Download Autotrophic and heterotrophic nanoplankton in the diet of the

Journal of Plankton Research Vol.19 no.7 pp.877-890, 1997
Autotrophic and heterotrophic nanoplankton in the diet of the
estuarine copepods Eurytemora affinis and Acartia bifilosa
Ste"phane Gasparini and Jacques Castel*
Laboratoire d'Odanographie Biologique, Universiti Bordeaux I, CNRS-URA
197, F-33120 Arcachon, France
t Deceased
Abstract. The ingestion of autotrophic and heterotrophic nanoplankton by two estuarine copepods,
Eurytemora affinis and Acartia bifilosa, was measured in various environmental conditions using the
incubation method and epifluorescence microscopy. Egg production of the species was also determined in order to estimate their carbon requirements. Assuming a gross efficiency of egg production
of 03, nanoplanktonic carbon ingested always met the carbon requirements suggesting that, most of
the time, other carbon sources could be unnecessary. Nanoplankton ingestion by A.bifilosa (from 128
to 1693 cells ind.~' h~') was dominated by autotrophic forms (60-97%) and was seriously affected by
high (>100 mg H) suspended particulate matter (SPM) concentrations. Nanoplankton ingestion by
E.affinis (from 300 to 1049 cells ind."1 h~') was relatively stable in comparison, but this latter species
seemed to switch its grazing pressure from autotrophic to heterotrophic forms when SPM concentrations increased. Thus, two copepod species, living in the same estuary, presented two different
feeding behaviours, probably to maximize energy input per unit of energy expenditure. Such differences could contribute to the spatial and seasonal segregation of these species which is usually
observed.
Introduction
Historically, the dominant view in zooplankton ecology has been that ingestion,
growth and fecundity of suspension-feeding copepods are governed by phytoplankton availability. Therefore, copepod herbivory has been largely investigated
(reviewed in Frost, 1980). More recently, numerous species have been thought to
be omnivorous (Carrick et aL, 1991; Ohman and Runge, 1994) and suggestions
have been repeatedly made that heterotrophic protists could provide a major
portion of the total nutrition, as well as much of the energy for growth and reproduction (Gifford and Dagg, 1988; Stoecker and Capuzzo, 1990). If protozoans are
effectively preyed upon by mesozooplankton, the nature of energy transfer in the
pelagic food web could be different or more complex than previously thought
(see Legendre and Rassoulzadegan, 1995). Additionally, diversity in mesozooplankton diets may introduce nutritional variability and, in turn, affect processes
such as growth and egg production (Kleppel et aL, 1991). Subsequently, the relative role of autotrophic and heterotrophic resources in the diet of planktonic crustaceans appears to be important in helping to understand the dynamics of pelagic
ecosystems.
Little is known, however, about the composition of the natural diets of most
copepods, and about the relative importance of autotrophic and heterotrophic
prey. Evidence from laboratory experiments, such as a higher clearance rate for
ciliates than for phytoplankton in Acartia tonsa (Stoecker and Egloff, 1987),
cannot be accurately extrapolated to the field where naturally occurring prey
assemblages are definitely more complex. Additionally, attempts to describe
© Oxford University Press
877
S.Gasparini and J.Castel
mesozooplankton diets in situ have frequently involved gut pigment content
determination (Mackas and Bohrer, 1976; Swadling and Marcus, 1994), providing little or no indication of the importance of the heterotrophic dietary component (but see Kleppel et al, 1988).
In turbid estuaries, several copepods are already known to be omnivorous.
