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Nutritive value and selection of food
particles by copepods during a spring
bloom of Phaeocystis sp. in the English
Channel, as determined by pigment and
fatty acid analyses
GWENAËLLE COTONNEC1, CHRISTOPHE BRUNET1, BENOIT SAUTOUR2 AND GUY THOUMELIN3
, B.P. ,  AVEVUE FOCH, WIMEREUX F-, FRANCE, 2 LOB, UNIVERSITÉ
,  RUE PR JOLYET, ARCACHON , FRANCE AND 3 LCAM, UNIVERSITÉ DE LILLE I, UPRES A ELICO , BÂT C,
VILLENEUVE D’ASCQ , FRANCE
1 MREN, UNIVERSITÉ DE LITTORAL-CÔTE D’OPALE, UPRES A ELICO
DE BORDEAUX, UMR EPOC
In this study phytoplankton pigments and fatty acids were used as biomarkers to study trophic relationships between phytoplankton and zooplankton. These markers permit the characterization of both
suspended matter and copepods, allowing examination of the transfers from food to zooplankton. A
drogue study was carried out to follow a water mass in the coastal waters off the eastern English
Channel over a 3-day period, with samples collected every 3 h. The study focused on the dominant
calanoid copepod species: Temora longicornis, Acartia clausi and Pseudocalanus elongatus. Our study
was performed during the spring phytoplankton bloom when solitary cells of Phaeocystis sp. formed
90% of the total phytoplankton. Fatty acid analyses provided an indication of the low nutritive
value of these algal cells; in contrast to other algal species which had higher nutritional value (e.g.
colony-forming diatoms, Cryptophytes and dinoflagellates). Our results suggest that all species selectively grazed on Phaeocystis sp. and non-selectively on diatoms. Dinoflagellates were avoided by all
species. Temora longicornis selectively grazed on Cryptophytes, which may be related to the nutritional value of this algae. The fatty acid composition of the three copepod species indicated an ‘herbivorous’ diet for P.elongatus and an omnivorous one for A. clausi and T. longicornis, which is less
opportunist.
I N T RO D U C T I O N
Planktonic copepods are considered to play a key role in
the transfer of material and energy between primary producers and higher trophic levels in coastal, shelf and
oceanic waters. Classically, this role as an intermediate
component of the marine food web is investigated by
determining the rate at which microalgae are grazed by
copepods. A number of field studies have shown that zooplankton selectively grazes on food particles. Selection can
be based on size of food particles (Tackx et al., 1989),
concentration (Turner and Tester, 1989) and biochemical
composition (Paffenhöffer et al., 1995). The selectivity
could also depend on the nutritional value of food particles, as phytoplankton species are acknowledged as
having different nutritional values (Koski et al., 1998).
© Oxford University Press 2001
Among microalgae, Phaeocystis sp. is particularly interesting due to the global distribution of reported blooms. This
alga is frequently reported as having negative effects on
the feeding activity of zooplankton, in particular on the
feeding activity of copepods (Hansen and van Bœkel,
1991; Bautista et al., 1992). The structure of the bloom
(solitary cells or colonies), the size of the colonies and the
excretion of toxic substances such as dimethyl sulphide
(DMS) (Hansen and van Bœkel, 1991) are often cited as
reasons for this. Nevertheless, its nutritive value is as yet
unclear.
Over the last decade, natural organic markers, such as
pigments [e.g. carotenoids; (Kleppel et al., 1988; Brunet et
al., 1996; Breton et al., 2000)] and fatty acids (Greave et al.,
1994), have been used to study the algal composition of
the feeding medium (Claustre et al., 1990). They also allow
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for the study of trophic relationships (Welschmeyer et al.,
1991; Desvilettes et al., 1994). Moreover, they can provide
information about the sestonic food if it is assumed that
polyunsaturated fatty acids (PUFAs) are a measure of food
nutritive value, as has been suggested (Ahlgren et al., 1997;
Brett and Müller-Navarra, 1997). High-nutritional value
algal food is rich in PUFAs. Nevertheless, fatty acids are
not the only biochemical components contributing to the
nutritive value of sestonic food. In effect, other studies
have shown that peptides and polysaccharides can also
play an important role.
