. See Montgomery, W.L., 243; 268
Marshall, N., 358; 401
See Rodelli, M.R., 406
Marshall, R.A.S. See Uys, C.J., 314; 335
Marshall, W.H. See Miller, K.A. 189; 268
Marszalek, D.S., 351, 354, 361; 401
Marten, G.G., 358; 401
Martin, A. See Le Grand, G., 283, 284; 333
Martin, J.H., 15; 42
Martin, K.R., 353; 401
Martin-Jezequel, V. See Moal, J., 42
Martinez, P., 371; 401
Martosewojo, S. See Hutomo, M., 377; 397
Martosubroto, P., 368; 401
Mason, C.F. See Long, S.P., 339; 400
Masson, M. See Gabrie, C., 351, 358, 363; 394
Mast, S.O., 56, 66, 67, 69, 70, 71, 72; 88
Master, I.M. See Fell, J.W., 369; 393
Mathais, J.A., 353; 401
See Chua, T.E., 340; 391
Mathieson, A.C. See Penniman, C.A., 34; 42
Matlock, C.B. See Best, B.R., 352; 388
Matricardi, G. See Relini, G., 139, 148; 163
Matthews, J. See Burchmore, J.J., 263
Matthews, J.P., 274, 287, 293, 294, 295, 296, 298, 315,
320, 322; 333
Matthews, W.J. See Power, M.E., 241; 269
Mattson Jr, W.J., 168, 231, 232, 233, 234; 267
May, R.M., 350; 401
Mayer, A.G., 342; 401
Mayer, J. See Rozin, P., 217; 270
Mayo, K.K., 383; 401
See Jupp, D.B.L., 398
McCabe, J., 360; 401
McCarthy, J.J. See Goldman, J.C., 15; 41
McComb, A.J. See Cambridge, M.L., 390
See Silberstein, K., 378; 408
McConnell, D.B. See Bryan, P.G., 359; 38
McCosh, G.K. See Grave, C., 52, 56, 60, 65, 68, 69; 87
McEdward, L.R. See Emlet, R.B., 63; 87
McGillivary, P.A. See Haney, J.C., 305; 332
McGinnity, P. See Oliver, J., 359; 404
372
McGowen, G.E. See Collette, B.B., 225; 264

McIvor, C.C. See Odum, W.E., 367, 369; 403
See Smith III, J.T., 365; 408
McKellar, H. See Dame, R., 392
McKinnon, D. See Klumpp, D.W., 234, 245; 267
McLachlan, J. See Bidwell, R.G.S., 26, 33; 39
McLaughlin, P.A., 92; 162
See Henry, D.P., 92; 160
McManus, J.W., 338, 356, 358; 401
McMeekin, T.A., 20; 42
McMillan, C. See Markly, J.L., 365; 401
See McRoy, C.P., 376; 402
McMurray, H.F. See Carter, R.A., 276; 330
McMurrich, J.P., 98; 162
McNeely, J.A., 384, 385; 401
McPherson, R. See Olson, R.R., 56, 59, 60, 64, 68, 72, 73,
81, 82; 88
McQuaid, L. See Wilson, R.P., 304; 335
McRoy, C.P., 339, 376, 377; 402
See Phillips, P.C., 339; 404
Medd, G.W., 254, 257, 260; 267
Mecklenburg, C.von See Emanuelsson, H., 54; 87
Medina, E. See Golley, F.B., 339; 395
Meehan, B., 364; 402
Meekan, M.G., 171, 182, 189, 194, 196, 225, 253, 259;
267
Meeuwis, J.M. See Lutjeharms, J.R.E., 276; 333
Mellis, A. See Demeter, S., 34; 40
Mendelsohn, J., 305; 333
Mendelsohn, J.M. See Clancey, P.A., 277; 330
Mendelssohn, I.A., 367; 402
Meng, W.T. See Seng, L.T., 407
Menge, B.A., 46, 48, 63, 242, 251; 88, 267
Menzel, D.W., 201, 204; 267
Mercer, D., 375; 402
Mergner, H., 353, 361; 402
Merrett, M.J. See Dixon, G.K., 26, 27; 40
Miclat, R.I. See Carpenter, K.E., 360; 390
Middleton, M.J. See Burchmore, J.J., 263
Mileikovsky, S.A., 343; 402
Millar, R.H., 45, 46, 49, 50, 52, 54, 55, 63, 66, 67, 70, 80,
82, 83; 88
Millard, N., 135, 139, 140; 162
Miller, A.C., 243; 268
Miller, B. See Thorhaug, A., 379; 410
Miller, K., 364, 383; 402
Miller, K.A., 189; 268
Miller, K.R. See McNeely, J.A., 384, 385; 401
Miller, R.C. See Johnson, M.W., 138; 161
Miller, R.L., 49; 88

Miller, W.T., 277; 333
Millikin, M.R., 231; 268
Mills, D.K., 14, 34; 42
Milton, K., 228; 268
Mimuro, M., 18; 42
Mitchell, A.W. See Furnas, M.J., 14; 40
Mitchell, B.G. See Iturriaga, R., 19; 41
Mitchell, R., 338, 361; 402
Mitchell, W.C., 353; 402
Mitchell-Innes, B.A. See Armstrong, D.A., 328
Mitchell-Tapping, H.J., 357; 402
Mito, S. See Collette, B.B., 225; 264
Miura, K. See Yokota, A., 44
Miyachi, S. See Aizawa, K., 26, 27; 39
Mizrahi, L. See Gilboa-Garber, N., 150; 159
Moal, J., 18; 42
Molenock, J., 138; 162
Moll, H. See Wijsman-Best, M., 360, 382; 413
Mollagee, F. See Wilson, R.P., 293; 335
Moloney, C.L. See Ryan, P.G., 284, 291, 303, 306, 307,
308, 310, 327; 334
Monniot, C., 75, 79; 88
Montaggioni, I. See Davies, P.J., 340, 347; 392
Montaggioni, L. See Poli, G., 404
Monteforte, M. See Poli, G., 404
Montevecchi, W.A. See Birt, V.L., 329
Montgomery, W.L., 182, 185, 189, 192, 193, 194, 199,
201, 202, 204, 207, 208, 210, 215, 220, 227, 230, 243,
247, 249, 250, 258; 268
See Fishelson, L., 171, 181, 191, 227; 264
Moore, H.B., 137, 138, 143, 146, 342, 343, 344, 346; 162,
402
Moore, L. See Cambridge, M.L., 390
Moore, L.B., 128, 129, 133, 143, 144; 162
Moore, P.G., 74; 88
Morales, J.T. See Alino, P.M., 387
Moran, M.J., 179, 185; 268
Moran, P.J., 338, 340, 349, 361, 362; 402
See Bradbury, R.H., 350; 389
Morant, P.D., 291, 319; 333
Morauta, L., 340; 402
Moreno, C.A., 169, 256, 257; 268
Morgan, T. See Kolehmainen, S., 374; 399
Morgan, T.H., 49; 88
Morgan, T.O., 57; 88
Moriarty, D.J.W., 218, 221, 222, 224, 238, 378; 268, 402
Morris, G. See Cintron, G., 346; 391
Morris, G.C., 383, 384; 402
AUTHOR INDEX
Morris, I., 30, 33; 42

See Beardall, J., 21, 28, 29; 39
See Glover, H.E., 14, 27, 29, 31, 33; 41
See Mukerji, D., 29; 42
Morris, W.J. See Hobson, L.A., 14; 41
Mortain-Bertrand, A., 14, 29, 31; 42
Morton, E.S., 234; 268
Moverley, J. See Saenger, P., 365; 407
Moyer, J.T., 361; 402
Moyse, J., 134, 153, 156; 162
See Hui, E., 92; 160
Muchacheep, S. See Srithanya, S., 360; 409
Mukerji, D., 29, 31; 42
See Beardall, J., 28; 39
Mulcherjee, A.K., 365; 402
Mller, F., 98; 162
Muller, G.J. See Andrews, J.C., 351; 387
Mller, H.R. See Andrews, T.J., 366; 387
Munn, E.A., 94; 162
Munro, J.L., 340, 341, 342, 344, 346, 349, 359, 381; 402
Murdoch, W. See Stewart-Oaten, A.W., 362; 409
Murphy, D.J., 23; 42
Murphy, G.I. See Pauly, D., 339; 404
Murray, S.N., 230; 268
See Horn, M.H., 169, 182, 188, 189, 192, 194, 198,
203, 217, 228, 230, 235, 255, 257; 266
Murray, S.P. See Roberts, H.H., 347; 406
Muzik, K., 338, 361; 402
Myers, J., 24; 42
Myklestad, S. See Vieira, A.A.H., 34; 44
Myrberg Jr, A.H. See Fishelson, L., 171, 181, 191, 227;
264
Naamin, N., 371; 402
See Martosubroto, P., 368; 401
Nagabhushanam, R. See Ganapati, P.N., 147; 159
Nagy, K.A., 233, 321, 322; 268, 333
Naim, O. See Nair, M.Y., 352; 402
See Poli, G., 404
Nair, A. See Harkantra, S.N., 160
Nair, M.Y., 368; 402
Nair, N.B. See Pillay, K.K., 94, 136, 147; 163
Nakai, T. See Furuya, K., 14; 40
Nakajima, J. See Honma, Y., 94, 138; 160
Nasr, D.H., 383, 384; 403
Naughton, S.P. See Salomon, C.H., 346, 349; 407
Navaluna, N.A., 349, 357; 403
Neale, P.J. See Demeter, S., 34; 40
373
See Vincent, W.F., 34; 44

Nedwell, D.B., 367, 373; 403
Neff, J.M., 353, 354; 403
Neighbors, M.A. See Horn, M.H., 188, 189, 191, 192, 193,
198, 203, 204, 217, 228; 266
Neimanis, S. See Deitz, K.-J., 13, 21; 40
Nelson, C.S. See Parrish, R.H., 273; 333
Nelson, D. See Dame, R., 392
Nelson, J.S., 181, 186, 188, 206, 254, 255; 268
Nelson, S.G., 200, 238; 268
Nelson, W.G. See Virnstein, R.W., 376; 412
Nemoto, T. See Furuya, K., 14; 40
Neori, A. See Thomas, W.H., 44
Nergel, J.E., 363; 403
Neudecker, S., 355; 403
New, N.B., 371, 375, 376; 403
Newell, N.D. See Stehli, F.G., 344; 409
Newell, S.Y. See Fell, J.W., 369; 393
Newman, G.G., 324; 333
Newman, W.A., 91, 92, 102, 103, 104, 105, 107, 109,
118, 120, 123, 125, 134; 162
See Dayton, P.K., 92, 132; 159
See Gomez, E.D., 92; 159
See Grygier, M.J., 102, 103, 105, 107; 160
See Ross, A., 102; 163
Ng, F.S.P., 371, 375; 403
Nicholls, G.H., 304, 307; 333
Nichols, P.D. See Klumpp, D.W., 201, 204, 205, 206,
208, 216, 217, 221, 225; 267
Nicholson, W.R. See Huntsman, G.R., 340; 397
Nicoll, P.A. See Grave, C.A., 63, 76, 77; 87
Niederholzer, R., 205; 268
Nieuwolt, S., 343; 403
Nigrelli, R.F. See Cheung, P.J., 94; 158
See Coln-Urban, R., 113, 116; 158
Nikolsky, G.V., 343, 344; 403
Nilsson-Cantell, C.-A., 98, 106, 108, 109, 112, 113, 114,
115, 116, 117, 118, 119, 120, 124, 127, 130, 131, 154;
162
Nishihira, M., 361, 362; 403
Nisizawa, K. See Akagawa, H., 28; 39
Nixon, S.W., 367; 403
Noll, F.C., 107; 162
Nomaguchi, T.A., 82, 83; 88
Norris, D.O. See Norris, J.S., 222; 268
Norris, E., 139; 162
Norris, J.N., 195; 268
See Griffith, P.C., 363; 395
See Lewis, S.M., 244; 267
374
Norris, J.S., 222; 268

Norris, K.S., 188, 198; 268
See Ray, G.C., 362, 384, 385; 405
North, W.J., 234, 251; 268
Nose, Y. See Sano, M., 360; 407
Noshkin, V.E., 356; 403
Nursall, J.R., 171, 215; 268
Nyholm, K.-G. See Blom, S.-E., 144; 157
OConnor, J.F., 363; 403
Ochi, T. See Yasumoto, T., 413
Odum, E.P., 363; 403
See Barrett, G.W., 363; 388
See Odum, H.T., 232; 268
Odum, H.T., 232, 343; 268, 403
Odum, W.E., 182, 208, 213, 216, 223, 224, 227, 238, 367,
369, 370, 373; 268, 403
See Lewis, R.R., 367; 400
Ogburn, M.V., 187, 207, 214, 220; 268
Ogden, J.C., 170, 171, 179, 180, 182, 183, 184, 185, 215,
225, 237, 241, 242, 243, 244, 251, 254, 260, 339, 340,
376, 377, 378, 379; 268, 403
See Buckman, N.S., 171; 263
See Lobel, P.S., 184, 202, 205, 233; 267
See Sammarco, P.W., 244; 270
See Targett, N.M., 184; 271
Ogden, J.C. See Thayer, G.W., 271, 409
Ogden, N.C. See Ogden, J.C., 376; 403
Ogg, J.G., 346, 349; 403
Ohad, I., 34; 42
Ohira, K. See Makino, A., 19; 42
Oka, H., 56; 88
Okada, K. See Doi, T., 369; 393
Okami, N. See Kishino, M., 25; 41
Olafson, R.W., 353; 403
Oliver, J., 338, 349, 357, 359, 384; 403, 404
See Dayton, P.K., 92, 132; 159
Oliver, J.K. See Babcock, R.C., 387
Ollason, J.G. See Pierce, G.J., 190; 269
Olley, J. See McMeekin, T.A., 42
Olsen, S., 384; 404
Olson, R.R., 55, 56, 59, 60, 63, 64, 65, 67, 68, 72, 73, 80,
81, 82, 83; 88
Olson, S.L., 281; 333
Omar, I.H. See Nair, M.Y., 368; 402
Ong, C.H. See Gong, W.K., 371; 395
Ong, J.E., 371; 404
See Wong, C.H., 371; 413

Ongkosongo, O.S.R., 358; 404
Onuf, C.P., 367; 404
quist, G. See Lidholm, J., 34; 42
See Samuelsson, G., 43
Ormond, R.F.G., 384; 404
See Walker, D.I., 352, 355; 412
Orth, R. See Zieman, J.C., 414
Orth, R.J. See Van Montfrans, J., 378; 411
Orton, J.H., 99, 100; 162
Osborne, B.A., 24; 42
See Geider, R.J., 37, 38; 40
Oshima, Y. See Yasumoto, T., 413
Osmond, C.B., 31, 34; 42
Otway, N.M., 131, 144; 162
Ovsyannikova, I.I., 137, 141; 162, 163
See Korn, O.M., 127, 141, 153; 161
Owen, D.F. See Wiegert, R.F., 244; 272
Owens, T.G. See Falkowski, P.G., 14, 37, 38; 40
Owings, W.J. See Sell, J.L., 232; 270
Page, H.M., 121, 127, 144, 151; 163
Paine, R.T., 75, 194, 243, 249; 88, 268
See Castilla, J.C., 251; 263
Palekar, V.C. See Karande, A.A., 127, 128, 136; 161
Palmer, A.R., 63; 88
Palmisano, A.C., 14; 42
Palmork, K.H. See Solbakken, J.E., 409
Panayotou, T., 381, 382; 404
Pandian, T.J., 169, 170, 215, 231; 268
Pannier, F., 371, 372, 373; 404
Pantastico, J.B., 205; 269
Parin, N.V. See Collette, B.B., 225; 264
Parker, K.R. See Stewart-Oaten, A.W., 362; 409
Parrish, J.D., 346, 379; 404
Parrish, J.D. See Munro, J.L., 359; 402
Parrish, R.H., 273; 333
Parsons, T.R. See Strickland, J.D.H., 15; 43
Parulekar, A.H., 344; 404
See Harkantra, S.N., 160
Pastorok, R.A., 340, 345, 351, 354, 355, 363; 404
Patel, B., 94, 112, 113, 136, 138, 142, 145, 153; 163
See Crisp, D.J., 95, 133, 134, 142, 146; 158
Patel, B.A., 114; 163
Pathak, S.M. See Singh, V.P., 370; 408
Pathmarajah, M., 338, 340, 351; 404
Patterson-Zucca, C., 372; 404
See Lugo, A.E., 365; 400
See Twilley, R.R., 370; 410
AUTHOR INDEX
Paul, J.S., 33; 42

Paul, M.D., 135, 147; 163
Paul, V.J., 183, 185, 194, 195, 197, 258; 269
See Hay, M.E., 265
See Sun, H.H., 194; 271
See Wylie, C.R., 183, 194, 195; 272
Paulson, A.C. See Smith, R.L., 183, 206, 216, 221, 225;
270
Pauly, D., 339, 344, 346, 368, 372, 375, 381; 404
See Longhurst, A.R., 339; 400
See Navaluna, N.A., 349, 357; 403
Pawlik, J.R., 99; 163
Paxton, S.R. See Gomon, M.F., 181, 235, 255; 265
Payne, A.I., 216, 221, 223, 224; 269
Payri, C. See Faure, G., 393
Pearse, J.S., 55; 89
Pearson, R., 340; 404
Pease, B.C. See Burchmore, J.J., 263
Peavey, D.G. See Goldman, J.C., 15; 41
Pecora, F.A. See Rogers, C.S., 349; 406
Pellenbarg, R.E. See Segar, D.A., 343; 407
Peltier, G., 36; 42
Penachetti, C.A. See Young, C.M., 90
Pendleton, D.E. See Marsh, J.A., 345; 401
Penniman, C.A., 34; 42
Penry, D.L., 228, 229, 231, 236; 269
Perera, M.K. See De Silva, S.S., 204; 264
Pernetta, J. See Morauta, L., 340; 402
Perrault, G.-H. See Bablet, J.-P., 356; 387
Peters, D.S. See Lewis, V.P., 169, 205; 267
Peters, E.C., 363; 404
Peyrot-Clausade, M., 351; 404
Pfeffer, R.A., 364; 404
Pfister, C.A. See Hay, M.E., 188; 265
Pheng, K.S. See Seng, L.T., 407
Phillips, P.C., 370; 404
Phillips, R.C., 339; 404
See Bridges, K.W., 389
See Fonseca, M.S., 379; 394
See Zieman, J.C., 414
Phinney, D.A. See Legendre, L., 42
Piatt, J.F. See Schneider, D.C., 274, 305, 328; 334
Piccinin, B.B. See Harris, G.P., 35; 41
Pickard, E. See Wolanski, E., 358; 413
Pickard, G.L., 347; 404
Pierce, G.J., 190; 269
Pierson, D.C. See Cullen, J.J., 15; 40
Pillai, N.K., 132, 136, 144, 147, 148; 163
Pillar, S.C. See Shannon, L.V., 274; 334
375
Pillay, K.K., 94, 136, 147; 163

