THE RELATIVE IMPORTANCE OF NANNOPLANKTON AND

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 environments studied, but netplankton productivity was significantly (P = 0.05) higher in neritic
than in oceanic waters. Mean neritic netplankton-nannoplankton
productivity and chlorophyll 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
The phytoplankton
can be divided into
two groups based on whether they escape
or are retained by fine-mesh nets. The
fraction retained by the phytoplankton
nets (aperture size 20-90 p) is commonly
called “netplankton”
or “microplankton”
and the fraction that escapes is referred
to as “nannoplankton.”
The ecological significance of these two categories lies in
the role of cell size in phytoplankton
community dynamics. Typically small cells
have shorter generation times and higher
growth rates in a given environment than
do larger cells, presumably owing to the
high surface area-to-volume
ratios of
smaller cells (e.g., Odum 1956; Saijo and
Takesue 1965; Williams 1964). In addil This research was supported in part by the
Organization for Tropical Studies Pilot Study
Grant No. 69-4 and The Society of the Sigma
Xi, in part by National Science Foundation Grants
GB 6870, GB 6871, and GB 8374, and in part by
National Institutes of Health Predoctoral Fellowship 5 FOl GM44363-02. Based on a thesis submittcd in partial fulfillment of the requirements
for a Ph.D. degree at Stanford University, Palo
Alto, California.
2 Present address: Department of Biology, The
City College of CUNY, Convent Ave. and 138th
St., New York, N.Y. 10031.
LIMNOLOGY
AND OCEANOGRAPHY
tion, the relative levels of nannoplankton
and netplankton
productivity
and standing crop should be reflected in the distributions and abundances of herbivores that
selectively graze one group or the other
(e.g., Thorson 1950; Strickland 1961; Mullin 1963) .
Geographic
variations
in netplankton
and nannoplankton
primary productivity
and standing crop are poorly documented
in the marine environment.
Recent investigations in both temperate (Yentsch and
Ryther 1959; Gilmartin
1964; Anderson
1965) and tropical
waters
( Steemann
Nielsen and Jensen 1957; Holmes 1958;
Teixcira
1963) have demonstrated
that
nannoplankton
are often responsible for
SO-99% of the observed phytoplankton
productivity.
Little information
is available on regions in which netplankton primary productivity
surpasses that of the
nannoplankton,
although
phytoplankton
communities dominated by netplankton in
terms of cell number ( Digby 1953) and
chlorophyll
concentration
( Subrahmanyan
and Sarma 1965) have been reported. It
seems surprising, therefore, that it has become almost axiomatic that netplanktcrs
tend to be the predominant primary producers in neritic waters and high latitudes
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 variations in netplankton
and nannoplankton
primary productivity
and standing crop
and relates these variations to spatial patterns 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 Administration
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 photosynthetic capacities and chlorophyll a concentrations 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 fluorescent 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 sample 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 directly 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% between phytoplankton
productivity
values
calculated from the sum of the nannoplankton and netplankton
fractions and
determined
directly from unfractionated
samples.
ChlorophyII a and pheopigment concentrations were determined by a fluorometric technique (Yentsch and Menzel 1963;
Holm-Hansen et al. 1965). Water samples
were fractionated by the same procedure
described for the carbon-uptake measurements, except Whatman GF/C glass-fiber
filters coated with 2 ml of a I%, suspension 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. Whenever 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 between Whatman GF/C glass filters and
AA Millipore filters coated with MgCOs.
Also, a preliminary analysis of chlorophyll
a concentrations estimated by the trichromatic method using glass-fiber and Sartorius 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 concentrations of 0.06-0.56 mg rnd3 (for tropical
oceanic phytoplankton ) .