In the present study, we described the selectivity of food
particles and their nutritional value based on fatty acids
for three copepods: Acartia clausi, Pseudocalanus elongatus and
Temora longicornis. These species are dominant in the
English Channel during the phytoplankton spring bloom
which is dominated by Phaeocystis sp. (Brylinski et al., 1984).
The objectives of our investigation were to: (i) determine
the lipid composition of the nutritive pool (i.e. pigment
and fatty acid composition), (ii) compare the diet of the
three copepod species during a period when Phaeocystis sp.
was found as solitary cells. A 3 day drogue study was conducted in the coastal waters off the Bay of Somme in
order to avoid any potential changes of both phytoplankton and zooplankton communities occurring with
water mass changes.
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3 h over a 3 day period at the end of April 1998. Vertical
profiles of hydrographic parameters were made with the
CTD SB 25. Water samples were collected with Niskin
bottles in the subsurface waters (–5 m) and near the
bottom of the water column. One subsample of sea water
(60 ml) was preserved in acid Lugol’s iodine solution for
identification and counting of phytoplankton cells. An
additional subsample (20 ml) was stored frozen, at –20°C,
to measure nutrients (i.e. nitrite and nitrate). Two other
subsamples (500 ml) were filtered at each depth. One was
filtered onto a Whatman GF/F to determine phytoplankton pigments. The filter was stored in liquid nitrogen
to avoid pigment destruction by light or chemical or biochemical endogenous enzymes. The second sample was
filtered onto a Whatman GF/F that had been precombusted at 450°C for 12 h to remove organic material in
order to measure the lipid composition of particulate
organic matter (POM). It was stored frozen at –20°C in 2
ml of methanol. For biochemical analysis (i.e. gut pigment
and fatty acid composition), zooplankton were collected
with a WP 2 net (200 µm mesh size) in oblique hauls. The
subsample for gut pigment content was immediately
stored in liquid nitrogen to prevent pigment degradation.
The subsample for lipid analysis was stored at –20°C until
analysis.
METHOD
Study area
The eastern English Channel is characterized by a shallow
depth and active hydrodynamics due to a strong tidal
regimen. A distinct hydrological structure has been
observed (Brylinski et al., 1984) along the French coast,
where many estuaries are located. The central input of
water from the Atlantic flows northwards and confines the
estuarine waters along the French coast. Thus, the coastal
vertically stratified waters are separated from well-mixed
offshore waters by a tidally generated front. The bays of
estuaries, with the Bay of Somme in particular, are known
to be highly productive. According to Grioche et al., the
plume of dilution of the Somme estuary may also act as a
retention zone where organisms would be retained for a
period before drifting northwards (Grioche et al., 2000).
Sampling
The study was carried out in the coastal waters off the Bay
of Somme (Figure 1). A drogue was launched in the offshore area. The drifter was composed of a cylindrical sock
8 m long attached to a buoy at 2 m below the surface. Its
geographical position was determined by satellite (Argos)
every 2 h. Sampling was carried out near the drifter every
Fig. 1. Location of the Bay of Somme. The black strait shows the trajectory of the drogue for 1 month. The numbers indicate the position of
the sampling stations over the 3 day period.
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Nutrients
Nutrients were measured by a Technicon Autoanalyser II
(Treguer and Le Corre, 1974).
Microscopic counts
Phytoplankton composition and abundance were determined with a Zeiss inverted microscope ( 400) according to the Ütermohl sedimentation technique (Ütermohl,
1958).
