Journal of Plankton Research Vol.19 no.3 pp.343-356, 1997
Implications of zooplankton stoichiometry on distribution of N
and P among planktonic size fractions
Ingrid Gismervik
University of Oslo, Department of Biology, Section of Marine Chemistry and
Marine Zoology, PO Box 1064, BUndent, N-0316 Oslo, Norway
Abstract Pooled samples from the upper 20 m at five stations in the Oslofjord (Norway) were size
fractionated and analysed for paniculate dry weight, carbon, nitrogen and phosphorus. The nano fraction (0.7-20 urn) dominated in biomass throughout the sampling period. The C:N ratios of the fractions did not differ much from each other. The C:P ratios of the nano- and microfraction (20-200 |jm)
were considerably higher than the ratio of the mesofraction (200-2000 um) throughout the sampling
period. High OP ratios and low phosphate concentrations above the pycnocline suggest that the
system was P-limited. The stoichiometry of mesozooplankton was more constant than the stoichiometry of the other fractions, and the zooplankton constituted consistently a higher percentage of the
phosphorus pool than of the carbon pool. This suggests that the mesozooplankton can act as a sink of
nutrients due to its invariable stoichiometry.
Introduction
Zooplankton influences the algal population by grazing and subsequent sequestration and regeneration of nutrients (Ketchum, 1962; Corner and Davis, 1971;
Bamstedt, 1985; Elser and George, 1993). Regeneration of nutrients depends
both on the stoichiometry of the zooplankton and of its food. Stoichiometry of
zooplankton fractions differs both from phytoplankton fractions and from the
customary accepted N:P ratio of 16:1 (Harris and Riley, 1956; Beers, 1966; Le
Borgne, 1982). An average N:P ratio of 25:1 was suggested by Corner and Davis
(1971) for mixed zooplankton fractions dominated by copepods, and a ratio of
16:1 for mixed phytoplankton. Further studies indicate that phytoplankton
stoichiometry varies in concert with growth rate (Goldman et al, 1979; Droop,
1983) and may deviate substantially from the Redfield (1958) ratio of 106:16:1
during nutrient limitation (Harrison et al., 1977; Jahnke et al, 1986; Ki0rboe,
1989). Studies of zooplankton however, indicate fairly constant elemental ratios,
even during starvation (Andersen and Hessen, 1991). The apparent low variability of zooplankton stoichiometry compared to phytoplankton thus suggests that
regeneration varies in concert with the nutritional status of the phytoplankton,
and that the role of zooplankton as sequesters of nutrients may be enhanced
during nutrient limitation.
Effects on zooplankton excretion products due to differences in stoichiometry
between grazers and prey have been documented in the laboratory (Butler et al,
1969; Morales, 1987), but less attention has been paid to such effects in the field.
Nixon (1981) suggested that a large flux of animal tissue out of the marine coastal
zone would result in a low residual N:P ratio in the water due to the discrepancy
between N:P ratio in the animals' food and their synthesizing tissue. He, however,
claims that since the secondary production is only a small fraction of the primary
production, this accumulation of nutrients in animal tissue is of minor importance.
© Oxford University Press
343
LGismervik
On the contrary, studies in freshwater have suggested that zooplankton may act
as a sink of nutrients (Elser and George, 1993). Different zooplankton taxa have
been shown to require specific elemental combinations, e.g. freshwater daphnids
have higher phosphorus demand than freshwater copepods (Hessen and Andersen, 1992). Consequently many shifts in the zooplankton community accompany
transition between N- and P-limited algal growth in some freshwater lakes (Elser
et al, 1988; Sterner et al, 1992).
In this paper I assess the role of zooplankton as accumulators of nutrients in a
brackish-marine system by evaluating stoichiometry of the different plankton
compartments.
Study area
The Oslofjord is the harbour and the recipient of several major cities, and has been
severely influenced by sewage discharge during the last century. This has caused
huge phytoplankton blooms and poor oxygen conditions in the deep basins
(Paasche and 0stergren, 1980). Over the past two decades the external nitrogen
load has increased continuously, while the phosphorus load has been dramatically
reduced due to sewage-cleaning efforts (Magnusson and Johnsen, 1994). The
sewage discharge sites and the sampling stations are shown in Figure 1. The inner
fjord is 150 m deep, and there is a narrow sound with a shallow sill (maximum
19 m) which connects the inner and the outer Oslofjord. Sampling stations were
chosen to cover the inner Oslofjord from the innermost part of the fjord (EP) to
outside the shallow sill of the fjord (IM), and previously used stations were
chosen. Sampling depth was chosen to cover the upper 20 m, to ensure that the
euphotic zone (as defined by 1% light depth) was sampled throughout the year.
