Journal of Plankton Research Vol.22 no.3 pp.569–588, 2000
Food web interactions in a Calanus finmarchicus dominated
pelagic ecosystem—a mesocosm study
B.W.Hansen, B.H.Hygum, M.Brozek, F.Jensen and C.Rey1
Roskilde University, Department of Life Sciences and Chemistry, PO Box 260,
DK-4000, Denmark and 1Université P. et M. Curie (Paris IV), C.N.R.S.- I.N.S.U.,
URA 2077, Station Zoologique, PB 28, F-06230 Villefranche-sur-Mer, France
Abstract. The significance of nauplii versus copepodite stage V of Calanus finmarchicus grazing and
their effects on the structure of the food web were investigated during two sampling periods of 7–8
days in March and April in experimental mesocosms held in a Norwegian fjord over a 2 month period.
The mesocosms were manipulated by the addition of two different levels of inorganic nutrients
(control versus enriched). During the ‘naupliar’ period in March, the phytoplankton was characterized by a diatom bloom while during the ‘copepodite’ period in April, it was in a post-bloom phase
characterized by small-celled species, mainly Phaeocystis pouchetii. Phytoplankton, bacterial and
protozooan biomass and production rates were measured in addition to copepod biomass. Copepod
grazing was estimated by three different methods: (i) gut fluorescence; (ii) chlorophyll clearance from
the water; and (iii) growth method measured as body carbon increase. The two latter methods gave
similar results for nauplii, but all three gave different results for the copepodites. Independent somatic
growth, based on changes in abundance and individual carbon content, and grazing estimates revealed
an overall growth efficiency of 0.66 ± 0.20 (mean ± S.E.) for copepodites. Empirical carbon flow
models were constructed, which indicated that the nauplii could not control either phytoplankton or
protozoan growth in either the control or in the enriched system. Ignoring recycling and sedimentation, the fate of the primary production for the nauplii-dominated community was to be grazed by
a diverse and abundant protozooplankton community. In the copepodite-dominated community, the
copepods grazed >100% of the daily primary production, and also grazed heavily on a protozooplankton community of low biomass and diversity and presumably on detritus. The fate of the primary
production in the two different copepod scenarios followed predicted routes for ‘low meso-zooplankton’ and for ‘high meso-zooplankton’ biomass systems, as suggested by Wassmann (Wassmann, 1998).
Introduction
Mesozooplankton production in the oceans is generally associated with seasonal
net-phytoplankton blooms, and during summer and autumn, copepod grazing
impact can match or even exceed the daily primary production in boreal and
arctic ecosystems (Hansen et al., 1990a; Kiørboe and Nielsen, 1994). However,
herbivorous impact on the early spring blooms may be negligible due to temperature-generated time lags in the copepod biomass (Tande, 1991; Nielsen and
Hansen, 1995; Keller et al., 1999).
One of the important copepod species in arctic-boreal waters is Calanus
finmarchicus. It has been suggested, based upon cohort analysis, that C.finmarchicus has one generation per year in its northernmost habitats, but two to three
generations in Western Norway and the North Sea (MacLellan, 1967; Tande,
1982, 1991; Gislason and Astthorsson, 1998). Stage composition during spring is
dominated numerically by juveniles (nauplii) and later on, by late stage copepodites (Melle and Skjoldal, 1998).
For a large part of the year, small zooplankton, including C.finmarchicus
nauplii, are responsible for a significant part of the energy turnover in some areas
[e.g. North Norwegian fjords (Barthel, 1995)]. The different developmental
© Oxford University Press 2000
569
B.W.Hansen et al.
stages of copepods have different food requirements in terms of prey sizes, with
nauplii generally catching smaller prey than the latter stages (Poulet, 1977;
Fernandez, 1979; Berggreen et al., 1988). Seasonal differences in the mesozooplankton developmental stage composition may therefore influence the structure
of the lower trophic levels. Top-down by mesozooplankton grazing on protozooplankton has been verified for a number of adult calanoid copepod species [e.g.
(Stoecker and Capuzzo, 1990; Gifford, 1991; Sanders and Wickham, 1993)] and
for Calanus spp. in particular (Barthel, 1988; Ohman and Runge, 1994). This is
not expected for any calanoid naupliar stages, however (Fernandez, 1979;
Berggreen et al., 1988), because protozooans are generally considered to be too
large to be efficiently consumed by nauplii. Optimal prey size for different
zooplankters is strongly related to their body size and species-specific feeding
behaviour [see (Hansen et al., 1994)]. Thus, microphageous microzooplankton,
like ciliates and copepod nauplii, are competitors for similar food items. The
interactions between all copepod stages and their prey may, in addition to influencing phytoplankton biomass and composition, be expected to cause shifts in
protozooplankton composition and biomass, and such effects may cascade
further down in the food web by influencing the prey organisms for protozoans
(i.e. by stimulating the bacterial and nano-phytoplankton communities).
Supposed structural changes in plankton can be analysed in situ by empirical
carbon budget models (Nielsen and Richardson, 1989; Nielsen et al., 1993;
Hansen et al., 1996), but setting up various simple mesocosm food webs enables
the study of specific interactions in the pelagic environment over a relatively long
period [e.g. (Bjørnsen et al., 1988; Riemann et al., 1990)]. These exercises can test
various mesozooplankton biomass and grazing impacts and interactions as they
affect other pelagic processes, including sedimentation (Wassmann et al., 1996;
Keller et al., 1999), and this has been demonstrated by Wassmann (Wassmann,
1998) in situ and in mesocosms.
In the present study, we investigate the quantitative significance of Calanus
finmarchicus grazing, and the qualitative influence of a nauplii- versus a copepodite-dominated copepod community, on the lower trophic levels in 18 m3
pelagic mesocosms in a Norwegian fjord.
Method
Mesocosms, and copepod material
Growth and development of a Calanus finmarchicus cohort was investigated
during a 2 month growth period from March 11 to May 12, 1997 in mesocosms
manipulated by addition of inorganic nutrients [see (Hygum et al., 2000a)]. The
mesocosms were installed at the Marine Biological Field Station Espegrend,
University of Bergen. Two 18 m3 mesocosms (depth 7 m, diameter 2 m) were
filled with 50 µm screened sea water to ensure intact phyto- and protozooplankton communities and prevent intrusion of other copepods and predators. The
mesocosms were enriched with different nutrient loads [see (Hygum et al.,
2000b)] and termed ‘control’ and ‘enriched’, respectively. The copepod cohorts
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Food web interactions in a pelagic ecosystem
were obtained from eggs produced in 100 l spawning chambers by a spawning
stock of copepods collected in Raunefjord (60°179N, 05°109E) [see (Hygum et al.,
2000a)].
