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THE RELATIVE IMPORTANCE OF NANNOPLANKTOlN

AND NETPLANKTON AS PRIMARY PRODUCERS


IN TROPICAL OCEANIC AND NERITIC
PHYTOPLANKTON COMMUNITIES1
Thomas C. Malone2
Hopkins Marine Station, Pacific Grove, California 93950

ABSTRACT
Nannoplankton and netplankton primary productivity and standing crop were measured
in a wide variety of neritic and oceanic environments in the eastern tropical Pacific and
Caribbean region. Nannoplankters were the most important producers in all the environ-
ments studied, but netplankton productivity was significantly (P = 0.05) higher in neritic
than in oceanic waters. Mean neritic netplankton-nannoplankton productivity and chloro-
phyll ratios were 0.50 + 0.14 and 0.62 -C 0.22 respectively, significantly higher than those
observed in oceanic waters.
Relative levels of netplankton standing crop and productivity were not systematically
related to corresponding levels of primary productivity and standing crop as a whole.
The patterns of variation in the relative importance of netplankton and nannoplankton
could be accounted for by the high netplankton growth rates and low grazing pressure
indices observed in neritic as compared to oceanic waters.

INTRODUCTION tion, the relative levels of nannoplankton


The phytoplankton can be divided into and netplankton productivity and stand-
two groups based on whether they escape ing crop should be reflected in the distri-
or are retained by fine-mesh nets. The butions and abundances of herbivores that
fraction retained by the phytoplankton selectively graze one group or the other
nets (aperture size 20-90 p) is commonly (e.g., Thorson 1950; Strickland 1961; Mul-
called “netplankton” or “microplankton” lin 1963) .
and the fraction that escapes is referred Geographic variations in netplankton
to as “nannoplankton.” The ecological sig- and nannoplankton primary productivity
nificance of these two categories lies in and standing crop are poorly documented
the role of cell size in phytoplankton in the marine environment. Recent inves-
community dynamics. Typically small cells tigations in both temperate (Yentsch and
have shorter generation times and higher Ryther 1959; Gilmartin 1964; Anderson
growth rates in a given environment than 1965) and tropical waters ( Steemann
do larger cells, presumably owing to the Nielsen and Jensen 1957; Holmes 1958;
high surface area-to-volume ratios of Teixcira 1963) have demonstrated that
smaller cells (e.g., Odum 1956; Saijo and nannoplankton are often responsible for
Takesue 1965; Williams 1964). In addi- SO-99% of the observed phytoplankton
productivity. Little information is avail-
l This research was supported in part by the able on regions in which netplankton pri-
Organization for Tropical Studies Pilot Study mary productivity surpasses that of the
Grant No. 69-4 and The Society of the Sigma nannoplankton, although phytoplankton
Xi, in part by National Science Foundation Grants
GB 6870, GB 6871, and GB 8374, and in part by communities dominated by netplankton in
National Institutes of Health Predoctoral Fellow- terms of cell number ( Digby 1953) and
ship 5 FOl GM44363-02. Based on a thesis sub- chlorophyll concentration ( Subrahmanyan
mittcd in partial fulfillment of the requirements and Sarma 1965) have been reported. It
for a Ph.D. degree at Stanford University, Palo seems surprising, therefore, that it has be-
Alto, California.
2 Present address: Department of Biology, The come almost axiomatic that netplanktcrs
City College of CUNY, Convent Ave. and 138th tend to be the predominant primary pro-
St., New York, N.Y. 10031. ducers in neritic waters and high latitudes
LIMNOLOGY AND OCEANOGRAPHY 633 JULY 1971, V. 16(4)
634 THOMAS C. MALONE