The stations had maximum depth of more than 100 m except for station BP, which
was -50 m deep.
Method
Five stations were sampled monthly at daytime from June 1993 till May 1994, in
order to assess the stoichiometry of the plankton at different seasons. Some
stations were not sampled during winter due to ice (Table I). Temperature and
salinity were recorded by CTD. Light transmission was measured by a scalar
irradiance meter (Biospherical QLS-100).Water samples were taken every second
metre from 20 to 0 m with Niskin water bottles (1.7 1), mixed, and then filtered
through 200 um mesh sieve. Chlorophyll (chl a), particulate carbon, nitrogen and
phosphorus samples, as well as a sample for ciliate enumeration (fixed in 1% v/v
acid Lugol's iodine) were taken from this pooled sample. The rest of the pooled
sample was subsequently concentrated in a 20 um net, and also analysed for
carbon, nitrogen and phosphorus mass. At one central station (DK), depth-stratified samples for nutrient analysis and chlorophyll were taken at 1,5,10 and 20 m
from August 1993.
Sea water for nutrient analysis was filtered through acid washed GF/F filters
(to remove particulate nitrogen and phosphorus) and frozen for analysis of
344
Stoichiometry among planktonk size fractions
Fig. L Map of Oslofjord with stations. Encircled station chosen as representative for the fjord. Arrows
indicate the two major sewage treatment plants.
ammonia (Reusch-Berg and Abdullah, 1977), nitrate (Brewer and Riley, 1965)
and phosphate (modified after Murphy and Riley, 1958) on an Autoanalyser.
Chi a was filtered and frozen on GF/F filters. The samples were subsequently
extracted in 10 ml 90% acetone for ~1 h, and then measured fluorometrically
before and after acidification on a Turner design fluorometer. Samples for
carbon, nitrogen and phosphate analysis were filtered on acid washed and precombusted GF/F filters. C:N analysis was performed on a Carlo Erba elemental
analyser, while P was analysed after persulphate (10 g H) digestion (1 h, at 120°C)
on an Autoanalyser.
345
LGismervik
Microplankton (20-200 um) from 16.7 1 was concentrated in a net (20 um mesh
size), and fixed in 4% buffered formaldehyde. During concentration of microplankton in the 20 um net, fragile ciliates other than tintinnids were expected to
be lost. Ciliate enumeration was therefore performed on separate samples after
50 ml sedimentations in Utermohl chamber for 24 h, and counted at 250X magnification. Cells were measured at 400 X magnification, and volume estimated from
simple geometrical shapes and converted to carbon by a factor of 0.19 pg C unr 3
(Putt and Stoecker, 1989).
Mesoplankton was sampled with a vertical towed WP2-net (180 um mesh) from
20 m to the surface, screened through a 2000 um mesh sieve to remove larger
plankton which were occasionally present, and split in a Folsom splitter. One half
was frozen for biochemical analysis (carbon, nitrogen and phosphorus, treated
like above) and one half was preserved in 4% buffered formaldehyde for species
identification. The latter sample (mesoplankton) was concentrated and washed in
a 200 urn sieve prior to counting. Species identification was only done for central
station: DK.
The nanoplankton (0.7 and 20 um) was calculated as the difference between total
paniculate matter from 0.7 to 200 urn and microplankton (20-200 urn), though this
term is customarily used for the 2-20 urn fraction (e.g. Sieburth et aL, 1978). The
purpose of the fractionation was to separate mesozooplankton and its prey. While
the largest size fraction (200-2000 um) consists of heterotrophs, the two smaller
fractions commonly includes both auto- and heterotrophs as well as detritus.
Results
The 20 m sampling depth covered the photic zone and the pycnocline with few
exceptions (Table I). Generally the salinity ranged between 20 and 32%o in the
upper 20 m (not shown). Vertical profiles at station DK revealed low values of
phosphate above the pycnocline during autumn and spring (Figure 2).