Pigment analysis
propan-2-ol (the percentage varying from 0% to 5%). UV
absorbance (Waters Lambda Max model 841spectrophotometer at 206 nm) was used to distinguish the methyl
esters from other lipids. Gas chromatography of the
methyl esters was carried out with a Hewlett Packard
model 5890 series II apparatus equipped with a flame ionization detector. The methyl esters were separated using a
free fatty acids phase (FFAP) polar phase capillary column
25 m in length with a 0.32 mm internal diameter. Hydrogen was used as carrier gas from 86 to 115 kPa. The detector temperature was maintained at 240°C. Peaks were
identified by means of reference standards. The results
were processed using a HP 3396 Series II integrator.
Phytoplankton pigments were extracted over a 2 h period
in 90% acetone (5 ml), at 4°C in dark conditions. For
copepod gut pigment content, pools of 300 individuals
(CV and CVI copepodites) of each species were sorted
using a binocular microscope at 0°C under cool light, and
gently and carefully rinsed. Gut pigments were extracted
over a 2 h period in 1.2 ml of 90% acetone; the samples
were kept at 4°C in dark conditions.
Pigment analysis was performed by high-performance
liquid chromatography (HPLC) according to the method
of Klein and Sournia and modified by Brunet (Klein and
Sournia, 1987; Brunet, 1994). UV absorbance (440 nm)
was used to detect chlorophyll and carotenoid pigments
using a Beckman model 168-photodiode array detector. A
fluorescence detector (Kontron model sfm 25 spectrofluorometer with an excitation at 407 nm and emission at
660 nm) was used to determine the level of chlorophyll
pigments present in the sample. The identification and
quantification of the peaks were made using standards
and predetermined calibration factors (see details in
Breton et al., 2000).
Food selection of copepods was estimated using the selectivity index E (Ivlev, 1961), given by E = (ri – pi)/(ri + pi)
where ri is the relative proportion of one phytoplankton
pigment in the diet of copepods and pi is the relative proportion of the same pigment in the POM. The selectivity
was estimated comparing the relative proportions of
phytoplanktonic pigments in the field with those detected
in copepods. Copepods selectively grazed when the difference between these proportions was significant. When the
difference between the proportions in phytoplankton and
those in copepods was not significant, copepods grazed
non-selectively. Thus, –0.25 < E < +0.25 indicates nonselective feeding, E > +0.25 indicates a preference, E <
–0.25 indicates discrimination against particular prey
items.
Fatty acid composition
Hydrology
The fatty acids were extracted according to Bligh and
Dyer (Bligh and Dyer, 1959). Copepods were sorted as for
pigment analysis. The fatty acid C23 : 0 was used as an
internal standard for the quantification.
The fatty acids were converted to methyl esters according to Metcalfe and Schmitz (Metcalfe and Schmitz, 1961)
by refluxing with 1 ml of 13% BF3 in methanol for 10 min
at 100°C. A nitrogen atmosphere was maintained at all
times. Methyl esters were separated successively from
other lipids (i.e. hydrocarbons and sterols) on a diol-Si
column and a Lichrosorb Si 60 column. The diol-Si
column improved the separation reproducibility. A
mixture of hexane : propan-2-ol (85 : 15) was added
(250 µl) to the sample after evaporation to dryness under
nitrogen flow. Methyl esters were separated using a
Lichrosorb Si 60 column. A diol-Si column was again
used to improve the separation reproducibility. The
mobile phase consisted of a step gradient of hexane and
The drifter described elliptic curves as it followed the tidal
excursions outside the Bay of the Somme during the first
2 days (Figure 1). On the third day, it started to drift northwards and reached the North Sea 15 days later.
The water column was vertically well-mixed throughout the sampling period (Figure 2). No significant changes
in temperature and salinity were encountered during the
northward drift.
Selectivity index
R E S U LT S
Nutrients
The water mass showed concentrations of nitrite of 0.097
± 0.035 µM l–1 in subsurface waters and 0.102 ± 0.034 µM
l–1 near the bottom (Figure 3). No significant variation was
observed between surface and bottom measurements
(Kruskall–Wallis, n = 18, P = 0.27). No temporal variations were observed in either surface or bottom waters.