Pillay, T.V.R., 223, 224; 269
Pilsbry, H.A., 116; 163
Pimm, S.W. See King, A.W., 350; 398
Pinto, L., 368; 404
Pirazzoli, P.A., 383; 404
Pirt, S.J., 19; 43
Pitman, R.L. See Au, D.W.K., 309; 329
Plante-Cuny, M.-R., 14; 43
Platt, T., 19; 43
See Smith, J.C., 27, 29; 43
See Smith, R.E.H., 35; 43
Plenge, M. See Duffy, D.C., 284; 331
Pochon-Masson, J. See Bocquet-Vdrine, J., 94; 158
See Turquier, Y., 94, 104; 165
Poiner, I.R., 376; 404
Poli, G., 338; 404
Poliakova, I.W. See Zevina, G.B., 92; 166
Pollak, P.E. See Montgomery, W.L., 208, 210, 220, 227;
268
Pollard, D.A. See Bell, J.D., 188, 211, 231, 252; 262
See Burchmore, J.J., 263
See Klumpp, D.W., 378; 399
Pollard, P.C. See Moriarty, D.J.W., 268, 402
Pollock, D.E. See Crawford, R.J.M., 274, 293, 298, 308,
312, 313, 326; 331
Polovina, J.J., 350; 404
See Marten, G.G., 358; 401
Polunin, N.V.C., 202, 213, 216, 234, 250, 251, 341, 351,
352, 359, 371, 382, 383; 269, 405
See Lubbock, H.R., 359; 400
See Robertson, D.R., 172, 259; 269
See Robinson, A., 383; 406
Pomroy, A.J. See Joint, I.R., 14; 41
Pooland, D.J. See Cintron, G., 346; 391
Pope, E. See Dakin, W.J., 75; 87
Pope, B.C., 126, 127; 163
Pople, W. See John, D.M., 243; 266
Popovic, R., 23; 43
Por, F.D., 339, 365; 405
Por, I. See Por, F.D., 365; 405
Porcher, M. See Gabrie, C., 351, 358, 363; 394
Porter, J.W., 349; 405
See White, M.W., 347; 412
Porter, W.J. See Kjerfve, B., 349; 399
Potts, D.A., 355; 405
Potts, D.C., 246; 269
Potts, F.A., 99; 163
376
Pough, F.H., 234; 269

Poulet, S.A. See Moal, J., 42
Powell, H.T., 127, 128, 153; 163
Power, M.E., 241; 269
Powles, S.B., 31; 43
Praseno, D.P., 383; 405
Prejs, A., 205; 269
Preobrozhensky, B.V., 347; 405
Prescott, J.H. See Norris, K.S., 188, 198; 268
Preston, R.D. See Mackie, W., 193, 205; 267
Przelin, B.B., 14, 17, 18, 29, 34; 43
See Samuelsson, G., 23; 43
Prigogine, I., 350; 405
Priscu, J.C., 24, 30; 43
Prosch, R.M. See Armstrong, M.J., 320, 323; 328, 329
Pulliam, H.R. See Pyke, G.H., 190; 269
Purdie, D.A. See Williams, P.J.le B., 14; 44
Putnam, G.B. See Lee, D.J., 217; 267
Putney, A., 350, 382; 405
See Geoghegan, T., 340; 395
Putro, S. See McMeekin, T.A., 42
Putt, M. See Przelin, B.B., 34; 43
See Rivkin, R.B., 14; 43
Pyefinch, A., 101, 124, 137, 143; 163
Pyke, G.H., 190; 269
Qasim, S.Z., 344; 405
Quast, J.C., 169, 174, 179, 180, 185, 187, 188, 195, 198,
251, 252, 254, 256; 269
Queen, W.H., 378; 405
Quinn, J.F. See Grosberg, R.K., 64; 87
Quinn, N.J., 368, 379, 383; 405
Qurashi, A.A. See El-Rayis, O.A., 354; 393
Rabanal, H.R. See New, N.B., 371, 375, 376; 403
Rabinowitz, D., 365; 405
Ragan, M.A., 193, 194; 269
Rahman, R.A. See Nair, M.Y., 368; 402
Ralph, P.M., 134; 163
Ralston, S.L., 179, 180, 217; 269
Ramachandra Reddy, A., 27; 43
Ramamoorthi, K. See Fernando, A.S., 147; 159
Rand, A.S., 234; 269
Rand, R.W., 274, 287, 291, 292, 293, 297, 300, 301, 302,
314, 315, 318, 320, 322, 324; 333
See Broekhuysen, G.J., 308; 329
Randall, B.M., 318; 333
See Randall, R.M., 277, 278, 280, 281, 287, 293, 298,
300, 304, 309, 315, 317; 333, 334
Randall, D.J. See Wu, R.S.S., 147; 165
Randall, J.E., 169, 175, 183, 184, 186, 187, 198, 206, 216,
222, 225, 235, 237, 238, 239, 241, 242, 243, 250, 256,
259, 359, 384; 269, 405
Randall, R., 312, 314; 333
Randall, R.H., 349; 405
See Birkeland, C.E., 349; 388
Randall, R.M., 277, 278, 280, 281, 287, 293, 298, 300,
303, 304, 309, 311, 314, 315, 317, 318, 321; 333, 334
See De Kock, A.C., 277, 291, 319; 331
See Duffy, D.C., 285; 331
See Heath, R.G.M., 274, 307, 308, 321; 332
See Morant, P.D., 319; 333
See Randall, B.M., 318; 333
Rao, A.N., 370; 405
See Soepadma, E., 339; 408
Rapport, D.J., 346, 363; 405
Rashid, R., 357, 360; 405
Rasmussen, T., 113, 117; 163
Ratkowsky, D.A. See McMeekin, T.A., 42
Rau, N., 361; 405
Raven, J.A., 26; 43
See Geider, R.J., 37; 40
See Johnston, A.M., 33; 41
See Richardson, K., 21, 35; 43
Ray, G.C., 339, 362, 384, 385; 405
See Robins, C.R., 235; 270
Raymond, R., 362; 405
Reaka, M.L., 339; 405
Redalje, D.G. See Laws, E.A., 12; 42
Reed, D.C. See Hughes, T.P., 244; 266
Reese, E.S., 180, 363; 269, 405
See Devaney, D.M., 339; 392
Reese, J.P., 58; 89
Reeson, P.H. See Munro, J.L., 344; 402
Reeves, P., 376; 405
Rege, M.S., 135, 148; 163
Regier, H.A. See Rapport, D.J., 346, 363; 405
Reihelt, R.E., 349, 363, 384; 405
See Bradbury, R.H., 338, 347, 350, 362, 384; 389
See Green, D.G., 350; 395
Reid, J.L. See Shulenberger, E., 15; 43
See Wooster, W.S., 273; 335
Reid, R.G.B. See Fankboner, P.V., 342; 393
Reid, R.O. See Whitaker, R.E., 377; 412
Reimer, A.A. See Birkeland, C.E., 353; 388
AUTHOR INDEX
Reinhard, E.G., 96, 97, 98, 99, 100, 101, 148; 163
Reischman, P.G., 92, 97, 98; 163
Relini, G., 126, 127, 135, 138, 139, 140, 148; 163
Ren, X., 112; 163
Renard, Y. See Geoghegan, T., 340; 394
Renaud, M.L., 342; 405
Renaud, P.E. See Hay, M.E., 188, 194; 265
Renaud-Mornant, J. See Salvat, B., 407
Renger, E.H. See Balch, W.M., 15; 39
Revelle, R., 342, 344; 406
Reverberi, G., 54; 89
Reyes Jr, D.M. See Pantastico, J.B., 205; 269
Ricard, M., 351; 406
See Salvat, B., 407
Rich, P.V., 281; 334
Richard, G. See Poli, G., 404
See Salvat, B., 407
Richards, W.J., 225, 348, 349; 269, 406
Richardson, K., 16, 21, 23, 24, 35, 37, 38; 43
Richerson, P.J. See Vincent, W.F., 34; 44
Richmond, R.H. See Jokiel, P.L., 339; 398
Ricklefs, R.E. See Duffy, D.C., 332
Ridd, P. See Wolanski, E., 373, 369; 413
Riegl, W. See Spackman, W., 365; 409
Riegle, K.C., 230; 269
Riemann, B. See Holm-Hansen, O., 17; 41
Rigo, L., 94; 163
Riley, G. See Grave, C.A., 53; 87
Riley, J.P., 342; 406
Rimmer, D.W., 170, 186, 187, 194, 196, 199, 212, 216,
217, 218, 221, 226, 227, 231, 234; 269
See Johannes, R.E., 398
Rinkevich, B., 353; 406
See Loya, Y., 340, 353, 354; 400
Rioux, R.H. See Summerhayes, C.P., 285; 335
Risk, M.J., 246; 269
See Sammarco, P.W., 237, 246; 270
Ritchie, L.E., 96, 97, 98, 100, 101; 163
See Heg, J.T., 96; 160
Ritz, D.A. See Crisp, D.J., 145; 158
Rivkin, R.B., 14, 15, 29, 38; 43
Robbin, D.M. See Hudson, J.H., 351, 352; 397
Robblee, M.B., 377; 406
See Smith III, T.J., 365; 408
See Zieman, J.C., 378; 414
Roberts, C.M., 171, 172; 269
Roberts, D.A. See Hallacher, L.E., 199, 207, 222; 265
Roberts, H.H., 347, 357; 406
377
See Walker, N.D., 346; 412

Robertson, A.I., 208, 212, 217, 225, 368, 369, 370, 380;
269, 406
See Hatcher, B.G., 337414
Robertson, D.R., 171, 172, 179, 238, 241, 259, 344; 269,
270, 406
See Lessios, H., 338, 349; 399
See Lessios, H.A., 245; 267
Robertson, H.G., 288, 304, 305; 334
See Cooper, J., 277; 330
Robins, C.R., 235; 270
Robinson, A., 383; 406
Robinson, A.H. See Salm, R.V., 363; 407
Robinson, A.R. See Lobel, P.S., 349; 400
Robinson, W.E., 52; 89
Robison, B.H., 207, 222, 254; 270
Rochet, M., 14; 43
Rodelli, M.R., 368; 406
Rodriquez, A., 338, 351; 406
Rogers, C.S., 338, 347, 349, 351, 358, 360, 380; 406
Rogers, R.A. See Jokiel, P.L., 339; 398
Rojas de Mendiola, B. See Strickland, J.D.H., 25; 43
Rollet, B., 340; 406
Romairone, V. See Geraci, S., 135, 138, 140; 159
Rose, B. See Ryan, P.G., 277, 278, 283, 284, 285, 288,
303, 304, 305, 307, 309, 310, 327; 334
Rose, C. See Sammarco, P.W., 246; 270
Rose, S.M., 57; 89
Resell, N.C., 110, 136; 163
Rosen, B.R., 347; 406
Rosenberg, M.J. See Horn, M.H., 189; 266
Rosenberg, R. See Barrett, G.W., 340; 388
Rosenblatt, R.H., 180; 270
Rosenqvist, E. See Samuelsson, G., 43
Roskell, J. See Bainbridge, V., 113, 115; 156
Ross, A., 102, 110; 163
See Newman, W.A., 102, 107, 109, 118, 120, 134; 162
Ross, G.J.B., 312; 334
See Batchelor, A.L., 287, 297, 298, 303, 309, 312, 314,
324, 326, 327; 329
See Randall, R., 312, 314; 333
See Randall, R.M., 280, 281; 333, 334
Ross, M. See Moyer, J.T., 361; 402
Rougerie, F., 354; 406
Roughgarden, J., 81, 82; 89
See Gaines, S.D., 196; 265
Round, F.E., 16, 33; 43
Rouse, L.J. See Walker, N.D., 346; 412
Rowe, F.W.E., 362; 406
378
Rowley, D. See Birkeland, C.E., 349; 388

Rowley, R.J. See Harris, L.G., 195; 265
Roy, J.P., 353; 406
Rozin, P., 217; 270
Rual, P. See Bour, W., 383; 389
Rubec, P.J., 359; 406
Ruddle, K., 339; 406
Ruggieri, G.D. See Coln-Urban, R., 113, 116; 158
Runnstrm, S., 137, 146, 149; 163
Russ, G., 180, 183, 239, 240, 241, 244, 340, 358, 385;
270, 406, 407
Russ, G.R., 247, 250; 270
Russell, B.C., 169, 173, 180, 185, 186, 188, 189, 194, 198,
217, 232, 253, 254, 256, 258, 259; 270
Russell, D.J., 360; 407
Russell, F.S., 343; 407
Russell-Hunter, W.D., 191; 270
Russo, A.R., 355; 407
Rutman, J., 343; 407
Ruyter van Steveninck, E.D.de, 243, 247; 270
Ryan, P., 283, 288, 304; 334
Ryan, P.G., 277, 278, 280, 283, 284, 285, 286, 310, 319,
327; 334
See Jackson, S., 293; 332
Ryther, J.H., 12, 37, 38, 39, 343; 43, 407
Rzepishevsky, I.K., 150; 163
Saenger, P., 340, 364, 365, 370, 371, 372, 373, 374, 376;
407
See Hutchings, P.A., 339; 397
See Ward, W.T., 339; 412
Sainsbury, K.J., 385; 407
Sakai, K., 363; 407
Sakshaug, E., 14, 18, 34; 43
Sale, P.F., 169, 180, 236, 239, 242, 340, 343, 348, 349,
358; 270, 407
See Moran, M.J., 179, 185; 268
Salesky, N. See Ogden, J.C., 243, 378; 268, 401
Salm, R.V., 338, 339, 340, 363, 384, 385; 407
Salomon, C.H., 346, 349; 407
Salvat, B., 338, 340, 347, 351, 358, 362, 384, 385; 407
See Dahl, A.L., 338, 346, 350; 392
Samain, J.-F. See Moal, J., 42
Sammarco, P.W., 237, 244, 245, 246, 247, 362, 363; 270,
407
See Baker, J.T., 339; 387
See Risk, M.J., 246; 269
See Wilkinson, C.R., 247; 272
Samuelsson, G., 23, 34; 43

See Richardson, K., 16; 43
Sanchez-Gil, P. See Soberon-Chavez, G., 408
Sander, F. See Tomascik, T., 346, 352, 354, 363, 364; 410
Sanders, H.L., 343, 344; 407
Sandison, E.E., 95, 126, 129, 130, 131, 132, 135, 136, 139,
140, 144, 147, 148; 163, 164
Sandmann, G., 23; 43
Sano, M., 360; 407
Santelices, B., 251; 270
Santnanam, R. See Venkataramanujam, R., 347, 383; 411
Sargent, J.R. See Cowey, C.B., 231; 264
Sasekumar, A. See Rodelli, M.R., 406
Sastry, A.N., 94; 164
Scarlatto, O.A. See Golikov, A.N., 343; 394
Schaeffer-Novelli, Y. See Cintron, G., 366; 391
Scheltema, R.S., 346; 407
Scherer, S., 37; 43
Schiel, D.R., 174, 256; 270
See Foster, M.S., 251; 264
See Kingsford, M.J., 256; 267
Schiemer, F. See Hofer, R., 215; 266
Schlager, W. See Hallock, P., 354; 396
Schlatter, R.P., 284; 334
Schlumpberger, J.L. See Schofield, V.L., 288, 291, 303,
304, 305, 306, 307, 308, 309, 49; 89
Schluter, D., 190; 270
Schmahl, G.P. See Tilmant, J.T., 357; 410
Schmid-Hempel, P. See Stearns, S.C., 190; 270
Schmidt, G.H., 75, 77; 89
Schmidtke, J., 49; 89
Schneider, D.C., 274, 284, 305, 328; 334
See Hunt Jr, G.L., 274, 305, 309, 328; 332
Schoener, T.W., 190; 270
Schofield, V.L., 49; 89
Scholander, P.F., 344, 366; 407
Schonewald-Cox, C.M., 384; 407
Schreiber, E.A. See Schreiber, R.W., 319; 334
Schreiber, R.W., 319; 334
See Croxall, J.P., 284, 310; 331
Schroeder, J.H., 338; 407
Sciscioli, M. See Lepore, E., 95, 138, 140; 161
Scoffin, T.P., 237, 348; 270, 407
See Brown, B.E., 352; 389
Scott, F.M., 52, 56; 89
Seapy, R.R. See Horn, M.H., 230; 266
Searl, C.E. See Solbakken, J.E., 409
Searles, R.B. See Lewis, S.M., 244; 267
See Stephenson, W., 242, 243, 244; 271
AUTHOR INDEX
Sebens, K.P., 73; 89

Segar, D.A., 343; 407
Segel, C.A., 361; 407
Seibert, D.L.R. See Thomas, W.H., 44
Seki, M.P. See Harrison, C.S., 309; 332
Seliger, H.H. See Rivkin, R.B., 38; 43
Sell, J.L., 232; 270
Semeniuk, V., 365, 369; 407
Seng, L.T., 353; 407
Senger, H. See Fleischhacker, P., 21; 40
Seow, R.C.W., 373; 408
etlk, I. See Allakhverdiev, S.I., 34; 39
etlkov, E. See Allakhverdiev, S.I., 34; 39
Sewell, R.B.S., 122, 123; 164
Shackleton, L.Y., 312; 334
Shaffer, M.L. See Sullivan, A.L., 385; 409
Shaklee, J.B., 347, 363; 408
Shannon, L.V., 274, 275, 276, 281, 305, 319; 334
See Agenbag, J.J., 276; 328
See Bergh, M.O., 320, 322; 329
See Chapman, P., 274; 330
See Crawford, R.J.M., 274, 293, 298, 308, 312, 313,
326; 331
Shapiro, L.P. See Legendre, L., 42
Shaughnessy, G. See Frost, P.G.H., 306; 332
Shaughnessy, P.D., 286, 291, 304, 311, 314, 317, 318,
326; 334
See Cooper, J., 277; 330
See Voisin, J.-F., 304, 307; 335
Sheldon, R.W., 15, 19, 344; 43, 408
Sheldon, J.M. See Robertson, D.R., 172; 269
Shelton, P.A., 276, 281, 291, 310, 311, 312, 313, 315, 317,
321, 325; 334
See Armstrong, M.J., 320, 323; 328, 329
See Cooper, J., 280, 310; 330
See Crawford, R.J.M., 274, 280, 281, 287, 291, 294,
295, 296, 297, 311, 312, 314, 315, 321, 324; 331
Shen, G.T., 353; 408
Sheppard, C.R.C., 352; 408
Shields, W.M., 64; 89
Shimizu, M. See Sano, M., 360; 407
Shinn, E.A., 348, 350; 408
See Hudson, J.H., 352; 397
Shirase, S., 99; 164
Shochat, S. See Ohad, I., 34; 42
Shoemaker, V.H. See Nagy, K.A., 233; 268
Short, F.T. See Howard, R.K., 378; 397
379
Shulenberger, E., 15; 43

Shumway, S.E. See Stickney, R.R., 205; 271
Sibly, R.M., 208; 270
Siefermann-Harms, D., 17, 34; 43
Siegfried, W.R., 281, 286, 291, 304, 324; 334, 335
See Duffy, D.C., 275, 284, 303, 307, 311, 312, 320,
322, 327; 331, 332
See Gardner, B.D., 319; 332
See Nagy, K.A., 321, 322; 333
Silberstein, K., 378; 408
Silpipat, S. See Windom, H.L., 413
Simberloff, D.S., 350; 408
Simmons, K.E.L. See Cramp, S., 291; 330, 331
Sims, N., 359; 408
Sinclair, J.C., 289, 291, 304, 305, 307, 323; 335
Singh, V.P., 370; 408
Skerman, T.M., 112, 113, 114, 115, 134, 136, 140; 164
Skjaeveland, S.H. See Gulliksen, B., 84; 87
Skyring, G.W. See Moriarty, D.J.W., 402
Slatyer, R.O. See Connell, J.H., 250, 348; 264, 391
Sleeter, T.D. See Dodge, R.E., 392
See Knap, A.H., 399
See Solbakken, J.E., 409
Slinger, S.J. See Atkinson, J.L., 204; 262
Smale, M.J., 309; 262, 335
See Berry, P.F., 262
Smit, H., 222; 270
See Kapoor, B.G., 169, 198, 222; 267
Smith, D.C., 226; 270
Smith, G., 95, 96, 97, 121; 164
Smith, G.B., 346; 408
Smith, G.J. See Porter, J.W., 349; 405
Smith, I.R., 376, 380, 382; 408
See Munro, J.L., 342, 346; 402
Smith, J.C., 14, 27, 29, 30; 43
Smith, J.L.B., 187; 270
Smith, M.M. See Smith, J.L.B., 187; 270
Smith, R.A. See De Silva, M.W.R.N., 358; 392
Smith, R.E.H., 35, 37; 43
Smith, R.G. See Windom, H.L., 413
Smith, R.L., 183, 206, 216, 221, 225; 270
Smith, S.R., 357; 408
See Knap, A.H., 399
Smith, S.V., 339, 354, 355, 356, 357, 361, 362; 408
See Hatcher, B.G., 348; 396
See Johannes, R.E., 398
380
Smith, T.J. See Odum, W.E., 367, 369; 403