Table I. Hydrography and 1 % light depth for all stations through the period of sampling
Pycnocline, m
EP
16 June 93
14 July 93
12 August 93
20 September 93
21 October 93
14 December 93
02 February 94
24 March 94
13 April 94
25 May 94
BP
8(0.3)
7 (3.8)
13(1.3)
3 (0.7)
15 (1.4) 15 (1.9)
3 (0.8) 1 (0.4)
14(2.6)
5 (1.7)
ice
ice
ice
ice
ice
2 (0.7)
13 (1.2)
12 (0.4)
4 (0.9)
9(1.9)
1% light deptlI
DK
FI
6(2.5)
6 (0.8)
11 (1-9)
8 (0.8)
12 (0.7)
10 (0.8)
13 (0.3)
14 (0.7)
17 (0.6)
8(1.1)
4(2.1)
10 (0.8)
15(12)
17 (0.5)
15 (1.4)
6(9.4)
nd
10 (0.3)
18 (0.4) 21 (13)
13 (0.5) 3(1.7)
10(1.4) 10(1.3)
6 (2.3)
9(1.9)
14(1.1)
6 (0.8)
8 (0.7)
11 (0.7)
IM
EP BP DK FI
IM
15
nd
13
16
7
16
nd
16
16
28
nd
11*
10
20
7
16
nd
10
16
6
16
nd
16
22
7
ice ice nd
ice ice 10*
ice
3
6
10 10 14
12 12 12
16
nd
14
18
23
nd
nd
9
16
10
* Measured by Secchi disk, ice, no sampling due to ice. nd, no data.
Pycnocline calculated as the depth with maximum density change across 1 m depth in the upper 20 m.
Density change given in parentheses.
346
Stoichiometiy among planktonk size fractions
UMNO 3 , uMNH4 , ^M PO 4 «10, \ig Chl a \10
5
10
15
20
0
5
I
1
1
1
1
i at
5 -<
xf
o.
1
1
10 -t
15
1
20
1
2'.
ifl
a
\
y "
15 -
1
1
1
1
>
V
•a
p
\ ^
Aug.
6V
E
1
,0
,CT
/^
r \
20 - /
Chi o
N
N
/
^
\
D
O
PO 4 NH 4
\
""«
\
b ^
NO3
???
\
/
Oct.
\
5-
Apr.
\
;
i
'
10-
«...
\
\
\
1520q
,
9
6 b
' • ' • • • •
*
Dec. '
B?
\
/1:
5-
i
10-
•
\
'
•
"
^
•
May
y'
*._
\
/
20i 0
[
t>
15-
\
" ' • • - .
bta
'
\
\
\\
\
\
\
>
\
\
' • - . .
\
\
,
D
1
1993
0
\
\
':
t]
1994
Kg. 2. Dissolved nutrients, chlorophyll a and density (<r) were sampled at some dates at station DK
Concentration of phosphorus multiplied by 10 to fit in scale. Horizontal line illustrates 1% light depth.
The carbon pool was dominated by particles < 20 urn during all seasons (Figure
3). Some larger ciliates will be included in this fraction, as they escape the concentration of the microplankton in the 20 um net (see Method) and the calculation of
the nanoplankton is based on the difference between 0.7 and 200 um material and
microplankton. However their contribution was minor throughout the year (Table
II). High numbers of a small oligotrich (Corliss, 1979) and a small scuticociliate
(Corliss, 1979) were found in August (Table II), but the carbon mass remained low.
Except for a considerable increase during the spring bloom, the seasonal differences of nanoplankton were low, with only slightly reduced biomasses during
347
LGismervik
Nanofraction
B) Microfraction
JA
SO
D F M A M
month (1993-94)
Fig. 3. Biomasses (g C m"2) of the (A) nanofraction, (B) microfraction and (C) mesofraction in the
upper 20 m. Open diamonds, EP; filled diamonds, BP; Qlled squares; DK; open circles, IM and filled
circles, FI. Line is mean value of all stations.
winter. The same pattern, with somewhat higher variation, was found for
microplankton, while there were considerably lower mesoplankton biomasses in
winter and early spring compared to the rest of the year.
The Chi a concentrations were low or moderate throughout the year, except for
a strong diatom spring bloom in March (Table II). The rest of the year, various
dinoflagellates dominated the microplankton numerically (Table II). The carbon
to Chi a ratios at station DK were high (218-2786 ng C/Chl a in the 0.7-200 urn
fraction) throughout the year except during the spring bloom in March, when the
ratio was 61.