Nitrate concentration was below the limits of detection
throughout the study.
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Fig. 2. Hydrological profiles of (A) salinity (p.s.u) and (B) temperature (°C) from the surface to the bottom throughout the study (white and black
areas indicate daily and nightly sampling respectively). LT, low tide; HT, high tide.
Fig. 3. Nitrite concentrations (µM l–1) in both surface and bottom waters.
Phytoplankton composition and pigment
biomarkers
Phytoplankton composition in both surface and bottom
waters showed that Phaeocystis sp. as solitary cells (3–5 µm
) were highly dominant, with around 27 ± 6 105 cells
l–1. Larger phytoplankton cells were dominated by

diatoms (20 µm 50 µm, 3 ± 0.9 105 cells l–1) which
were found mainly in chains. Other taxa were represented
by very low concentrations of dinoflagellates (20–100 µm
, 5 ± 2 103 cells l–1) and cryptophytes (7–8 µm , 6 ±
3 103 cells l–1).
Chlorophyll a (Chl a) concentrations (Figure 4) were not
significantly different (Kruskall–Wallis, n = 18, P = 0.76)
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Fig. 4. Evolution of chlorophyll a concentrations (mg m–3) in both surface and bottom waters.
Table I: Correlations (Spearman rank, n = 18, P < 0.001) between the pigments found in
the field in both surface and (bottom) waters
Chl c3
Chl c
Diadinoxanthin
Chl c
0.85 (0.96)
Diadinoxanthin
0.92 (0.91)
0.84 (0.95)
Fucoxanthin
0.92 (0.89)
0.88 (0.95)
0.87 (0.95)
Chl a
0.88 (0.84)
0.94 (0.91)
0.85 (0.85)
Fucoxathin
0.86 (0.83)
Table II : Mean and standard error (SE) of the pigment
concentrations (mg m–3) for the suspended matter
Surface
Bottom
Mean
SE
Mean
SE
Chlorophyll c3
0.39
0.17
0.31
0.21
Chlorophyll c
3.06
1.22
2.40
1.39
Diadinoxanthin
0.82
0.39
0.64
0.39
Fucoxanthin
6.75
2.90
5.88
3.42
between the surface and bottom waters (5.19 ± 1.20 mg
m–3, and 4.87 ± 1.71 mg m–3, respectively). Five other pigments were detected; Chl c (c1 + c2), Chl c3, fucoxanthin,
diadinoxanthin and carotene. All these pigments were
highly positively correlated with Chl a (Table I), indicating
similar patterns of concentration to Chl a. The fucoxanthin was the dominating pigment during our study, with
up to 42% of the total pigment biomass (Table II).
Although it is the dominant carotenoid of Phaeocystis sp. in
the Northern Hemisphere (Gieskes and Kraay, 1986) it
cannot be used as a specific marker because it is also found
in diatoms (Kleppel et al., 1988). Chl c3, Chl c and diadinoxanthin contributed on average 2%, 18% and 5% to
the total pigment biomass respectively. Chl c3 is a marker
of Phaeocystis sp. (Hooks et al., 1988; Breton et al., 2000). For
Prymnesiophytes such as Phaeocystis sp., 19-hexanoyloxyfucoxanthin is often used as a marker (Hooks et al., 1988;
Breton et al., 2000). In our study, this pigment was not
detected by HPLC. However, Breton et al. showed that the
19-hexanoyloxyfucoxanthin is a very minor pigment of
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The Chl c, Chl c3 and fucoxanthin were detected in the
three copepod species (Figure 5). The fucoxanthin was the
dominant pigment in the three species (42–70% of the
total pigment biomass). The Chl c3 was the less abundant
in all species (9–12%). Alloxanthin was detected in T. longicornis only. It was the second most dominant pigment in
the gut of this species (32% of the total pigment biomass)
and it was never observed in the other two species. In contrast to alloxanthin, the peridinin was not detected in
copepods.