Primary producers
Water samples taken every second day during two, one week periods, 17–23
March and 28 April–4 May, using a 3 l heart-valve water sampler at several depths
(0, 1, 2, 3, 4 and 5 m), were pooled in a bucket. All samples for phytoplankton,
bacteria and protozooplankton were taken from this ‘integrated’ 18 l water subsample.
Phytoplankton biomass in terms of chlorophyll (Chl) a was estimated by filtering 1–2 l onto GF/F filters and, after extraction for 24 h in 96% ethanol, measured
by spectrophotometer or fluorometer (Strickland and Parsons, 1972; Jespersen
and Christoffersen, 1987). Particulate organic carbon (POC) was obtained by
filtering 1 l onto pre-combusted GF/F filters and analysing using a EA 1110 CE
Instruments CHNS analyser. Phytoplankton composition was analysed to major
taxonomic groups using inverted microscopy at 3200–400 magnification in 1%
acid Lugol fixed samples in 25 ml settling chambers. Diatoms were measured and
carbon content calculated according to Strathmann (Strathmann, 1967) and Edler
(Edler, 1979).
Primary production was estimated by the in situ 14C-method, using ‘integrated’
water samples placed in three light and one dark bottle (115 ml) and incubated for
2 h around true noon at depths of 1 and 2.5 m in each mesocosm; 4 µCi H14CO3–
were added to each bottle. After incubation the contents of bottles were filtered
onto GF/F filters and treated as described by Nielsen and Hansen (Nielsen and
Hansen, 1995). To calculate daily production, light irradiance was measured
continuously on the mesocosm raft using a 2 phi Li-Cor Li-190SA sensor and a LiCor 1000 Datalogger. Daily area production was calculated using the trapezoid
method for water strata of 0–2 m and 2–7 m depth in each mesocosm.
Bacterioplankton
Bacterial cell numbers were determined by epifluorescence microscopy on preparations stained with 49,6 diamino-2-phenylindole (DAPI) following the procedure
of Porter and Feig (Porter and Feig, 1980). The bacterial cells in 10 microscope
fields (corresponding to an average of 200–400 cells) were counted and the length
and width of 40 cells were measured. Bacterial cell numbers were converted to
biomass by volume calculations and carbon density according to Simon and Azam
(Simon and Azam, 1989).
Net production rates of bacterioplankton were estimated from measurements
of 3H-leucine incorporation to measure bacterial protein synthesis rates in the
mesocosms following the procedure of Smith and Azam (Smith and Azam, 1992).
3H-leucine incorporation rates were converted to bacterial production using a
conversion factor of 1.1 g C mol–1 incorporated (Servais, 1995).
571
B.W.Hansen et al.
Protozooplankton
Protozooplankton identification and biomass estimation were obtained by inverted
microscopy in a similar manner as for the phytoplankton. Protozooplankton was
identified to main groups, i.e., thecate dinoflagellates, athecate dinoflagellates,
naked ciliates and tintinnids. Cell sizes were determined and cell volumes calculated
using simple geometric formulae. The biomass was obtained using a carbon:volume
ratio of 0.13 pg C µm–3 for thecate dinoflagellates and 0.11 pg C µm–3 for all other
groups (Edler, 1979; Fenchel, 1982; Hansen et al., 1997). Protozooplankton growth
was determined using the size fractionation method, where sea water was gently
fractionated by 200 µm by inverse filtration to minimize the risk of predation upon
protozoans by mesozooplankton (Carrick et al., 1992). The screened water was incubated in acid-cleaned, 2350 ml polycarbonate bottles in situ next to the mesocosms
at 1 m depth. Growth was estimated by counting abundance of organisms from
Lugol-fixed initial samples and after 24 and 48 h of incubation, assuming logarithmic growth (Nielsen and Kiørboe, 1994). Production of protozooplankton was calculated as maximum potential specific growth rate 3 standing stock of the mean of all
protozooplankton groups day by day. Grazing was estimated assuming a specific
growth efficiency of 0.33 (Hansen et al., 1997).
Copepods
Copepods were sampled by vertical hauls of a 25 cm diameter 90 µm plankton
net during the nauplii-dominated period. After experiencing substantial variability with this method (Hansen et al., submitted), nauplii and copepodites were
thereafter sampled by 10 casts of a heart-valve water sampler in each of the six
descrete depths; these were combined to give a 180 l ‘integrated’ sample and
concentrated on a 45 µm screen. Given the sampling problem during the first
sampling in the nauplii-dominated period, the abundance of nauplii was assumed
to be that initially added to the mesocosms, i.e. 4.5 individuals l–1, which was
assumed to be a good approximation since mortality was negligible (Hygum
et al., 2000a). The copepods were sampled every second day during the naupliidominated period and every third day during the copepodite-dominated period.
They were immideately fixed by 2% buffered formalin and later analysed in the
laboratory. At least 300 individuals were staged per sample. Individual carbon
contents were obtained from measurements on an infrared gas analyser (IRGA
ADC 225 MK3) for the nauplii and using an EA 1110 CE Instruments CHNS
analyser for the copepodites (Hygum et al., 2000a,b). Copepod biomass was calculated as abundance 3 individual mean carbon contents.
Grazing experiments with nauplii and copepodites were performed using two
different methods: (i) gut fluorescence; and (ii) chlorophyll clearance. During the
nauplii-dominated period, four experiments were performed. Due to their small
body size, gut fluorescence measurements were not feasible with nauplii. For the
chlorophyll clearance method, approximately 150–190 individually picked nauplii
(N III – V) were put into ‘integrated’ 200 µm screened whole water samples (the
size fractionation to ensure intact phyto- and protozooplankton communities,
572
Food web interactions in a pelagic ecosystem
including colonial forms), in each of three replicates, using 2350 ml acid-cleaned
polycarbonate bottles which were incubated for 24 h next to the mesocosms at
1 m depth. Chlorophyll ingestion rates were estimated by measuring chlorophyll
concentrations in 200 ml sub-samples before and after incubation, according to
the expressions of Frost (Frost, 1972). Three bottles without nauplii were used as
controls. During the copepodite-dominated period, three grazing experiments
were carried out. Three experiments with five replicates (8–20 C V per bottle)
were incubated as the nauplii had been. Immediately after incubation, all individuals were pipetted into 5 ml methanol and their gut contents extracted for 24 h
in the dark (Huntley et al., 1987). Gut fluorescence was measured by a Turner
Designs fluorometer before and after the addition of acid (Strickland and
Parsons, 1972). Grazing of plant pigments (Chl a + phaeopigments) was calculated assuming no digestion of chlorophyll during gut passage and a gut clearance
rate of 0.015 min–1 (Hansen et al., 1990a). Numerous controls for background
fluorescence with copepodites incubated in GF/F filtered sea water and later
measured for gut content were performed. These values were subtracted from gut
fluorescence data for grazing individuals.