The C:N ratio of the nanofraction declined from 11.5 (mean value) in June 1993
to 4.5 in October, and remained low during winter and spring (Figure 4A). The
348
Stoichiometry among pbnktonlc size fractions
Table IL Chlorophyll a and species composition in pooled samples from 0-20 m at station DK
J
J
A
S
D
O
F
M
A
M
Chi a (mg nr 2 )
CUiate biomass
(mg C nr 2 )
Aloricate, ^20 ujn
Aloricate, >20 urn
Tintinnids
CUiate abundance
(X 10 6 m- 2 )
Aloricate, ^20 |jun
Aloricate, >20 (jjn
Tintinnids
Microplankton
(X 1O1 m-2)
Diatoms
Silicoflagellates
Dinoflagellates
Aloricate ciliates
Tintinnids
Empty tintinnid
lonca
Eggs
Crustacean nauplii
Copepodites
Faecal pellets
Merozooplankton
Mesoplankton
(X l C n r 2 )
Calanoid copepods
Cyclopoid copepods
Harpacticoid
copepods
Oadocerans
Larvaceans
Merozooplankton
Euphausiacea nauplii
Coscinodtscui spp.
30
38
43
19
7
8
2
316
9
13
7
5
10
nd
nd
nd
29
40
8
6
35
<1
4
6
5
6
2
1
12
15
261
1
2
169
57
32
13
4
24
4
16
nd
nd
nd
135
39
12
24
28
2
10
6
10
5
1
7
11
33
18
1
4
25
12
76
10
2
135
2009
4
1.7X10
81
74
205
665
46 40
2.8X1O4
6800
4.6X10* 3.2X104 7228 8687 126
1.8X104
1
60
60
285
4552
53
61
535
1917
1023
339
34
665
317
1209
438
212
15
376
975
188
103
137
109
266
73
111
545
74
12
25
151
116
165
29
131
30
142
7
58
12
3
45
1
6
1
6
7
8
53
4
81
<1
4
1
2
1
2
1
1
2 4X107
563
54
72
274
3637 1193
15
1769
7
156 107
13
14
3
2
<1 <1
<1
1
1
2
96
84
19
7
29
2142
50
349
174
101
374
29
230
86
18
1
48
1
258
10
<1
4
3
1
502
70
13
11
19
1
3
Peak biomasses of aloricate ciliates in spring due to large Strombidium species, while peak abundance of smaller
ciliates were found in August The microfraction was dominated numerically by large algae; peak abundance of
diatoms in spring and dinoflagellatej in summer and autumn. High numbers of a silicoflagellate (Disiephanus
speculum) in September. Also occasionally high numbers of crustacean developmental stages. The mesoplankton was
dominated by copepods, mainly calanoids, except in March when large diatoms (Cosanodiscus spp.) were present.
Micro- and mesoplankton groups with less than 1 ind I"' were not included, while dates where no specimens were
recorded in the examined sample were left as open space.
microfraction generally had ratios between 8.5 and 10 (except in December) (Figure
4B), while the mesoplankton had mean ratios between 5.5 and 8.8 (Figure 4C).
There was a striking difference between the C:P ratio of the mesofraction and
the other two fractions (Figure 5).While the mesofraction displayed fairly constant ratios (218 ± 61, mean ± SD for all stations and all sampling dates), the
nanofraction and the microfraction displayed high ratios and high variability
during the study (466 ± 202 and 940 ± 478, respectively). A similar pattern was
349
I.Gismervik
A) Nanofraction
C:N
B) Microfraction
C:N
C) Mesofraction
C:N
J J A
S O
D
F
M A M
month (1993-94)
Fig. 4. C:N ratios of the (A) nanofraction, (B) microfraction and (C) mesofraction. Symbols as in
Figure 3. Straight line is Redfield ratio (6.6).
found for the N:P ratios (Figure 6). The N:P ratios increased during the sampling
period, thus highest ratios were found in spring 1994.
There were different taxa and species contributing to the mesofraction through
the year (Table II), but still the elemental composition of the pooled mesoplankton samples as a function of dry weight (not shown) was quite constant as illustrated by linear regressions: ug C = 0.52 ug dw - 1.43, r2 = 0.98; ug N = 0.08 ug dw
- 0.21, r2 = 0.93 and ug P = 0.007 ug dw - 0.05, r2 = 0.88.