Smith III, T.J., 365, 370; 408
Smyth, M.J., 102, 104, 106; 164
Snedaker, J.G. See Lugo, A.E., 340; 400
See Snedaker, S.C., 340; 408
Snedaker, S.C., 340, 368; 408
See Hamilton, L.S., 340, 371, 372, 376; 396
Soberon-Chavez, G., 368; 408
Soegiarto, A., 364, 372, 382, 383; 408
See Maragos, J.E., 383; 401
Soepadmo, E., 339, 368, 372; 408
Solbakken, J.E., 353; 409
SooHoo, J.B. See Palmisano, A.C., 42
SooHoo, S.L. See Palmisano, A.C., 42
Sorenson, J., 382; 409
Soule, M.E., 340; 409
Southward, A.J., 125, 126, 128; 164
Southward, E. See Southward, A.J., 125, 126; 164
Soysa, C.H. See Chia, L.S., 340; 390
Spackman, W., 365; 409
Spain, A.V. See Heinsohn, C.E., 377; 396
Spearpoint, J.A. See Every, B., 280; 332
Spies, R.B., 356; 409
Spivey, H.R., 106, 108; 164
Spurrier, J. See Dame, R., 392
Squire, B.A. See Coles, R.G., 391
Squire, L.C. See Coles, R.G., 391
Srirattanahai, S. See Srithanya, S., 360; 409
Srithanya, S., 360; 409
Stancyk, S. See Dame, R., 392
Stanford, W.P., 323; 335
Stanley, S.O., 370; 409
Staples, D.J., 368, 377; 409
See Poiner, I.R., 376; 404
Stark, K.P., 384; 409
See Baker, J.T., 339; 387
See James, M., 350, 384; 397
Steam, C.W. See Frydl, P., 237; 265
See Scoffin, T.P., 270, 407
Stearns, S.C., 190; 270
Stebbing, A.R.D., 352; 409
Stebbing, T.R.R., 112, 115; 164
Steele, D.H., 154, 155; 164
Steele, V.J. See Steele, D.H., 155; 164
Steemann Nielsen, E., 14, 15; 43
Stefoni, D.L., 133, 141; 164
Stehli, F.G., 342, 343, 344; 409
Stein, R.A. See Johnson, B.L., 381; 398
Steinberg, P.D., 193, 194, 195, 197, 258; 270, 271
See Estes, J.A., 193, 195, 197, 225, 227, 256, 258; 264
Steinitz, H. See Clark, E., 259; 263
Steneck, R.S., 194, 244, 245; 271
See Adey, W.H., 347, 348; 386
Stenseth, N.C., 190; 271
Stephens, D.W., 190; 271
Stephens Jr, J.S., 169, 174, 256; 271
Stephenson, T.A., 75; 89
Stephenson, W., 242, 243, 244; 271
Stevenson, H. See Dame, R., 392
Stewart, F.H., 120; 164
Stewart, T.C. See Reinhard, E.G., 96, 99; 163
Stewart-Oaten, A.W., 362; 409
Stickney, R.R., 205; 271
Stitt, M., 13; 43
See Krmer, S., 37; 42
Stockner, J.G., 19; 43
Stockton, P. See Lutjeharms, J.R.E., 276; 333
Stoddart, D.R., 338, 340; 409
Stoddart, J.A., 363; 409
Stoecker, D., 73; 89
Stone, R.L., 123, 124, 125, 143; 164
See Barnes, H., 95, 124, 125, 143, 145; 157
Stoner, A.W., 187, 207; 271
Strasburg, D.W. See Hiatt, R.W., 169, 170, 176, 178, 183,
184, 185, 186, 198, 232, 237, 256; 266
Strathmann, M.F. See Strathmann, R.R., 46, 48; 89
Strathmann, R.R., 46, 48, 82, 154; 89, 164
See Emlet, R.B., 63; 87
See Jackson, G.A., 63, 64, 74; 88
See Palmer, A.R., 63; 88
Straughan, D., 121, 123; 164
Strickland, J.D.H., 14, 15, 25; 43
Stuart, S.N. See Collar, N.J., 308; 330
Stubbings, H.G., 110, 112, 120, 126, 133; 164
Sturzl, E. See Scherer, S., 37; 43
Stutterheim, C.J. See Ryan, P.G., 277, 280; 334
Subba Rao, D.V. See Platt, T., 19; 43
Suchanek, T.H. See Paine, R.T., 75; 88
See Rogers, C.S., 349; 406
Suharsono, W., 342; 409
Suhayda, J.N. See Roberts, H.H., 347, 357; 406
Sukarno, See Praseno, D.P., 383; 405
Sukenik, A., 19, 21, 24, 27, 29; 43
Sukumaran, N. See Venkataramanujam, R., 347, 382; 411
Sullivan, A.L., 385; 409
Sullivan, C.W. See Palmisano, A.C., 42
Summerhayes, C.P., 285; 335
Sun, H.H., 194; 271
AUTHOR INDEX
See Paul, V.J., 194; 269

Sutcliffe, W.H., 368; 409
See Sheldon, R.W., 15, 19; 43
Suter, W. See Walter, C.B., 286, 290, 291, 308, 326; 335
Sutherland, J.P., 84, 85; 89
Suyehiro, Y., 169, 206, 211, 214, 231; 271
Suzuki, R., 17; 43
Svane, I., 4590; 47, 54, 55, 59, 60, 63, 68, 69, 70, 77, 80,
82, 83, 84, 85, 120; 89, 164
See Havenhand, J.N., 75, 77, 78; 87
Sverdrup, H.U., 342; 409
Swart, P.K. See Potts, D.A., 355; 405
Sweatman, H.P.A. See Robertson, D.R., 171; 270
Swift, E. See Rivkin, R.B., 38; 43
Sybesma, J. See Duyl, F.C.van, 55, 68, 77; 87
Symonds, P.A., 348; 409
Syrett, P.J. See Everest, S.A., 28; 40
Szmant-Froelich, A. See Dodge, R.E., 340; 392
Taborsky, M., 179, 182; 271
Tacon, A.G.J., 231; 271
Taghon, G.L., 228; 271
Taguchi, S., 14, 37; 43
Takahashi, M. See Bienfang, P.K., 14; 39
See Kishino, M., 25; 41
Talbot, C., 199, 204; 271
Talbot, F.H., 178, 183, 256; 271
See Goldman, B., 343; 394
See Munro, J.L., 359; 402
Tamaru, C.S. See Shaklee, J.B., 347, 363; 408
Tan, G.T. See Seng, L.T., 407
Targett, N.M., 184, 194, 195; 271
Targett, T.E., 256; 271
See Targett, N.M., 184; 271
Taylor, D.L., 339; 409
Taylor, P.R. See Hay, M.E., 244; 265
See Littler, M.M., 186, 194, 197, 227, 243, 258; 267
Teal, J.M See Onuf, C.P., 367; 404
Teas, H.J., 339; 409
Tegner, J.M., 346; 409
Tenerelli, V., 94, 127; 164
Terashima, I., 13, 27; 43
Thayer, G. See Zieman, J.C., 414
Thayer, G.W., 169, 184, 225, 233, 251, 367, 377, 378;
271, 409, 410
See Zieman, J.C., 378; 414
Therriault, J.-C. See Legendre, L., 42
Thibault, P. See Peltier, C., 36; 42
Thinh, L.-V., 14; 44
381
Thom, B.G., 365, 373; 410

Thoman, T.A. See Heck, K.L., 378; 396
Thomas, M.K. See Karande, A.A., 111, 127, 128, 131,
135, 136, 141; 161
Thomas, W.H., 25; 44
Thomassin, B.A. See Faure, G., 393
Thompson, D., 381; 410
Thompson, G.A. See Markly, J.L., 365; 401
Thompson, R. See Munro, J.L., 344; 402
Thomson, D.A., 174, 188, 256; 271
See Kotrschal, K., 207, 211, 215; 267
Thomson, J.M., 198, 212, 213, 218, 225; 271
Thorhaug, A., 378, 379; 410
See Marcus, J., 355, 356; 401
See Zieman, J.C., 414
Thorner, E., 113, 115, 117, 119; 164
Thorson, G., 59, 63, 66, 68, 70, 74, 80, 82, 343, 344; 89,
410
Thorsson, W.M. See Burch, B.L., 346; 390
Thresher, R., 343; 410
Thresher, R.E., 239, 254; 271
See Emery, A.R., 185; 264
Tighe-Ford, D.J., 143; 164
Tilmant, J.T., 357, 358, 360; 410
Tisdell, C., 364, 382; 410
Titcomb, M., 187; 271
Tiwari, K.K. See Mulcherjee, A.K., 365; 402
Todd, C.D., 84, 85; 89
Toffart, J.L. See Delesalle, B., 392
Togstad, H.A. See Grant, J.J., 251; 265
Tokioka, T. See Watanabe, H., 57; 90
Tolbert, N.E. See Husic, D.W., 36; 41
Tomascik, T., 346, 352, 354, 363, 364; 410
Tomlinson, J., 94, 103; 164
Tomlinson, J.T., 102, 103, 104, 105, 106, 107, 108; 164
See Batham, E.J., 102, 103, 104, 105, 107, 108; 157
See Newman, W.A., 105; 162
See Wells, H.W., 102, 104, 107; 165
Tooke, N.E., 145; 164
Torrence, S.A., 52, 53, 54, 67, 78; 89
Townsend, C.R., 190; 271
Trason, W.B., 55; 89
Tribble, G.W. See Pfeffer, R.A., 364; 404
Trindell, R.N. See Hay, M.E., 265
Tromp, B.B.S. See Boyd, A.J., 276;329
Trondle, J. See Poli, G., 404
Troyer, K., 228, 233; 271
Tsubata, B. See Hirai, E., 57, 58; 87
Tsuda, R.T., 184, 185, 351, 360; 271, 410
382

Tsuzuki, M. See Aizawa, K., 26; 39
Tubb, J.A., 116; 164
Tucker, J. See Hay, M.E., 265
Tundisi, J.G., 343; 410
Turner, R.E., 368, 372; 410
Turner, S.J. See Todd, C.D., 84, 85; 89
Turon, X., 54; 89
Turpin, D.H. See Weger, H.G., 36; 44
Turquier, Y., 94, 102, 103, 104, 105, 106, 107, 108, 109;
164, 165
Twilley, R.R., 370; 410
Tyler, W.A. See Fitzhardinge, R.C., 342, 356; 394
Tyler, W.B. See Briggs, K.T., 305, 321; 329
UNDP-UNESCO, 341, 371; 410
UNEP, 338, 340, 351, 358, 383, 385; 410, 411
UNEP-IUCN, 340; 411
UNESCO, 339, 340, 363, 378, 383; 411
UNESCO-UNEP, 340; 411
Underhill, L.G. See Whitelaw, D.A., 277; 335
Underwood, A.J., 75, 81, 154; 89, 165
See Denley, E.J., 130, 131; 159
See Otway, N.M., 131, 144; 162
Untawale, A.G., 370; 411
Urquhart, K.A.F., 169, 189, 205, 216, 217, 218, 220, 231;
271
Usher, G.F., 346; 411
Usuda, H., 13, 19; 44
Utinomi, H., 102, 103, 104, 105, 106, 107, 108, 112; 165
Uys, C.J., 314; 335
Vadas, R.L. See Paine, R.T., 194; 268
Vail, L. See Rowe, F.W.E., 362; 406
Valentine, J.W., 344; 411
Valiela, I. See Onuf, C.P., 367; 404
Van Alstyne, K.L. See Paul, V.J., 185, 194, 195, 197; 269
Van Baalen, C., 18; 44
Van Buurt, G. See Van den Hoek, C., 243; 271
Van Dyne, G.M. See Barrett, G.W., 363; 388
Van Kampen, P.N., 97; 165
Van Montfrans, J., 378; 411
Van Soest, P.J. See Demment, M.W., 236; 264
Van den Hoek, C., 243; 271
Van der Elst, R.P. See Berry, P.F., 262
Van tHof, T., 360, 364, 385; 411
Vance, D.J. See Staples, D.J., 368, 377; 409
Vance, R.R., 48, 63, 154; 89, 165
VanPraet, M. See Faure, G., 393
Vasseur, P. See Faure, G., 393

Vastano, A.C. See Whitaker, R.E., 377; 412
Vaughan, F.A., 187, 202, 204; 271
Vedder, K. See Branscomb, E.S., 137, 138; 158
Veil, J.A. See Vermeij, G.J., 344; 412
Veillet, A., 92, 96, 97, 98, 99, 100; 165
Veldhuis, H. See Duffy, D.C., 332
Venkataramanujam, R., 347, 383; 411
Venrick, E.L., 14; 44
Vergonzanne, G. See Salvat, B., 407
Verheye-Dua, F. See Armstrong, D.A., 328
Verighina, I.A. See Kapoor, B.G., 169, 198, 222; 267
Vermeij, G.J., 344; 411, 412
Vernberg, F.J., 342, 344; 412
Vernberg, J. See Dame, R., 392
Vernotte, C. See Kirilovsky, D., 34; 41
Vesilev, B.P. See Nikolsky, G.V., 343, 344; 403
Vesk, M., 17, 18; 44
Vicente, V. See Williams, E.H., 338; 413
Victor, B.C. See Wellington, G.M., 172; 272
Vidaver, W. See Popovic, R., 23; 43
Videau, C., 14; 44
Vieira, A.A.H., 34; 44
Villalobos, C.R., 127, 128, 130, 131, 146; 165
Vincent, W.F., 34; 44
Vine, P.J., 241, 246, 247; 271
Virnstein, R.W., 376, 378; 412
Visscher, J.P., 105, 108; 165
Vivekanandan, E. See Pandian, T.J., 169, 170, 215, 231;
268
Vogel, S., 60, 65; 89
Voisin, J.-F., 304, 307; 335
Volcani, B.E. See Paul, J.S., 33; 42
Volkouinsky, V.V. See Koblentz-Mishke, O.J., 399
Von Caemmerer, S., 21; 44
Voris, H.K. See Jeffries, W.B., 116, 117; 160
Vorontsova, M.N., 54; 90
Vrolijk, N.H. See Targett, N.M., 184; 271
Wadano, A. See Yokota, A., 44
Wade, B.A., 343; 412
Wadman, H. See Appleby, G., 29; 39
Wagh, A.B., 127, 135, 136, 140; 165
Wahbeh, M.I., 376; 412
Wainwright, P.C. See Lewis, S.M., 239, 259; 267
Wake, J. See Heinsohn, C.E., 377; 396
Waldron, H. See Armstrong, D.A., 328
Walhe, C.M., 362; 412
Walker, C.W. See Pearse, J.S., 55; 89
AUTHOR INDEX
Walker, D., 12, 25; 44

Walker, D.A., 27; 44
See Delaney, M.E., 15, 24, 27; 40
See Lilley, R.McM., 27; 42
Walker, D.I., 172, 352, 355, 377; 271, 412
Walker, G., 92, 93, 94, 100; 165
Walker, N.D., 346, 349; 412
Wallace, C.C., 349; 412
See Babcock, R.C., 387
Walley, L.J., 93, 94; 165
Walsh, G.E., 340, 367, 370; 412
Walsh, R.C. See Loomis, J.B., 384, 385; 400
Walsh, T.W. See Kimmerer, W.J., 345; 398
Walsh, W.J., 346, 349, 358; 412
Walter, C.B., 286, 290, 291, 307, 308, 326; 335
Walters, V. See Scholander, P.F., 344; 407
Wanders, J.B.W., 243; 271
Waples, R.S. See Shaklee, J.B., 347, 363; 408
Ward, W.T., 339; 412
Warne, D.K., 383; 412
Watanabe, H., 56, 57, 58, 59; 90
See Hashimoto, K., 57; 87
Watling, L. See Steneck, R.S., 194; 271
Watson, J.G., 364, 365, 371, 372; 412
Waugh, G.D See Knight-Jones, E.W., 133, 134; 161
Wauthy, B. See Rougerie, F., 354; 406
Weger, H.G., 36; 44
Weiler, C. See Schmidtke, J., 49; 89
Weinstein, M.P., 205; 271
Weismann, I.L. See Schofield, V.L., 49; 89
Weiss, C.M., 135, 138, 139, 144; 165
Weiss, M.P., 351; 412
Weldon, W.F.R. See Smith, G., 121; 164
Wellington, G.M., 172, 246; 271, 272
Wellington, J.T. See Boto, K.G., 367; 389
Wells, A.G., 365; 412
Wells, H.W., 102, 104, 107; 165
Wells, J.W. See Stehli, F.G., 344; 409
Wells, K.F. See Uys, C.J., 314; 335
Wells, S.M., 338, 347, 359, 362, 363; 412
Wenno, J.J. See McManus, J.W., 356; 401
Werner Jr, W.E., 94, 141, 146; 165
West, A.B., 57, 58, 59; 90
West, L.A. See Schofield, V.L., 49; 89
Westernhagen, H.von, 185; 272
Westley, L.C. See Howe, H.F., 170; 266
Westoby, M., 191; 272
383
Wethey, D.S., 146, 147; 165

Wetstone, G.S. See Heck, K.L., 378; 396
Wetzel, R. See Van Montfrans, J., 378; 411
Weyer, D., 384; 412
Wheeler, A., 169; 272
Whitaker, R.E., 377; 412
White, A.T., 352, 364, 382, 383, 384; 412
See Cabanban, A.S., 364, 383; 390
White, D.C. See Moriarty, D.J.W., 402
White, F., 105;165
White, F. See Walley, L.J., 94; 165
White, M.W., 347;412
White, T.C.R., 207, 234; 272
Whitelaw, D.A., 277, 278; 335
Whitfield, A.K., 277, 291, 306; 335
Whittaker, J.R., 46, 54; 90
Whittaker, R.H., 12, 13, 17, 23;44
Whittingham, D.G., 57, 58; 90
Wiebe, W.J., 354, 377, 379; 413
See Johannes, R.E., 354; 398
See Rimmer, D.W., 170, 186, 187, 194, 196, 199, 212,
216, 217, 218, 221, 226, 227, 231; 269
Wiegert, R.F., 244; 272
Wiesenburg, D.A. See Lohrenz, S.E., 42
Wijsman-Best, M., 360, 382; 413
Wilber, G.G., 342; 413
Wilcox, B.A. See Soule, M.E., 340; 409
Wilkins, M.B., 222; 272
Wilkins, S.C. See Marsh, J.A., 345; 401
Wilkins, S. De C. See Nelson, S.G., 200, 238; 268
Wilkinson, C.R., 247; 272
Wilkinson, M. See Mills, D.K., 14, 34; 42
Wilkinson, M.T. See Elston, R.A., 99; 159
Willemoes-Suhm, R. von, 112, 113, 115; 165
Williams, A.H., 247, 249; 272
See Sammarco, P.W., 245, 246; 270
Williams, A.J., 281, 287, 291, 292, 293, 306, 319; 335
See Cooper, J., 277, 311, 321; 330
See Crawford, R.J.M., 310, 314; 331
Williams, D.C. See Williams, G.C., 188; 272
Williams, D.M., 349, 357; 413
See Munro, J.L., 340, 341, 346, 349; 402
See Sale, P.F., 348; 407
Williams, E.H., 338; 413
Williams, G.C., 188; 272
Williams, P.J.le B., 14; 44
Williams, R.B. See Thayer, G.W., 378; 410
384
Williams, S., 378; 413