Chlorophyll ingestion rates were estimated by measuring Chl a and phaeopigment concentration initially and after incubation, as for the grazing experiments
with nauplii. Less than 20% of the chlorophyll-containing material was removed
during the incubations. Three bottles without copepodites served as controls.
Naupliar and copepodite grazing demand was also estimated by the growth
method where: population grazing = copepod biomass 3 specific growth rate
[naupliicontrol = 0.24–0.29 day–1, naupliienriched = 0.23 day–1; copepoditecontrol = 0.04
day–1, copepoditeenriched = 0.04 day–1 from (Hygum et al., 2000a,b)] 3 3 [growth
efficiency of 0.33 (Hansen et al., 1997)]. All grazing upon phytoplankton was
converted to carbon units by the carbon:Chl a ratio calculated from regressions
between measured POC versus Chl a [Table I, see (Hygum et al., 2000a,b)].
Results
Phytoplankton biomass, in terms of Chl a, increased from initial values of 1 µg l–1
in both mesocosms to 8 in the control and 12 µg l–1 in the enriched mesocosms
during the nauplii-dominated period. During the copepodite-dominated period,
Chl a was between 1–2 µg l–1 and increased to approximately 2 in both mesocosms
(Table I and Figures 1 and 2). Temperature during the two intensive sampling
periods was relatively stable at 4.8–7.7°C. The developmental stage composition
of the nauplii-dominated community (NIII-V) was more advanced in the control
versus the enriched mesocosms, due to earlier initiation of the control bag (1–2
days) (Hygum et al., 2000b). During the copepodite-dominated community,
>95% of the copepods were CV (Table I).
Nauplii-dominated period
The phytoplankton community was totally dominated by diatoms. Phytoplankton
biomass, in terms of Chl a and POC, increased at similar rates in both mesocosms
573
B.W.Hansen et al.
Fig. 1. Nauplii-dominated community in a control and an enriched 18 m3 mesocosm. Symbols:
phytoplankton biomass (d) and primary production (m), bacterial biomass (d) and production (m),
protozooplankton biomass (open = thecate dinoflagellates, diagonal hatching up from left to right =
athecate dinoflagellates, diagonal hatching up from right to left = naked ciliates, cross hatching =
tintinnids) and production (m), and copepod biomass (d) and individual carbon content in µgC (s)
of Calanus finmarchicus.
(Figure 1). The POC:Chl a ratio, the calculated carbon:Chl a ratios (Table I) and
phytoplankton carbon, calculated from Hygum et al. (Hygum et al., 2000a,b),
resulted in a factor of 2 higher phytoplankton biomass in the enriched mesocosms
(Figure 4). The rate of primary production was similar in both mesocosms.
Phytoplankton, bacteria and protozooplankton developed in a similar way in
574
Food web interactions in a pelagic ecosystem
Fig. 2. Copepodite-dominated community in a control and an enriched 18 m3 mesocosm. Phytoplankton biomass and primary production, bacterial biomass and production, protozooplankton
biomass and production and copepod biomass and individual carbon content of Calanus finmarchicus (note different y-axis than in Figure 2). Symbols as in Figure 1.
the two mesocosms, with a tendency towards an increasing biomass during the
week of observation. The composition of the protozooplankton community was
similar in the two mesocosms; the biomass was dominated by naked ciliates and
athecate dinoflagellates, with <10% thecate dinoflagellates and only a minor
contribution from tintinnids.
Measurements of potential maximum protozooan specific growth rate revealed
575
576
cChl
a.
bTotal
et al. (2000a,b).
plant pigment.
aHygum
Control
Nauplii-dominated
Copepodite-dominated
Enriched
Nauplii-dominated
Copepodite-dominated
Treatment
2.8 ± 2.6
1.5 ± 0.2
4.0 ± 4.1
1.7 ± 0.3
4.8–5.1
7.3–7.7
Chlorophyll a
Mean ± S.D.
4.8–5.1
7.3–7.7
Temperature
°C
0.99
1.19
0.96
1.34
11.97
2.10
7.84
1.73
33.6
29.3
44.4
30.6
119 ± 46 b
718 ± 116c
Phytoplankton
Carbon:Chl aa
169 ± 21b
426 ± 40c
Chlorophyll a
POC:Chl aa
————————– Mean ± S.D.
min
max
N III–N IV
CV
N III–N V
CV
Stage
composition
Table I. Temperature, chlorophyll a concentration, POC and stage compositions in control and enriched mesocosms during the two periods in March and
April/May characterized by dominance of either nauplii or copepodites of Calanus finmarchicus
B.W.Hansen et al.
Food web interactions in a pelagic ecosystem
Table II. Potential maximum specific growth rate, community growth and community grazing by
protozooplankton in 18 m3 control and nutrient-enriched mesocosms during the two periods in March
and April/May characterized by dominance of nauplii or copepodites of Calanus finmarchicus
Date
Specific growth rate
day–1
Nauplii-dominated period
Control
March 17
0.35
March 19
0.57
March 21
0.16
March 23
0.24
X ± S.E.
0.33 ± 0.08
Enriched
?
?
0.23
?
0.23
Copepodite-dominated period
Control
Enriched
April 28
0.10
0.34
April 30
0.10
0.71
May 2
0.47
0.11
May 4
0.34
0.26
X ± S.E.
0.25 ± 0.08 0.36 ± 0.11
Community growtha
µg C l–1 day–1
Community grazingb
µg C l–1 day–1
Control
3.04
4.29
1.92
2.16
2.85 ± 0.46
Enriched
?
?
3.10
?
3.10
Control
9.12
12.87
5.76
6.48
8.56 ± 1.39
Enriched
?
?
9.30
?
9.30
Control
0.07
0.15
1.53
0.25
0.50 ± 0.30
Enriched
0.37
1.37
0.21
0.52
0.62 ± 0.22
Control
0.21
0.45
4.59
0.75
1.50 ± 0.90
Enriched
1.11
4.11
0.63
1.56
1.85 ± 0.67
? = No growth obtained in the incubations.
aOverall protozoan potential specific growth rate 3 biomass.
bOverall protozoan potential specific growth rate 3 biomass 3 3 (growth yield of 33%, Hansen et al.,
1997).
that protozooa only grew on one of the sampling days in the incubations of water
from the enriched mesocosm, but grew on all the sampling days in the control
water (Table II). Growth rates ranged from 0.16 to 0.57 day–1. The calculated
protozooplankton community production was 2.85 ± 0.46 µg C l–1 day–1 (mean ±
S.E.) in the control.