Euryternora ajfinis, for instance, can ingest ciliates (Berk et al, 1977) or detritus
(Heinle et al., 1977) as well as algae. However, information about the relative
contribution of the different food sources to in situ ingestion and to natural
growth is limited. Part of this scarcity stems from the large amount of terrestrial
inert particles in estuarine waters which renders it difficult to apply most of the
methods used in other aquatic environments. In the Gironde estuary, suspended
particulate matter (SPM) is mainly composed of silt (Castaing et al, 1984). SPM
concentrations often exceed 500 mg I"1 at the water surface and 1 g I"1 near the
bottom. By comparison, chlorophyll (Chi) concentrations rarely exceed 10-20 u.g
H (Irigoien and Castel, 1996). Because of the high SPM concentration, which
induces light limitation, the primary production in such an environment is often
very low and contrasts with the high densities of copepods (Castel, 1981). These
observations highlight the question of the relative role of heterotrophic food since
the primary production is probably not sufficient to sustain the secondary production (Heinle and Flemer, 1975; Castel and Feurtet, 1989).
Copepods can consume prey ranging in size from 5 to 200 u.m. In general, they
retain the largest particles more efficiently than the smallest ones (Frost, 1972;
Price et al., 1983). However, in estuaries, and especially in the Gironde, the largest
particles (>20 u.m) are scarce compared to the large amount of smaller particles
(Castaing et al., 1984). In such conditions, it has been demonstrated by Richman
et al (1977) that estuarine copepods graze predominantly on nanoplanktonic size
prey (5-20 u.m), probably because they shift their grazing pressure to the size
where the peak concentration of the particles occurs (Poulet, 1973,1974).
Thus, the aim of this study was to quantify the in situ ingestion of autotrophic
and heterotrophic nanoplankton by the dominant copepod species of the
Gironde estuary (E.ajfinis and Acartia bifilosa). It was also examined whether (i)
the ingestion of one or the other of these prey groups is sufficient, (ii) both are
necessary or (iii) another food source (non-living particles, larger prey) has to be
included to sustain the production which was measured by the fecundity. This
investigation was conducted taking into account the environmental factors which
could influence copepod ingestion.
Method
Sampling and experiments were carried out once a month from April to
November 1995 at two stations of the Gironde estuary (Figure 1). Station F was
located in the downstream area of the estuary where A.bifilosa is generally the
dominant species, whereas station E was located in the middle part of the
estuary where E.affinis is the most abundant. All samples were taken 0.5 m
below the surface.
Temperature and salinity were measured using a conductivity-temperature
878
NanopUnkton in the diet of E.affinis and A.bifilosa
°40'W
Br*ud »t
St Louis
Pk30
10km
Bardvaax
Rg. 1. Map of the Gironde estuary (SW France) showing the sampling stations.
879
S.Gasparini and J.Caste)
system YSI 33, and oxygen concentrations were obtained with an Orbisphere
Model 2609 oxymeter. SPM water content was determined as dry weight (60°C,
24 h) after filtration of 100-250 ml of water through 47 mm Whatman GF/C filters.
For ingestion experiments, copepods were collected using a standard WP2
plankton net (200 |im mesh size). Nine glass bottles were filled with 100 ml of
natural filtered (63 ^m) estuarine water and -30 adults of the dominant copepod
species (E.affinis or A.bifilosa) were gently pipetted and distributed into three of
them (final density 10 adults per 100 ml, mainly females). Three bottles without
copepods werefixedimmediately, whereas the other bottles (three with copepods
and three controls) were incubated in a tank for 24 h under natural conditions of
temperature and light, corresponding to the sampling depth. Nothing was added
to the control bottles to compensate for copepod excretion as it was assumed to
be negligible compared to nutrient concentrations of the water (N = 100 JJLM; P
= 2-5 p,M; Irigoien and Castel, 1996). Samples were preserved with 1%
glutaraldehyde and 0.1% paraformaldehyde (final concentrations) and stored in
the dark at 4°C (Lovejoy et aL, 1993).