Astaxanthin and its derivative product that are characteristic of copepod tissues were also detected (Juhl et al.,
1996). However, these pigments constitute a minor part of
the total lipids in the zooplankton (Ohman et al., 1989).
Phaeocystis sp. in the eastern English Channel (Breton et al.,
1999). But, the concentration of this pigment was sometimes below the limit of detection or not clearly identifiable in accordance with our results. Thus, these authors
suggest that the Chl c3 is a better marker of Phaeocystis sp.
than the 19-hexanoyloxyfucoxanthin in this area.
Diadinoxanthin and Chl c are markers of brown algae
(Klein and Sournia, 1987; Head and Harris, 1992).
Although crytophytes and dinoflagellates were observed
in microscopy, their pigment markers, alloxanthin (Klein
and Sournia, 1987) and peridinin, respectively (Kleppel et
al., 1988), were not detected, probably due to their low
concentrations.
Fatty acid composition of POM
Thirty-two fatty acids were detected during our investigation (Table III). Saturated fatty acids, and more accurately C14:0, C16:0 and C18:0, were dominant (90% of
total lipid content) in both surface and bottom waters.
Unsaturated fatty acids and branched fatty acids (iC15:0,
aC15:0) represented about 3% and 6% of total lipid composition respectively. The C14:0, C16:0 and C18:0 fatty
acids are characteristic of Phaeocystis sp. (Claustre et al.,
1990; Nichols et al., 1991). C18:19 fatty acid was also
found in Phaeocystis sp. in the Irish Sea (Claustre et al.,
1990), but was not detected in our study. Low levels of
C20:53, C16:17 and C16:3 corroborate the low
concentration of diatoms (Volkman et al., 1981). In contrast to pigments, low levels of lipid markers of cryptophytes (C18:3, C20:1) and dinoflagellates (C22:63) were
observed. The odd-numbered FAs indicated the presence
of heterotrophic bacteria.
Globally, the low proportions of PUFAs indicate a low
nutritive value of food particles. The absence of C18:19,
cited as the unique unsaturated fatty acid in Phaeocystis sp.
in literature (Claustre et al., 1990; Nichols et al., 1991), indicates a lower nutritive value for this alga than for other
algal taxa which contained unsaturated fatty acids.
Pigment composition of copepods
Pigment composition of copepods results, at least partially, from ingested phytoplankton. Some pigment may
come from copepod tissues, such as astaxanthin and its
derivative product (i.e. astaxanthin like). It is now well
known that pigments resulting from phytoplankton ingestion are partially degraded or destroyed in uncoloured
products during their passage through the gut. The products of degradation and destruction therefore have to be
taken into account in quantitative studies estimating fluxes
between the nutritive pool and grazers. In our qualitative
study, the fluxes resulting from trophic transfers were not
estimated and derivative products of pigments were not
taken into account.
Fig. 5. Mean proportions (%) and quartiles of marker pigments both
in the POM and the gut of the three species of copepods.