The biomass of the copepod nauplii increased from <2 to >6 µg C l–1, reflecting the individual body carbon increase during development, although there was
no obvious difference between the two mesocosms (Figure 1).
Copepodite-dominated period
During the copepodite-dominated period, the phytoplankton community was
characterized by small flagellates, mostly Phaeocystis pouchetii. Only 1% of the
phytoplankton biomass in the control and the enriched mesocosm were diatoms.
Chl a values were relatively stable and much lower than during the nauplii-dominated period (Table I). However, the POC values were high, especially in the
enriched mesocosms, presumably reflecting an increasing amount of detritus. The
rate of primary production was stable at 17 ± 5 and 20 ± 3 µg C l–1 day–1 (mean ±
S.D.) in the control and in the enriched mesocosm, respectively (Figures 2 and 4).
During the nauplii-dominated period, the trophic structures and dynamics in
control and enriched mesocosms were quite similar. During the copepoditedominated period, however, the community structure among the heterotrophic
organisms differed both from that seen in the nauplii-dominated period and
between the two mesocosms. Bacterial biomass was generally higher than during
577
B.W.Hansen et al.
the nauplii-dominated period, particularly in the enriched mesocosm, indicating
stimulation. The protozooplankton assemblage consisted, virtually, of only athecate dinoflagellates <30 µm in cell size, with an equal and very low biomass in
both mesocosms. Measurements of maximum protozooplankton-specific growth
rates revealed that protozooplankton grew on all sampling days in both mesocosms (Table II). Ths specific growth rate ranged from 0.10 to 0.47 day–1 (mean
± S.E.) in the control and 0.11 to 0.71 day–1 in the enriched mesocosm. Calculated
protozooplankton production was 0.5 ± 0.6 µg C l–1 day–1 in the control and 0.6
± 0.2 µg C l–1 day–1 in the enriched mesocosm (Table I and Figure 4).
The copepodite community in both mesocosms was composed of CV and the
biomass amounted to 241 and 185 µg C l–1, and 627 and 389 µg C l–1, on the two
sampling dates in the control and the enriched mesocosm, respectively.
Grazing methods
Naupliar grazing rates, determined using the chlorophyll clearance method, gave
a mean ± S.E. of 0.23 ± 0.13 µg C nauplii–1 day–1 for the enriched mesocosm
(Figure 3). For the copepodites, grazing rates estimated from measurements of
gut fluorescence gave values of 3.6 ± 0.9 and 10.6 ± 2.4 µg C copepodite–1 day–1
for control and enriched mesocosms, respectively. Using the chlorophyll clearance method, grazing rates of 0 and 2.5 ± 0.3 µg C copepodite–1 day–1 were
obtained for control and enriched mesocosms, respectively (Figure 3).
Table III. Mean ± S.E. copepod community grazing of chlorophyll-containing material during the two
periods in March and April/May characterized by dominance of nauplii or copepodites of Calanus
finmarchicus. Three methods were used: (i) gut fluorescence method; (ii) chlorophyll clearance
method; and (iii) growth method (see Methods). The abundance of copepods was approximately 4.5
l–1 for nauplii, which was close to initial density. Because of the difficulties in abundance estimates due
to variability of net samplings (see Hansen et al., submitted) and a very low actual mortality of less
than 1% of the cohort per day (see Hygum et al., 2000a), copepodite abundance was calculated as a
mean of two samplings. Carbon:Chl a ratio from Hygum et al. (2000a,b) see Table I
Gut
fluorescence
methoda
µg C l–1 day–1
Chlorophyll
clearance
methodb
µg C l–1 day–1
Nauplii-dominated
period
Control 4.5 ind l–1
Enriched 4.5 ind l–1
n.d.
n.d.
0
1.04
Copepodite-dominated
period
Control 1.53 ind l–1
Enriched 2.05 ind l–1
5.5 ± 1.4
21.6 ± 5.0
0
5.1 ± 0.5d
Growth
methodc
µg C l–1 day–1
2.8 ± 0.6
2.2 ± 1.0
25.6
60.9
Mean
values for
Figure 4
µg C l–1 day–1
2.8
1.6
15.6
29.2
aFrom bottle experiments with mesocosm water, gut clearance rate = 0.015 min–1 (Hansen et al.,
1990a), and assumption of no Chl a destruction.
bFrom bottle experiments, grazing calculated according to Frost (1972).
cI = biomass 3 specific growth rate (Hygum et al., 2000a,b) 3 3 [growth yield 33%, (Hansen et al.,
1997)].
dExcluding negative grazing value (Figure 3).
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Food web interactions in a pelagic ecosystem
Fig. 3. Individual mean ± S.D. ingestion rates for Calanus finmarchicus calculated according to three
methods: (i) gut fluorescence method; (ii) chlorophyll clearance method; (iii) growth method for
nauplii and copepodites in a control and an enriched 18 m3 mesocosm.
Calculations of grazing rate from growth measurements suggested daily grazing
rates of 0.6 ± 0.1 and 0.5 ± 0.2 µg C nauplii–1 day–1 and 16.7 and 29.3 µg C copepodite–1 day–1 for the control and enriched mesocosms, respectively (Figure 3 and
Table III).
The mean carbon specific ingestion rate calculated using the Chl a clearance
method for the nauplii in the enriched mesocosm was 0.32 day–1. The mean
carbon specific ingestion rates calculated using the gut fluorescence method for
the copepodites in the control and enriched mesocosms were 0.03 day–1 and 0.04
day–1. Based on the chlorophyll clearance method, carbon specific ingestion rate
was 0.01 day–1 in the enriched mesocosm. This gave a growth efficiency (specific
ingestion of phytoplankton/specific growth) of 0.66 ± 0.20 for the copepodites.
Carbon budgets
Empirical pelagic carbon budgets of the mean biomass, production and loss rates
were constructed for the nauplii- and copepodite-dominated periods. This was
tested at different nutrient regimes in order to evaluate the quantitative significance, as well as possible structuring effects on lower trophic levels, of the
579
B.W.Hansen et al.
Fig. 4. Carbon flow schemes for control and enriched nauplii and copepodite communities in 18 m3
mesocosms. Data for Chl a, primary production, bacterial biomas and production, protozooplankton
biomass, production and grazing, and copepod biomass were mean values from Figures 1 and 2.
Copepod grazing were mean values from Table III. Mean carbon pools in boxes, carbon production
in arrows leaving the boxes and carbon demand in arrows entering the boxes. Units in µg C l–1 (day–1).
copepods (Figure 4). Since not all grazing experiments yielded valid results,
copepod community grazing is presented as mean results from one or more
methods (Table III).