while nannoplankters tend to predominate and duplicate values for each fraction
in oceanic waters and low latitudes ( cf. were averaged, The mean coefficient of
Yentsch and Ryther 1959; Wood 1963; variation between replicate light bottles
Ryther 1969 ) , was 7 * 2% (P = 0.05) and 22 -+ 5% be-
This study documents geographic varia- tween phytoplankton productivity values
tions in netplankton and nannoplankton calculated from the sum of the nanno-
primary productivity and standing crop plankton and netplankton fractions and
and relates these variations to spatial pat- determined directly from unfractionated
terns of phytoplankton productivity as a samples.
whole in tropical oceanic and neritic ChlorophyII a and pheopigment concen-
environments. trations were determined by a fluoromet-
I am grateful to Dr. M. Gilmartin for ric technique (Yentsch and Menzel 1963;
providing ship time on the RVs Te Vega Holm-Hansen et al. 1965). Water samples
and Proteus, to Dr. F. A. Richards for ship were fractionated by the same procedure
time on the RV Thomas G. Thompson, and described for the carbon-uptake measure-
to the Environmental Science Service Ad- ments, except Whatman GF/C glass-fiber
ministration and Mr. J, Tyler of SCOR filters coated with 2 ml of a I%, suspen-
Working Group 15 for ship time on the sion of MgC03 were used in place of
USC+GS Ship Discoverer. I thank Mr. R. membrane filters and the netplankton
Olund and Dr. J. Alberts for the NO,-N chlorophyh fraction was calculated from
analyses. the difference between fractionated and
unfractionated values. Duplicate values
MATERIALS AND METHODS for each fraction were averaged. When-
Net plankton and nannoplankton photo- ever possible, water for pigment analysis
synthetic capacities and chlorophyll a con- was collected from at least five additional
centrations were estimated from duplicate depths within the photic zone and one
water samples collected 3 hr before local below it.
apparent noon from 2 m below the surface The USC of glass filters may have led
with van Dorn bottles. Four light and two to an underestimation of nannoplankton
dark bottles (125ml Pyrex) were drawn chlorophyll a. However, Strickland and
from each sample, inoculated with 5 &i Parsons ( 1968) report little difference be-
of 14C-Na&03, and incubated under fluo- tween Whatman GF/C glass filters and
rescent light (about 0.06 ly/min) for 2-3 AA Millipore filters coated with MgCOs.
hr at sea surface temperatures (Doty and Also, a preliminary analysis of chlorophyll
Oguri 1958 ) . Following incubation, two a concentrations estimated by the trichro-
light and one dark bottle from each sam- matic method using glass-fiber and Sar-
ple were fractionated by passing the water torius 0.50-p membrane filters (Baird,
first through a Nytex-net disk with 22-p unpublished) indicates that glass filters
apertures (netplankton) and then through retained an average of 89% of the total
an HA Millipore filter ( nannoplankton) . chlorophyll a over a range of concentra-
The remaining bottles were passed di- tions of 0.06-0.56 mg rnd3 (for tropical
rectly through the HA Milhpore filter. The oceanic phytoplankton ) .
filter disks were washed with about 30 ml Surface NOs-N concentrations and mixed
of filtered seawater, dried in a COz-free layer depths were determined in conjunc-
atmosphere, and their activity measured tion with productivity and pigment mea-
with a Nuclear Chicago scalar (model surements, The N03-N was measured
l6lA) equipped with a model D47 gas using an AutoAnalyzer on the RV Thomas
flow chamber with a micromil window. G. Thompson (Stephens 1970); otherwise
Each filter was counted for at least 5 min. the manual procedure described by Strick-
Rates of carbon fixation were calculated land and Parsons ( 1968) was used. The
as described by Doty and Oguri ( 1958) depth of the mixed layer was determined
NANNO- AND NETPLANKTON PRIMARY PRODUCI’IVITY 635

TABLE 1. Mean NOs-N concentrations (pg-atom/


liter), water column pheopigment-chlorophyll ra-
tios (P: C), and mixed layer depths (2%~ = meters)
with !Xyo confidence limits in neritic waters, the
Peru Current region (I), tropical surface water
(II), and the Caribbean region (III)

