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

FIG. 1. Stations occwied in the tropical Pa-
cific and Caribbean segregated into four regions:
Circles-neritic (November 1968, August 1969,
January 1970); squaws-Peru Current (May
1970); triangles-tropical surface (December
1969 ) ; polygons-Caribbean ( May 1970 ) ,
from BT and STD casts. In addition, the
ratio of pheopigmcnts to chlorophyll in
the water column was calculated and as-
sumcd to provide a crude index of relative
grazing pressure on the phytoplankton
standing crop ( Lorenzen 1967).
RESULTS AND DISCUSSION
Measurements of netplankton and nan-
noplankton photosynthetic capacity and
standing crop were made at 44 stations in
the eastern tropical Pacific Ocean and
Caribbean Sea ( Fig. 1) during cruises of
the vessels mentioned in the introduction.
The stations were located between 10” S
and 30” N in surface water temperatures
of over 20C. Stations located within 100
km of land or in less than 600 m of water
are classified as neritic. The remaining sta-
tions are considered oceanic and are fur-
ther segregated into three groups based on
surface N03-N concentrations and mixed
layer depth (Table 1 and Fig. 1). Grazing
pressure indices were much higher in all
three oceanic zones than in the neritic
environments studied.
Values for netplankton and nannoplank-
ton primary productivity and chlorophyll
a concentration are presented in Table 2.
phyll a concentrations in neritic and Peru
Current waters ranged from l-5 mgC rno3
hr-1 and 0.15-0.70 mg m-3 respectively.
Much lower levels of phytoplankton pro-
ductivity were observed in the other two
oceanic regions where values rarely ex-
ceeded 1 mgC m-3 hr-l. However, surface
concentrations of chlorophyll a were higher
by nearly an order of magnitude in trop-
ical surface water than in the Caribbean
region.
Surface productivity and chlorophyll a
concentrations of the nannoplankton frac-
tion exceeded that of the netplankton at
all stations in both neritic and oceanic
waters ( Table 2). Neritic nannoplankton
productivity averaged 1.54 + 0.46 mgC
m-3 hr-l and varied from 0.60-2.96 (Fig. 2).
Oceanic nannoplankton productivity var-
ied over a much wider range with a low
of 0.11 and a high of 6.48. The average
productivity of oceanic nannoplankton
was 1.16 2 0.50 which does not differ sig-
nificantly (P = 0.05) from that observed
in neritic waters. Netplankton productiv-
ity varied from 0.32-1.98 in neritic waters
in contrast with 0.0 to 0.43 for oceanic
waters. Mean neritic netplankton produc-
tivity was significantly higher at 0.74 A
0.31 than the mean value of oceanic net-
plankton productivity of 0.10 * 0.04. Thus,
the high level of productivity observed in
neritic waters was due primarily to higher
levels of netplankton productivity, al-
though mean nannoplankton productivity
values were significantly higher than the
corresponding netplankton values in both
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
findings of McAllister et al. (1964) and ANDERSON, G. C. 1965. Fractionation of phyto-
Curl and Small ( 1965) which suggest that plankton communities off the Washington
productivity indices below 3 are indica- and Oregon Coasts. Limnol. Oceanogr. 10 :
tive of a nutrient deficiency while those 477480.
CURL, H., AND L. F. SMALL. 1965. Variations in
above 5 indicate nutrient-rich waters. The photosynthetic assimilation ratios in natural
high productivity indices in neritic water, marine phytoplankton communities. Lim-
despite negligible N03-N concentrations, nol. Oceanogr. lO( Suppl. >: R67-R73.
 NANNO- AND NETPLANKTON
DIGBY, P. S. B. 1953. Plankton production in
Scoresby Sound, East Greenland. J. Anim.
Ecol. 22: 289-322.
DOTY, M. S., AND M. OGURI. 1958. Selcctcd
features of the isotopic carbon primary pro-
ductivity technique. Rapp. Proc. Verb.,
Cons. Int. Explor. Mer 144: 47-55.
GILMARTIN, M . 1964. The primary production
of a British Columbia fjord. J. Fish. Res.
Bd. Can. 21: 505-538.
HOLMES, R. W. 1958. Size fractionation of pho-
tosynthetic phytoplankton. Spec. Sci. Rep.
Fish. 279, p. 69~71.