Nauplii-dominated period. For the nauplii-dominated period, the only difference
between the control and the enriched mesocosms was the mean phytoplankton
biomass, with the enriched situation attaining twice the phytoplankton concentration of the control. Therefore, the two budgets are discussed together. There
580
Food web interactions in a pelagic ecosystem
was positive carbon balance in terms of primary production versus loss due to
grazing requirements in both mesocosms, which led phytoplankton biomass to
increase throughout the period (Figure 1). Following our measurements and
literature biomass turnover considerations [e.g. (Andersen, 1988; Hansen et al.,
1999)], protozooans were judged to be much more important grazers than nauplii.
Copepodite-dominated period. For the copepodite period, phytoplankton standing stocks were much lower than for the nauplii-dominated period, but the
chlorophyll specific primary production rate was higher by a factor of 3–5 (Figure
4). The bacterial biomass in the control copepodite mesocosm was similar to that
seen in both mesocosms during the nauplii-dominated period, and these values
were lower than those seen in the enriched mesocosm during the copepodite
dominance. In addition, during the copepodite-dominated period, bacterial
production was higher for the enriched mesocosm, although specific production
was not.
The protozooplankton communities were of similar low biomass in both mesocosms but still had a daily specific production rate in the range of 0.24–0.36 (Table
II), similar to production rates observed for the nauplii-dominated period. The
taxonomic composition was skewed towards small (<30 µm diameter) athecate
dinoflagellates, which were probably grazing on nanoflagellates.
Copepod biomass was very high [although fluctuating due to sampling problems (Riemann et al., 1990; Hansen et al., submitted)], revealing that they were
by far the most important grazers, especially in the enriched mesocosm (Figure
4). There was apparently a balanced carbon budget in the control mesocosm but
a negative carbon balance (grazing exceeded primary production) in the enriched
mesocosm.
Discussion
The two sampling periods dominated by either nauplii or copepodites in the
mesocosms were representations of the expected developmental succession that
might occur in situ where the main mesozooplankton species have only one
generation per year. In the present study, total mesozooplankton biomass
increased by up to two orders of magnitude from the nauplii- to the copepodite
V-dominated systems. A succession also took place within the phytoplankton
where a bloom of diatoms prevailed during the first (bloom) sampling period, and
small-celled flagellates during the second (post-bloom) period. The exact same
scenario within phytoplankton was observed in parrallel in the fjord outside the
mesocosms (Hygum et al., 2000a).
Copepod grazing measurements
Three different methodologies were used to estimate the grazing by copepods
(Figure 3 and Table III). Two of them, gut fluorescence and chlorophyll clearance, take only phytoplankton grazing into account. This is too simplistic (Penry
and Frost, 1990), since copepods probably select prey according to size rather
581
B.W.Hansen et al.
than type if the prey motility is limited (Tiselius, 1989; Hansen et al., 1994), so
that small heterotrophs are also consumed. We also know that chlorophyll, once
ingested, will be degradated to colourless products to a certain extent, rendering
an underestimate of ingestion rate [e.g. (Head and Harris, 1996)]. Therefore, it
could be argued that it is more appropriate to use the growth method to calculate ingestion, since it is an integrative method taking total food availability into
account. There was reasonable agreement between ingestion rates obtained for
the chlorophyll clearance and the growth methods for the nauplii, but large differences for estimates using the three different methods for the copepodites. Generally, the chlorophyll clearance method gave the lowest values, followed by the gut
fluorescence method, and the growth method gave values five times higher for
the control and three times higher for the enriched mesocosms compared with
the gut fluorescence method. This indicates non-phytoplankton food sources.
The differences are much higher than reported in comparable studies elsewhere
(Kiørboe et al., 1985b; Head, 1986), but the range of individual specific grazing
rates published in the literature is quite large (Table IV) and our values fall within
it, especially for the results obtained using the gut fluorescense method.
The observed growth rates, based on individual carbon increment (Hygum
et al., 2000a,b), and the measured grazing rates in the present study, are reasonably comparable. Mean carbon growth efficiency based on phytoplankton food,
however, was twice as high as reported elsewhere (Corner et al., 1967; Kiørboe
et al., 1985a; Hansen et al., 1997). In view of the differences in results obtained with
the different methods, and although not statistically different, we consider it
acceptable since several methodologies were implied and the results, even if twice
as high, will not violate the overall conclusion (Figure 4). Therefore we feel confident about using the mean grazing data in the carbon budget models (see later).
Comparison of nauplii- and copepodite-dominated food webs
Due to the similarity in standing stocks and production of the various heterotrophic planktonic organisms in the control and the enriched mesocosm, it seems
likely that the nauplii, despite their relatively high natural abundance, which were
in the high end of in situ observed abundances {1–10 l–1 [Barents Sea] (Melle and
Skjoldal, 1989); <2 l–1 [North Sea] (Nielsen and Richardson, 1989); 0.2–0.5 l–1
[Balsfjord] (Barthel, 1995); up to 7 l–1 [Hylsfjord] Andersen and Nielsen, unpublished)}, were not capable of controlling the biomass of organisms at lower
trophic levels. However, the species-rich standing stock of protozooplankton had
a much greater grazing impact than the nauplii. Despite potential uncertainties
and errors concerning all the methods applied, inherent in all comparative interdiciplinary studies, we conclude that for each nauplii-dominated mesocosm there
was a positive carbon balance allowing build-up of phytoplankton biomass and
subsequent sedimentation.
If the experiments had been performed with the same naupliar biomass as that
for copepodites during the copepodite-dominated period, however, grazing by
nauplii would probably have exceeded that of the protozoans and even growth
by the phytoplankton.
582
laboratory
mesocosm
mesocosm
in situ
in situ
bottle
bottle
mesocosm
bottle
bottle
in situ
in situ
C.helgolanducus NIII-IV
C.finmarchicus CV
C.finmarchicus CV
C.finmarchicus CV
C.finmarchicus CV
C.finmarchicus CIV
C.finmarchicus CIV-V
C.finmarchicus females
C.finmarchicus females
C.hyperboreus CIV-V
C.hyperboreus females
Calanus spp. CV
nd = no data.
Experiment
Species
and stage
clearance
clearance
gut fluor
gut fluor
gut fluor
gut fluor
clearance
clearance
4 methods
gut fluoro
gut fluoro
gut fluoro
Method
0.74
2.5
3.6–10.6
nd
nd
15.8–25.3
21 ± 10
nd
7.6–9.6
6.1–33.4
348–674
10.6–373.4
Grazing
µg C ind–1
185
1
3–4
0.5–16.8
10
nd
36
22–25
8–10
2.2–12.4
10–19
2.6–92.3
Daily ration
% of body carbon
(Rey et al., 2000)
present study
present study
(Tande and Båmstedt, 1987)
(Båmstedt et al., 1991)
(Hansen et al., 1990b)
(Hansen et al., 1994)
(Nejstgaard et al., 1997)
(Kiørboe et al., 1985b)
(Huntley et al., 1987)
(Nielsen and Hansen, 1995)
(Hansen et al., 1990a)
Reference
Table IV. A selection of data of specific maximum grazing by Calanus spp. CIV–adult measured by chlorophyll clearance or gut fluorescence grazing methods
on relevant algal food
Food web interactions in a pelagic ecosystem
583
B.W.Hansen et al.