When back in the laboratory, the nanoplankton were enumerated in each
bottle. The sample was gently mixed by inversion and left to stain for 15 min with
the fluorochrome 4'-6-diamidino-2-phenylindole (DAPI; final concentration of
0.1 jig ml"1). Three to ten millilitre quantities (depending on SPM concentration)
were carefully filtered through 25 mm diameter, 5 jxm pore size, translucent
isopore membranes at a vacuum of <5 mmHg. Then, the membranes were
mounted on a glass slide and examined by epifluorescence microscopy with a UV
excitation filter block and 1000X oil immersion. Using this procedure, it was possible to locate and differentiate the nanozooplankton from the nanophytoplankton by visualizing the DAPI-stained nuclei (blue) and the Chi a autofluorescence
(red). Translucent membranes were preferred to black ones because they allowed
organisms to be identified in the most turbid samples by alternating epifluorescence and transmission microscopy. The 5 p,m pore size was chosen as it allowed
an important part of suspended mineral particles to go through and because it
was not our purpose to count bacteria.
The number of cells per unit volume was calculated according to Sherr and
Sherr (1983) by multiplying the average number of cells per microscope field by
the number offieldsper membrane, and dividing the result by the volume filtered.
For each slide, at least 100 fields were examined, and between 30 and 130 cells
per 100 fields were usually counted.
Finally, nanoplankton ingestion rates of copepods were calculated as the
number of cells ingested per individual and per hour using the equations of Frost
(1972). These ingestion rates were converted to terms of carbon using the mean
volume of 30 cells and a conversion factor of 0.15 g C ml"1 (Carrick et aL, 1991).
The carbon requirement (Cr) of adult copepods can be estimated by the egg
production rate, using the equation Cr = (F X Ce)IKi (Peterson et aL, 1990),
where Fis the egg production rate (eggs female"1 day"1), Ce is the carbon content
of an egg and Ki is the gross efficiency of egg production.
The egg production rates were estimated using the method of Kimmerer (1984).
Approximately 100 adults from the same haul as for ingestion experiments were
880
NaDopbnkton in the dkt of Kajfinls and A.bifilosa
pipetted and placed in 5 1 incubation bottles filled with natural filtered (63 \ira)
water. Three replicates were incubated for 24 h at in situ temperature. Concerning
experiments conducted with E.affinis, which is an egg-carrying species, eggs were
introduced with females at the beginning of the incubation. Therefore, subsamples
were taken andfixedwith 5% formalin at the beginning and at the end of the incubation. From each subsample, the number of females and the total number of eggs
and nauplii were counted (only females appearing intact were taken into account).
The egg production rate was calculated from the change in the mean number of
eggs per female against time, considering nauplii as eggs and assuming that the egg
production rate remains linear during the experiment. Concerning experiments
conducted with A.bifilosz, which is a free-spawning species, there were no eggs at
the beginning of the incubation. In this case, the egg production rate was calculated
from the total number of eggs and nauplii collected at the end of the incubation,
divided by the number of females and by the duration of the experiment.
For each experiment, the carbon content was estimated from the mean volume
of 30 eggs and applying a carbon to volume conversion factor of 0.14 g C ml"1
(Ki0rboeefa/.,1985).
The gross efficiency of egg production for estuarine copepods is variable,
between 0.09 and 0.18 (Heinle et ai, 1977) for E.affinis and 0.49 (Ki0rboe et al,
1985) for A.tonsa (no data are available for A.bifilosa). A mean value of 0.30 was
assumed for the calculation, but the consequences of another choice will be discussed.
Results
Results of nanoplankton ingestion experiments are summarized in Table I. There
was a significant ingestion of nanophytoplankton (Student's f-test, HO: prey
number in control bottles = prey number in copepod bottles) for all experiments
with E.affinis and for 5/8 of the experiments with A.bifilosa. Nanozooplankton
were less often significantly ingested: 3/8 with E.affinis and 1/8 with A.bifilosa.
Thus, even if nanophytoplankton seem to be more frequently ingested than
nanozooplankton, both autotrophic and heterotrophic nanoplankton can be
included in the natural diet of these copepods, at least in some circumstances.