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Table III: Fatty acid composition (in percentage) relative to the total fatty acids (FA) of the
particulate organic matter and of three species of copepods
Suspended matter
Fatty acids
Subsurface
Copepods
Bottom
A. clausi
–
P. elongatus
–
T. longicornis
13:0
1.03
1.50
14:0
36.77
41.92
11.32
6.46
12.07
–
i15:0
0.72
0.88
0.66
0.14
0.13
a15:0
0.62
0.83
0.24
0.04
0.14
15:0
2.78
2.95
0.81
0.33
0.60
i16:0
0.32
0.31
0.22
0.03
0.11
16:0
36.48
31.90
21.19
17.25
22.33
16:17
0.17
–
11.90
9.00
7.44
16:19
–
–
0.19
0.02
0.32
16:24
–
–
0.32
0.53
0.43
16:3
0.04
–
0.42
0.04
0.02
i17:0
0.10
–
0.32
0.58
0.62
a17:0
0.26
–
–
–
–
17:0
1.21
1.11
0.72
0.42
0.50
i18:0
0.13
–
0.16
0.08
0.05
a18:0
–
–
0.70
2.27
1.76
4.29
2.57
2.55
18:0
13.28
11.38
18:17
–
–
2.79
0.34
2.93
18:19
–
–
2.37
20.23
1.34
18:26
–
–
1.02
0.83
0.56
18:36
0.74
–
1.31
0.96
0.58
18:3’
–
–
5.54
2.68
1.34
19:0
0.19
0.14
–
0.04
–
20:0
0.84
0.92
1.03
0.01
–
20:1
0.11
–
0.98
0.27
0.38
20:46
1.18
0.17
0.79
1.28
1.38
20:53
0.14
0.36
18.87
22.69
22.80
21:0
0.74
–
–
–
–
22:0
1.80
1.92
0.07
–
0.04
22:1
0.02
–
0.17
0.14
0.24
22:63
0.29
–
11.18
10.72
19.29
24:0
0.03
0.16
–
–
–
TOTAL:
Saturated FA
91.61
90.56
38.9
28.74
38.9
Unsaturated FA
2.71
0.17
57.8
69.5
58.7
Branched FA
5.69
5.78
3.19
Fatty acid composition of copepods
A general opinion is that fatty acids in copepods are
principally derived from food ingestion. Copepods are
unable to synthesize de novo these compounds (Fraser et al.,
1.52
2.04
1989). However, a further elongation and desaturation of
previously ingested compounds such as C18:3 may not be
excluded (Gulati and De Mott, 1997).
In contrast to the POM, the unsaturated fatty acids
were found to be predominant in copepods (Table III),
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particularly the C20:53, C22:63 and C16:17 fatty
acids. The C20:53 and C22:63 were the major fatty
acids in all the species. The saturated fatty acids were
mainly composed of mixtures of C14:0, C16:0 and C18:0
and represented about 30% of total lipid composition.
Approximately 2% of the fatty acids were branched in all
the species.
The major fatty acid components of A. clausi were the
C14:0, C16:0, C16:17, C20:53 and the C22:63,
which comprised about 78% of all fatty acids. The
monounsaturated fatty acids C16:19, C18:17,
C18:19, C20:1 and C22:1 were found in small amounts
(5% of all fatty acids). The fatty acid composition of P.
elongatus was dominated by the same fatty acids as A. clausi
plus the C18:19 (86% of all fatty acids). The other
monounsaturated fatty acids represented less than 1% of
all fatty acids. The fatty acid composition of T. longicornis
resembled that of A.clausi more than that of P. elongatus.
Predominant fatty acids in T. longicornis were the C14:0,
C16:0, C16:17, C20:53 and C22:63 (84% of all fatty
acids), followed by small amounts of C16:19, C18:17,
C18:19, C20:1 and C22:1 (5%).
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Table IV: Mean selectivity index
(calculated from data of Figure 5)
during the study [according to (Ivlev,
1961)]
P. elongatus
T. longicornis
A. clausi
Fucoxanthin
0.04
–0.18
Chl c3
0.50
0.38
0.46
–0.12
0.24
–0.19
Chl c
Alloxanthin
Selectivity
The E values (Table IV) and the significant differences
between the mean proportions of Chl c3 in the POM and
copepods (Figure 5) indicate a selective feeding on Phaeocystis sp. during the spring bloom. Although the cryptophytes were at very low concentrations, T. longicornis
exerted a high preference for this algal class. The lack of
detectable levels of alloxanthin in the field, and presence
in the gut of copepods would suggest a strong concentration of this pigment by copepod (Figure 5). By contrast
with Phaeocystis sp. and cryptophytes, the selectivity index
and pigment proportions show a non-selective feeding on
diatoms for all copepods although they represented 10%
of phytoplankton cells. As for the POM, the peridinin was
not detected in the gut content of the copepods.