HOIX-HANSEN, O., C. J. LORENZEN, R. W.
HONES, AND J. D. H. STRICKLAND. 1965.
Fluorometric determination of chlorophyll.
J. Cons., Cons. Penn. Int. Explor. Mer 30:
3-15.
LORENZEN, C. J. 1967. Vertical distribution of
chlorophyll and phaeopigments: Baja Cali-
fornia. Deep-Sea Rcs. 14: 735-745.
MCALLISTER, C, D., T. R. PARSONS, AND J. D. H.
STIUCKLAND. 1959. Primary productivity at
station “P” in the north-east Pacific Ocean.
J. Cons., Cons. Perm. Int. Explor. Mer 25:
240-259.
- N. SHAH, AND J, D. I-1. STRICKLAND.
l&4. Marine phytoplankton photosynthesis
as a function of light intensity. J. Fish. Res.
Bd. Can. 21: 159~181.
MARTIN, J. II. 1970. Phytoplankton-zooplank-
ton relationships in Narragansett Bay, 4.
Limnol. Oceanogr. 15: 413418.
MULLIN, M. M. 1963. Some factors affecting
the feeding of marine copepods of the genus
Ca.?unus. Limnol. Oceanogr. 8: 239-250.
MUNK, W. H., AND G. A. RILEY. 1952. Abso,rp-
tion of nutrients by aquatic plants. J. Mar.
Rcs. 11: 215-240.
ODUM, H. T. 1956. Efficiencies, size of orga-
nisms, and community structure. Ecology
37 : 592-597.
RICIXXUN, S., AND J. N. ROGERS. 1969, The
feeding of Calanus helgolandicus on syn-
chronously growing populations of the ma-
rine diatom Ditylum brightwellii. Limnol.
Oceanogr. 14: 701-709.
RYTHXR, J. I-1. 1969. Pho tosynthcsis and fish
production in the sea. Science 166: 72-76.
PRIMARY PRODUCTIVITY 639
SAIJO, Y., AND K. TAKESUE. 1965. Further stud-
ies on the size distribution of photosynthesiz-
ing phytoplankton in the Indian Ocean. J.
Oceanogr. Sot. Jap. 20: 264-271.
STEEMANN NIELSEN, E., AND E. A. JENSEN. 1957.
Primary oceanic production. The autotrophic
production of organic matter in the ocean.
Galathca Rep. 1: 49-136.
STEPHENS, K. 1970. Automated measurement
of dissolved nutrients. Deep-Sea Res. 17:
393-386.
STRICKIXND, J, D. H. 1961. Significance of
the values obtained by primary productivity
measurements, p, 172-183. In M. S. Doty
[ed.], Primary productivity measurement, ma-
rine and freshwater. USAEC TID-7633.
-, AND T. R. PARSONS. 1968. A practical
handbook of seawater analysis. Bull. Fish.
Res. Bd. Can. 167. 3811 p.
SUDRAEXMANYAN, R., AND A. 1-I. V. SARMA. 1965.
Studies on the phytoplankton of the west
coast of India. Part 4. J. Mar. Biol. Ass.
India 7: 406-4191.
TEIXEIRA, C. 1963. Relative rates of photo-
synthesis and standing stock of net phyto-
plankton and nannoplankton. Bol. Inst.
Oceanogr. Sao Paula 13: 53-60.
THORSON, G. 1950. Reproductive and larval
ecology of m<arine bottom invertebrates.
Biol. Rev. Cambridge Phil. Sot. 25: 145.
WILLIAMS, R. B. 1964. Division rates of salt
marsh diatoms in relation to salinity and cell
size. Ecology 45: 877-880.
WOOD, E. J. F. 1963. The relative importance
of groups of protozoa and algae in marine
environments of the southwest Pacific and
East Indian Ocean, p. 236-240. In C. I-1.
Oppenheimer I:cd.], Symposium on marine
microbiology, Thomas.
YENTSCH, C. S., AND D. W. MENZEL. 1963. A
method for the determination of phytoplank-
ton, chlorophyll and phaeophytin by fluones-
cence. Deep-Sea Res. 10: 221-231.
-> AND J, II. RYTHER. 1959. Relative sig-
nificance of the net phytoplankton and nan-
noplankton in the waters of Vineyard Sound.
J. Cons., Cons. Perm. Int. Explor. Mer 24:
231-238.