Williams, S.L. See Thayer, G.W., 271, 409
Willis, B.L. See Babcock, R.C., 387
See Oliver, J., 349, 357; 404
Willoughby, N.G., 356; 413
Wilson, E.O. See MacArthur, R.H., 385; 401
Wilson, K.A. See Heck, K.L., 378; 396
Wilson, K.C. See Grant, J.J., 251; 265
Wilson, M.-P. See Duffy, D.C., 293, 298; 332
See Wilson, R.P., 274, 293, 298, 304, 306, 307, 318;
335
Wilson, R.P., 231, 274, 287, 293, 298, 300, 302, 304, 306,
307, 308, 318, 326; 272, 335
See Duffy, D.C., 293, 298, 318, 326; 332
See Nagy, K.A., 321, 322; 333
See Ryan, P.G., 304; 334
Wimpenny, R.S., 343; 413
Wimpenny, J.W.T. See Hughes, D.E., 223; 266
Windell, J.T. See Morris, J.S., 222; 268
Windom, H.L., 352; 413
Winter, K. See Demmig, B., 34; 40
Winterbottom, J.M., 283; 335
Wirtz, P. See Goldschmid, A., 199, 207, 211, 223; 365
Wisely, B., 110, 111, 126, 128, 129, 130, 131, 133, 134,
135, 138; 165
Withers, T.H. See Newman, W.A., 91; 162
Witschi, E., 113, 114; 165
Woelkerling, W.J. See Walker, D.I., 377; 412
Wohlschlag, D.E., 344; 413
Wolanski, E., 358, 369, 373; 413
See Williams, D.M., 349, 357; 413
Wolf, N.G., 183, 184, 197; 272
Wolfe, D.A. See Thayer, G.W., 378; 410
Womersley, H.B.S., 344; 413
Wong, C.H., 371; 413
See Gong, W.K., 371; 395
Wong, K.M. See Noshkin, V.E:, 356; 403
Wood, E., 343, 359; 413
Wood, E.J.F., 339; 413
Wood, E.M., 338; 413
Wood, L.F., 345; 413
Wood, L.W., 17; 44
Wood, W.F., 35; 44
Woodbridge, H., 67, 69, 80, 81; 90
See Grave, C.A., 52, 57, 60, 65, 68, 69; 87
Woodland, D.J., 357; 413
Woodley, J.D., 346, 349, 382, 384; 413
See Kjerfve, B., 349; 399

Woollacot, R.M., 58; 90
Wooster, W.S., 273; 335
Wortzlavski, A. See Achituv, Y., 126, 129, 130, 150; 156
Wrench, P.M. See Hiller, R.G., 23; 41
Wright, G.D., 382; 413
Wu, R.S.S., 138, 145, 146, 147, 148; 165
Wyers, S.C. See Knap, A.H., 399
Wylie, C.R., 183, 194, 195; 272
Wyman, K. See Dubinsky, Z., 24; 40
Yamaguchi, M., 56, 57, 58, 59, 60, 83; 90
Yamaguchi, T., 141, 142, 349, 350, 361; 165, 413
Yamamoto, N., 238; 272
Yamazato, K., 351, 352; 413
See Sakai, K., 363; 407
Yan,W., 140; 166
Yanagimachi, R., 92, 96, 97, 98, 100; 166
See Ichikawa, A., 92, 96, 97, 100; 160
See Shitase, S., 99; 164
Yanez-Arancibia, A., 367; 413
See Soberon-Chavez, G., 408
Yap, H.T., 352, 355, 363, 382; 413
See Alino, P.M., 387
See Gomez, E.D., 359, 383, 384; 395
Yasuda, T., 138, 139, 140, 141; 166
Yasugi, R. See Ishida, S., 108, 135; 160
Yasumoto, T., 361; 413
Yen, S., 359; 413
Yentsch, C.M. See Legendre, L., 16; 42
Yentsch, C.S., 14, 16; 44
See Legendre, L., 16; 42
Yokota, A., 27, 33, 37; 44
York, R.H. See Jokiel, P.L., 35, 345; 41, 398
Yoshida, M. See Kajiwara, S., 70, 72; 88
Young, C.M., 46, 53, 57, 58, 59, 60, 63, 64, 66, 67, 68, 69,
70, 73, 74, 75, 76, 77, 78, 79, 80, 81, 82, 83, 84; 90
See Chia, F.-S., 46, 60; 86
See Svane, I., 4590
Young, D.K., 378; 413
Young, J.R. See Birkeland, C.E., 353; 388
Young, J.W. See Blaber, S.J. M., 370; 388
Young, M.W. See Young, D.K., 378; 413
Young, P.C., 377; 414
See Bradbury, R.H., 347, 349, 357; 389
See Bridges, K.W., 389
AUTHOR INDEX
See Kirkman, H., 377; 399

Younge, M., 350; 414
Zann, L.P., 94, 113, 114, 116, 132; 166
Zell, L.D., 364; 414
Zeller, D.C., 247, 251; 272
Zenvirth, D., 26; 44
Zerba, K.E. See Stephens Jr, J.S., 169, 174, 256; 271
Zevina, G.B., 92, 118, 119, 123, 137, 138, 139; 166
Zhu, M. See Cullen, J.J., 15; 40
Zieman, J.C., 376, 377, 378, 379; 414
See Ogden, J.C., 377, 379; 403
See Robblee, M.B., 377; 406
See Thayer, G.W., 271, 409
Zieman, R.T. See Zieman, J.C., 378; 414
Zingmark, R. See Dame, R., 392
Zullo, V.A., 91, 102; 166
See Newman, W.A., 91; 162
385
SYSTEMATIC INDEX
Abudefduf amabilis, 177

biocellatus, 177
dicki, 177
glaucus, 177
lacrymatus, 177
saxatilis, 177, 235
septemfasciatus, 177
sindonis, 175
sordidus, 175, 177
taurus, 176, 235
Acanthaster, 340
Acanthuridae, 167, 173, 174, 175, 176, 178, 179, 183, 200,
209, 216, 219, 220, 224, 255, 257
Acanthuroidei, 255
Acanthurus, 223
achilles, 175, 176, 209
aliala, 176
bahianus, 175, 197
bariene, 178
bicommatus, 178
bleekeri, 220
chirurgicus, 175
coeruleus, 175, 197
dussumieri, 175, 209, 240
fuliginosus, 178
gahhm, 176, 220
glaucopareius, 175, 209, 220, 240
guttatus, 175, 176, 200, 209, 220
leucopareius, 175, 209
leucosternon, 172, 178

lineatus, 172, 174, 176, 220, 239, 240, 241
lineolatus, 178
mata, 175, 176, 209, 220, 240
nigricauda, 240
nigrofuscus, 175, 191, 208, 209, 210, 218, 219, 220,
227, 240, 241
nigroris, 175, 176, 209
olivaceus, 175, 176, 200, 210, 220
sandvicensis, 175, 183, 209
triostegus, 174, 176, 200, 220
triostegus sandvicensis, 183, 206, 216
xanthopterus, 173, 175, 177, 220
Acasta spongites, 134
Acipenser transmontanus, 230
Acropora, 246
palifera, 246
Acroscalpellum, 118, 154, 155
africanum, 118
angulare, 118
darwinii, 118, 120
Acrostichum, 371
Acrothoracica, 91, 92, 93, 102, 103, 106, 120
Alcidae, 284
Alcippe lampas, 102, 104, 105, 106, 108
(=Trypetesa) lampas, 105
Alcyonium siderium, 73
Aldrichetta forsteri, 212
Alepas intermedia, 116
386
SYSTEMATIC INDEX
morula, 116
pacifica, 116
Allolumpenus hypochromus, 236
Alutera choepfi, 176
Amblyglyphidodon, 222
Ammodytes, 292
capensis, 301
Amphidinium carterae, 29
Anacystis nidulans, 18
Anelasma, 110
squalicola, 112, 154, 156
Anisarchus medius, 236
Anoplarchus insignis, 236
purpurescens, 236
Anous stolidus, 279
tenuirostris, 280
Aplidium (Amaroucium) constellation, 56, 65, 68, 69
(Amaroucium) pellucidum, 69
antillense, 56
constellatum, 66, 67, 71
stellatum, 56, 73, 80, 82
Aplodactylidae, 167, 173, 174, 180, 188, 211, 221, 255
Aplodactylus arctidens, 173, 181, 182, 208, 211, 221, 224
etheridgi, 174
Aplousobranchiata, 50, 52
Apoda, 91
Apolemichthys trimaculatus, 178
xanthopunctatus, 220
Aptenodytes patagonicus, 279
Archaeobalanidae, 134
Archosargus probatocephalus, 187, 214, 220
rhomboidalis, 176, 187, 202, 204
Arctocephalus pusillus pusillus, 281
Ascidia, 49, 62
atra, 62
callosa, 49, 60, 66, 69, 77
ceratodes, 49
curvata, 62
mammillata, 62
mentula, 49, 62, 63, 69, 70, 75, 76, 77, 78, 83, 84
nigra, 63, 69, 70, 74, 76, 77, 81, 83, 84
paratropa, 69
prunum, 62
Ascidiella, 83
aspersa, 60, 62
scabra, 77
Ascidiidae, 52, 69
Ascothoracica, 91, 92
Atheriniformes, 255
387
Australophialus pecorus, 103, 105, 106, 108

tomlinsoni, 102
turbonis, 104, 105
Austrobalanus imperator, 130
Austromegabalanus nigrescens, 141
Avicennia marina, 374
Awous stamineus, 211
Balaenoptera edeni, 309
Balanidae, 134
Balanodytes taiwanus, 105
Balanoidea, 109, 132
Balanomorpha, 109, 125, 154
Balanus, 134, 135, 146
alatus, 135
aligcola, 95, 135, 148
amaryllis, 135
amaryllis euamaryllis, 135
amphitrite, 94, 95, 144, 145
amphitrite albicostatus, 108, 135
amphitrite amphitrite, 94, 135, 147, 148
amphitrite cirratus, 136
amphitrite communis, 94, 136, 148
amphitrite denticulata, 134, 136
amphitrite hawaiiensis, 136, 147
amphitrite saltonensis, 146
amphitrite variegatus, 136
Balanus Austrobalanus flosculus, 141
balanoides, 94, 95, 134, 136, 142, 143, 144, 145, 146,
147, 148, 149, 150, 151, 152, 153, 154
balanus, 94, 95, 134, 137, 143, 146, 148, 149, 150,
154
calceolus, 137
carisous, 137
crenatus, 94, 108, 137, 142, 143, 145
eburneus, 94, 95, 138, 142, 146, 147, 148, 154
galeatus, 138
glandula, 138, 142, 143, 144, 145, 146, 147, 148, 151
hameri, 138, 143, 146, 148
hesperius, 138
imperator, 138
improvisus, 94, 95, 139, 144, 146, 148
kondakovi, 139
maxillaris, 139
Megabalanus psittacus, 141
Megabalanus rosa, 141, 142
Megabalanus volcano, 141, 142
nubilus, 139
pacificus, 139, 146, 152
388
pallidus, 147
pallidus stutsburi, 139
perforatus, 94, 95, 139, 142, 145, 150, 151, 154
reticulatus, 140, 152
rostratus, 95, 140, 146, 149
terebratus, 140
tintinnabulum tintinnabulum, 140
trigonus, 94, 140, 146
variegatus, 141, 147
variegatus cirratus, 141
venustus, 141
vestitus, 141
Balistidae, 175, 176, 177, 201, 255
Balistoidei, 255
Bathylasma corolliforme, 132
Berndtia, 105
nodosa, 102
purpurea, 102, 103, 105, 107, 108
Blenniidae, 173, 175, 176, 177, 179, 207, 211, 254, 255,
292
Blennioidei, 255
Blennius cristatus, 176
marmoreus, 176
sanguinolentus, 173, 211
Bocquetia rosea, 99
Boleophthalmus pectinirostris, 211
Boltenia, 62
echinata, 47, 83
villosa, 51, 65, 69, 78, 79, 80
Bolteniopsis prenenti, 75
Boodlea, 184
composita, 184
Boschmaella balani, 96
Botryllinae, 52
Botrylloides mutabilis, 57
nigrum, 57
Botryllus, 54
planus, 50, 57
schlosseri, 48, 53, 57, 64, 65, 67, 68, 69, 77, 81
Brevoortia tyrannus, 205
Bryozoichthys marjorius, 235
Bulweria bulwerii, 279
Calantica, 117
pollicipedoides, 118
Calonectris, diomedea, 278, 303
Calotomus spinidens, 178
Cantherines sandwichiensis, 175
Canthigaster amboinensis, 175
solandri, 177
Canthigasteridae, 175, 177
Carassius auratus, 191
Carcharinus brachyurus, 309
Carcinus maenas, 101
Carpophyllum, 181, 253
Catharacta antarctica, 279
maccormicki, 279
subantarctica, 305
Catophragmus polymerus, 129, 130
Caulerpa, 184
Cebidichthys violaceus, 173, 180, 188, 189, 190, 191,
192, 193, 194, 198, 203, 204, 205, 208, 214, 216, 217,
218, 220, 228, 230, 231, 235
Centroceras clavulatum, 184
Centropyge argi, 176
bispinosus, 178
flavissimus, 177, 220
potteri, 175
Cephalopoda, 290, 295, 300
Ceramium, 186
Ceratium longipes, 14
Ceratoscopelus warmingii, 222, 254
Chaetodon ephippium, 177
reticalatus, 177
Chaetodontidae, 175, 176, 177
Chamaesipho brunnea, 128, 129, 149
columna, 128, 129, 144
Chanidae, 220, 255
Chanoidei, 255
Chanos chanos, 205, 220, 222
Charadriidae, 282
Charadriiformes, 277, 279, 281, 284
Chelonibia, 132
restudinaria, 132
Chelonobia, 132
patula, 92, 148
Chelyosoma production, 49, 57, 69, 70, 75, 77, 78
Chionelasmatoidea, 109, 125
Chirolophis decoratus, 235
nugator, 236
Chirona tenuis, 92
Chlamydomonas reinhardtii, 35
Chlidonias leucoptera, 278
niger, 279, 283
Chlorella, 14, 19, 20
Chlorophyta, 183
Chondria, 252
Chorisochismus, 292
SYSTEMATIC INDEX
Chromis, 222
cyanea, 235
enchrysurus, 235
insolatus, 235
multilineata, 235
scotti, 235
Chrysophyta, 183
Chthamaloidea, 109, 125, 128, 129
Chthamalophilidae, 96
Chthamalophilus delagi, 96, 98
Chthamalus, 94, 95, 125, 126, 128, 129, 146
anisopoma, 126, 143, 146
antennatus, 126
challenged, 126, 128, 149
dalli, 125, 126;146, 148, 153
dentatus, 126, 148, 150
depressus, 126, 128
fissus, 126, 128, 142, 144, 146, 151
fragilis, 125, 146
fragilis var. denticulata, 148
intertextus, 127
malayensis, 127, 128, 148
montagui, 127, 128, 150
stellatus, 94, 95, 125, 127, 128, 142, 145, 146, 150,
151, 153
withersi, 127, 128, 148
Cichlidae, 191
Ciona, 62
intestinalis, 49, 51, 54, 57, 58, 63, 69, 70, 74, 76, 80,
83, 84
savignyi, 70, 72
Cionidae, 52, 57, 69
Cirripectus sebae, 177
variolosus, 175, 177
Cirripedia, 91, 92, 109
Cladophora, 186
Cladophoropsis, 184
Clavelina oblonga, 49, 56, 73
picta, 49, 76
Clinidae, 292
Clinocottus globiceps, 173
Clistosaccidae, 96
Clistosaccus paguri, 96, 97, 98, 101
Cnemidocarpa finmarkiensis, 54, 69, 70
Conchoderma auritum, 113, 116
virgatum, 116, 117
Corallina officinalis, 194
Corella, 62
inflata, 47, 49, 51, 57, 60, 61, 64, 69, 75, 84
parallelogramma, 57, 60
willmeriana, 57, 60, 69, 70
Corellidae, 52, 57, 69
Coronulidae, 132
Coronuloidea, 109, 130, 154
Coryphopterus glaucofraenum, 176
Cottidae, 173
Crenimugil crenilabis, 177, 221
Crinodus lophodon, 173
Crustacea, 91
Cryptophialidae, 103, 105, 106, 108
Cryptophialus coronophorus, 102, 106
epacrus, 104
heterodontus, 104
lanceolatus, 106
melampygos, 102, 103, 104, 105, 107, 108
minutus, 103, 107, 108
rossi, 104
tomlinsoni, 107
zulloi, 104
Cryptotomus spinidens, 178
Ctenochaetus, 237, 238, 240
cyanoguttatus, 220
hawaiiensis, 175, 210
striatus, 177, 178, 200, 220, 238, 241
strigosus, 175, 178, 210
Ctenopharyngodon idella, 230
Culicia tenella, 73
Cyanophyta, 183
Cyprinus carpio, 208, 230
Cystodytes lobatus, 56
Daption capense, 278, 308
Delphinus delphis, 309
Dendrocia, 80
Dendrodoa, 54, 62
grossularia, 64, 69, 75, 76
Diadema, 244, 245, 247
antillarum, 237, 244, 245, 247, 249
Diazona, 62
Diazonidae, 52
Dichelaspis darwini, 116
mlleri, 116
Dictyota bartayresii, 250
dichotoma, 188, 195, 196
Didemnidae, 56, 69
Didemnum, 83
molle, 56, 59, 63, 73, 80, 81
Diomedia cauta, 278, 308
389
390
chlororhynchos, 278, 303

chrysostoma, 278, 283
epomophora, 279
exulans, 278
immutabilis, 280
melanophris, 278, 303
Diomedeidae, 282
Diplodus caudimacula, 176
holbrooki, 187, 196, 253, 260
Diplosoma listerianum, 56, 66, 68, 69, 77, 81
macdonaldi, 50, 53
similis, 56
Dischistodus perspicillatus, 246
Distaplia, 55, 58, 69
corolla, 56
occidentalis, 50, 55, 56, 58
Distomus, 62
Drepanorchis neglecta, 98
villosa, 98
Dunaliella, 18, 21, 26
euchlora, 37
tertiolecta, 19, 21, 29
Duplorbis, 95, 97
Echiniscoides, 148
Echinometra lucunter, 237
viridis, 249
Ecklonia, 306
radiata, 181, 253
Ecteinascidia turbinata, 49, 56, 64, 68, 73
Ectocarpus, 186
Elminius, 132, 133, 134
covertus, 132, 133, 134
kingii, 132, 133
modestus, 94, 132, 133, 134, 142, 143, 145, 146, 148,
151
plicatus, 133, 143
Embiotocidae, 254
Endocladia muricata, 193
Engraulis japonicus capensis, 273, 290, 291, 294, 295,
296, 297, 300, 301
Enteromorpha, 183, 184, 185, 186, 200, 204, 253
clathrata, 202
compressa, 202
flexuosa, 202
intestinalis, 201
salina, 201
Entomacrodus chiostictus, 211
nigricans, 176
Etrumeus whiteheadii, 290, 298, 300, 301, 303