For the copepodite-dominated mesocosms, the abundances of CV were high
compared with reported in situ values. Actual densities in upper water strata from
selected literature do sometimes show high abundances of Calanus copepodites:
0.5–0.7 l–1 [Skagerrak (Peterson et al., 1991)], >2 l–1 [Barents Sea (Pedersen et al.,
1995); 0.5–8 l–1 [Saudafjorden (Kaartved, 1996)]; 3 l–1 [Hylsfjord (Andersen and
Nielsen, unpublished)]. The variability in observed copepod biomass is a general
problem in mesocosms [e.g. (Keller et al., 1999)] and is probably due to inadequate sampling techniques [see discussion in (Hansen et al., submitted)]. In the
present study, we do not consider the two samplings of copepodites as appropriate for estimating biomass and growth, but we use it as a level for biomass and
apply a within-stage growth rate determined for copepodite stage V from Hygum
et al. (Hygum et al., 2000a). However, for the purpose of evaluating principles for
structuring effects within constructed food webs, we feel confident with our
experimental set-up.
The relative grazing impacts of protozooplankton and copepodites in the copepodite-dominated mesocosms were the inverse of the pattern seen in the naupliidominated mesocosms. There was a negative carbon balance in the enriched
mesocosm and most likely, significant grazing on the protozooans [e.g. (Barthel,
1988; Ohman and Runge, 1994)]. Grazing on protozoans was indicated by the fact
that they had a very low biomass despite a high specific production rate. As the
phytoplankton was dominated by small cells (Phaeocystis pouchetii sp. 4.5 µm
diameter), it was not available for the large-celled heterotrophic thecate dinoflagellates, which were virtually absent. These organisms prefer to catch larger
particles such as diatoms (Hansen, 1991; Tiselius and Keylenstierne, 1996;
Buskey, 1997). The protozooplankton community was reduced in complexity and
was composed more or less entirely of athecate dinoflagellates of <30 µm. This
protozooplankton composition presumably resulted from the prevailing phytoplankton composition (nano-size fraction) and in addition, suggests that the
copepod prey selection was towards, for example, naked ciliates as observed by
Jonsson and Tiselius (Jonsson and Tiselius, 1990) and by Ohman and Runge
(Ohman and Runge, 1994).
The copepodite-dominated mesocosms were several weeks (7–8) old and probably had high levels of detritus, as suggested by high POC levels. High detritus
concentrations were presumably due to heavy sedimentation of the diatom-dominated phytoplankton during the period when grazer demands were much lower
than primary production, e.g. during our nauplii-dominated period, heavy aggregation of the post-bloom mucous-rich nanoflagellate phytoplankton, and sedimentation of large faecal pellets during the copepodite-dominated period
(Wassmann, 1998). The same observation has been reported for cold-water mesocosms (Keller et al., 1999). Detritus could have been a potential food source for
the copepodites [e.g. (Roman, 1984)]. The copepodites grazed, and probably
limited the growth of primarily large-celled phytoplankton. However, the food
requirement for the copepodites must have included protozoans and detritus in
order to explain the constant, low level phytoplankton biomass, and to fulfill their
growth and metabolic requirements.
According to Wassmann [(Wassmann, 1998) Figure 7], it is possible to construct
584
Food web interactions in a pelagic ecosystem
‘schematic presentations of the influence of various zooplankton trophic impact
on recycling and export of phytoplankton with respect to meso-zooplankton as
the governing factor upon the primary producers’. Our nauplii-dominated mesocosms followed Wassmann’s carbon flow type A ‘low meso-zooplankton biomass’
system. In his example, the fate of the primary production was predicted as
follows: mesozooplankton grazing 10%, microzooplankton grazing 40%, aggregation plus faecal pellet production (which is recycled matter) 53%. In our study,
it appeared that during the nauplii-dominated period, mesozooplankton grazing
accounted for 20%, microzooplankton grazing for 55–60% and aggregation and
pellet production for 4–11%, if we assume that no carbon was recycled. Our copepodite-dominated mesocosm followed Wassmann’s type B ‘high meso-zooplankton biomass: herbivory’ system. In his example, meso-zooplankton grazing
accounted for 70%, micro-zooplankton grazing for 20%, and aggregation and
faecal pellet production for 33%. In our case, mesozooplankton accounted for
95–105% of the primary production, microzooplankton, 9–11% and aggregation
and faecal pellet production for 6–10% if no carbon was recycled. Thus, the
grazer food chains in our two simple mesocosm systems actually operated in
accordance with Wassmann’s model predictions (Wassmann, 1988).
Acknowledgements
We want to thank F.L.Fotel and M.Martinussen for technical assistance and
G.T.Banta for linguistic correction. The study was supported by European
Community (DG XII) contract no. MAS3-CT95-0039 (T.A.S.C.) and TMR
(Training and Mobility of Researchers) Programme from The European
Commission Contract no. ERBFMGECT 950013.
References
Andersen,P. (1988) The quantitative importance of the ‘microbial loop’ in the marine pelagic: a case
study from the North Bering/Chukchi Sea. Arch. Hydrobiol., 31, 243–251.
Båmstedt,U., Eilertsen,H.C., Tande,K.S., Slagstad,D. and Skjoldal,H.R. (1991) Copepod grazing and
its potential impact on the phytoplankton development in the Barents Sea. Polar Res., 10, 339–353.
Barthel,KG. (1988) Feeding of three Calanus species on different phytoplankton assemblages in the
Greenland Sea. Meeresforsch., 32, 92–106.
Barthel,KG. (1995) Zooplankton dynamics in Balsfjorden, northern Norway. In Skjoldal,H.R.,
Hopkins,C., Erikstad,K.E. and Leinaas,H.P. (eds), Ecology of Fjords and Coastal Waters. Elsevier
Science B.V. Amsterdam, pp. 113–126.
Berggreen,U., Hansen,B. and Kiørboe,T. (1988) Food size spectra, ingestion and growth of the
copepod Acartia tonsa during development: implications for determination of copepod production.
Mar. Biol., 99, 341–352.
Bjørnsen,P.K., Riemann,B., Horsted,S.J., Nielsen,T.G. and Pock-Sten,J. (1988) Trophic interactions
between heterotrophic nanoflagellates and bacterioplankton in manipulated seawater enclosures.