For A.bifilosa, the ingestion of total nanoplankton (autotrophic + heterotrophic) varied seasonally (Table I) with a maximum in June (1693 ± 213 cells
ind."1 h"1). This period usually corresponds to the maximum development rate of
this species (Castel, 1993). Most of the variability was due to changes in nanophytoplankton ingestion, whereas in comparison nanozooplankton ingestion alone
remained relatively low and stable (June excepted). Moreover, nanophytoplankton ingestion by A.bifilosa was higher than nanozooplankton ingestion in most of
the experiments (significantly for 4/8).
For E.affinis, the ingestion rate of total nanoplankton did not vary significantly
between experiments: only the value obtained in July (300 ± 86 cells ind.-1 h"1)
was significantly different from the others (between 1049 ± 90 and 876 ± 65 cells
indr1 h"1). Conversely, nanophytoplankton ingestion or nanozooplankton ingestion alone were clearly more variable, with changes depending on stations (in
881
S.GaspaiinJ and J.Castel
Table L Ingestion of nanophytoplankton and of nanozooplankton by the dominant copepod species
of the Gironde estuary. Values correspond to means ± SE
Species
Date
Eurytemora 11/04
12/04
affinis
23/05
07/06
05/07
15/11
Acartia
bifilosa
22/05
06/06
04/07
19/09
20/09
17/10
18/10
14/11
Station
F
E
E
E
E
E
F
F
F
F
E
F
E
F
Heterotrophic
cells ingested
(cells indr'h- 1 )
Significance
level
±79
±17
±122
±47
±35
±44
55 ±11
694 ± 157
712 ± 298
67 ±35
100 ±51
628 ± 21
*
•
323 ±56
1015 ±145
730 ±47
172 ±94
196 ±103
902 ± 26
132 ±66
95 ±31
9±9
678 ±68
77 ±52
131 ±131
163 ± 55
112 ±60
195 ±98
33 ±18
Autotrophic
Significance
cells ingested
level
(cells indr 1 rr 1 )
994
212
314
824
200
248
*•
*
••
••
• P < 0.05, **P < 0.01, ••*/> < 0.001, HO: prey number in control bottles = prey number in copepod
bottles.
April) as well as on seasons. Nanophytoplankton ingestion was sometimes higher
(significantly in April, station F) and sometimes lower (significantly in November, station E) than nanozooplankton ingestion. This suggests that the composition of E.affinis diet could change in relation to environmental conditions.
Environmental conditions corresponding to ingestion experiments are grouped
in Table II. For both copepod species, no clear relationships have been found
between ingestion rates and the environmental parameters (temperature, prey
concentration) which are classically known to affect ingestion. This lack of
relationships could be due to the dependence of ingestion rate on several of these
factors (or other ones). Furthermore, supposed relationships were not compulsorily linear. Conversely, ingestion rates appeared to be affected by SPM concentration (Figure 2A and B). Maximum nanophytoplankton ingestion rates by
E.affinis corresponded to relatively low SPM concentrations, whereas maximum
nanozooplankton ingestion rates corresponded to higher SPM values (Figure
2A). The results suggest that this copepod shifted its grazing pressure from one
kind of prey to the other when the SPM concentration increased. On the other
hand, maximum ingestion rates by A.bifilosa always corresponded to low (<100
mg I"1) SPM values (Figure 2B), suggesting that ingestion of this latter species
was strongly limited for higher concentrations.