Oceanic
Neritic I II III

NOrN 0 5.3 & 3.3 0 0.2 k 0.1


P:C 0.2 10.1 1.0 +- 0.3 1.2 -c 0.1 1.1 -r- 0.1
z YL 12 -t- 6 32 zk 8 24 k 7 84 zk 31

Phytoplankton productivity and chloro-


phyll a concentrations in neritic and Peru
Current waters ranged from l-5 mgC rno3
FIG. 1. Stations occwied in the tropical Pa- hr-1 and 0.15-0.70 mg m-3 respectively.
cific and Caribbean segregated into four regions: Much lower levels of phytoplankton pro-
Circles-neritic (November 1968, August 1969, ductivity were observed in the other two
January 1970); squaws-Peru Current (May
1970); triangles-tropical surface (December oceanic regions where values rarely ex-
1969 ) ; polygons-Caribbean ( May 1970 ) , ceeded 1 mgC m-3 hr-l. However, surface
concentrations of chlorophyll a were higher
by nearly an order of magnitude in trop-
from BT and STD casts. In addition, the ical surface water than in the Caribbean
ratio of pheopigmcnts to chlorophyll in region.
the water column was calculated and as- Surface productivity and chlorophyll a
sumcd to provide a crude index of relative concentrations of the nannoplankton frac-
grazing pressure on the phytoplankton tion exceeded that of the netplankton at
standing crop ( Lorenzen 1967). all stations in both neritic and oceanic
waters ( Table 2). Neritic nannoplankton
RESULTS AND DISCUSSION productivity averaged 1.54 + 0.46 mgC
Measurements of netplankton and nan- m-3 hr-l and varied from 0.60-2.96 (Fig. 2).
noplankton photosynthetic capacity and Oceanic nannoplankton productivity var-
standing crop were made at 44 stations in ied over a much wider range with a low
the eastern tropical Pacific Ocean and of 0.11 and a high of 6.48. The average
Caribbean Sea ( Fig. 1) during cruises of productivity of oceanic nannoplankton
the vessels mentioned in the introduction. was 1.16 2 0.50 which does not differ sig-
The stations were located between 10” S nificantly (P = 0.05) from that observed
and 30” N in surface water temperatures in neritic waters. Netplankton productiv-
of over 20C. Stations located within 100 ity varied from 0.32-1.98 in neritic waters
km of land or in less than 600 m of water in contrast with 0.0 to 0.43 for oceanic
are classified as neritic. The remaining sta- waters. Mean neritic netplankton produc-
tions are considered oceanic and are fur- tivity was significantly higher at 0.74 A
ther segregated into three groups based on 0.31 than the mean value of oceanic net-
surface N03-N concentrations and mixed plankton productivity of 0.10 * 0.04. Thus,
layer depth (Table 1 and Fig. 1). Grazing the high level of productivity observed in
pressure indices were much higher in all neritic waters was due primarily to higher
three oceanic zones than in the neritic levels of netplankton productivity, al-
environments studied. though mean nannoplankton productivity
Values for netplankton and nannoplank- values were significantly higher than the
ton primary productivity and chlorophyll corresponding netplankton values in both
a concentration are presented in Table 2. oceanic and neritic environments.
636 THOMAS C. MALONE

TABLE 2. Nannoplankton and netplankton primary productivity (PI’ = mgC m-” hrl), standing crop
(SC = mgChl a m-‘, m-‘), and productivity indices (PI = mgC mgChl a-’ hr-‘) for the four regions
studied