Limnol. Oceanogr., 3, 409–420.
Buskey,E.J. (1997) Behavioural components of feeding selectivity of the heterotrophic dinoflagellate
Protoperidinium pellucidum. Mar. Ecol. Prog. Ser., 153, 77–89.
Carrick,H.J., Fahnstiel,G.L. and Taylor,W.D. (1992) Growth and production of planktonic protozoa
in Lake Michigan: In situ versus in vitro comparisons and importance to food web dynamics.
Limnol. Oceanogr., 37, 1221–1235.
Corner,E.D.S., Cowey,C.B. and Marshall,S.M. (1967) On the nutrition and metabolism of zooplankton V. Feeding efficiency of Calanus finmarchicus. J. Mar. Biol. Assoc. UK, 47, 259–270.
585
B.W.Hansen et al.
Edler,L. (1979) Recommendations for marine biological studies in the Baltic sea. The Baltic Marine
Biologists Publ., 5, 1–38.
Fenchel,T. (1982) Ecology of heterotrophic microflagellates. II. Bioenergetics and growth. Mar. Ecol.
Prog. Ser., 8, 225–231.
Fernandez,F. (1979) Particle selection in the nauplius of Calanus pacificus. J. Plankton Res., 1,
313–328.
Frost,B.W. (1972) Effects of size and concentration of food particles of the feeding behaviour of the
marine planktonic copepod Calanus pacificus. Limnol. Oceanogr., 17, 805–815.
Gifford,D.J. (1991) The protozoan-metazoan trophic link in pelagic ecosystems. J. Protozool., 38,
81–86.
Gislason,A. and Astthorsson,O.S. (1998) Seasonal variations in biomass, abundance and composition
of zooplankton in the subarctic waters north of Iceland. Polar Biol., 20, 85–94.
Hansen,B., Berggreen,U.C., Tande,K.S. and Eilertsen,H.C. (1990a) Post-bloom grazing by Calanus
glacialis, C.finmarchicus and C.hyperboreus in the region of the Polar Front, Barents Sea. Mar.
Biol., 104, 5–14.
Hansen,B., Tande,K.S. and Berggreen,U.C. (1990b) On the trophic fate of Phaeocystis pouchetii
(Hariot). III. functional responses in grazing demonstrated on juvenile stages of Calanus finmarchicus (Copepoda) fed diatoms and Phaeocystis. J. Plankton Res., 12, 1173–1187.
Hansen,B., Hansen,P.J. and Bjørnsen,P.K. (1994) The size ratio between planktonic predators and
their prey. Limnol. Oceanogr., 39, 395–403.
Hansen,B., Verity,P., Falkenhaug,T., Tande,K.S. and Norrbin,F. (1994) On the trophic fate of Phaeocystis pouchetii (Hariot). V. Trophic relationships between Phaeocystis and zooplankton: an assessment of methods and size dependence. J. Plankton Res., 16, 487–511.
Hansen,B., Christiansen,S. and Pedersen,G. (1996) Plankton dynamics in the marginal ice zone of the
central Barents Sea during spring: carbon flow and structure of the grazer food chain. Polar Biol.,
16, 115–128.
Hansen,B.W., Nielsen,T.G. and Levinsen,H. (1999) Plankton community structure and carbon cycling
on the western coast of Greenland during the stratified summer situation. III. Mesozooplankton.
Aquat. Microb. Ecol., 16, 233–249.
Hansen,B.W., Hygum,B.H., Rey,C., Marker,T, Andreassen,P. and Pedersen,L.W. (submitted)
Mesocosms as a tool for autecology and systems ecology studies of Calanus finmarchicus—an
assessment of methods. ICES J. Mar. Sci.
Hansen,P.J. (1991) Quantitative importance and trophic role of heterotrophic dinoflagellates in a
coastal pelagial food web. Mar. Ecol. Prog. Ser., 73, 253–261.
Hansen,P.J., Bjørnsen,P.K. and Hansen,B.W. (1997) Zooplankton grazing and growth: scaling within
the 2–2,000 µm body size range. Limnol. Oceanogr., 42, 687–704.
Head,E.J.H. (1986) Estimation of Arctic copepod grazing rates in vivo and comparison with in vitro
methods. Mar. Biol., 92, 371–379.
Head,E.J.H. and Harris,L.R. (1996) Chlorophyll destruction by Calanus spp. grazing on phytoplankton: kinetics, effects of ingestion rate and feeding history, and a mechanistic interpretation.
Mar. Ecol. Prog. Ser., 135, 223–235.
Huntley,M., Tande,K. and Eilertsen,H.C. (1987) On the trophic fate of Phaeocystis pouchetii (Hariot).
II. Grazing rates of Calanus hyperboreus (Krøyer) on diatoms and different size categories of
Phaeocystis pouchetii. J. Exp. Mar. Biol. Ecol., 110, 197–212.
Hygum,B.H., Rey,C., Hansen,B.W. and Tande,K.S. (2000a) Importance of food quantity to structural
growth rate and neutral lipid reserves accumulated in Calanus finmarchicus (Gunnerus). Mar. Biol.,
in press.
Hygum,B.H., Rey,C. and Hansen,B.W. (2000b) Growth and development rates of Calanus finmarchicus (Gunnerus) nauplii during a diatom spring bloom, in press.
Jespersen,A.M. and Christoffersen,K. (1987) Measuring chlorophyll-a from phytoplankton using
ethanol as extraction solvent. Arch. Hydrobiol., 109, 445–454.
Jonsson,P.R. and Tiselius,P. (1990) Feeding behaviour, prey detection and capture efficiency of the
copepod Acartia tonsa feeding on planktonic ciliates. Mar. Ecol. Prog. Ser., 60, 35–44.
Kaartved,S. (1996) Habitat preference during overwintering and timing of seasonal vertical migration
of Calanus finmarchicus. Ophelia., 44, 145–156.
Keller,A.A., Candace,A.O, Walker,H.A. and Hawk,J.D. (1999) Predicted impacts of elevated temperature on the magnitude of the winter-spring phytoplankton bloom in temperate coastal waters: A
mesocosm study. Limnol. Oceanogr., 44, 344–356.
Kiørboe,T. and Nielsen,T.G. (1994) Regulation of zooplankton biomass and production in a
temperate, coastal ecosystem. 1. Copepods. Limnol. Oceanogr., 39, 493–507.
Kiørboe,T., Møhlenberg,F. and Hamburger,K. (1985a) Bioenergetics of the planktonic copepod
586
Food web interactions in a pelagic ecosystem
Acartia tonsa: relations between feeding, egg production and respiration, and composition of
specific dynamic action. Mar. Ecol. Prog. Ser., 26, 85–97.