Additional information was obtained by plotting the ratio of autotrophic:total
nanoplankton ingested against the same ratio in the water (Figure 3). Only
experiments where ingestion was significantly different from zero have been
used. The plot shows that the ratio ingested is often significantly above, or very
near, the ratio in the water and never below for both species. This result indicates that nanophytoplankton were eaten in disproportion to their numerical
abundance in the nanoplankton. In other words, the predation pressure exerted
882
Nanoplankton in the diet of Kaflwls and A.blfilosa
TaWe IL Nanoplankton abundances (means ± SE), temperatures (T), salinities (S), oxygen
saturations (O 2 ) and suspended paniculate matter concentrations (SPM) at the begining of
ingestion experiments
Date
Station
Autotrophic
cells (no. mh 1 )
Heterotrophic
cells (no. ml-1)
T
S
(psu)
o2
(%)
SPM
CO
727 ±44
512 ±128
4510 ± 885
3936 ± 588
4223 ±872
1148 ±144
2O5±22
3442 ±226
9021 ±1459
5043 ±668
10661± 603
3451± 266
12.3
14.1
173
20.0
24.5
15.1
8.5
0.8
4.0
5.1
7.2
8.5
_
_
83.7
78.5
82.1
84.0
57
305
410
136
225
252
3936 ± 596
4202 ± 526
4920 ± 376
4510 ± 249
6424 ± 731
3954 ± 609
3826 ±623
348 ± 6 1
2870 ± 241
3219 ± 397
1967 ±161
3075 ±702
8952 ±566
1558 ±177
5125 ±1097
697 ± 9 3
17.5
18.9
22.1
18.3
22.0
18.8
19J
13.5
8.8
11.4
14.9
21.2
8.7
16.1
8.0
14.9
83.9
82.8
82.6
86.6
84.0
80.5
77.7
85.8
94
87
48
78
284
49
374
111
(mgH)
E.affinis
11/04
12/04
23/05
07/06
05/07
15/11
F
E
E
E
E
E
A.bifilosa
22/05
06/06
04/07
19/09
20/09
17/10
18/10
14/11
F
F
F
F
E
F
E
F
on nanophytoplankton was significantly higher than that on nanozooplankton.
Nevertheless, concerning E.affinis, the ratio ingested tended to increase with the
ratio in the water. This could partially explain the relationship with SPM concentration described above since the autotrophictotal nanoplankton ratio in the
water decreased strongly as SPM increased (Figure 4). A similar observation
cannot be made for A.bifilosa.
Finally, carbon requirements to sustain observed egg production (see Method)
were compared with carbon ingestion (Figure 5). Egg production values, ranging
from 0.30 to 5.49 eggs female"1 day 1 for A.bifilosa and from 0.34 to 4.79 eggs
female"1 day"1 for E.affinis, will be detailed in a further paper. For both species,
total nanoplanktonic carbon ingested was always above or very near the carbon
requirement. This suggests that nanoplankton (auto and/or heterotrophic) could
provide an important part of the energetic requirements and that other food
sources could be unnecessary. Concerning E.affinis, ingestion of nanophytoplankton alone was not always sufficient to meet carbon requirement (2/6 significant differences, P < 0.05), whereas total nanoplankton ingestion, including
nanozooplankton, appeared to be always sufficient. On the other hand, nanophytoplankton ingestion by A.bifilosa never differed significantly from the carbon
requirements. The relative importance of nanozooplanktonic cell carbon seems
very low for this latter species. In the only experiment where nanozooplankton
ingestion was significant, ingested carbon exceeded carbon requirement.
Discussion
The results of this study suggest that both copepods A.bifilosa and E.affinis ate
nanophytoplankton when available instead of nanozooplankton. Considering the
883
S.Gasparuri and J.Castel
14W
E. afflnis
1200
i
1000
i
800
•
{
1
•
600
;
400
200
2
s
o
0
I
100
0
100
200
300
400
500
SPM (mg.l"')
Fig- 2. Nanophytoplanlcton (black squares) and nanozooplankton (open circles) ingested by E.affinis
(upper panel) and by A.bifilosa (lower panel) as a function of SPM concentrations (means ± SE).
classical food chain in aquatic environments, a trophic relationship between copepods and phytoplankton is not surprising. However, in estuarine turbid environments such as the Gironde, where phytoplankton resources are in relatively short
supply, and considering that omnivory has been demonstrated for estuarine copepods (Berk et ah, YTI1; Stoecker and Egloff, 1987), the important relative role of
nanophytoplankton in the diet of the studied species was not expected. Furthermore, it can be reasonably supposed that nanophytoplankton were selected from
the total amount of nanoplankton since they were often eaten in disproportion
to their relative abundance in the 5-20 u.m size range.
