British Phycological Journal

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The life history and sexual reproduction of

Colpomenia peregrina (Scytosiphonaceae,
Phaeophyta) in Australia

Margaret N. Clayton

To cite this article: Margaret N. Clayton (1979) The life history and sexual reproduction of
Colpomenia peregrina (Scytosiphonaceae, Phaeophyta) in Australia, British Phycological Journal,
14:1, 1-10, DOI: 10.1080/00071617900650011

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Br. phycol. J. 14:1-10
1 March 1979

THE LIFE H I S T O R Y AND SEXUAL

R E P R O D U C T I O N OF C O L P O M E N I A
PEREGRINA (SCYTOSIPHONACEAE,
P H A E O P H Y T A ) IN A U S T R A L I A

By MARGARET N. CLAYTON
Botany Department, Monash University, Clayton 3168, Victoria, Australia

Although Colpomenia peregrina (Sauvageau) Hamel reproduces throughout most of the

year in Australia, functional gametophytes are extremely rare, Gametophytes occur in late
winter, they are dioecious and reproduction is anisogamous. The zygotes, female gametes,
and the majority of male gametes develop into filamentous sporophytes bearing unilocular
sporangia. Zoosporcs from the sporophyte generatiorts mostly give rise to saccate C. peregrina.
Cultured strains derived from wild C. peregrina differ in their reproductive potential.
Sporophyte generations were only found in strains derived from parthenogametes or zygotes.
Several other strains produced saccate progeny, irrespective of the culture conditions. The
evidence that such strains may be asexually reproducing, "morphological" gametophytes is
discussed.

Colpomenia peregrina (Sauvageau) Hamel is widespread in temperate coastal

regions of the world. In Australia it m a y be f o u n d t h r o u g h o u t the year growing
on rocky surfaces, and as an epiphyte in the eulittoral or upper sublittoral
zones (Clayton, 1975).
The reproductive organs are plurilocular sporangia, but very little is k n o w n
about the life history o f C. peregrina. Unilocular sporangia have never been
reported. Sauvageau (1927) and D a n g e a r d (1963) described the direct develop-
ment of zooids o f C. peregrina into filamentous protonemata u p o n which the
new Colpomenia thalli were formed. Both authors also noted some filamentous
microthalli bearing plurilocular sporangia in some o f their cultures, but their
origin, role, and significance were not fully explained. Sauvageau (1927) at-
tributed the fertility of the filamentous microthalli to their advanced age, and
suggested that they were h o m o l o g o u s with the normal saccate thalli. Sexual
reproduction has not previously been reported for C. peregrina. However, a
few studies of other species of Colpomenia have presented evidence for both
sexual and asexual reproduction. Although there is a very obvious need for
more research to confirm and elaborate these studies, it is apparent that there
are various modes o f syngamy and several kinds of filamentous microthalli
amongst Colpomenia spp.
The present study is part o f a larger investigation o f the Scytosiphonaceae of
southern Australia in which one of the aims is the documentation o f the life
histories o f the various species.
1
000%1617/79/010001 q- 10802"00/0 1979 British Phycological Society
2 M.N. CLAYTON

MATERIAL AND METHODS

Fertile specimens of C. peregrina were collected from several different localities at various
times of year (Table I). Segments of thalli bearing mature plurilocular sporangia were cut out,
washed in sterile seawater, and placed in Provasoli's ES medium (Clayton, 1974) in individual
Petri dishes. Whenever zooids were released in sufficient quantity, their phototactic behaviour
was observed under unilateral illumination. Mixtures of zooids from different parent thalli
were prepared and checked for mating reactions and zygote formation. Cultures were
established by pipetting gametes or zooids, derived from individual parent thalli, and also
zygotes, into Pyrex storage dishes (No. 3250) containing 150 ml ES medium. Generally, at
least three, and up to ten cultures were set up from each collection depending upon the number
of good fertile specimens. Replicates of the cultures were maintained at 16C in one or more
daylength regimes (Table I), with lighting furnished by Grolux wide spectrum fluorescent tubes,
giving an illuminance of about 2000 Ix. All cultures were examined weekly and the medium
was changed at least every fortnight.