Kiørboe,T., Møhlenberg,F. and Riisgaard,H.U. (1985b) In situ feeding rates of planktonic copepods:
a comparison of four methods. J. Exp. Mar. Biol. Ecol., 88, 67–81.
MacLellan,D.C. (1967) The annual cycle of certain calanoid species in West Greenland. Can. J. Zool.,
45, 101–115.
Melle,W. and Skjoldal,H.R. (1989) Zooplankton reproduction in the Barents Sea: vertical distribution
of eggs and nauplii of Calanus finmarchicus in relation to spring phytoplankton development. In
Rydland,J.S. and Tyler,P.A. (eds), Reproduction, Genetics and Distribution of Marine Organisms.
Proceedings of the 23rd European Marine Biology Symposium. Olsen & Olsen, Frederiksberg,
Denmark, pp. 137–148.
Melle,W. and Skjoldal,H.R. (1998) Reproduction and development of Calanus finmarchicus, C.
glacialis and C.hyperboreus in the Barents Sea. Mar. Ecol. Prog. Ser., 169, 211–228.
Nejstgaard,J.C., Gismervik,I. and Solberg,P.T. (1997) Feeding and reproduction by Calanus
finmarchicus, and microzooplankton grazing during mesocosm blooms of diatoms and the coccolithophore Emiliania huxleyi. Mar. Ecol. Prog. Ser., 147, 197–217.
Nielsen,T.G. and Hansen,B. (1995) Plankton community structure and carbon cycling on the western
coast of Greenland during and after the sedimentation of a diatom bloom. Mar. Ecol. Prog. Ser.,
125, 239–257.
Nielsen,T.G. and Kiørboe,T. (1994) Regulation of zooplankton biomass and production in a
temperate, coastal ecosystem, 2. Ciliates. Limnol. 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. Ser., 56, 75–87.
Nielsen,T.G., Løkkegaard,B., Richardson,K., Pedersen,F.B. and Hansen,L. (1993) Structure of
plankton communities in the Dogger Bank area (North Sea) during a stratified situation. Mar. Ecol.
Prog. Ser., 95, 115–131.
Ohmann,M.D. and Runge, J.A. (1994) Sustained fecundity when phytoplankton resources are in short
supply: Omnivory by Calanus finmarchicus in the Gulf of St. Lawrence. Limnol. Oceanogr., 39,
21–36.
Pedersen,G., Tande,K.S. and Nielssen,E.M. (1995) Temporal and regional variation in the copepod
community in the central Barents Sea during spring and early summer 1988 and 1989. J. Plankton
Res., 17, 263–282.
Penry,D.L. and Frost,B.W. (1990) Re-evaluation of the gut-fullness (gut fluorescence) method for
inferring ingestion rates of suspension-feeding copepods. Limnol. Oceanogr., 35, 1207–1214.
Peterson,W.T., Tiselius,P. and Kiørboe,T. (1991) Copepod egg production, moulting and growth rates,
and secondary production, in the Skagerrak in August 1988. J. Plankton Res., 13, 131–154.
Porter,K.G. and Feig,Y.S. (1980) The use of DAPI for identifying and counting aquatic microflora.
Limnol. Oceanogr., 25, 943–948.
Poulet,S.A. (1977) Grazing of marine copepod developmental stages on naturally occurring particles.
J. Fish. Res. Board Can., 34, 2381–2387.
Rey,C., Harris,R., Irigoin,X., Head,R. and Carlotti,F. (2000) Influence of algal diet on growth and
ingestion of Calanus helgolandicus nauplii. Mar. Ecol. Prog. Ser., in press.
Riemann,B., Sørensen,H.M., Bjørnsen,P.K., Horsted,S.J., Jensen,L.M., Nielsen,T.G. and Søndergaard,M. (1990) Carbon budgets of the microbial food web in estuarine enclosures. Mar. Ecol. Prog.
Ser., 65, 159–170.
Roman,M. (1984) Utilisation of detritus by the copepod Acartia tonsa. Limnol. Oceanogr., 29,
949–959.
Sanders,R.W. and Wickham,S.A. (1993) Planktonic protozoa and metazoa: predation, food quality
and population control. Mar. Microb. Food Webs, 7, 197–223.
Servais,P. (1995) Measurements of the incorporation rates of four amino acids into proteins for estimating bacterial production. Microb. Ecol., 29, 115–128.
Simon,M. and Azam,F. (1989) Protein content and protein synthesis rates of planktonic marine
bacteria. Mar. Ecol. Prog. Ser., 51, 201–213.
Smith,D.C. and Azam,F. (1992) A simple, economical method for measuring bacterial protein
synthesis rates in seawater. Mar. Microb. Food Webs, 6, 107–114.
Stoecker,D.K. and Capuzzo,J.M. (1990) Predation on protozoa: its importance to zooplankton. J.
Plankton Res., 12, 891–908.
Strathmann,R.R. (1967) Estimating the organic carbon content of phytoplankton from cell volume
or plasma volume. Limnol. Oceanogr., 12, 411–418.
Strickland,J.D.H. and Parsons,T.R. (1972) A practical handbook of seawater analysis. Bull. Fish.
Board Can., 167, 1–310.
587
B.W.Hansen et al.
Tande,K.S. (1982) Ecological investigations on the zooplankton community of Balsfjorden, Northern
Norway: generation cycles, and variations in body weight and body content of carbon and nitrogen
related to overwintering and reproduction in the copepod Calanus finmarchicus (Gunnerus). J.
Exp. Mar. Biol. Ecol., 62, 129–142.
Tande,K.S. (1991) Calanus in North Norwegian fjords and in the Barents Sea. Polar Res., 10, 389–408.
Tande,K.S. and Båmstedt,U. (1987) On the trophic fate of Phaeocystis pouchetii. I. Copepod feeding
rates on solitary cells and colonies of P.pouchetii. Sarsia, 72, 313–320.
Tiselius,P. (1989) Contribution of aloricate ciliates to the diet of Acartia clausi and Centropages
hamatus in coastal waters. Mar. Ecol. Prog. Ser., 56, 49–56.
Tiselius,P. and Keylenstierne,M. (1996) Growth and decline of a diatom spring bloom: phytoplankton
species composition, formation of marine snow and the role of heterotrophic dinoflagellates. J.
Plankton Res., 18, 133–155.
Wassmann,P. (1998) Retention versus export food chains: processes controlling sinking loss from
marine pelagic systems. Hydrobiologia, 363, 29–57.
Wassmann,P., Egge,J.K., Reighstad,M. and Aksnes,D. (1996) Influence of dissolved silicate on
vertical flux of particulate biogenic matter. Mar. Pol. Bull., 33, 10–21.
Received on June 8, 1999; accepted on October 7, 1999
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