Discussion
Succession of primary and secondary producers, as well as biomass ranges were
typical for temperate regions (e.g. Fransz and Gieskes, 1984; Paasche and Erga,
350
Stoichlometry among planktonic size fractions
7000
Nanofraction
1500 C:P
o
1000 -
t
500 0 B) Microfraction
C:P
2000
C) Mesofraction
1500C:P
1000 500-
O
•ft—o0 J J A S O
-S-te--fl
D
F M A M
month (1993-94)
1 J ' ChP,rr tiOS °Dth.r( M} n a n °fr a c t i o n '( B ) microfraction and (C) mesofraction. Symbols as in Figure
3. Straight line is Redfield ratio (106). One outlier (2830) is missing for the microfraction.
1988; Ki0rboe, 1993; Kivi et al, 1993; Riegman et al., 1993): fairly constant biomasses
through summer which decline through autumn towards winter, and a characteristic diatom bloom in early spring, accompanied by an increase in nanoplankton and
ciliates. An increase in copepods was not evident until May. This time lag between
the spring diatom bloom and enhanced metazoan biomass (Ki0rboe, 1993) will
result in sedimentation of a large part of the bloom (Smetacek et al, 1978; Nielsen
and Richardson, 1989; Olesen, 1993). This time lag also allows a characteristic
biomass peak of fast growing ciliates in spring, during a time of high food abundance
and low predation pressure. Similar patterns have been found in the Kiel Bight, in
the Baltic and in the Kattegat, and predation control of ciliate biomass has been suggested (Stegmann and Peinert, 1984; Kivi et al, 1993; Nielsen and Ki0rboe, 1994).
351
LGismerrik
A) Nanofraction
200150 •
N:P
1
100 •
'ff^f• o
50 •
0 •
B) Microfraction
200 •
•
150 •
N:P
Tiff
100 •
50 -
•:-
° • •
0C) Mesofraction
N:P
J J A S n
n
F M A M
month (1993-94)
Fig. 6. N:P ratios of the (A) nanofraction, (B) microfraction and (C) mesofraction. Symbols as in Figure
3. Straight line is Redfield ratio (16). One outlier (350) is missing for the microfraction.
The C.P and N:P ratios of the particulate material <200 um were more than
twice as high as the ratios found in 1986 in the Oslofjord (Paasche and Erga, 1988).
Also the seasonal development was different. While the ratios increased during
the year in 1988 (Paasche and Erga, 1988), the ratios increased through the sampling period in this study, i.e. from 1993 till 1994. This may be due to efficient waste
water plant removal of phosphorus compared to nitrogen in the last decade (the
efficiency of cleaning P from the waste water is -95% while the efficiency of N
removal is 15%, this yields a total N/total P ratio of 150-200 by atoms in the waste
water). In 1986 nitrogen was the limiting nutrient during spring while later on
phosphorus became the limiting component. During summer and autumn in 1986
both nitrogen and phosphorus were considered potentially limiting (Paasche and
352
Stoichiomerry among planktonic size fractions
Erga, 1988). Paasche and Erga (1988) defined C:P ratios >200 and C:N ratios >10
as potential indicators of nutrient limitation with respect to phosphorus and
nitrate/ammonia. The high C:P ratios and the low inorganic phosphorus concentration found in this study, suggest that inorganic phosphorus was a likely candidate as a limiting nutrient for phytoplankton. However, during summer 1993 the
C:N ratios of the nanoplankton were >10 for all stations except the innermost one,
thus potential nitrogen limitation cannot be ruled out.
The low Chi a concentrations combined with high C/Chl a ratios found during
most of the year indicate that a major portion of the nanofraction was of a heterotrophic or detrital origin. The low C:N ratio of the nanoplankton (except during
summer) indicates that the fraction is mainly composed of living organisms, as
detritus generally have higher C:N ratios (Nixon, 1981). In contrast to what was
noted by Nixon (1981), the heterotrophic biomass in this system is not a small fraction of the autotrophic biomass, but may be sufficiently large to play an important
role in allocation of nutrients in the water column. Both protozoans (Goldman et
al., 1987; Nakano, 1994) and bacteria (Vadstein et al., 1988), which may have contributed to the nanofraction, would be expected to have lower C:P ratios than
phytoplankton during P-limitation, and thus reduce rather than enhance the
differences in stoichiometry between compartments. The microplankton consisted both of proto- and metazooplankton as well as large phytoplankton (Table
II). The high C:N and C:P ratios indicated that there was also a large fraction of
detritus in this compartment (this was verified, but not quantified, during microscopic analysis). A similar result was found by Le Borgne (1989), who calculated
that as much as 70% of the dry weight of the 35-200 um size fraction at Tikehau
Atoll was non-living material.