TABLE I. Cultures of Colpomenia peregrina

Zooid Phototactic No. thalli Daylength (h)

No. Locality Date size:~ response Ft cultured L : D 8:16 I1:13 16:8

1 Hinders 29. viii. 75 large -- filamentous 10 X

2 San Remo 29. xi. 75 large -- C. peregrina 10 X
3 Heron Is. 23. xi. 76 large C. peregrina 10
4 Sorrento 28. iv. 77 large C. peregrina 6 X
5(a) Flinders 26. vii. 77 large* ve filamentous 2 X X
(b) Flinders 26. vii. 77 small* --ve filamentous 99%I"
C. peregrina 1 ~ f 2 X X
(c) Flinders 26. vii. 77 zygotes filamentous 3 X X
6 Flinders 17. ix. 77 large + ve C. peregrina 4 X X
7 Sorrento 4. x. 77 large ve C. peregrina 5 X

* Zygotes were obtained from three different combinations of these gametes.

t Correct to nearest 1%.
+, Precise size ranges given in text.

In cultures of saccate C. peregrina, three or four individuals were allowed to develop in

each dish, and when the plants became fertile the zooids were examined to ascertain whether
they were male or female gametes, or asexual. In cultures of the smaller filamentous micro-
thalli, a greater number of individuals was maintained in a dish. When they developed together
with C. peregrina, the latter were all carefully removed as soon as the morphological differences
were apparent, and they were grown separately. The progeny of all cultured plants were
separated from the parent thalli as soon as their appearance was noted.
Unfortunately, the difficulty of devising a successful staining technique in order to examine
chromosome number has precluded cytological studies, but it is hoped that it will be feasible
to do this in the future.

OBSERVATIONS

M o s t o f t h e s a m p l e s o f C. peregrina w h i c h w e r e e x a m i n e d ( T a b l e I, N o s 1-4,
6 a n d 7) c o n s i s t e d o f m a t u r e thalli b e a r i n g p l u r i l o c u l a r o r g a n s f r o m w h i c h
large z o o i d s (Fig. 1), m e a s u r i n g 8 - 1 2 x 4 - 6 p m w e r e released. S u c h z o o i d s
h a v e a t y p i c a l p h a e o p h y c e a n s t r u c t u r e i n c l u d i n g o n e p l a s t i d a n d an e y e s p o t ,
a n d t w o l a t e r a l l y i n s e r t e d flagella. T h e s h o r t a n t e r i o r f l a g e l l u m h a s a n a r r o w e d
distal s e c t i o n . T h e z o o i d s u s u a l l y settle w i t h i n t h r e e h o u r s a f t e r release. W h e n
r e l e a s e d in sufficient q u a n t i t y ( N o s 6 a n d 7), the z o o i d s c o u l d b e o b s e r v e d as a
b r o w n c l o u d c o n g r e g a t i n g o n t h e side o f the p e t r i d i s h n e a r e s t t h e l i g h t s o u r c e .
 Life history of Colpomenia in Australia 3

FIGS 1-5. Micrographs of Colpomenia peregrina. Fig. 1. Zoospore showing thin distal
segment of anterior flagellum (phase contrast). Fig. 2. Anisogamy showing smaller, male
gametes clustered around the larger, female gamete. Fig. 3. Zygote and unfused gametes.
Fig. 4. Male gametangia and unicellular paraphysis. Fig. 5. Female gametangia and
unicellular paraphysis.
~.~

L--
~. >

g~ 0
~.~" Z

.~'~

~2.

ga
 Life history of Colpomenia in Australia

A single collection of C. p e r e g r i n a (No. 5) yielded sexual thalli. They were