PP SC (m”) SC (m2) PI
Station Nanno Net Nanno Net Nanno Net Nanno Net

l-001 2.96 1.12


005 1.51 0.40
006 2.17 1.98
007 0.60 0.37
008 1.56 0.48
010 1.48 0.54
2-001 0.98 0.76 0.198 0.160 5.0 4.8
002 2.00 1.04 0.143 0.090 13.15 9.41 14.0 11.6
003 0.82 0.32 0.114 0.050 11.89 5.27 7.2 6.4
004 2.04 0.57 0.301 0.124 14.42 17.92 6.8 4.6
3-033 0.82 0.58 0.385 0.319 17.85 15.69 2.1 1.8
Peru Current region
4-006 3.79 0.05 0.272 0.032 34.45 3.10 13.9
007 2.28 0.26 0.254 0.048 24.10 1.70 9.0 ifi
008 2.14 0.32 0.241 0.060 11.62 0.69 8.9 5:3
010 1.18 0.10 0.198 0.020 17.46 1.76 5.0
011 1.26 0.10 0.212 0.024 17.00 1.00 E 4.2
012 1.24 0.14 0.158 0.023 10.75 1.63 718 6.1
013 3.15 0.06 0.222 0.010 12.02 1.21 14.2 6.0
015 2.76 0.12 0.202 0.017 14.32 0.58 13.7 7.1
016 6.48 0.43 0.269 0.061 22.23 2.69 24.1 7.1
Tropical surface water
l-002 1.28 0.27
003 1.12 0.20
004 1.82 0.42
009 0.97 0.01
3-001 0.71 0.05 0.192 0.030 20.05 2.24 3.7 1.8
005 0.22 0 0.180 0.014 22.52 3.30 1.2 0
009 0.24 0 0.126 0.052 13.40 1.07 1.9 0
013 0.12 0.02 0.116 0.006 20.34 3.75 1.0 3.3
020 - - 0.158 0.006 15.30 0.54
022 - - 0.142 0 21.02 5.35
025 0.36 0.02 0.178 0.047 2.0 0.4
028 0.68 0.17 0.326 0.168 2.1 1.0
031 0.14 0.02 0.169 0.045 20.76 4.78 0.8 0.4
038 0.35 0.09 0.152 0.021 28.74 3.88 2.3 4.3
041 0.44 0.04 0.134 0.014 24.35 1.85 3.3 2.9
044 0.88 0.06 0.192 0.064 4.6 0.9
Caribbean region
4-001 0.46 0.01 0.066 0.012 7.0 0.8
002 0.11 0.01 0.032 0.004 11.54 0.94 3.4 2.5
003 0.16 0.01 0.046 0.008 18.38 0.38 3.5 1.2
004 0.28 0.03 0.060 0.010 17.60 0.52 4.7 3.0
017 0.54 0.08 0.068 0.011 16.89 2.87 8.0 7.3
018 0.24 0.04 0.046 0.006 13.62 1.50 5.2 6.7
019 0.31 0.01 0.038 0.006 9.87 1.66 8.2 1.7
021 0.28 0.02 0.026 0.003 9.96 1.78 10.8 6.7
NANNO- AND NETPLANKTON PI3IMARY PRODUCTIVITY 637

This contrast is even more pronounced 4.0


if netplankton-nannoplankton (net : nanno)
productivity and chlorophyll ratios arc
considered (Fig, 2). The mean net : nanno
productivity ratio for the neritic environ-
ment was 0.50 * 0.14, significantly higher
than the oceanic mean of 0.10 2 0.03. A
similar pattern was observed for chloro- .
phyll a concentrations at the surface and PP .6 m
in the water column, except that the net-
plankton were relatively more important l 8- I
.4 P
in terms of plant biomass than in terms of
productivity in both environments (Fig. 2).
Within the oceanic environment, nanno-
.2 - .
P
plankton productivity and surface chloro- 0
phyll concentrations were relatively high
in the Peru Current region (mean = 2.70 -t-
1.22 mgC mm3 hr-l ), moderate in tropical