The stoichiometry of the mesoplankton was quite constant despite variable
species composition through the year. The percentage of nitrogen (8%) and phosphorus (0.7%) of dry weight in this study compares well with the numbers found
by e.g. Butler et al. (1969) and Le Borgne (1982). The percentage of carbon (52%)
of dry weight is in the same range as found in the North Pacific by Omori (1969),
and the same is true for the C:N ratios. However, compared to C:N and C:P ratios
found by Gismervik (1997) in the same area, the mixed samples somewhat underestimated the real nitrogen and phosphorus content of individual copepods.
The N:P ratio found for mesozooplankton in this study do not deviate much
from ratios found in other areas, despite the fact that the N:P ratios of the supposed food fractions differ considerably due to unlike limiting factors (Table III).
Table IIL Atomic N:P ratios reported for zooplanlcton fractions and seston fractions at various sites
N:P ratios
Zooplankton fraction
N:P ratios
Seston fraction
30
20
27
24
24
74
39
20
16
18
(200-2000 um)
(>153 tun)
(>153 (jjn)
(>415 um)
(200-5000 (i.m)
(<20 (im)
(<83 ^.m)
(<83 (im)
(<75 urn)
(<50 \im)
Reference
Oslofjord
Lakes
Marine sites
Long Island Sound
Tropical Atlantic Ocean
This study
Elser and Hassett, 1994
Elser and Hassett, 1994
Harris and Riley, 1956
Le Borgne, 1982
Only mean value of all reported ratios in each study is shown.
353
LGbmervik
0
20
40
60
80
100
% mesoplankton of the paniculate C pool
Fig. 7. Percentage of mesoplankton (200-2000 |im) of the paniculate (0.7-2000 um) carbon and phosphorus pool. Symbols as in Figure 3. Line indicates a one to one relationship.
Thus, the declining phosphorus load to the Oslofjord had variable effect on the
stoichiometry of the different plankton compartments; while the ratios of the
mesozooplankton probably have remained fairly constant, the ratios of the nanoand microfraction have increased. Consequently it can be hypothesized that the
distinct stoichiometry of nano- and mesozooplankton found in the Oslofjord may
have affected the regeneration of nutrients by the mesozooplankton. Although
the mesoplankton was a small part of the total organic carbon pool, it retained as
much as 60% of the paniculate phosphorus (Figure 7). A similar result was found
by Elser and George (1993) in Castle Lake. They also found that the N:P ratios of
the zooplankton were fairly constant (11-22 by atoms) while the ratios of the
seston pool varied by factors of 7-15 across depth and sampling dates. Thus they
derived that the zooplankton potentially enhanced P limitation in the lake. Elser
and Hassett (1994) suggested that although the N:P ratios in producers and consumers do not differ as much in marine systems as in freshwater systems, the slight
difference might still amplify nitrogen deficiency. This study suggests that the
marine mesozooplankton also have the potential to amplify phosphorus limitation due to their accumulation of somatic phosphorus in phosphorus-limited
systems Zooplankton may thus indirectly influence both production and species
composition of the plankton community, by altering nutrient composition and
competition among algal species (Sterner, 1990; Hessen and Andersen, 1992).
Acknowledgements
I would like to thank T.Andersen, D.O.Hessen and S.Kaartvedt for help initiating
the research, and the crew of F/FTrygve Braarud for assistance on the cruises. The
assistance of R.Amundsen and S.0veras on the cruises and in the laboratory is
greatly appreciated. They also analysed the chlorophyll and biochemical samples.
354
Stoichiometry among pbmktonic size fractions
I am grateful to D.O.Hessen and S.Kaartvedt for valuable criticism of the manuscript. This study forms a part of the research programme on marine pollution,
financed by the Norwegian Research Council (NFR).
References
Andersen.T. and HessenJ).O. (1991) Carbon, nitrogen, and phosphorus content of freshwater zooplankton. Limnol. Oceanogr., 36,807-814.
Bamstedt.U. (1985) Seasonal excretion rates of macrozooplankton from the Swedish west coast.