dioecious and produced anisogametes most of which were negatively photo-
tactic. The female gametes (Fig. 2) were indistinguishable in size, appearance
and settling characteristics from the zoo~ds described above. The male gametes
(Fig. 2) were much smaller, about 4 pm in diameter when they had settled, and
they retained their motility for several hours longer than the female gametes.
In suspension, male gametes were distinguished from female gametes by their
milky appearance, the female gametes being distinctly brown in colour. When
male and female gametes were mixed, a characteristic mating reaction (Fig. 2)
took place. The smaller male gametes swarmed around those female gametes
which had come to rest, causing the entire cluster to rotate. As soon as one
male became attached to the female, movement ceased and the group broke
apart. After two to three hours zygotes could be seen with two eyespots (Fig. 3).
The differences between the male and female gametangia were clearly ap-
parent. The male gametangia (Fig. 4) measured 20-44/~m long and comprised
7-12 tiers of loculi, each 3 - 4 / t m long. The female gametangia (Fig. 5) measured
12-50/tin in length and consisted of 4-8 loculi. Plurilocular organs from which
the large zooids originated were indistinguishable from the female gametangia.
In culture, the large zooids derived from plurilocular organs on most of the
samples of wild C. p e r e g r i n a developed into similar thalli (Table I, Nos 2-4, 6
and 7) in much the same manner as that described by Sauvageau (1927) and
Dangeard (1963). After settling, the zooids developed more or less directly
into small, spherical balls of cells which became hollow at an early stage in
their growth. Only occasional germlings developed a conspicuous filamentous
protonema prior to the initiation of the saccate thallus.
From the collection of C. p e r e g r i n a made on 26 July 1977 parthenogametes
from two male and two female thalli, and zygotes obtained from three out of
the four possible matings were cultured (Table l). Attempts were made to
isolate zygotes from unfused gametes but these proved to be difficult and
unreliable. However, the development of the parthenogametes and zygotes
was similar. Initially prostrate discs of spreading filaments were formed (Fig. 6),
from which arose short, erect filaments, up to five cells in length (Fig. 7). The
microthalli were no more than 2-3 mm in diameter, and had the appearance of

TABLE II. Colpomenia peregrina: reproduction of saccate plants in different daylengths in

culture

No. Generation 8:16h 11 :13h 16:Sh

5(a) (9) F2 -+ C. peregrina F3 filamentous F3 --

5(b) (~) FI -+ C. peregrina F2 filamentous 99~ t --
C. peregrina 1% t
F2
6 FI -+ C. peregrina F2 C. peregrina F2 --
7 F1 -+ C. peregrina F2 -- --
2 FI -+ C. peregrina F2 -- C. peregrina F2

t Correct to nearest 1 ~.
6 M.N. CLAYTON

small brown cushions. After about 5 weeks in culture, terminal unilocular

sporangia developed on the erect filaments (Fig. 8). Paraphyses were observed
on some of the microthalli (sporophytes). Zoospores from the unilocular
sporangia gave rise to an F2 generation of C. peregrina (Fig. 9). In addition, the
F2 progeny of the zygotic sporophytes included a few (about 1%) sporophytes.
There were no differences amongst cultures of parthenogametes and zygotes
in the different daylength conditions (Table I).
In culture saccate C. peregrina took 8-14 weeks to reach maturity. The
highest growth rate occurred in an intermediate daylength, L: D 11 : ] 3h, and
the maximum diameter was 3-4 cm, although smaller plants were often fertile.
In general, cultured plants closely resembled wild forms. The progeny of
cultured thalli consisted of similar plants, sporophytes, or a mixture of ap-
proximately 99 % sporophytes and 1% saccate plants (Table II). Furthermore,
different strains of C. peregrina showed different reproductive characteristics.

,.~]l~ GA~METOPHYTE
] ]GAMETOPHY~TE
~
| o, nip [ ]pl~ n I '~

FIG. 10. Diagram of life history of C. peregrina. U--unilocular sporangia, P--

plurilocular gametangia, Pl--plurilocular sporangia, dotted lines indicate the fate of
a small proportion of progeny.

For example, no sporophytes at all occurred in the progeny of isolates of

Nos 2, 6 or 7, although they were grown under a variety of daylengths. Only the
strains (Nos 5a-c) which were originally isolated from parthenogametes or
from zygotes gave rise to sporophyte generations. The results (Table II) also
indicate a possible effect of daylength on the reproduction of these sexual
strains. This is currently under further investigation.
The life history of C. peregrina is summarised in Fig. 10.