Eucheuma, 360
Eudistoma capsulatum, 50, 56
digitatum, 50
hepaticum, 56
olivaceum, 56
ritteri, 55
Eudyptes chrysocome, 279
chrysolophus, 279
Euglena obtusa, 34
Euherdmania claviformis, 55
Eupomacentrus, 235
acapulcoensis, 246
dorsopunicans, 171
fuscus, 235
leucostictus, 235
lividus, 250
nigricans, 220, 246
partitus, 235
planifrons, 179, 220, 235, 246, 249, 250
rectifraenum, 174, 185, 186, 192, 201
variabilis, 235
Euraphia depressa, 126
Euscalpellum, 117
Evasteria troschelii, 79
Exallias brevis, 177
Exocoetoidei, 255
Fregata minor, 279
Fregatidae, 284
Fregetta grallaria, 279
tropica, 279, 285
Fucales, 194
Fucus distichus, 193
Fulmarus glacialoides, 278, 283
Fusitriton oregonensis, 79
Gelidiopsis, 186
intricata, 184
Gelochelidon nilotica, 278
Gigartina, 252
Girella cyanea, 174
elevata, 173, 211
fimbriatus, 174
nigricans, 174, 195, 234, 251, 252
simplicidens, 174
tricuspidata, 173, 188, 199, 200, 201, 211, 223, 253
Girellidae, 167, 173, 174, 188, 200, 211, 255
Girellinae, 186
SYSTEMATIC INDEX
Glenodinium, 14
Gnatholepis thompsoni, 176
Gobiidae, 176, 207, 211, 254, 255
Gobioidei, 255
Gonorhynchiformes, 255
Gonorhyncus gonorhyncus, 303
Gracilaria, 186, 252
Haletta semifasciata, 235
Halimeda, 184, 195, 197
incrassata, 184
Halobaena caerulea, 279, 319
Halocynthia aurantium, 61
igaboja, 51, 69, 78, 79
roretzi, 57, 58
Halodule, 377
Halophila, 377
Hemiglyphidodon plagiometopon, 250
Hemioniscus, 148
balani, 148
Hemirhamphidae, 176, 201, 212, 216, 221, 255
Hemirhamphus brasiliensis, 176
Hepsetia breviceps, 290, 291
Herdmania momus, 54
Heritiera fomes, 372
Hermosilla azurea, 174, 187, 251
Heteralepadoidea, 109, 110, 112, 151
Heteralepas, 110
cornuta, 110, 112
minuta, 112
smilius, 112
Heteromycteris, 292
Heterosaccus ruginosus, 98
Heterozostera tasmanica, 201
Hexaminius, 133
popeiana, 132, 133
Holacanthus bermudensis, 201, 204
Hydrobates pelagicus, 279, 304
Hydrobatidae, 282, 284
Hydroprogne caspia, 277, 278
Hypnea, 187
musciformis, 252
Hyporhamphus melanochir, 201, 205, 208, 212, 216, 217,
221, 225
Hypsistozoa fasmeriana, 46, 50, 51
Hypsypops rubicunda, 179
Ibla, 110, 156
atlantica, 110
391
cumingi, 110, 111, 154, 156

idiotica, 110, 111, 154
pygmaea, 110, 111
quadrivalvis, 110, 111, 154
segmentata, 110
sibogae, 110, 111
Ibloidea, 109, 110, 111
Ictalurus punctatus, 229, 230
Iridaea cordata var. cordata, 191
flaccida, 191
Istiblennius coronatus, 177
paulus, 177
Jasus lalandii, 293
Kasatkia, 236
Katsuwonus pelamis, 309
Kochlorine bocqueti, 104, 107
floridana, 102, 104, 107
hamata, 107
ulula, 104
Kyphosidae, 167, 173, 174, 175, 176, 177, 178, 186, 212,
216, 219, 221, 255
Kyphosinae, 186
Kyphosus, 186, 187, 227
cinerascens, 175, 177
cornelii, 186, 196, 212, 221, 226, 227, 234
fuscus, 174
incisor, 176
sectatrix, 176
sydneyanus, 173, 186, 196, 212, 216, 217, 218, 219,
221, 226, 227, 231, 233
tahmel, 212
Labridae, 180, 206, 225
Labroidei, 255
Lagenidium callinectes, 148
chthamalophilum, 148
Lagenorhyncus obscurus, 309
Lagodon rhomboides, 73, 187, 205, 253
Laminaria, 309
Laminariales, 194
Lampanyctodes hectoris, 290, 291
Laridae, 281, 282, 283, 284
Larus argentatus, 278
cirrocephalus, 277
dominicanus, 277
dominicanus vetula, 280
fuscus, 278
392
hartlaubii, 277, 280, 290

pipixcan, 278
ridibundus, 278
sabini, 279, 303
Lates calcarifer, 368
Laurencia, 185
obtusa, 185
Lepadoidea, 109, 112, 113, 116, 121
Lepadomorpha, 109
Lepas, 112, 113, 114, 116
anatifera, 112, 113, 114, 145
anatifera var. testudinata, 112, 113
anserifera, 112, 113, 115
australis, 112, 115
fascicularis, 112, 113, 115, 117
hilli, 112, 113, 115
pectinata, 112, 115
Leptoclinum mitsukurii, 56
Lernaeodiscidae, 96, 97
Lernaeodiscus cornutus, 98
galatheae, 98
porcellanae, 96, 97, 98, 100, 101
Liriopsis pygmaea, 148
patella, 56, 64, 68, 72, 73
Lissoclinum voeltzkowi, 56
Lithoglyptes, 104, 105
hirsutus, 104
indicus, 102, 105
mitis, 105, 107
scamborachis, 105, 107
tectoscrobis, 103, 105, 107, 108
Lithoglyptidae, 103, 105, 107, 108
Lithotrya, 122, 123
dorsalislis, 122, 123
nicobarica, 122, 123
truncata, 122, 123
Liza argentea, 212
dumerilii, 213, 216, 221
dussumieri, 212
facipinnis, 216, 221, 224
richardsonii, 213, 290, 291
tricuspidens, 213
Lumpenella longirostris, 235
Lumpenus maculatus, 236
sagitta, 235
Macrocystis, 204, 251, 252
integrifolia, 193
Macronectes giganteus, 278
halli, 278
Maxillopoda, 91, 92
Mechanichthys immaculatus, 173
Medialuna californiensis, 174, 195, 234, 251, 252
Megalasma (Megalasma) minus, 116
minus, 116
Melichthys niger, 175, 176
vidua, 177
Merluccius, 290, 292, 294, 295, 296, 297, 301, 303
Metandrocarpa taylori, 55, 57, 58, 67, 69
Metridium senile, 73
Microcladia coulteri, 191
Microcosmus exasperatus, 81
vulgaris, 75
Microdictyon umbilicatum, 201
Microlepas diademae, 116
Microspathodon chrysurus, 171, 176, 235
dorsalis, 186, 192, 202, 247, 249, 250
Molgula, 62
citrina, 53, 57, 59, 69, 70
complanata, 75, 77
manhattensis, 53, 57, 58, 75
occidentalis, 51, 53, 75, 78
occulata, 75
pacifica, 53, 57, 58, 61, 75
Molgulidae, 52, 57, 69
Monacanthidae, 175, 176, 201
Monacanthus chinensis, 201, 253
hispidus, 253
Monostroma, 204
oxysperma, 201
Morone saxatilis, 229
Morus capensis, 273, 274, 277, 294, 297, 298, 302, 322,
325
serrator, 279
Mugil auratus, 212
cephalus, 208, 212, 213, 216, 218, 219, 221, 223, 224,
227
curema, 174, 176, 221
georgii, 212
Mugilidae, 174, 176, 177, 212, 216, 219, 221, 223, 255
Mugiloidei, 255
Mycale, 80
Mycetomorpha, 97
Myctophidae, 207
Myxus elongatus, 213
Nannochloris atomis, 14
Naso brevirostris, 175, 178, 210
SYSTEMATIC INDEX
lituratus, 175, 177, 178, 183, 210, 240

unicornis, 175, 177, 187, 210
Neomyxus chavtali, 177
Neoodax balteatus, 235
Neoscorpis lithophilus, 174
Notomegabalanus, algicola, 141
Notothenia neglecta, 257
Oceanites oceanicus, 279
Oceanodroma leucorhoa, 279
Octolasmis aymonini geryonophila, 113, 116
grayii, 116, 117
lowei, 116
mlleri, 116, 117
warwickii, 94, 116
Octomeris angulosa, 129, 130, 150
Odacidae, 167, 170, 173, 180, 188, 213, 221, 234, 235,
255
Odax acroptilus, 235
cyanoallix, 235
cyanomelas, 235
pullus, 173, 181, 189, 196, 208, 213, 221, 225, 234,
235, 253
Olisthops cyanomelas, 173
Ophioblennius atlanticus, 171, 176
steindachneri, 211
Oxyjulis californica, 252
Pachylasmatoidea, 109, 125
Pachyptila belcheri, 279
turtur, 279
vittata, 278, 307
Padina, 253
jamaicensis, 197, 244
Parablennius sanguinolentus, 179
Paralepas, 110
minuta, 112
scyllarusi, 112
Parma alboscapularis, 173, 174, 179
kermadecensus, 174
microlepis, 173, 179
oligolepis, 173
polylepis, 173, 174
unifasciata, 173
Pavona, 246
Pelagococcus, 17
subviridis, 18
Pelecanidae, 282, 284
Pelecaniformes, 277, 279, 281, 284
393
Pelecanoididae, 284
Pelecanus onocrotalus, 177, 278
thagus, 283
Pelonia corrugata, 46
Peltogaster paguri, 97, 98, 100, 101, 148
sulcatus, 98
Peltogasterella, 97
gracilis, 96, 98, 100
socialis, 99, 100
subterminalis, 99
Peltogastridae, 96, 97
Penaeus merguiensis, 368
Penicillis, 184
Perca, 206
Perciformes, 167, 254, 255, 257
Percoidei, 255
Perophora viridis, 56, 65, 68, 69
Perophoridae, 56, 69
Phaeodactylum tricornutum, 14, 21, 25, 29
Phaeophyta, 183
Phaethon aethereus, 279
lepturus, 279
rubricauda, 279
Phaethontidae, 284
Phalacrocoracidae, 279, 281, 282, 284
Phalacrocorax africanus, 279, 280, 288
capensis, 273, 274, 277, 296, 298, 301, 302, 322
carbo lucidus, 277, 280
coronatus, 277, 280
neglectus, 277, 281
Phalaropus fulicarius, 279, 304
Phoebetria fusca, 279
palpebrata, 279
Phyllospadix scouleri, 193
Phytichthys chirus, 236
Pinna bicolor, 85
Plagiogrammus hopkinsii, 236
Platylepas, 132
hexastylos, 132
ophiophilus, 94, 132
Plectobranchus evides, 236
Plectroglyphidodon lacrymatus, 202, 213, 216, 250, 251
Pleuronectiformes, 291
Pleurosigma angulatum, 34
Pocillopora, 246
Pocockiella, 183
Podiceps nigricollis, 278, 283, 288
Podicipedidae, 282
Podicipediformes, 278
394
Podoclavella moluccensis, 55, 58, 64, 73, 80, 82, 83

Poecilasma carinatum, 116
obliquum, 116
Pollicipes, 110, 121, 122
cornucopia, 121, 122, 123, 150, 154
(Mitella) spinosus, 154
polymerus, 121, 122, 123, 142, 144, 150, 151, 154
spinosus, 121, 122, 123, 154
Polyandrocarpa, 76, 77
gravei, 69
misakiensis, 57
tincta, 57, 69
Polycarpa, 54, 62
pomaria, 47
tinctor, 46
Polycitor mutabilis, 56
Polycitoridae, 56, 69
Polyclinidae, 56, 69
Polysiphonia, 183, 186, 202, 247, 250
subtilissima, 202
Pomacanthidae, 175, 176, 177, 178, 201, 220, 255
Pomacentridae, 167, 171, 173, 174, 175, 176, 177, 179,
185, 201, 207, 213, 216, 220, 234, 235, 255
Pomacentrus, 222
albofasciatus, 177
flavicauda, 171, 172
fuscus, 177
jenkinsi, 175, 177
lepidogenys, 73
nigricans, 177
vaiulili, 177
Porites, 355
Poroclinus rothrocki, 235
Porphyra perforata, 191
Posidonia austrails, 201
Prionitis lanceolata, 193
Prionurus microlepidotus, 173
Procellaria aequinoctialis, 278, 303
cinerea, 279
Procellaridae, 282, 283, 284
Procellariiformes, 278, 279, 281, 284
Prochloron, 59, 81
Prorocentrum mariae-lebouriae, 14, 18
Protolepas bivincta, 91
Pseudogobius javanicus, 211
Pseudoscarus ghobbam, 213, 221
harid, 214, 221
Pterodroma brevirostris, 279
incerta, 279
lessonii, 279
macroptera, 278, 284
mollis, 278, 308
Pterosmaris axillaris, 301
Pterygosquilla armata, 290
Puffinus, 304
assimilis, 279, 303
carneipes, 279
gravis, 279, 284, 285
griseus, 279, 303
lherminieri, 280
pacificus, 280
puffinus, 279, 303
Pycnoclavella stanleyi, 55
Pyrgoma, 134
anglicum, 134
jedani, 134
Pyrocystis noctiluca, 14, 29
Pyura, 75
chilensis, 75
haustor, 69, 70, 75, 76, 77, 78, 79
pachydermatina, 75
praeputialis, 75
stolonifera, 75
tessellata, 83, 85
Pyuridae, 52, 57, 69
Rhinecanthus aculeatus, 177
rectangulus, 177
Rhizocephala, 91, 92, 93, 95, 98, 120
Rhizophora, 370
mangle, 374
Rhizosolenia, 254
Rhodophyta, 183
Rhynchopidae, 284
Rissa tridactyla, 279
Sacculina, 99
carcini, 99, 100, 101
inflata, 97
micracantha, 99
papposa, 99
rotundata, 99
senta, 100
setosa, 99
sulcata, 96, 97, 99
Sacculinidae, 97
Salarias fasciatus, 171, 211
Salmo gairdneri, 229
SYSTEMATIC INDEX
Sardinops ocellatus, 273, 277, 290, 294, 295, 296, 297,

300, 301, 325
Sargassum, 187, 188, 239, 253
polyceratium, 197
Sarpa salpa, 174, 187, 203, 204, 205, 214, 216
Scalpelloidea, 109, 117, 118, 120
Scalpellum, 113, 117, 118, 119, 154, 155
(Acroscalpellum) balanoides, 118
(Acroscalpellum) brevicaulis, 118
(Acroscalpellum) compressum, 118
(Acroscalpellum) eugenic, 118
(Acroscalpellum) eumitos, 118
(Acroscalpellum) gracile, 118
(Acroscalpellum) hexagonum, 118
(Acroscalpellum) micrum, 118
(Acroscalpellum) regium, 118
(Acroscalpellum) sergi, 118
(Acroscalpellum) sessile, 118
agulhense, 118
balanoides, 118
botellinae, 118
brachium-cancri, 118
brevicaulis, 118
cancellatum, 118
capense, 118
chiliense, 118
compactum, 118
compression, 118
convexum, 119
cornutum, 119
eumitos, 119
faurei, 119
gibberum, 119
gracile, 119
micrum, 119
natalense, 119
ornatum, 119
parallelogramma, 119
perlongum, 119
regina, 119
return, 119, 120
scalpellum, 119, 120, 121
sessile, 119
sinuatum, 119
squamuliferum, 120
stearnsi, 119
stroemi, 119
subalatum, 119
triangulare, 119
uncinatum, 119
valvulifer, 119
velutinum, 119
ventricosum, 119
vulgare, 119
Scaridae, 167, 170, 175, 176, 178, 179, 180, 183, 202,
213, 216, 219, 221, 225, 257
Scarus, 178, 240
aeruginosus, 178
africanus, 178
bicolorlor, 178
bipallidus, 178
brevifillis, 240
coelestinus, 176
croicensis, 171, 176, 179, 237
forsteri, 178
gibbus, 216, 221, 240, 241
globiceps, 178
guacamaia, 176
guttatus, 178
harid, 178
javanicus, 178
jonesi, 216, 221
microrhinos, 178
niger, 178
pectoralis, 178
rivulatus, 240
rubroviolaceus, 175, 180, 181, 208, 214, 217, 218,
219
scaber, 178
sordidus, 175, 178
taeniopterus, 176
taeniurus, 175
vermiculatus, 178
vetulala, 176
Scenedesmus obliquus, 21
Scomberesox saurus, 293, 294, 297
Scorpaenidae, 207
Scorpididae, 174
Scorpidinae, 186
Sebastes, 222
mystinus, 222
Selenastrum minutum, 35
Septodiscus flabellum, 99
Septosaccus cuenoti, 99
Seriola lalandii, 309
Sesarminae, 369
Sicyases sanguineus, 234
395
396
Siganidae, 167, 173, 178, 184, 202, 214, 216, 255, 257
Siganus doliatus, 240
fuscescens, 214
oramin, 178
rivulatus, 185
rostratus, 178, 185
spinus, 173, 184, 185, 202, 214, 216
stellatus, 178
Siphonognathus argyrophanes, 235
attenuatus, 235
beddomei, 235
caninus, 235
radiatus, 235
tanyourus, 235
Skeletonema, 14, 18
costatum, 14, 17, 18, 29, 149
Smilium, 117
hypocrites, 119
Smithora naiadum, 191
Solidobalanus hesperius, 141
hesperius hesperius, 141
Sparidae, 167, 174, 176, 187, 202, 214, 216, 220, 287, 292
Sparisoma, 197
aurofrenatum, 176
chrysopterum, 176
radians, 176, 184, 202, 205, 220, 233
rubripinne, 176
viride, 176
Sparodon durbanensis, 291
Sphacelaria, 186
tribuloides, 184
Spheniscidae, 282, 284
Sphenisciformes, 277, 279, 281, 284
Spheniscus demersus, 273, 274, 277, 295, 298, 300, 302,
322
Spyridia, 187
Stegastes dorsopunicans, 247
fasciolatus, 172, 174, 247, 248, 249
lividus, 186, 199, 202, 213, 216
planifrons, 247
Stercoraridae, 282
Stercorarius longicaudus, 279, 283
parasiticus, 279, 305
pomarinus, 279, 283
Sterna albifrons, 279
anaethetus, 279, 280
balaenarum, 277, 290
bergii bergii, 277, 280, 290
dougalii, 277, 278, 279

fuscata, 279
hirundo, 279, 306
hirundo/paradisaea, 305
maxima, 279
paradisaea, 279, 284
repressa, 280
sandvicensis, 279, 306
vittata, 279, 283
Stichaeidae, 167, 173, 188, 203, 207, 214, 216, 220, 234,
235, 255
Stichaeopsis, 235
Stichaeus punctatus, 235
Stolonica, 62
Styela, 62
coriacea, 51, 69
gibbsii, 60, 67, 69, 75, 78, 79, 80
montereyensis, 61, 69, 70, 76, 78
partita, 54, 57, 69, 70
plicata, 57, 58, 59, 60
Styelidae, 52, 57, 69
Sufflogobius bibarbatus, 290, 291, 292, 294, 295, 296,
297, 300, 301
Sula leucogaster, 280
Sulidae, 282, 284
Sylon, 96, 97
challengeri, 99
hippolytes, 96, 99, 100, 101
schneideri, 99
Sylonidae, 96, 97
Symplegma, 62
viridae, 69
viride, 57
Synechococcus, 14, 18, 26, 29, 34
Synechocystis, 59
Syngnathus, 292
Tesseropora, 131
rosea, 130, 131, 144, 147
Tethyum, 62
Tetraclita, 91, 110, 130, 131, 132, 146, 154, 155
divisa, 130, 131, 132, 154, 155
japonica, 131
karandei, 131
panamensis, 146
purpurascens, 131
rubescens, 130, 131, 154
serrata, 131, 154
squamosa, 151, 154
SYSTEMATIC INDEX
squamosa japonica, 130

squamosa rubescens, 131, 132, 146, 151
squamosa rufotincta, 130, 131, 132, 146, 150, 154,
155
squamosa stalactifera, 130, 131
stalactifera, 131, 146
(Tesseropora) pacifica, 130, 131, 154, 155
(Tesseropora) rosea, 131
Tetraclitella, 131
karandei, 130
purpurascens, 130, 131
Tetraclitidae, 130
Tetraodontidae, 175, 177, 255
Tetraodontiformes, 255
Tetraodontoidei, 255
Thalassia, 184, 245, 377
testudinum, 184, 244
Thalassiosira, 18, 96, 97
fluviatilis, 14
pseudonana, 34
Thalassoica antarctica, 279
Thompsonia, 99
cubensis, 99
Thoracica, 91, 92, 93, 94, 109, 154
Thunnus alalunga, 309
albacares, 309
Thyrsites atun, 303
Tilapia, 206
nilotica, 222
zillii, 230
Trachurus capensis, 290, 291, 294, 295, 296, 297
Triangulus galatheae, 96, 99
Trididemnum solidum, 56, 64, 69, 77
Triglidae, 292
Trilasmis (Poecilasma) obliqua, 116
Trypetesa, 104, 105
(=Alcippe) lampas, 106
(=Alcippe) nassarioides, 94
habei, 102, 104, 106
lampas, 102, 104, 105, 106, 108
lateralis, 102, 103, 104, 105, 106, 108
nassarioides, 102, 104, 105, 106, 108
Trypetesidae, 103, 105, 106, 108
Turbinaria, 239
turbinata, 197
Ulva, 26, 186, 252, 253
lactuca, 187, 203
lobata, 222
397
Valamugil buchanani, 174