Surface NOs-N concentrations and mixed
layer depths were determined in conjunction with productivity
and pigment measurements,
The N03-N was measured
using an AutoAnalyzer on the RV Thomas
G. Thompson (Stephens 1970); otherwise
the manual procedure described by Strickland and Parsons ( 1968) was used. The
depth of the mixed layer was determined
NANNO-
AND NETPLANKTON
PRIMARY
635
PRODUCI’IVITY
TABLE 1. Mean NOs-N concentrations
(pg-atom/
liter), water column pheopigment-chlorophyll
ratios (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
NOrN
P:C
z YL
FIG. 1. Stations occwied in the tropical Pacific and Caribbean segregated into four regions:
Circles-neritic
(November 1968, August 1969,
January 1970); squaws-Peru
Current (May
surface (December
1970); triangles-tropical
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 assumcd to provide a crude index of relative
grazing pressure on the phytoplankton
standing crop ( Lorenzen 1967).
RESULTS AND DISCUSSION
Measurements of netplankton and nannoplankton
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 stations are considered oceanic and are further 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 nannoplankton primary productivity
and chlorophyll
a concentration are presented in Table 2.
0
0.2 10.1
12 -t- 6
I
II
III
0.2 k 0.1
5.3 & 3.3
0
1.0 +- 0.3 1.2 -c 0.1 1.1 -r- 0.1
24 k 7
84 zk 31
32 zk 8
Phytoplankton
productivity
and chlorophyll 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
productivity were observed in the other two
oceanic regions where values rarely exceeded 1 mgC m-3 hr-l. However, surface
concentrations of chlorophyll a were higher
by nearly an order of magnitude in tropical surface water than in the Caribbean
region.
Surface productivity
and chlorophyll
a
concentrations of the nannoplankton fraction 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
varied over a much wider range with a low
of 0.11 and a high of 6.48. The average
of oceanic nannoplankton
productivity
was 1.16 2 0.50 which does not differ significantly
(P = 0.05) from that observed
in neritic waters. Netplankton productivity varied from 0.32-1.98 in neritic waters
in contrast with 0.0 to 0.43 for oceanic
waters. Mean neritic netplankton productivity was significantly
higher at 0.74 A
0.31 than the mean value of oceanic netplankton 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,
although mean nannoplankton
productivity
values were significantly
higher than the
corresponding netplankton values in both
oceanic and neritic environments.
636
THOMAS
TABLE 2. Nannoplankton
and netplankton
(SC = mgChl a m-‘, m-‘), and productivity
PP
C. MALONE
primary productivity
(PI’ = mgC m-” hrl),
standing crop
indices (PI = mgC mgChl a-’ hr-‘) for the four regions
studied
SC (m”)
SC (m2)
PI
Station
Nanno
Net
Nanno
Net
Nanno
Net
Nanno
Net
l-001
005
006
007
008
010
2-001
002
003
004
3-033
2.96
1.51
2.17
0.60
1.56
1.48
0.98
2.00
0.82
2.04
0.82
1.12
0.40
1.98
0.37
0.48
0.54
0.76
1.04
0.32
0.57
0.58
0.198
0.143
0.114
0.301
0.385
0.160
0.090
0.050
0.124
0.319
5.0
13.15
11.89
14.42
17.85
9.41
5.27
17.92
15.69
14.0
7.2
6.8
2.1
4.8
11.6
6.4
4.6
1.8
4-006
007
008
010
011
012
013
015
016
3.79
2.28
2.14
1.18
1.26
1.24
3.15
2.76
6.48
0.05
0.26
0.32
0.10
0.10
0.14
0.06
0.12
0.43
0.272
0.254
0.241
0.198