DISCUSSION
It is well established that there are filamentous and crustose stages bearing
unilocular sporangia in the life history of species in the Scytosiphonaceae, and
in Scytosiphon lomentaria (Lyngbye) Link and Petalonia fascia (O. F. Mfiller)
 Life history of Colpomeniain Australia
Kuntze the effects of temperature, daylength, and nutrition on the induction
of microthalli are thoroughly documented (Wynne & Loiseaux, 1976). Recent
research has also demonstrated the roles of microthalli in relation to the process
of sexual reproduction. In several species of Scytosiphonaceae, haploid and
diploid microthalli bearing unilocular sporangia, generated by partheno-
gametes and zygotes respectively, have been shown (Nakamura & Tatewaki,
1975) to have a functional role comparable with the roles of the haploid and
diploid sporophytes in the life history of Ectocarpus siliculosus (Dillwyn)
Lyngbye (Mfiller, 1972).
The life history of C. peregrina (Fig. 10) exhibits several of the features which
we are now beginning to recognize as being common in, and perhaps character-
istic of, the Scytosiphonaceae. The saccate plants are potentially dioecious
gametophytes, and the germination of zygotes and gametes produces mainly
filamentous sporophytes. Zoospores from the unilocular sporangia on the
sporophytes mostly develop into C. peregrina. The ability of a small proportion
of what appear to be male parthenogametes to reproduce the gametophyte
generation raises the question as to whether such zooids are potential gametes,
or simply zoospores intermixed with the gametes. The phenomenon requires
further investigation. It also occurs in the germination of gametes of both
sexes in Colpomenia bullosa Yamada, and to a greater extent in S. lomentaria,
Petalonia zoster(folia (Reinke) Kuntze, and Endarachne binghamiae J. Agardh
(Nakamura & Tatewaki, 1975). Furthermore, in these species, unlike C.
peregrina, temperature and photoperiod affect the proportion of gametophytes
developing from parthenogametes.
The life history of C. bullosa (Nakamura & Tatewaki, 1975) has overall
similarities with that of C. peregrina, but sexual reproduction is isogamous,
whereas it is anisogamous in C. peregrina. Wynne (1972) asserted that C.
peregrina and C. bullosa, growing along the Pacific coast of North America,
could not be distinguished on the basis of morphology but in Australia, where
C. peregrina is common (Clayton, 1975), there are no records of any plants
approaching the form of C. bullosa. It is therefore probably advisable to
continue to recognize the two species.
Knowledge of the life history of Colpomenia sinuosa (Roth) Derbes et Solier
is fragmentary, and resemblances with the life history of C. peregrina are more
tenuous. Kunieda & Suto (1938) obtained filamentous microthalli from female
parthenogametes and zygotes grown in culture, but no sporangia were observed
before their observations were terminated. Cultures of zooids from C. sinuosa
f. deformans Setchell et Gardner (Wynne, 1972) produced filamentous plants
bearing plurilocular sporangia, and these subsequently gave rise to successive
generations of saccate thalli. However, Wynne presented no evidence to indicate
the sexual or asexual character of the parent thalli. The presence of plurilocular
sporangia on microthalli belonging to a species in the Scytosiphonaceae is
unusual, although not without precedent (Sauvageau, 1927; Dangeard, 1963;
Clayton, 1978). More work is needed in order to explain their role and signific-
ance in the life histories of the various species.
Reports of the reproduction and life history of species in the Scytosiphona-
ceae have given a conflicting and inconsistent impression of the reproductive
role of the larger thalli. Nakamura & Tatewaki (1975) observed only sexual
8 M.N. CLAYTON