Verruca, 109, 123, 124, 125
striata, 124, 125
stroemia, 94, 123, 124, 125, 142, 143, 144, 145
Verrucomorpha, 109, 123
Weltneria, 105
exargilla, 102, 103, 105, 107, 108
hessleri, 102, 104
reticulata, 105, 107
spinosa, 105, 107
zibrowii, 105, 107
Xenopoclininae, 291
Xiphister atropurpureus, 235
mucosus, 173, 188, 189, 190, 191, 192, 193, 194, 198,
203, 208, 214, 257
Zebrasoma flavescens, 175, 210
rostratum, 220
scopas, 178
veliferum, 175, 177, 178, 210
Zoarcoidei, 255
SUBJECT INDEX
References to complete articles are given in heavy type ; references to sections of articles are given in
italics; references to pages are given in normal type.
Acanthurids, 171, 172, 180, 183, 184, 187, 193, 194, 198,
218, 223, 227, 233, 241
Acasta, breeding season, 134
size and number of eggs, 134
Acipenserid, 230
Acoustic survey to estimate fish stocks, 320, 324, 325
Acrothoracica, breeding season, 106, 107, 108
dwarf males, 102, 104
egg production, 102109
incubation time, 106, 107
number of eggs per brood and size of female, 108
size and number of young, 103, 105, 106, 107
spermatozoa, 104
spermatogenesis, 104
young hatch as nauplii or cyprids, 105
Activity patterns, fishes, 181, 197, 217
Adriatic Sea, Acasta, 134
Balanus species, 136, 138, 140
Coronulidae, 132
Africa, 180, 187
conservation practice, 383
environmental degradation, 338
fish conservation, 381, 382
Age and size effect on egg production in cir
ripedes, 145146
Agulhas Bank, 274, 275, 276, 280, 281, 306, 315, 318,
319, 320, 321
Current, 276, 280

Alaska, 235, 237
rhizocephalans, 99
Albatross, 305
blackbrowed, 278, 289, 303, 308
greyheaded, 278, 283, 289
Laysan, 280
light mantled sooty, 279
royal, 279
sooty, 279
shy, 278, 289, 303
wandering, 278, 289
yellownosed, 278, 289, 303
Alcids, 283
Aldabra, 172
Algae, as food for fishes, 167262
morphological types, 197
Algal assemblages, 250
diversity, 243, 247, 249, 251
productivity, 246, 247, 249, 253, 261
Algoa Bay, 275, 277, 278, 280, 281, 291, 297, 298, 300,
303, 309, 312, 313, 314, 317, 323, 324
America, east coast Lepadoidea, 116, 117
Amphipods, 195, 196, 229
Anchovy, 273, 286, 287, 291, 293, 298, 302, 303, 312,
314, 315, 318, 320, 321, 323, 324
Andaman Islands, Balanus species, 135, 141
398
SUBJECT INDEX
Anecdysis in cirripedes, 145

Angelfish, 204
Angola, 280
Mocamedes province, 283
Angola-Benguela front, 275
Antarctic, 256, 257
Ascothoracica, 107
assimilation numbers, 14
Convergence, 102
Coronulidae, 132
Lepas species, 114
Anthropogenic activities, coral reefs, 362, 363, 364
disturbances, coral reefs, 361
effects on coral reefs, 350362
on mangrove communities, 370374
Aplodactylids, 179, 180, 181, 208, 224, 244
Arabian Gulf, Lepadoidea, 116
Arcachon, France, Balanus species, 139, 140, 142
Artisanal fishers, 381
Ascension Islands, Lepadoidea, 116
Ascidian biology, reviews of, 45, 46
cannibalism, 73, 74
coronet cells, 54
eggs, adaptations, 60, 61
block to polyspermy, 49
larvae adhesive papillae on trunk, 53
aposematic coloration, 73
cerebral vesicle, 53, 54, 56
hydrostatic pressure receptors, 54
modes of release, 4648
ocellus and statocyte structure, 54
philopatry, 64
predators of, 73
release observed by divers, 59
responses to light, 66, 67, 69
sizes of, 50, 51
spermatozoa, 48, 49
chemotactic attraction to eggs, 49
swimming speeds, 65
Ascidians, block to self-fertilisation, 49
fecundity, 85
generalised life cycles, 47, 48
habitat selection, 63
larvae, anatomy of, 4954
dispersal and duration of planktonic period, 6065
ecology and behaviour, 4590
geotaxis, 6772
locomotion, dynamics of, 65;46
mortality, 7274
399
survival, 63
pelagic period, 6074
orientation with respect to physical cues, 6672
photokinesis, 6667
phototaxis, 6772
metamorphosis, 46, 52, 53, 63, 68, 74, 76, 77, 78, 79
chemical cues, 76, 77
photoreceptor, 55, 58
recruitment, role of reproduction and larval
processes in, 8185
reproduction, larval release and spawning,
diel patterns of, 5559
seasonal patterns of, 5455
timing and synchrony, 5459
settlement, 7481
larval responses to conspecifics, 7579
to other organisms, 7980
to physical cues, 8081
Asia, 205
Asian countries, trawl fisheries, 368
mangroves, mans impact on, 341
Assimilation efficiency, 200204;199, 222, 238
numbers, 16, 17, 18, 19, 24, 27, 29
Atlantic compared with Pacific tropical eco
systems, 380
Atlantic Ocean, growth of coral reefs, 347
ATP, 22, 26, 36, 37
Auckland Islands, 256
Australia, 169, 173, 179, 180, 181, 186, 195, 197, 217,
226, 235, 247, 252, 253, 256, 257, 258
Balanus species, 136, 141
Chthamaloidea, 127, 129
Chthamalus species, 126
Coronulidae, 132
development of MicroBRIAN, 383
Elminius species, 132, 133
Ibloidea, 110, 111
juvenile fish communities, 368
Lepadoidea, 116
mangroves, 364, 365, 366, 367, 368, 369, 370, 372,
376
oil spills, 373, 374
seagrass communities, 376, 377
Tetraclitidae, 130, 131
Australian Institute of Marine Science, 384
Survey and Land Information Group, 384
Auto trophic cells, 19
Bacteria, 204, 218, 223, 226, 233, 243
400
Bacterial infection, coral reefs, 361

Bahamas, ascidians, 76
Baja California, 180, 235
Balanus, species, 139, 152
Balanoidea, egg production, 132134
Balanomorpha, classification of, 109, 125
Balanus species, age of maturity, 146
and related species, breeding seasons, 135, 136, 137,
138, 139, 140, 141
number of broods, 135, 136, 137, 138, 139, 140, 141
size and number of young, 135, 136, 137, 138, 139,
140, 141
Bali Action Plan, 385
Bangladesh, mangroves, 371, 372, 375
Barbados, Pollicipes, 122
Barramundi, 368
Bay of Biscay, Acrothoracica, 107
Bedford Basin, assimilation numbers, 14
photosynthesis, 29
Blehrdek equation, 20
Benguela Current, 284
ecosystem, seabirds, 273335
energy flow and nutrient cycling, 320323
feeding ecology, 285309
northern sector, 276, 278
oceanography, 274276
seabird assemblage, 277285
seabirds in fisheries management, 323 326
southern sector, 276, 278, 302
population dynamics, 309319
upwelling system, 273, 281, 285
Benin, mangroves, 371
Bering Sea, rhizocephalans, 98, 99
Biliproteins, 17
Biochemical determinants of Pmax, 2021
Bioerosion and sediment formation by fishes, 237238
Bird Island, 291, 312
Bird Rock platform, 278
Black Sea, Balanus species, 138, 139
rhizocephalans, 99
Blennies, 171, 172, 179, 215, 286, 287, 289
Blenniids, 171, 223, 261
Body size, herbivorous fishes, 235, 236
Bombay, India, Balanus species, 135, 136, 140, 141
Booby, brown, 280

Boothbay Harbor, Balanus species, 153
photosynthesis, 29
Boreo-arctic cirripedes, 95
Botany Bay, 253
Bottom-trawling, 273, 275, 284, 303, 305
Brazil, mangroves, 375
Breeding season, Acasta, 134
Acrothoracica, 106, 107, 108
Balanus and related species, 135, 136, 137, 138, 139,
140, 141
Chthamaloidea, 126, 127, 128, 129, 130
Elminius species, 133, 134
Ibloidea, 111
Lepadoidea, 114, 115, 116, 117
Pollicipes species, 122
rhizocephalans, 98, 99
Verrucomorpha, 125
British Columbian coast, assimilation numbers, 14
waters, Pyrgoma, 134
Scalpelloidea, 119, 120
Brittany coast, assimilation numbers, 14
Brittlestars, 229
Burma, mangroves, 375
Burrowing cirripedes, 102
C3 plants, 13, 17, 29, 31
C4 plants, 13, 28, 29, 30, 31
Caging experiments, 247, 252
California, 173, 174, 179, 187, 195, 251, 252, 256, 257,
305
Acrothoracica, 106, 108
Chthamalus species, 128, 143, 146
Current, 121, 283
system, 283, 284, 285
Pollicipes, 122
rhizocephalans, 99
Tetraclita species, 146
upwelling system, 283, 284
Calvin cycle, 27, 28, 29, 30, 33
CAM plants, 28, 29, 30
Canada, Balanus species, 137, 143, 146, 152
Canary Current, 283
system, 283, 284
Cape Agulhas, 275
SUBJECT INDEX
Banks Marine Scientific Research Area of Australia,

147
Columbine, 275, 276
Cross, 275, 280
Peninsula, 275, 276
Point, 275
Cape, South Africa, eastern, 317
southern, 291
southwestern, 292, 300, 301, 302, 322
western, 293, 298, 302, 309, 312, 314
Cape Town, 275
Capture fisheries, mangroves, 375
Carbohydrates, 193, 194
Carbon: chlorophyll a ratios, 19
Carbon dioxide fixation, 14C experiments, 16
Carbonic anhydrase, 102
Carboxylase, 16
Carboxylation of PEP, 16
Carboxylation reaction, 20
Caribbean, 171, 184, 185, 197, 237, 239, 243, 244, 245,
246
barrier reef, 348
conservation practices, 383
decline in mangroves, 338
reef fish biomass, 379
resource management, 341
seagrass communities, 376, 377
species-poor, 380
waters, phosphate concentrations, 345
Carnivory, fishes, 233, 234
Carotenoids, 17, 34
Caspian Sea, Balanus species, 138, 139
Cell growth rates, 1920
immunological techniques, 47
lineage studies, fluorescent markers, 47
Cellulase, 167, 205
Cellulolytic enzymes, 169, 205, 206, 218
microflora, 205
Cellulose, 193, 226
carboxymethyl, 205
crystalline, 205
methyl, 205
Celtic Sea, assimilation numbers, 14
Cephalopods, 293, 303
Cetaceans, 309, 326
Chaenopsids, 215
Chaetognaths, 229
Chagos Archipelago, corals, 385
401
Chanids, 223
Charcoal production from mangroves, 371, 375
Chemical composition of cirripede eggs, 150
pollution, effect on coral reefs, 352354
Chile, 181, 256, 257
ascidians, 75
Balanus species, 141
Elminius species, 133
China, mangroves, 372
Chinese waters, Heteralepadoidea, 112
Chlorophyll, 1619;13
Chlorophyll a, 17, 18, 19, 21, 23
Chlorophyll b, 17
Chlorophyll c, 17
Chlorophyll, cellular chlorophyll a content, 1719
content of open ocean, 23
estimation of, 1617
extraction from intact cells, 17
Chlorophyllide a, 17
Chloroplast membranes, 22
Chordate phytogeny, 45
Chthamaloidea, breeding seasons, 126, 127, 128, 129, 130
sizes and number of young, 126, 127, 128, 129
Chukchi Sea, Chthamalus species, 125, 126
Cichlids, 218, 222, 225, 230
Cirripedes, abbreviated embryonic development, 156
age and number of eggs, 146
anecdysis, 145
apertural males, 92
burrowing, 123
and non-parasitic, 102
classification of, 91, 92
cold tolerance, 145
complemental males, 92
copulation, 92, 93
cross-fertilisation, 93, 94
dwarf males, 92, 110
effect of lecithotrophy, on time of embryonic
development, 154
eggs, 150154
chemical composition, 150
production, 91166
size and shape, 152154
eurythermic, 142
factors affecting breeding, 134149
fecundity, 150, 151
fertilisation, 9394
402
food reserves, 95
hermophrodites, 92
lecithotrophic larvae, 110, 154, 155, 156
lecithotrophy, effect on egg shape, 154
loss of penis, 95
metabolic efficiency of egg production, 151
method of burrowing, 102
nauplius stages, 93
number of eggs, 150152
related to size of parent, 150, 151
oogenesis, 94, 95
oviposition, 95
parasitic castration, 148
post-hatching ecdysis, 145
pseudo-copulation, 93
release of embryos, 149150
and diatom outbursts, 149, 150
and salinity, 149
and shore ice, 149, 150
and weather conditions, 149
as nauplii or cyprids, merits of, 101, 102
reproductive effort, 151
reproductive gonads, 9495
reproductive output, 151
self-destruction, 147
self-fertilisation, 93, 94
separate sexes, 92
sex of cyprids, 92
spermatogenesis, 94
spermatozoa, 93, 94, 95
stenothermic, 142
synchronous breeding, 142
transfer of spermatozoa, 92, 93
Clinids, 287, 291, 293
Clupeid, 205
Cochin, India, Balanus species, 135, 136
Coevolution, 196
Cold tolerance of cirripedes, 145
Commercial fisheries, mangroves, 372
Community interactions in tropical marine
ecosystems, 379380
Competition, exploitation, 172
interference, 172
Complemental males, Scalpelloidea, 117
Coral reefs, 347364;167, 169, 171, 175, 176, 178, 236,
237, 238, 239, 242, 243, 244, 245, 250, 257, 261
ability to regenerate, 357, 358
and fishes, 349, 350, 352
and synergism, 360362
anthropogenic activities, 362, 363, 364

disturbances, 361
effects, 350362
bacterial infection, 361
catastrophes, 349
chlorinated hydrocarbons, 353, 354
destructive fishing practices, 360
dynamite fishing, 338, 358, 359
effect of chemical pollution, 352354
extractive activities, 358360
hydrodynamic influences, 356357
metals, 353
oil, 353
physical disturbance, 357358
radioactive pollution, 356
sedimentation, 351352
sewage pollution, 354355
thermal pollution, 355356
tourism, 360
UV radiation, 361
exploitation for human consumption, 359
fundamental research, 347350
herbicides, 353
herbivorous fishes, 359
holding strategy, 362
indicator species, 363
introduction of new species, 360
monitoring regrowth, 362, 363
natural disasters, 349
over-fishing, 359
pesticides, 353
plastic debris, 356
research for management, 362364
shut-down syndrome, 361
transplantation of living corals, 363
volcanic eruptions, 349
Coral skeletons, density bands in, 352
Cormorant, 281, 283, 304, 319
bank, 277, 281, 287, 291, 292, 306, 307, 310, 311,
319, 327
Cape, 273, 274, 277, 280, 287, 291, 293, 296, 298,
299, 301, 302, 303, 304 ,306,307,308, 309, 310, 311,
313, 314, 315, 316, 318, 320, 322, 326, 327
crowned, 277, 280, 281, 287, 292, 293, 306, 307, 311,
319,
reed, 279, 288, 304, 307
whitebreasted, 277, 280, 285, 287, 291, 292, 306, 307,
311, 319
Coronulidae, size and number of eggs, 132
SUBJECT INDEX
Coronuloidea, egg production, 130132

Costa Rica, Tetraclita species, 146
Crassulacean acid metabolism (CAM), 29
Cross-fertilisation, cirripedes, 93, 94
Crowding effect on egg production in cirripedes, 146147
Crown-of-Thorns outbreaks, 338, 349, 384
Crustaceans, 217, 247, 251
Cuba, rhizocephalans, 99
Cumberland Sound, Balanus species, 143
Cunene River, 275, 277, 280
Cuxhaven, Germany, Balanus species, 148
Cyanobacteria, 18, 33
Cyprinid, 208, 230
Cytochrome b6, 23
Cytochrome c, 58
Cytochrome f, 21, 22, 23
Dakar to Barbados, Lepas on ships, 112
Damselflshes, 167, 169, 171, 172, 179, 185, 222, 237, 243,
245, 246, 247, 248, 249, 250, 251, 261
Dassen Island, 301, 302, 306, 324
Denmark, rhizocephalans, 99
Dentition, fishes, 187, 188, 197
Destructive fishing practices, coral reefs, 360
Detritus, 174, 175, 176, 177, 183, 200, 205, 224, 227,
233, 238
Diatoms, 168, 174, 175, 176, 177, 183, 199, 200, 204, 223,
224, 234, 238, 243, 257
Diet selection, fishes, 189197
Digestive enzymes, herbivorous fishes, 205 207
Dissolved organic carbon (DOC), 370
Dolphins, common, 309
dusky, 309
Dugongs, 132, 377
Dwarf males, cirripedes, 110
Scalpelloidea, 117
Dyer Island, 275, 278, 280, 301, 313, 314, 315, 318
Dynamite fishing, coral reefs, 358, 359
East American coast, Chthamalus species, 146
and South China Sea, Balanus species, 140, 152
Falkland Islands, Scalpelloidea, 119
Eastern-boundary, current regions, 273, 281, 283
upwelling zones, 281
Eastern Pacific, Heteralepadoidea, 110
Ecuador, mangroves, 368
oil spills, 373
Efficiencies of marine production, 38
403
Egg production, Acrothoracica, 102109