0.212
0.158
0.222
0.202
0.269
34.45
24.10
11.62
17.46
17.00
10.75
12.02
14.32
22.23
3.10
1.70
0.69
1.76
1.00
1.63
1.21
0.58
2.69
13.9
9.0
8.9
l-002
003
004
009
3-001
005
009
013
020
022
025
028
031
038
041
044
1.28
1.12
1.82
0.97
0.71
0.22
0.24
0.12
0.36
0.68
0.14
0.35
0.44
0.88
0.27
0.20
0.42
0.01
0.05
0
0
0.02
0.02
0.17
0.02
0.09
0.04
0.06
Peru Current
Tropical
0.192
0.180
0.126
0.116
0.158
0.142
0.178
0.326
0.169
0.152
0.134
0.192
surface
0.46
0.11
0.16
0.28
0.54
0.24
0.31
0.28
0.01
0.01
0.01
0.03
0.08
0.04
0.01
0.02
0.066
0.032
0.046
0.060
0.068
0.046
0.038
0.026
0.012
0.004
0.008
0.010
0.011
0.006
0.006
0.003
E
718
14.2
13.7
24.1
ifi
5:3
5.0
4.2
6.1
6.0
7.1
7.1
3.7
1.2
1.9
1.0
1.8
0
0
3.3
2.0
2.1
0.8
2.3
3.3
4.6
0.4
1.0
0.4
4.3
2.9
0.9
7.0
3.4
3.5
4.7
8.0
5.2
8.2
10.8
0.8
2.5
1.2
3.0
7.3
6.7
1.7
6.7
water
0.030
0.014
0.052
0.006
0.006
0
0.047
0.168
0.045
0.021
0.014
0.064
Caribbean
4-001
002
003
004
017
018
019
021
region
0.032
0.048
0.060
0.020
0.024
0.023
0.010
0.017
0.061
20.05
22.52
13.40
20.34
15.30
21.02
2.24
3.30
1.07
3.75
0.54
5.35
20.76
28.74
24.35
4.78
3.88
1.85
11.54
18.38
17.60
16.89
13.62
9.87
9.96
0.94
0.38
0.52
2.87
1.50
1.66
1.78
region
NANNO-
AND NETPLANKTON
This contrast is even more pronounced
if netplankton-nannoplankton
(net : nanno)
productivity
and chlorophyll
ratios arc
considered (Fig, 2). The mean net : nanno
productivity
ratio for the neritic environment was 0.50 * 0.14, significantly
higher
than the oceanic mean of 0.10 2 0.03. A
similar pattern was observed for chlorophyll a concentrations at the surface and
in the water column, except that the netplankton were relatively more important
in terms of plant biomass than in terms of
productivity
in both environments (Fig. 2).
Within the oceanic environment, nannoplankton productivity
and surface chlorophyll concentrations were relatively high
in the Peru Current region (mean = 2.70 -t1.22 mgC mm3 hr-l ), moderate in tropical
surface water (mean = 0.67 -I- 0.28), and
low in the Caribbean (mean = 0.30 2 0.11).
Variations in the standing crop of nannoplankton followed the same pattern. Netplankton productivity
(mean = 0.03 + 0.02)
and chlorophyll
content (mean = 0.008 -t0.002 mg m-” ) were especially low in the
Caribbean, but no significant
difference
was observed in the mean net : nanno ratios of productivity
and chlorophyll
concentrations in the three regions ( Fig. 2).
Variations in the relative standing crop
and productivity
of the netplankton fraction were not systematically
related to
concurrent
variations
in phytoplankton
productivity
and standing crop as a whole
as seen by comparing neritic with Peru
Current waters, The levels of phytoplankton productivity
and standing crop were
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).
PI3IMARY
637
PRODUCTIVITY
4.0
PP
.
.6 m
l 8- I
.4
P
.
P
.2 0
.3 -
.2 L
SC
.l -
0
I.
1
,
P
d
NET
NAN
.3 FIG. 2.
Regional mean values of nannoplankton ( squares) and netplankton ( circles ) primary
productivity (PP = mgC m-’ hr-‘), chlorophyll n
concentration (SC = mgChl a m-‘), and netplankton-nannoplankton
(NET : NAN)
productivity
( squares ) and chlorophyll a ( circles ) ratios with
95% confidence limits: neritic ( N), Peru Current
region ( I ) , tropical surface water ( II ) , and the
Caribbean region ( III ) .