reproduction in Colpomenia bullosa, Seytosiphon lomentaria, Petalonia zosteri-

folia, and Endarachne binghamiae. Yet there are many accounts of asexual
reproduction in S. Iomentaria, and some also for P. zosterifolia (Dangeard,
1963), and E. binghamiae (Wynne, 1969), so that it appears that all these species
reproduce both sexually and asexually. Both kinds of reproduction are reported
to occur in Colpomenia sinuosa (Kunieda & Suto, 1938). Gametophytes were
found in spring, and asexual plants in autumn. The progeny resulting from
asexual reproduction in C. sinuosa, unlike the the products of sexual reproduc-
tion, resembled the saccate parents.
However, the distinction between sexual and asexual reproduction may
not be as clear-cut as it seems. It is evident from the present observations on
C. peregrina that, although functional gametophytes are immediately recogniz-
able when both mating strains are present, and in this particular anisogamous
species the male gametophytes are also readily identified, it is quite possible
that in this and in other related species, one sex on its own may be mistaken
for an asexual plant, and vice versa. A further problem complicating the
differentiation between gametes and zoospores is the elusive nature of the
mating reaction in these algae. It cannot be assumed the attraction of male
by female gametes is maintained at a constant level from the time of their
release. Indeed, evidence from studies of ectocarpene secretion by Ectocarpus
siliculosus gametes indicates that secretion and the consequent attraction of
male gametes is initiated only as the female gamete comes to rest (Jaenicke,
1977). Observations of mating in C. peregrina suggest that a similar pheno-
menon could occur in this species. Therefore, even the non-reaction of male
gametes cannot be taken as conclusive evidence of the asexual character of
zooids, as it may be the consequence of the metabolic state of female gametes.
Thus, there do not seem to be any unequivocal means of distinguishing
gametes from possible asexual zoospores produced by plurilocular organs, and
it is important, therefore, to regard any such distinctions with caution. The
morphological difference between the progeny of gametophytes and so-called
asexual C. sinuosa noted by Kunieda & Suto (1938) could reflect the different
environmental conditions under which the wild parents had developed, rather
than any inherent difference in morphogenetic potential between gametes
and "zoospores". This suggestion is supported by observations (Nakamura &
Tatewaki, 1975) that culture conditions may affect the morphological character
of the progeny of gametophytes of various species of Scytosiphonaceae. Clearly,
further investigation is required to solve these and other related problems.
One particularly puzzling element is the apparent rarity of sexual reproduction
in the life history of C. peregrina. Only one (late winter) collection of functional
gametophytes of both sexes was made in the present study.* This contrasts
sharply with the Scytosiphonaceae examined by Nakamura & Tatewaki (1975)
all of which (with the exception of P. fascia) showed sexual reproduction. This
may possibly have been due to the fact that the plants were collected in winter
or spring and cultures were established exclusively from negatively phototactic
zooids. The studies of C. sinuosa (Kunieda & Suto, 1938) indicate that sex is
also a spring phenomenon in that species!
* Since going to press two more collections of C. peregrina gametophytes have been made
in August 1978.
 Life history of Colpomenia in Australia

T h e p h o t o t a c t i c responses o f z o o i d s described in this p a p e r were o b s e r v e d

under artificial a n d n a t u r a l illumination. O b s e r v a t i o n s using direct sunlight
were f o u n d to p r o d u c e less consistent responses. S o m e c a u t i o n is needed in
using p h o t o t a c t i c responses to identify a n d separate gametes a n d zoospores,
as they are k n o w n to be affected by light intensity and wavelength ( R o u n d ,
1973).
The n a r r o w t e r m i n a l section, n o t e d on the a n t e r i o r flagellum o f z o o s p o r e s
a n d female gametes o f C. peregrina, also occurs in zooids o f E. siliculosus a n d
Sorocarpus micromorus (Bory) Silva (Mftller, 1965). I n the case o f gametes o f
E. siliculosus, it is the first p a r t to establish contact d u r i n g the p a i r i n g process
(Mfiller, 1967).
The evidence p r e s e n t e d c o n c e r n i n g the effects o f culture c o n d i t i o n s on
r e p r o d u c t i o n in C. peregrina is scant and p r e l i m i n a r y in character. However, a
n o t a b l e p o i n t o f difference between these and the results o f N a k a m u r a &
T a t e w a k i (1975) w o r k i n g with C. bullosa, is the o c c u r r e n c e in C. peregrina o f
strains which r e p r o d u c e only saccate thalli irrespective o f daylength. This m a y
also reflect their highly selective m e t h o d s o f establishing cultures a n d the
short season over which this was done. Thus C. peregrina strains differ in their
potential for p r o d u c i n g s p o r o p h y t e generations. D o e s this m e a n t h a t t h e y
also differ in their p o t e n t i a l for g a m e t o g e n e s i s ? The difficulties inherent in
solving this p r o b l e m have been discussed, and it is the subject o f c o n t i n u i n g
research. N o c o m p a r a b l e i n f o r m a t i o n is available for o t h e r closely r e l a t e d
species b u t " m o r p h o l o g i c a l " g a m e t o p h y t e s which only r e p r o d u c e asexually
are k n o w n to o c c u r in E. siliculosus (Mfiller, 1976).

ACKNOWLEDGEMENTS
I wish to thank Mrs Iona Christianson for technical assistance and for reading the manu-
script. The project was supported financially by the Australian Research Grants Committee.
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(Accepted 13 October 1978)