Balanoidea, 132134
Balanomorpha, 125134
Chthamaloidea, 125130
Coronuloidea, 130132
Heteralepadoidea, 110112
Ibloidea, 110
in cirripedes, 91166
effect of age and size, 145146
crowding, 146147
feeding, 144145
latitude, 143144
light, 144
monsoons, 147, 148
moulting, 145
parasites, 148149
pollution, 148
salinity, 147148
seaweed cover, 147
temperature, 142143
factors effecting breeding, 134149
Lepadoidea, 112117
Lepadomorpha, 109123
Rhizocephala, 95702
Scalpelloidea, 117123
Thoracica, 109154
Verrucomorpha, 123125
Egg size and shape in cirripedes, 152154
Eggs of cirripedes, 150154
Elatol, 185
Elminius breeding seasons, 133, 134
size and number of young, 133, 134
El Nine, 342
mortality and breeding failure of seabirds in Pacific
Ocean, 318, 319
Embryogenesis, rhizocephalans, 97
Embryonic development, duration of in ascidians and egg
size, 60, 62
and temperature, 60, 62
Embryos, release of in cirripedes, 149150
Endemism, 283
Energy maximisation premise, 190
Enewetak, 239, 243
England, rhizocephalans, 99
Epibionts, 169, 204
Epipelagic fish, 273, 275, 276, 286, 293, 303, 308, 311,
325, 327
Eukaryotic photosynthetic cells, 18
Europe, Balanus species, 135, 143, 149, 152
404
Chthamalus species, 126, 127, 128, 146, 153

Elminius species, 132, 133, 134
Extracellular carbohydrates, 192
Extractive activities effects on coral reefs, 358 360
Factors affecting breeding in cirripedes, experimental
work, 134, 142
Fecundity, cirripedes, 150, 151
Feeding behaviour, herbivorous fishes, 170 197
effect on egg production in cirripedes, 144 145
of Polticipes, 121
Fertilisation, ascidians, 4849
cirripedes, 9394
Fiji, mangroves, 376
Finfish, 372
Firth of Forth, assimilation numbers, 14
Fishes, biology of marine herbivores, 167272
coral reefs, 349, 350, 352
surface-dwelling, 304
Fisheries conservation in tropical marine ecosystems, 380
382
Fish-pond production in tropics, 371
Flagellates, 227
Flat fish, 291
Flavonoid compounds, 35
Florida, Acrothoracica, 106, 108
ascidians, 81
Balanus species, 135, 139, 141, 144
Keys, 235, 247
mangrove communities, 364, 365, 367, 369, 370, 380
oil spills, 373
Pollicipes, 122
Food reserves, cirripedes, 95
webs, 168
Foraminiferans, 177, 178
France, 256
rhizocephalans, 99
French Polynesia, 238
coral reefs, 356
Friday Harbor, Balanus species, 138, 139
Frigatebird, greater, 279
Frobisher Bay, Balanus species, 143
Fulmar, Antarctic, 278, 283, 289
Gambia, mangroves, 371
Gannet, 281, 305, 309, 312, 314
Australian, 279
Cape, 273, 274, 277, 280, 281, 286, 287, 293, 294,
297, 298, 299, 302, 303, 304, 307, 308, 309, 311, 312,
313, 314, 316, 318, 320, 322, 324, 325, 326, 327
Geotaxis ascidian larvae, 6772
Germany, Balanus species, 139
Giant clams, coral reefs, 352, 359
Girellids, 180, 186, 188, 195, 198, 199, 251, 258, 261
Global net productivity of terrestrial and marine plants, 13
Glucose uptake, fishes, 230
Gobiids, 261
Goby, pelagic, 286, 287, 291, 293, 298, 303, 310, 312,
315, 317, 327
Goleta Point, Pollicipes, 121
Great Barrier Reef, 239, 240, 242, 244, 246, 247, 250,
348, 384
ascidians, 64, 73, 80
fish populations, 385
lagoon sediment, bacterial production, 368
Marine Park Authority, 384
rhizocephalans, 99
Great Britain, Balanus species, 137, 138, 139, 152, 153
Grebe, blacknecked, 278, 283, 288, 304, 305, 307
Greenland, Balanus species, 137, 150, 153
Green turtles, 377
Growth, fishes, 191, 204, 205, 261
Grunts, 377
Guam, 184, 185, 186, 247
Acrothoracica, 106
Guano, 273, 311, 314, 317, 321, 323, 324, 326
platforms, 278, 280, 314, 315, 316, 317
Guilds of herbivorous fishes, 239, 240, 241
Gulf of Aqaba, 241
California, 185, 192, 248
Carpentaria, seagrass communities, 376
Elat, Ibloidea, 111
Fos, assimilation numbers, 14
Guinea, 308
Heteralepadoidea, 112
Maine, assimilation numbers, 14
photosynthesis, 29
Mexico, ascidians, 73, 80
Gull, 304, 305
blackheaded, 278
Franklins, 278
SUBJECT INDEX
greyheaded, 277
Hartlaubs, 277, 280, 281, 286, 290, 304, 307, 308,
310, 311
herring, 278
kelp, 277, 280, 286, 291, 304, 307, 308, 310, 311
lesser blackbacked, 278
Sabines, 279, 289, 303, 304, 305, 307
Gullmarsfjorden, Sweden, ascidians, 76, 80, 83
Gut pH, herbivorous fishes, 218223; 224, 225, 227, 261
transit times, fishes, 216, 229
Hake, 287, 303, 313, 327
Hakodate, Chthamalus species, 126, 128
Halifax Island, 295, 326
Hawaii, 175, 183, 243, 246, 247, 248, 256
coral reefs, 355, 356
Lepas species, 115
Heligoland, Acrothoracica, 106, 108
Elminius, 133, 134
Hemiramphids, 205, 206, 208, 217, 225
Herbivorous fishes on coral reefs, 359
Herbivorous marine fishes, alimentary canal types, 217
228
gizzard-like stomach, 223224
highly acidic stomach, 218223
hindgut fermentation chamber, 226227
pharyngeal mill, 224225
assimilation efficiencies, 200204; 199, 222, 238
biology of, 167272
comparative feeding behaviour, 180182
densities, 259
diets, 173178
and food preferences, 182189
temperate families, 188189
tropical families, 183186
tropical-temperate families, 186188
digestion and digestive mechanisms, 197 231
digestive enzymes, 205207
endogenous cellulases, 205206
other enzymes, 206207
digestive mechanisms, 207231
distribution, diversity, abundance, 254260
abundance, 260
diversity, 254260
latitudinal patterns, 254260
ecological impacts, 236253
bioerosion and sediment formation, 237 238
roving species compared with sea urchins, 244245
405
on algal communities, 242244

on coral reefs, 239242
temperate habitats, 251253
territorial damselfishes, 245251
tropical habitats, 237251
evidence for digestion and assimilation of algae, 197
205
assimilation of seaweed compounds, 199 204
diets largely of seaweeds, 198
growth on a seaweed diet, 204205
specialised alimentary canal, 198199
evolutionary responses to nitrogen shortage, 232236
factors affecting diet selection, 189197
food quality, 190193
seaweed defences, 193197
feeding behaviour, 170197
types, 173175
food and feeding, 170197
geographical distribution, 255, 256
group foraging, 179180
gut length, 207215
gut transit times, 215217
guts as chemical reactors, 228229
home ranges, 180
intestinal nutrient transport, 229231
protein requirements, 231232
territorial defence, temperate species, 172, 179
tropical species, 171172
Heron Island, 242, 243
Herring, round, 298
Heteralepadoidea, egg production, 110112
size of young, 112
Hexaminius, size and number of young, 133
Hokkaido, rhizocephalans, 98
Horse mackerel, Cape, 287, 291, 298, 302
Hudson Bay, assimilation number, 14
Strait, Balanus species, 143
Humboldt Current, 283, 284
Hydras, 229
Hydroids, 229
Hydrodynamic influences, effect on coral reefs, 356357
Ibloidea, breeding seasons, 111
egg production, 170
Ichaboe Island, 291, 292, 294, 295, 296, 298, 306, 310,
311, 312, 315, 316, 326
Ictalurid, 229
406
Incubation time, Acrothoracica, 106, 107

rhizocephalans, 98, 99, 100
India, Balanus species, 135, 139, 144
conservation practice, 383
Coronulidae, 132
Ibloidea, 111
mangroves, 371
Indian Ocean, 172
Indicator species, coral reefs, 363
mussels, 363
Indonesia, coral reefs, 353
Ibloidea, 111
mangroves, 371, 375
marine reserves, 384
marine resources, 341
tamback mariculture, 382
Indo-Pacific, 184, 239, 257
countries, decline in mangroves, 338
mangroves, 369, 370
seagrass communities, 376
Intermediate disturbance hypothesis, 247, 248, 249
Isla Pico Feo, 237
IUCN Conservation Monitoring Centre, 340
Working Group on Mangrove Ecosystems, 376
Jamaica, 249
Japan, Acrothoracica, 106, 107
Lepas species, 115
mangrove communities, 364
rhizocephalans, 98, 99
Johnstone Island, 183
Kaneohe Bay, coral reefs, 355
sewage, 357, 361
Kei Islands, Balanus species, 140
Kelp bed, 174, 188, 251, 256
forest, 252
Kerala backwaters, India, Balanus species, 136, 148
Kerguelen Islands, Scalpelloidea, 118
Kermadec Islands, 174, 256
-ketoglutarate synthesis, 35, 36
Keystone species, 248, 249
Kittiwake, blacklegged, 279
Krebs cycle (tricarboxylic acid cycle), 35, 36
Kyphosids, 186, 187, 188, 193, 194, 195, 196, 199, 226,
227, 229, 233, 251, 258, 261
Kyusyu, Heteralepadoidea, 112
Labrids, 206, 225, 261

Lagos, Nigeria, Balanus species, 139
Lake Titicaca (PeruBolivia), photoinhibition of
photosynthesis, 34
Lamberts Bay, 275, 280, 297, 301, 302, 312, 313, 314,
324, 325
Lanternfish, 291
Larvae of ascidians, anatomy, 4954
dispersal potential, 6065
duration of planktonic period, 6065
ecology and behaviour, 4590
locomotion, 65
mortality, 7274
orientation, 6672
pelagic period, 6074
Latigo Point, Pollicipes, 121
Latitude, effect on breeding in cirripedes, 143 144
Lecithotrophic larvae, cirripedes, 110, 154, 155, 156
rhizocephalans, 101
Tetraclitidae, 130
Lecithotrophy, effect on egg shape in cirripedes, 154
effect on time of embryonic development in cirripedes,
154
Lepadoidea, egg production, 112117
on floating objects, 112
release of young, 117
size and number of eggs, 112, 113, 114, 115, 116
Lepadomorpha, egg production, 109123
Lepas, size at maturity, 112, 113
number of eggs per brood, 112, 113, 114, 115
Light, effect on breeding in cirripedes, 144
Light-harvesting potential of phytoplankton, 2325
Lithotrya, size of young, 122
Lizard Island, Great Barrier Reef, ascidians, 63
Long Island, U.S.A., Balanus species, 138
Luderick, 223
Lderitz, 275, 276, 283, 298, 315, 317, 321
Macroalgae, 168, 169, 188, 190, 193, 204, 225, 257
Madagascar, Acrothoracica, 107
Madras, India, Balanus species, 135
rhizocephalans, 99
Malay Archipelago, Tetraclitidae, 131
Malay Peninsula, Lepadoidea, 117
Malaya, Charcoal production from mangroves, 364
Malaysia, coral reefs, 353
effluent from oil-palm factories, 373
mangroves, 368, 371, 375
SUBJECT INDEX

oil spills, 374
river systems, 367
Malgas Island, 297, 301, 302, 312, 313, 314, 324, 325
Management of coral reefs, 362364
mangrove communities, 374376
tropical marine ecosystems, 382386
Mandapam Camp, India, removal of reef, 338
Mangrove communities, 364376
anthropogenic effects, 370374
fundamental research, 365370
management of, 374376
Mangroves and freezing, 364
and outwelling, 367
as nurseries for coral reef fishes, 379
capture fisheries, 375
charcoal production, 371, 375
commercial fisheries, 372
effect of cyclones, 365
effect of temperature, 365
frequency of tidal inundation, 365, 366
freshwater flow, 365, 366
hurricanes, 365
leaf litter to fish, 370
outwelling, 368
particulate organic carbon (POC), 368
matter (POM), 368
prawns, 368, 369, 372, 375
primary production, 366, 367
sedimentation, 365, 366
sesarmid crab, 369, 370
shrimp catches, 375
soil chemistry, 365, 366
soil salinity, 365, 366
tidal currents, 369370
used in charcoal production, 364
woodchip production, 370, 371
Mannitol in brown algae, 31
Maputo, 283
Marcus Island, 292, 300, 301, 302, 307, 317, 318
Marine algae and photorespiration, 3133
and terrestrial photosynthesis compared;
biochemical perspective, 1144
avifauna, 273335
aquarium trade, 359
bacteria, 16
faunal zones, 281
Antarctic, 281, 282
Arctic, 281, 282
407
boreal, 281, 282

northern subtropical, 281, 282
southern subtropical, 281, 282
subantarctic, 281, 282
tropical, 281, 282
mammals, danger of flotsam to, 357
phytoplankton, chlorophyll a content, 18
production, efficiencies of, 38
Marseilles, Balanus species, 135, 140
Marshall Islands, 176, 239, 243, 256
nuclear weapons tests, 356
Matang forest, Malaysia, 371
Mayotte Island, Indian Ocean, lagoonal sediments, 382
McMurdo Sound, assimilation numbers, 14
Mediterranean Sea, 173, 187
Chthamalus species, 126, 127
Lepadoidea, 116
Lepas larvae, 113, 114, 115
Scalpelloidea, 119
Mehler reaction, 34
Mekong Delta, mangroves, 371
Mercury Island, 291, 294, 295, 296, 298, 306, 310, 311,
312, 316, 317
Mexico, 174, 187, 256
Lepadoidea, 116
mangroves, 367
Microbial fermentation system, 170, 217
flora of fish guts, 167, 205, 226, 227, 233
MicroBRIAN, 383, 384
Micronesia, fish conservation, 381
Milkfish, 222
Miocene avifauna, 281
Mitochondrial respiration and photosynthesis, 3538
Moambique, 280
Mola Strait, Ibloidea, 111
Molluscs, 194, 206, 251
Monacanthid, 253
Monosaccharides, 193
Moorea, 238
Moulting, effect on egg production in cirripedes, 145
Mugilids, 198, 223, 227
Mullet, 208, 223, 224, 233
southern, 291
Multi-species fisheries models, 381
Murman region, Balanus species, 150
Murmansk, Balanus species, 152, 153
408
Musselcracker, 291
Mussels as indicator species, 363
Myctophids, 222
NADPH, 22, 23, 32, 33, 36, 37
Namibia, 275, 280, 281, 293, 298, 315, 317
central Namibian coast, 277, 278, 291, 294, 295, 296,
298, 299
Conchoderma, 113
northern Namibian coast, 280, 304, 315, 319
southern Namibian coast, 294, 295, 296, 298, 299,
312, 315, 316
Narragansett Bay, assimilation numbers, 14
Natal, 291, 308
National Mangrove Plans, 376
Neah Bay, Washington, ascidians, 76
Netherlands, Balanus species, 139
New Caledonia, conservation methods, 341
coral reefs, 359
New England waters, phosphate concentrations, 345
Newfoundland, Balanus species, 137, 153
New South Wales, Australia, 253
ascidians, 75
New species, effect on coral reefs, 360
New World mangroves, 365
New Zealand, 169, 173, 179, 180, 181, 186, 189, 195, 197,
235, 253, 256, 257, 258
ascidians, 75
Chamaesipho, 144, 149
Chthamaloidea, 128, 129
Elminius species, 132, 133, 143
Pollicipes, 121, 122, 123
Tetraclitidae, 131
waters, Lepas on buoys, 112, 113, 114, 115
Nigeria, oil spills, 373
Noody, common, 279
lesser, 280
North Africa, Acrothoracica, 106, 107
North America, Balanus species, 143
Pacific coast, Chthamalus species, 126, 153
Pollicipes, 121
west coast, Balanus species, 138
North Atlantic Ocean, 253
Lepas larvae, 113
North Carolina, U.S.A., 252, 260
North Europe, Balanus species, 137
North Pacific Gyre, 254
North Pacific Ocean, 251, 253, 256, 257, 258
North Sea, Heteralepadoidea, 112
Lepas larvae, 113, 114, 115
Northern European waters, Verrucomorpha, 123
Norway, Balanus species, 137
Nototheniid, 257
Nuclear weapons tests, coral reefs, 356
French Polynesia, 356
Number of broods, Balanus and related species, 135, 136,
137, 138, 139, 140, 141
eggs and age cirripedes, 146
Nutrient depletion, 276
enrichment, 323
Oceania, environmental degradation, 338
natural resources, 341
Odacids, 170, 180, 182, 193, 195, 196, 198, 206, 207,
217, 225, 258, 261
Oil pollution, seagrass communities, 378, 379
Oil spills, effect on jackass penguins, 319
mangroves, 373, 374
Old World mangroves, 369
Olifants River, 275
Omnivory, fishes, 234
Oogenesis, cirripedes, 94, 95
Optimal diets, 190, 191, 228
Optimal foraging theory, 190
Orange River, 275, 276, 283, 317
Otago, New Zealand, Acrothoracica, 107, 108
Ibloidea, 111
Over-fishing on coral reefs, 359
Oviposition, cirripedes, 95
Oxygen-evolving units (OEUs), 23, 24
Pachydictyol-A, 196
Pacific Islands, conservation practices, 383
giant clams, 359
Pacific mangroves, mans impact on, 341
Pacific Ocean, 188, 246, 319
growth of coral reefs, 347
Panama, 171, 237
coral reefs, 353
Papua New Guinea, 250
fish fauna in mangroves, 379
mangroves, 366, 368
Parasites, effect on egg production in cirripedes, 148149
SUBJECT INDEX
Parrotfishes, 167, 170, 171, 179, 180, 181, 182, 184, 185,
194, 195, 198, 205, 208, 225, 233, 237, 241, 242, 243,
244, 377
Particulate organic carbon (POC), 369
Pedunculate cirripedes, 109, 110
Pelican, 283
brown, 283
white, 277, 278, 281, 283, 284, 285, 286, 291, 304,
306, 307, 311
Penguin, 281, 283, 304, 308, 309, 315, 317, 318, 321, 326
jackass, 273, 274, 277, 281, 287, 293, 295, 298, 299,
300, 302, 303, 304, 306, 307, 308, 309, 310, 311, 313,
315, 316, 317, 318, 319, 320, 321, 322, 324, 326, 327
king, 279
macaroni, 279
rockhopper, 279
Penis loss, cirripedes, 95
PEP carboxykinase, 28, 30
carboxylase, 28, 29, 30
Percichthyid, 229
Peru, 181
coast of, photosynthesis, 25
Peter the Great Bay, Sea of Japan, Balanus species, 140,
149
Petrel, 281, 309
Atlantic, 279
Antarctic, 279
blue, 279, 319
Bulwers, 279
greatwinged, 278, 284, 289
grey, 279
Kerguelen, 279
northern giant, 278, 289
pintado, 278, 289, 305, 308, 319
softplumaged, 278, 289, 308
southern giant, 278, 289
whitechinned, 278, 289, 303, 305, 308, 309
whiteheaded, 279
Phaeophorbide a, 17
Phalarope, grey, 279, 288, 304, 305
Phenolic compounds, 184, 233
Philippines, Balanus species, 136
decline in mangroves, 338
Ibloidea, 110
Lithotyra, 122
mangroves, 372, 375, 376
409
Phlorotannins, 194, 195, 196, 197, 225, 258