.2 .1 0
P. P
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
1
0
0
II
III
Nanno
<3
3-s
>5
mean
1
3
8.23 r4 5.46
9
11.50 + 4.16
1
2
2
6.83 zk 4.49
1
2
6
5.30 4 1.22
7
3
0
2.29 k 0.83
0
3
5
6.33 -L 2,.02
8
2
0
1.50 -t- 1.02
4
1
3
3.73 * 2.10
Net
<3
3-5
>5
mean
Nannoplankton
growth rates, as indicated by the productivity index (PI = mg@
mgChl u-l hr-l) were higher than netplankton growth rates with a frequency of 88%,
but regional means for the two fractions
did not differ significantly
except in Peru
Current water where the nannoplankton
PI was double that of the netplankton
(Table 3). Nannoplankton PI values were
highest on the average in Peru Current
water, and for the netplankton they tended
to be highest in neritic waters. These
values were generally greater than 5 in
neritic waters and Peru Current and Caribbean regions and less than 3 in tropical
surface waters ( Table 3). The PI values
average 2.3 -L 0.8 for the nannoplankton
and 1.5 -I 1.0 for the netplankton in tropical surface waters with N03-N concentrations of 0. These values are significantly
less than the corresponding
means observed in the remaining oceanic regions
where measurable N03-N concentrations
were found with the exception of the mean
netplankton PI in the Caribbean (Table
3). These data are consistent with the
findings of McAllister
et al. (1964) and
Curl and Small ( 1965) which suggest that
productivity
indices below 3 are indicative of a nutrient deficiency while those
above 5 indicate nutrient-rich
waters. The
high productivity
indices in neritic water,
despite negligible
N03-N concentrations,
may reflect rapid regeneration
newal from terrestrial sources.
and re-
CONCLUSIONS
In terms of productivity
and standing
crop, nannoplankters were the most important primary producers in both neritic and
oceanic environments.
Mean netplankton
productivity
and net : nanno productivity
and chlorophyll
ratios were significantly
higher in neritic than in oceanic waters,
however. In addition, the relative importance of the netplankton fraction was not
necessarily greater in regions of high phytoplankton productivity
than in regions of
The implication
that
low productivity.
grazing pressure selects against larger phytoplankters is supported by the work of
McAllister
et al. (1959), Mullin
(1963),
Richman and Rogers ( 1969), and Martin
( 1970). These patterns could reflect the
relatively high rates of netplankton growth
and low grazing pressure indices observed
in neritic as compared to oceanic waters.
REFERENCES
ANDERSON, G. C.
1965. Fractionation of phytoplankton communities off the Washington
and Oregon Coasts. Limnol. Oceanogr. 10 :
477480.
L. F. SMALL. 1965. Variations in
photosynthetic assimilation ratios in natural
marine phytoplankton
communities.
Limnol. Oceanogr. lO( Suppl. >: R67-R73.
CURL, H., AND
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 proRapp. Proc. Verb.,
ductivity
technique.
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 photosynthetic 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 California. 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-zooplankton 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,rption of nutrients by aquatic plants. J. Mar.
Rcs. 11: 215-240.
ODUM, H. T. 1956. Efficiencies, size of organisms, 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 mabrightwellii.
rine diatom Ditylum
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 studies on the size distribution of photosynthesizing 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, marine 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 photosynthesis and standing stock of net phytoBol. Inst.
plankton and nannoplankton.
Oceanogr. Sao Paula 13: 53-60.
Reproductive and larval
THORSON, G.
1950.
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 phytoplankton, chlorophyll and phaeophytin by fluonescence. Deep-Sea Res. 10: 221-231.
AND J, II. RYTHER. 1959. Relative sig->
nificance of the net phytoplankton and nannoplankton in the waters of Vineyard Sound.
J. Cons., Cons. Perm. Int. Explor. Mer 24:
231-238.