Nevertheless, nanozooplankton cannot be excluded as a possible complementary or alternative food source. From this point of view, results were substantially
different between the studied species. For A.bifilosa, nanozooplankton ingestion
was rarely important (7/8 values were <200 cells indr 1 h"1) and the only significant value occurred when nanophytoplankton ingestion was also high. Thus,
nanozooplankton sometimes appeared as a complementary food source for this
copepod, but never as its bulk food. On the contrary, E.affinis nanozooplankton
ingestion was important only when nanophytoplankton ingestion was low. This
884
Nanoplankton in the diet otE.aflinis and A.bifilosa
80
100
40
60
Autotrophic : Total nanoplankton in th« water (%)
Autotrophic : Total nanoplankton in the water (%)
Dmo 1
P ™*™ "»««««» by E.affinis (opper p«nel) and by A.bifilosa
e same ratio in the water (mean ± SE).
suggests that E.affinis could use nanozooplankton as an alternative food to compensate for low nanophytoplankton availability, and thereby that nanozooplankton could sometimes be its bulk food if larger (and not investigated) prey were
not ingested at a higher rate. This latter species seems then to present an opportunistic feeding behaviour, eating most available food rather than specific food
Assuming a gross efficiency of egg production of 0.3, the total nanoplanktonic
carbon ingested always met the carbon requirements, thus suggesting that other
carbon sources could be unnecessary. For A.bifilosa, nanophytoplankton alone
seemed to cover the largest part of the energetic requirements during most of the
expenments, whereas nanozooplankton did not. On the contrary, the energetic
requirements of E.affinis were sometimes covered by nanophytoplankton alone
(4/6 of expenments) and sometimes by nanozooplankton alone (2/6 of experiments).
^
However, if the use of another gross efficiency of egg production does not
affect the ratio between autotrophic and heterotrophic nanoplankton ingestion,
885
S.Gasparini and J.Castel
100
100
200
300
400
500
SPM(mg.l 1)
Fig. 4. Ratio of autotrophic:total nanoplankton in the water as a function of SPM concentrations
(means ± SE).
a lower value should make other food sources indispensable. Concerning
E.affinis, the use of the lowest gross efficiency value found in the literature (0.09;
Heinle et al, 1977) reduces the part of carbon requirements covered by nanoplankton ingestion to 74% on average. Then, detritus (Heinle et al, 1977) or
microzooplankton (White and Roman, 1992) could constitute part of the diet of
this copepod, even if nanoplankton remain its bulk food. Moreover, applying the
same minimum gross efficiency to data obtained with A.bifilosa, carbon requirements covered by nanoplankton do not exceed 43% on average. In this case,
other prey than nanoplankton, such as detritus, large ciliates, rotifers or nauplii,
could represent the main source of carbon, even if nanoplankton remain a significant food for this species. Such low values of the gross efficiency of egg production are relatively scarce in the literature and correspond usually to
laboratory experiments with high levels of food. Egg production rates measured
in this study (see Results) were very low compared to values usually reported in
the literature for E.affinis (up to 34 eggs female"1 day-1; Ban, 1994) or for Acartia
sp. (>40 eggs female"1 day"1; Ki0rboe et al., 1985). These observations probably
reflected poor feeding conditions in the Gironde estuary (Burdloff et al, submitted). In such conditions, a generally well-accepted view is that the gross
efficiency of egg production is high (Heinle et aL, 1977). Thus, a gross efficiency
value around 0.3 seems realistic and has been confirmed during preliminary
experiments (unpublished data).