Limnol. Oceanogr., 30,607-617.
BeersJ.R. (1966) Studies on the chemical composition of the major zooplankton groups in the Sargasso Sea off Bermuda. Limnol. Oceanogr, 11,520-528.
Brewer^P.G. and RileyJ.P. (1965) The automatic determination of nitrate in sea water. Deep-Sea Res.,
12,765-772.
Butler,E.I., Corner.E.D.S. and Marshall.S.M. (1969) The nutrition and metabolism of zooplankton. VI.
Feeding efficiency of Calanus in terms of nitrogen and phosphorus. J. Mar. Biol. Assoc UK, 49,
977-1001.
CorlissJ.O. (1979) The Ciliated Protozoa. Pergamon Press, Oxford, 455 pp.
Corner.E.D.S. and Davis^A.G. (1971) Plankton as a factor in the nitrogen and the phosphorus cycles
in the sea. Adv. Mar. BioL, 9,101-204.
Droop,M.R. (1983) 25 years of algal growth kinetics. A personal view. Bot. Mar., 26,99-112.
ElserJJ. and George,N.R (1993) The stoichiometry of N and P in the pelagic zone of Castle Lake, California. J. Plankton Res., 15,977,992.
ElserJJ. and Hassett,R.P. (1994) A stoichiometric analysis of the zooplankton-phytoplankton interaction in marine and freshwater ecosystems. Nature, 370,211-213.
ElserJJ., Elser,M.M., MacKay,N.A. and Carpenter,S.R. (1988) Zooplankton-mediated transitions
between N- and P-limited algal growth. Limnol Oceanogr., 33,1-14.
Fransz.H.G. and Gieskes,W.W.C. (1984) The unbalance of phytoplankton and copepods in the North
Sea. Rapp. P.-V. Riun., Cons. Int. Explor. Mer, 183,218-255.
Gismervik j . (1997) Stoichiometry of some marine planktonic crustaceans. /. Plankton Res., 19, in press.
Goldman J., McCarthyJJ. and PeaveyJD.G. (1979) Growth rate influence on the chemical composition
in phytoplankton in oceanic waters. Nature, 279,210-214.
GoldmanJ.G., CaronJD.A. and Dennett,M.R. (1987) Nutrient cycling in a microflagellate food chain:
IV. Phytoplankton-microflagellate interactions. Mar. EcoL Prog. Ser., 38,75-87.
Harris^, and Riley.G.A. (1956) Oceanography of Long Island Sound, 1952-1954. VIII. Chemical composition of the plankton. Bull. Bingham Oceanogr. ColL, 15,315-323.
Harrison.PJ., ConwayJI.L., Holmes,R.W. and Davis,C.O. (1977) Marine diatoms grown in chemostats
under silicate or ammonium limitation. III. Cellular chemical composition and morphology of
Chaetoceros debilis, Skeletonema costatum, and Thalassiosira gravida. Mar. Biol, 43,19-31.
HessenJJ.O. and Andersen.T. (1992) The algae-grazer interface: feedback mechanisms linked to elemental ratios and nutrient cycling. Arch. Hydrobiol Beth., 35,111-120.
Jahnke J., Rick,H.-J. and Aletsee,L. (1986) On the light and temperature dependence of the minimum
and maximum phosphorus contents in cells of the marine plankton diatom Thalassiosira rotula
Meunier. /. Plankton Res., 8,549-555.
Ketchum,B.H. (1962) Regeneration of nutrients by zooplankton. Rapp. P.-V. Rtun., Cons. Int. Explor.
Mer, 153,142-147.
Kivi.K., Kaitala.S., Kuosa,H., KuparinenJ., Leskinen^E., LigneUJl., Marcussen,B- and Tamminen.T.
(1993) Nutrient limitation and grazing control of the Baltic plankton community during annual succession. Limnol Oceanogr., 38,893-905.
Ki0rboe,T. (1989) Phytoplankton growth rate and nitrogen content: implications for feeding and
fecundity in a herbivorous copepod. Mar. Ecol Prog. Ser., 55,229-234.
Ki0rboe,T. (1993) Turbulence, phytoplankton cell size, and the structure of pelagic food webs. Adv.
Mar. BioL, 29,1-72.
Le Borgne.R. (1982) Zooplankton production in the eastern tropical atlantic ocean: Net growth
efficiency and P:B in terms of carbon, nitrogen, and phosphorus. Limnol Oceanogr., 27,681-698.