Phosphoenolpyrute (PEP), 16
Phosphorus transfer from sediments, 367
Photoinhibition, 3435
Photokinesis, ascidian larvae, 6667
Photorespiration and marine algae, 3133
and productivity estimates, 33
a release valve, 31
Photosynthesis, assimilation numbers, 11, 12, 13, 14, 15
14C techniques, 15
carboxylation, 2731
dark fixation, 16
dark (mitochodrial) respiration, 3538
efficiency of conversion of radiant energy to biomass,
25
in bacteria, 16
in nutrient-poor tropical oceans, 12
in nutrient-rich in northern and southern oceans, 12
inorganic carbon uptake, 2627
marine and terrestrial, actual photo
synthesis, 1213
14C technique, 1516
compared: biochemical perspective, 1144
estimates of, 1216
potential photosynthesis, 1315
temperature, 20
off Americas, 12
off west coast of Africa, 12
PEP carboxylation, 2831
poisoned, 16
RuBP carboxylation, 2728
terrestrial, maximum rates, 11
Photosynthetic biochemistry, 15
carbon dioxide fixation, 15
efficiencies, 19, 20
electron transport, 2223; 13, 17, 20, 21
and light-harvesting potential of phytoplankton, 22
27
Phototaxis, ascidian larvae, 6772
Phycobilipigments, 18
Phycobiliprotein, 23
Physical disturbances, effects on coral reefs, 357358
Phytoplankton, 168, 197
light-harvesting potential and photosynthetic electron
transport, 2225
open ocean, 12, 13
Picoplankton, 18, 19
Pilchard, 273, 277, 287, 293, 298, 302, 303, 312, 314, 315,
317, 323, 324, 325, 326, 327
410
Pinfish, 73, 196

Planktivores, 183, 185
Plankton blooms, 276
Recorder, plankton samples, 113
Plant-herbivore relationships, 170, 196
Plastic debris, coral reefs, 356
pellets ingested by birds, 319
Plastocyanin, 22
Plastoquinone (PQ), 21, 22, 23
Platanna-kilpfishes, food of bank cormorant, 291
Pliocene avifauna, 281
Point Conception, Pollicipes, 121
Pollicipes, feeding of, 121
number of broods, 121, 122
size and number of eggs, 122, 123
Pollution, effect on breeding of seabirds, 319
egg production in cirripedes, 148
Polychaetes, 195, 229, 318
Polynesia, fish conservation, 381
Polysaccharides, 193
Pomacanthids, 218, 223
Possession Island, 290, 291, 294, 295, 296, 298, 312, 316,
326
Post-hatching ecdysis, cirripedes, 145
Power generator cooling systems, effect on seagrasses,
379
station effluent, effect on coral reefs, 356
Prawn culture, 371
fishery and seagrasses, 377
Prdation on herbivorous fishes, 241, 242, 243
Pricklebacks, 188
Primary production, 273, 323, 326
mangroves, 366, 367
Prion, 303, 305
broadbilled, 278, 288, 304, 307
fairy, 279
slenderbilled, 279
Procellariform species, 283, 285, 303, 319, 327
Productivity estimates and mitochondrial respiration, 37
38
and photorespiration, 33
Pmax, 23, 27
estimates, 39
for land plants, 16
marine phytoplankton, 12
photosynthesis at saturating light carbon dioxide and
ambient temperature, 11
phytoplankton, 13
Productivity of food fishes and lobsters feeding in

seagrass beds, 380
Protein/energy (P/E) ratio, 191, 192, 198, 232
Protein requirements, herbivorous fishes, 231, 232
Protozoans, 226, 227
Puerto Rico, 175, 247, 256
mangroves, 372, 374
oil spills, 373
Puget Sound, Washington, ascidians, 79, 81, 83
Purse-seine fishery, 273, 298, 302, 313, 317, 318
Pyrgoma, size and number of eggs, 134
Q10 values, 20
Rabbitfishes, 184, 185, 195, 242, 243
Radioactive pollution, effect on coral reefs, 356
Radiotelemetry, 307
Ratfish, 303
Recruitment, ascidians, role of reproductive and larval
processes in, 8185
Red Sea, 184, 185, 207, 227, 241
coral reefs, 353
Reef organisms, population genetics, 363
Reefs, artificial, 251
temperate, 232
tropical, 183, 184, 185, 232, 236, 239, 241
rocky, 253, 256
Remote sensing devices, 307
Reproduction, ascidians, larval release and spawning, 55
59
modes of, 4648
seasonal patterns, 5455
timing and synchrony, 5459
Reproductive gonads, cirripedes, 9495
rhythms, 134
Research relevant to the conservation of shal
low tropical marine ecosystems, a review, 337414
Reynolds number, 60, 65
Rhizocephala, breeding seasons, 98, 99
embryogenesis, 97
externa, 96, 97, 100, 101, 102
and male cyprids, 96, 97
incubation time, 98, 99, 100
interna, 96, 97
kentrogon stage, 93, 95, 96
lecithotrophic nauplii, 101
SUBJECT INDEX
number of broods, 100

number of eggs, 98, 99, 101
sex of cyprids, 96, 100
size of eggs, 100
size of ova and eggs, 97, 98, 99
spermatogenesis, 97
transfer of spermatozoa, 92
trichogon stage, 93, 97
Rhizocephalans as parasites, 95, 96
Ribulose-1,5-bisphosphate carboxylase (RuBP
carboxylase), 16, 19, 21, 26, 27, 28, 29, 30, 31
Robben Island, 317, 318
Rock lobster, 293
Rocky intertidal, 173, 174, 180, 188, 217, 243
littoral, 173, 174
subtidal, 173, 174
Roscoff, France, Acrothoracica, 106, 108
RuBP oxygenase activity, 33
Rudderfishes, 186, 217
Sabah, mangroves, 371
St. Croix, U.S. Virgin Islands, 171, 245, 300, 307, 317,
318
oil spills, 374
St. Helena Bay, 275, 276
Salawater Island, Balanus species, 137
Saldanha Bay, 275, 290, 300, 301, 302, 307, 317, 320,
321, 323
Salinity, effect on egg production in cirripedes, 147148
Salmonids, 229
San Bias Islands, Panama, 171
Sandwich Harbour, 278, 281
San Juan Islands, ascidians, 70, 75, 76
Pollicipes, 122, 123
Santa Catalina Island, Pollicipes, 121
Saudi Arabia, oil spills, 373
Saury, 287, 293, 298, 303, 313, 326, 327
Scalpelloidea, abbreviated embryonic development, 117
dwarf and complemental males, 117, 120
size and number of young, 118, 119, 120
time of breeding, 118, 119, 120
two types of cyprids, 120
Scalpellum species, female or hermaphrodite, 117, 118,
119
shallow and deep-water, 117
Scarids, 171, 180, 184, 185, 206, 217, 225, 241, 244, 245,
261
Schooling, 179
411
Scorpaenids, 222
Scorpidids, 186, 188, 195, 251, 261
Scotland, 256
SCUBA diving, 360
Sea anemone, 73, 229
Sea bass, 368
Seabirds, Benguela ecosystem, 273335
breeding, 273, 274, 277, 281, 282, 283, 284, 304, 306,
307, 308, 310, 311, 321, 326, 327, 328
breeding failure, 318, 319
diet, 285304; 274
feeding techniques, 286, 287, 288, 289
feeding zone, 285289
food consumption, 320323
habitats, 306
mixed species feeding assemblages, 273, 305, 307,
308, 309, 328
mortality rates, 309, 310, 314, 319
oil-related, 319
toxicant-related, 319
non-breeding, 273, 274, 277, 280, 281, 282, 283, 284,
285, 303, 304, 307, 308, 310, 321, 327, 328
population dynamics, 311319; 273
Seagrass communities, 251
beds, 183, 187, 243
cyclones, 377
oil pollution, 378, 379
replanted, 379
Seagrasses, 168, 175, 176, 182, 184, 193, 194, 202, 208,
217, 225, 233, 244
epiphytic algae, 378
prawn fishery, 377
productivity, 253
rhizosphere, 377
Sea of Azov, Balanus species, 138, 139
Sea of Japan, Balanus species, 137, 141
Sea otters, 258
Sea snakes, 132
Sea urchins, 167, 169, 194, 196, 197, 237, 241, 242, 244,
245, 249, 251, 258, 377
Seaweed calcification and toughness, 194
combined defences, 197
communities, 167, 169, 237, 238, 239, 242, 244, 251,
261
cover, effect on egg production in cirripedes, 147
defences, 193197
digestibility, 193194
412
secondary compounds, 194196

Secondary metabolites, 184, 193, 194, 196, 261
Sedimentation, effect on coral reefs, 351352
Self-fertilisation, cirripedes, 93, 94
Senegal, Heteralepadoidea, 112
Settlement, ascidians, 7481
Sewage pollution, effect on coral reefs, 354 355
Shallow marine organisms and UV radiation, 345
Shallow tropical marine ecosystems, distinctiveness of,
341346
literature, 339341
review of research relevant to conservation of, 377
414
Sharks, 309
danger of flotsam, 357
Shearwater, 304, 307
Audubons, 280
Corys, 278, 289, 303, 307, 309
fleshfooted, 279
great, 279, 285, 288, 303, 319
little, 279, 288, 303
Manx, 279, 288, 303
sooty, 279, 288, 303, 305, 307, 309
wedgetailed, 280
Shrimps, mangroves, 372
Siboga Expedition, 98, 99
Siganids, 184, 185, 193, 194, 223
Silverside, Cape, 291
Sipunculids, 246
Size and number of eggs, Acasta, 134
Coronulidae, 132
Pollicipes, 122
Pyrgoma, 134
Size and number of young, Balanus and related species,
135, 136, 137, 138, 139, 140, 141
Chthamaloidea, 126, 127, 128
Elminius, 133, 134
Hexaminius, 133
Tetraclitidae, 130
Verruca, 124
Skipjack, 309
Skua, 304, 305
Arctic, 279, 289, 305
longtailed, 279, 283, 289, 304, 305
pomarine, 279, 283, 289
subantarctic, 279, 289, 305
south polar, 279
Snappers, 377
Snoek, 303, 324, 325, 326
yellowtail, 309
Solar energy and fish, 38
South Africa, 273335; 174, 256
ascidians, 75
Balanus species, 141
cirripedes, 95
Lepadoidea, 116
Scalpelloidea, 118, 119
Tetraclitidae, 131
South America, Elminius species, 132
fish conservation, 382
South Europe, Pollicipes, 121, 122, 123
South Georgia, Scalpelloidea, 119
South Pacific, 258
Southeast Asia, conservation practices, 383
mangroves, 365, 371
Southern Africa, 273335
Southern Australia, ascidians, 83
Southern oceanic avifauna, 283
Southern Oscillation, 319
Sparids, 187, 204, 205, 207, 223, 253, 291
Sperm morphology in Ascothoracica, 91
Spermatogenesis, Acrothoracica, 104
cirripedes, 94
rhizocephalans, 97
Spermatozoa, Acrothoracica, 104
cirripedes, 93, 94, 95
Spitsbergen, Balanus species, 137, 143, 150
Sponges, 246
Squid, 291, 303
Squirrelfishes, 377
Starfishes, 229
Station Jedan, Pyrgoma, 134
Stichaeids, 179, 188, 189, 190, 191, 198, 205, 207,
208, 217, 218, 223, 228, 230, 233
Stomatopods, 318
Storm petrel, 303, 304, 305
blackbellied, 279, 285
European, 279, 288, 304
Leachs, 279, 288
whitebellied, 279
Wilsons, 279
Strandfontein, 301
Submersibles, use of, 239
Sula Sea, Balanus species, 135
Sumatra, Lepadoidea, 116
Sumba, Lepadoidea, 116
SUBJECT INDEX
Surfperches, 252
Surgeonfishes, 167, 172, 183, 191, 195, 197, 206, 208,
223, 224, 227, 237, 241, 242, 243, 245, 261, 377
Surinam, mangroves, 372
Swakopmund, 275, 280, 286
Sweden, Balanus species, 139, 144
rhizocephalans, 98
Scalpelloidea, 120
Sydney, Australia, 252
Balanus species, 135, 136, 138, 140, 141
Chamaesipho, 144
Synchrony in breeding in cirripedes, 134, 142, 144, 145
Synergism and coral reefs, 360362
Table Bay, S. Africa, Balanus species, 135, 140
Tanabe Bay, Japan, Balanus species, 141, 142
Tanzania, 178, 256
Tarante, Italy, cirripides, 95
Tasmania, south of, assimilation numbers, 14
Lepadoidea, 116
Teleosts, 167, 180, 257
Temperature barrier to breeding, cirripedes, 142, 143
effect on breeding in cirripedes, 142143
effect on mangroves, 365
Tern, 303, 304, 305, 306, 309
Antarctic, 279, 283, 289, 290
Arctic, 279, 284, 289
black, 279, 283, 289
blacknaped, 280
bridled, 279
Caspian, 277, 278, 281, 285, 286, 291, 304, 306, 307,
311
common, 279, 289, 306
comic, 305
Damara, 277, 280, 283, 285, 286, 290, 291, 304, 306,
307, 308, 311
gullbilled, 278
little, 279, 289
roseate, 277, 278, 279, 303, 304, 311
royal, 279
Sandwich, 279, 289, 306
sooty, 279
swift, 277, 280, 281, 286, 291, 304, 308, 311, 327
whitewinged, 278
whitecheeked, 280
Terpenoids, 185, 195, 197
Territorial defence, fishes, 171, 172, 179
Territories, fish, 245251; 171, 172, 179, 236, 241
Tetraclitidae, abbreviated embryonic development, 130
413
breeding seasons, 130, 131

lecithotrophic larvae, 130
Thailand, mangroves, 375
Thermal front, 276
pollution, effect on coral reefs, 355356
Thermo-saline front, 305
Thoracica, diversity of order, 109
Tongo, Acrothoracica, 107
Torres Strait, seagrass communities, 376
Tourism, effect on coral reefs, 360
Trawl offal, 285, 286, 291, 293, 304, 305, 307, 309, 310,
323, 327
Trinidad, mangroves, 372
Tropic bird, redbilled, 279
redtailed, 279
whitetailed, 279
Tropical and temperate marine ecosystems, differences
between, 342, 343, 344
Atlantic, assimilation numbers, 14
fisheries managers, problems of, 341
fishermen and conservation, 381, 382
marine ecosystems, community interactions, 379380
degradation in, 338
fisheries conservation, 380382
methods of management, 382386
marine pollution, 339
organisms and their lower oxygen limits, 342
and their thermal limits, 342
Pacific assimilation numbers, 14
surface waters and nutrients, 345
waters, biological uptake of pollutants, 345
Tuna, 309, 326
longfin, 309
yellowfin, 309
Turtles, 132, 377
danger of flotsam to, 357
Tyrrhenian Sea, Balanus species, 135
Uchiura Bay, Japan, Balanus species, 138, 139, 140, 141
UNEP Regional Seas Reports and Studies Series, 340
UNESCO Reports in Marine Science, 340
United Kingdom, Balanus species, 136, 137
United States Congress Office of Technology
Assessment, 341
United States, Virgin Islands, oil spills, 373
Upwelling, 276, 281, 285, 323
414
wind-driven, 273
UV radiation and shallow marine organisms, 345
effect on coral reefs, 361
Venezuela, barrages on river systems, 372
mangroves, 371
Verruca, size of young, 124
Verrucomorpha, asymmetrical barnacles, 123, 125
breeding seasons, 125
Viet Nam, defoliants used in war, effect on mangroves,
370, 371
Vineyard Sound, assimilation numbers, 14
Virgin Islands, 171, 175, 244, 245, 256
Virtual Population Analysis (VPA) to estimate fish
stocks, 320, 323 324
Vladivostok, Balanus species, 141
Walvis Bay, 275, 278, 280, 281, 283, 294, 295, 296, 310,
317, 322
West Indies, Lepadoidea, 116
Pollicipes, 122
Whale, Brydes, 309
White Sea, Balanus species, 137, 138
Woods Hole, Acrothoracica, 108
ascidians, 64
World National Parks Congress, 1982, 385
Zooplankton, 183, 204

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OCEANOGRAPHY AND MARINE BIOLOGY

OCEANOGRAPHY AND MARINE

HAROLD BARNES, Founder Editor

ABERDEEN UNIVERSITY PRESS

FIRST PUBLISHED IN 1989

ISBN 0-203-19 130-7 (Adobe eReader Format)

A Comparison of Marine Photosynthesis with Terrestrial Photosynthesis: a Biochemical

The Ecology and Behaviour of Ascidian Larvae

Egg Production in Cirripedes

Biology of Marine Herbivorous Fishes

The Benguela Ecosystem. Part VI. Seabirds

Review of Research Relevant to the Conservation of Shallow Tropical Marine Ecosystems

Oceanogr. Mar. Biol. Annu. Rev., 1989, 27,

A COMPARISON OF MARINE PHOTOSYNTHESIS WITH

PHOTOSYNTHESIS: A BIOCHEMICAL PERSPECTIVE

Chlorophyll 107 tonnes

Biomass 109 tonnes dry

Continental shelves, estuaries, seaweed beds, reefs.

Assimilation numbers mg Cmg chl a

Various oceanic waters

Steemann Nielsen & Hansen, 1961

Assimilation numbers mg Cmg chl a

Various oceanic waters

Eppley, 1972 (average of 17 values,

PHOTOSYNTHESIS: A BIOCHEMICAL PERSPECTIVE

Assimilation numbers mg Cmg chl a

Rivkin & Putt, 1987

THE 14C TECHNIQUE

PHOTOSYNTHESIS: A BIOCHEMICAL PERSPECTIVE

Chlorophyll a content of marine phytoplankton

Chlorophyll a % dry weight

PHOTOSYNTHESIS: A BIOCHEMICAL PERSPECTIVE

PHOTOSYNTHESIS: A BIOCHEMICAL PERSPECTIVE

associated light-harvesting pigment-proteins and proteins involved in water-splitting, (2) cytochromes b6

PHOTOSYNTHESIS: A BIOCHEMICAL PERSPECTIVE

INORGANIC CARBON UPTAKE

PHOTOSYNTHESIS: A BIOCHEMICAL PERSPECTIVE

Photo-synthesis chl a Carboxylase/

Beardall & Morris,

Approximate mean values.

PHOTOSYNTHESIS: A BIOCHEMICAL PERSPECTIVE

PHOTOSYNTHESIS: A BIOCHEMICAL PERSPECTIVE

PHOTOSYNTHESIS: A BIOCHEMICAL PERSPECTIVE

PHOTOSYNTHESIS: A BIOCHEMICAL PERSPECTIVE

PHOTOSYNTHESIS: A BIOCHEMICAL PERSPECTIVE

Jenkins, W.J., 1982. Nature (London), 300, 246248.

PHOTOSYNTHESIS: A BIOCHEMICAL PERSPECTIVE

Shulenberger, E. & Reid, J.L., 1981. Deep-Sea Res., 28A, 901919.

Oceanogr. Mar. Biol. Annu. Rev., 1989, 27, 4590

THE ECOLOGY AND BEHAVIOUR OF ASCIDIAN

* Harbor Branch Contribution No. 678.

THE ECOLOGY AND BEHAVIOUR OF ASCIDIAN LARVAE

Order of authorship is alphabetical.

IB SVANE AND CRAIG M.YOUNG

Fig 2.Generalised life cycle of a molgulid ascidian with anural development.

THE ECOLOGY AND BEHAVIOUR OF ASCIDIAN LARVAE

IB SVANE AND CRAIG M.YOUNG

THE ECOLOGY AND BEHAVIOUR OF ASCIDIAN LARVAE

IB SVANE AND CRAIG M.YOUNG

THE ECOLOGY AND BEHAVIOUR OF ASCIDIAN LARVAE

Average spawning latency Spawning time Settlement time References

Scott, 1954; Mast, 1921

Watanabe & Lambert,

Crisp & Ghobashy, 1971