Concerning relationships between nanoplankton ingestion and environmental factors, the type and/or the quantity of ingested nanoplanktonic prey
seems to be linked to SPM concentration, whereas temperature or nanoplankton abundances had no distinguishable influence during experiments. Because
the SPM concentration and nanophytoplankton ratio in the water were closely
related, it cannot be decided whether the SPM impact on ingestion was direct
(hindering prey capture, for instance), indirect (influencing prey availability),
886
Nanopbukton In the diet of E.qflinls and A.bifilosa
0
300
600
900
1200
Carbon requirements (ngC.ind.V)
0
300
600
900
1200
Carbon requirements (ngC.ind/'.d"')
g 5. Nanophytoplanktonic carbon ingested (black squares) and nanophytoplanktonic + nanozooplanktonic carbon ingested (open circles) against carbon requirements to sustain observed e«z production of EMffinis (upper panel) and of A.bifilosa (lower panel). Carbon requirements are defined
from egg production using a gross efficiency of 0.3. Symbols correspond to means ± SE.
or both. Consequently, in the following assumptions, SPM is just used as an indicator of nutritional conditions.
For E.affinis, total nanoplankton ingestion appeared relatively stable, whereas
the ratio of ingested nanophytoplanktonic prey decreased when SPM increased.
Phytoplanktonic prey are usually selected by this copepod for relatively low
(<100 mg/1) SPM concentration (Tackx et al, 1995). Thus, it can be supposed that
the above observation corresponded to a decrease in selection efficiency and that
this species did not significantly reduce or stop feeding when its preferred food
was not available. On the other hand, the proportion of nanophytoplankton in
the diet of A.bifilosa did not show any significant changes as a function of SPM
and remained relatively high. It was the total nanoplankton ingestion (dominated
by autotrophic forms) which seemed to decrease strongly when SPM increased.
We can subsequently suppose that A.bifilosa reduced its ingestion rate rather than
887
S.Gasparini and J.Castel
ingest a lot of 'undesirable' prey by reducing selection. Thus, in the same estuary,
two copepod species present two different feeding behaviours which could correspond to different ways to maximize energy input per unit of energy expenditure.
Such differences in feeding behaviour have already been suggested by Irigoien
et al. (1996) and they proposed E.affinis as a species adapted to highly turbid
environments while A.bifilosa would be food limited. Results obtained in this
study corroborate these assumptions. However, if E.affinis seemed able to maintain ingestion in terms of quantity, this does not mean that the nutritional value
of ingested prey does not change. In fact, there are some indications in the literature of a lower copepod development linked to high SPM concentration (Castel
and Feurtet, 1993; Gasparini et al, submitted). Therefore nanozooplankton,
which seem to be dominant in this case, could have a lower nutritional value than
nanophytoplankton (a lower C:N ratio for instance).
In macrotidal estuaries such as the Gironde, both dominant calanoid copepods
are clearly spatially and seasonally separated. Acartia bifilosa lives in the mesohaline area and is more abundant in summer, whereas E.affinis lives in the oligohaline area with maximum abundances during spring and autumn (Castel, 1993).
The oligohaline area corresponds generally to the most turbid zone. With the help
of the above observations, it can be supposed that environmental factors such as
salinity or temperature are not sufficient to explain this distribution, and that
more complex mechanisms like feeding behaviour must be involved. Acartia
bifilosa seems to profit from the summer phytoplankton bloom seaward of the
maximum turbidity zone (Irigoien et al, 1996) and is probably not able to use
food resources when turbidity becomes too high. On the contrary, E.affinis seems
able to use several food sources in or slightly upstream of the maximum turbidity zone with a preference for phytoplankton. The apparent discrepancy of a
phytoplankton selection in a turbid environment, where primary production is
very low, could correspond to the use of inputs from the upper river or from the
bank by the copepods. Therefore, the origin of phytoplankton appears to be an
interesting question for future research.
Acknowledgements
This study was supported by the 'Region Aquitaine' (Aquitaine/Euskadi project)
and by IFREMER (Contract 95-2-480 402 DEL). Thanks are due to G.Oggian,
captain of the RV 'Ebalia'.
References
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Berk,S.G., BrownleeJ).C., HeinleJJ.R., KlingJU. and Colwell,R.R. (1977) Ciliates as food source
for marine planktonic copepods. Microb. EcoL, 4, 27-40.
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Received on August 31, 1996; accepted on February 2, 1997
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