Le Borgne^R. (1989) Zooplankton of Tikehau atoll (Tuamotu archipelago) and its relationship to particulate matter. Mar. BioL,!1!!!,341-353.
MagnussonJ. and Johnsen.T. (1994) Overvakning av forurensningssituasjonen i indre Oslofjord 1993.
Report no. 565/94. Norwegian Institute of Water Research.
355
LGbmervik
Morales,C.E. (1987) Carbon and nitrogen content of copepod faecaJ pellets: effects of food concentration and feeding behaviour. Mar. Ecol. Prog. Sen, 36,107-114.
MurphyJ. and RileyJ.P. (1958) A single-solution method for the determination of soluble phosphate
in sea water. / Mar. Biol. Assoc UK., 37,9-14.
Nakano,S.I. (1994) Carbon:nitrogen:phosphorus ratios and nutrient regeneration of a heterotrophic
flagellate fed on bacteria with different elemental ratios. Arch. Hydrobioi, 129,257-271.
Nielsen.T.G. and Ki0rboe,T. (1994) Regulation of zooplankton biomass and production in a temperate, coastal ecosystem. 2. Ciliates. UmnoL Oceanogr., 39,508-519.
Nielsen,T.G. and Richardson.K. (1989) Food chain structure of the North Sea plankton communities:
seasonal variations of the role of the microbial loop. Mar. EcoL Prog. Sen, 56,75-87.
Nixon,S.W. (1981) Remineralization and nutrient cycling in coastal marine systems. In Neilson3J- and
Cronin.L.E. (eds), Estuaries and Nutrients. The Humana Press Inc., New Jersey, pp. 111-138.
Olesen,M. (1993) The fate of an early diatom spring bloom in the Kattegat. Ophelia, 37,51-66.
Omori.M. (1969) Weight and chemical composition of some important oceanic zooplankton in the
North Pacific Ocean. Mar. Biol., 3,4-10.
Paasche.E. and Erga,S.R. (1988) Phosphorus and nitrogen limitation of phytoplankton in the inner
Oslofjord (Norway). Sarsia, 73,229-243.
Paasche,E. and 0stergren,l. (1980) The annual cycle of plankton diatom growth and silica production
in the inner Oslofjord. Limnol. Oceanogr., 25,481^194.
Putt,M. and Stoecker.D. (1989) An experimentally determined carbon: volume ratio for marine 'oligotrichous' ciliates from estuarine coastal waters. Limnol Oceanogr., 34,1097-1103.
Redfield.A.C. (1958) The biological control of chemical factors in the environment. Am. Set, 46,
205-222.
Reusch-BergJ'.L. and AbdullahJvl.I. (1977) An automatic method for the determination of ammonia
in sea water. Water Res., 11,637-638.
Riegman.R., Kuipers,B.R., Noordeloos^A.A.M. and Witte.H.J. (1993) Size-differential control of
phytoplankton and the structure of plankton communities. Neth. J. Sea Res., 31,255-265.
SieburthrI.M.,Smetacek,V. and LenzaX (1978) Pelagic ecosystem structure: Heterotrophic compartments and their relationship to plankton size fractions. Limnol Oceanogr., 23,1256-1263.
Smetacek.V, von Brdckel.K., Zeitzschel,R and Zenk.W. (1978) Sedimentation of paniculate matter
during a phytoplankton spring bloom in relation to the hydrographical regime. Mar. Biol., 47,
211-226.
Stegmann.P. and Peinert.R. (1984) Interrelationships between herbivorous zooplankton and phytoplankton and their effect on production and sedimentation of organic matter in Kiel Bight. Limnologica, 15,487^*95.
Stemer.R. (1990) The ratio of nitrogen to phosphorus resupplied by herbivores: zooplankton and the
competitive arena. Am. Nat., 136,209-229.
Sterner,R.W., ElserJJ. and Hessen.D.O. (1992) Stoichiometric relationships among producers, consumers and nutrient cycling in pelagic ecosystems. Biogeochemistry, 17,49-67.
Vadstein.O., Jensen^A., Olsen.Y. and Reinertsenji. (1988) Growth and phosphorus status of limnetic
phytoplankton and bacteria. Limnol. Oceanogr., 33,489-503.
Received on April 1,1996; accepted on October 18,1996
356