I.
surface water (mean = 0.67 -I- 0.28), and .3 -
low in the Caribbean (mean = 0.30 2 0.11).
Variations in the standing crop of nanno-
plankton followed the same pattern. Net-
plankton productivity (mean = 0.03 + 0.02)
.2 L
,
P
and chlorophyll content (mean = 0.008 -t-
0.002 mg m-” ) were especially low in the SC
Caribbean, but no significant difference
was observed in the mean net : nanno ra-
tios of productivity and chlorophyll
centrations in the three regions ( Fig. 2).
Variations in the relative standing crop
and productivity of the netplankton frac-
tion were not systematically
concurrent variations
con-

related to
in phytoplankton
.l -

0
1 d
productivity and standing crop as a whole
as seen by comparing neritic with Peru NET
Current waters, The levels of phytoplank-
ton productivity and standing crop were NAN
roughly equivalent in the two regions, but
net : nanno ratios were nearly an order of
magnitude lower in the region of the Peru
Current ( Fig. 2).

.3 -
FIG. 2. Regional mean values of nannoplank-
ton ( squares) and netplankton ( circles ) primary .2 -
productivity (PP = mgC m-’ hr-‘), chlorophyll n

P. P
concentration (SC = mgChl a m-‘), and netplank- .1 -
ton-nannoplankton (NET : NAN) productivity
( squares ) and chlorophyll a ( circles ) ratios with
95% confidence limits: neritic ( N), Peru Current 0
region ( I ) , tropical surface water ( II ) , and the
Caribbean region ( III ) .
I
638 TIIOMAS C. MALONE

TABLE 3. Frequency distribution of nannoplankton and netplankton productivity indices (PI = mgC
mgChl a-j hr-‘) including regional means and with 9570 confidence limits for neritic waters, the Peru
Current region (I), Tropical surface waters (II), and the Caribbean region (III)

Oceanic
PI Neritic I II III
Nanno
<3 1 0 7 0
3-s 1 0 3 3
>5 3 9 0 5
mean 8.23 r4 5.46 11.50 + 4.16 2.29 k 0.83 6.33 -L 2,.02
Net
<3 1 1 8 4
3-5 2 2 2 1
>5 2 6 0 3
mean 6.83 zk 4.49 5.30 4 1.22 1.50 -t- 1.02 3.73 * 2.10

Nannoplankton growth rates, as indi- may reflect rapid regeneration and re-
cated by the productivity index (PI = mg@ newal from terrestrial sources.
mgChl u-l hr-l) were higher than netplank-
ton growth rates with a frequency of 88%, CONCLUSIONS
but regional means for the two fractions In terms of productivity and standing
did not differ significantly except in Peru crop, nannoplankters were the most impor-
Current water where the nannoplankton tant primary producers in both neritic and
PI was double that of the netplankton oceanic environments. Mean netplankton
(Table 3). Nannoplankton PI values were productivity and net : nanno productivity
highest on the average in Peru Current and chlorophyll ratios were significantly
water, and for the netplankton they tended higher in neritic than in oceanic waters,
to be highest in neritic waters. These however. In addition, the relative impor-
values were generally greater than 5 in tance of the netplankton fraction was not
neritic waters and Peru Current and Ca- necessarily greater in regions of high phy-
ribbean regions and less than 3 in tropical toplankton productivity than in regions of
surface waters ( Table 3). The PI values low productivity. The implication that
average 2.3 -L 0.8 for the nannoplankton grazing pressure selects against larger phy-
and 1.5 -I 1.0 for the netplankton in tropi- toplankters is supported by the work of
cal surface waters with N03-N concentra- McAllister et al. (1959), Mullin (1963),
tions of 0. These values are significantly Richman and Rogers ( 1969), and Martin
less than the corresponding means ob- ( 1970). These patterns could reflect the
served in the remaining oceanic regions relatively high rates of netplankton growth
where measurable N03-N concentrations and low grazing pressure indices observed
were found with the exception of the mean in neritic as compared to oceanic waters.
netplankton PI in the Caribbean (Table
3). These data are consistent with the REFERENCES
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NANNO- AND NETPLANKTON PRIMARY PRODUCTIVITY 639

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