DISCUSSION
The drift of the drogue was due to the strong hydrodynamic effect of strong tidal currents and the entry of
the Atlantic waters into the English Channel. As indicated
by the hydrographic data, the study occurred in the same
water mass that was retained for 2 days in front of the Bay
of Somme.
Numerous investigations have been performed on
trophic transfers between phytoplankton and copepods
using pigment markers. The utilization of pigments as
trophic markers supposes a conservation of these pigments during their passage through the gut of copepods.
Nevertheless, pigment degradation or destruction occurs

0.07
1
during the ingestion and digestion of phytoplankton cells
by the copepods. Consequently, many studies have been
performed to estimate the rates of pigment degradation
or destruction occurring in the gut of copepods (Head and
Harris, 1992, 1996; Stacey et al., 1999). Varying degrees of
pigment destruction have been observed, ranging from 0
to 100%, and corrections must be considered for quantitative studies.
Classically, these estimates are made in the laboratory,
with copepods having grazed on monospecific algal
culture after a period of acclimatization, and the methods
used vary according to the authors [sonication to extract
pigment, time of pigment extraction, number of copepods often low … (Stacey et al., 1999)]. Thus, it is not possible to generalize the fates of pigments reported in the
literature. In both, degradation or destruction of pigments
depends not only on environmental parameters such as
light and temperature (Kleppel, 1998), but also on food
concentration, algal species (Stacey et al., 1999) and
feeding history. In situ conditions are very different from
the conditions described in these laboratory experiments.
The aim of our study was not to quantify the trophic
transfers between the phytoplankton and the copepods,
but to estimate the selectivity of food particles by different
species of copepods and point out the importance of the
nutritive value of food particles in the selectivity.
As shown by our results, the nutritive pool was mainly
composed of Phaeocystis sp., which has a low nutritive value
(absence of PUFAs). According to Sargent et al. (Sargent
et al., 1985), P. pouchetii cells may contain high levels of
PUFAs if nutrients are not limiting. In our investigation,
the lack of nitrate and low levels of nitrite could explain
the nutritional poverty of Phaeocystis sp. Other algal taxa
(i.e. diatoms, cryptophytes, dinoflagellates) were in low
concentrations but revealed a higher nutritional value
than Phaeocystis sp. during our study. These particular
dietary components are of great interest for copepods
because PUFAs are vital components of cell membranes
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G. COTONNEC ET AL.
FOOD SELECTION AND NUTRITIVE VALUE IN COPEPODS
and because animals such as copepods cannot synthesize
some essential PUFAs (e.g: C20 and C22 PUFAs).
Our biochemical results for pigments and fatty acids
indicate that copepods grazed on phytoplankton and on
heterotrophic bacteria, which were probably attached to
phytoplankton cells and/or detritus.
Our data show that Phaeocystis sp. were consumed selectively by copepods. The ingestion of this alga by copepods
has been reported by many authors (Hansen and van
Boekel, 1991; Bautista et al., 1992). Some authors suggest
that Phaeocystis sp. constitute an important food source for
copepods during the spring (Weiße, 1983). Nevertheless,
the selection of Phaeocystis sp. appears surprising here due
to its size and its low nutritive value. We argue that the
value of the selectivity index did not result from a selection but from a low rejection of this alga by copepods due
to its very high concentration in the field. On the other
hand, the Chl c3 concentration in copepods might have
been overestimated due to the presence of Phaeocystis sp.
cells attached to copepods, although copepods were gently
rinsed with filtered sea water.
As indicated by biomarkers, all copepods ingested
diatoms but non-selectively despite their high nutritive
value. Cowles et al. suggest that the copepods select
diatoms according to their quality (Cowles et al., 1988).
However, some diatoms have a negative effect on copepods in terms of egg production and hatching rates
(Poulet et al., 1994). Nevertheless, diatoms are thought to
occur predominantly in the diet of copepods in highly
productive areas (Cushing, 1989). Meyer-Harms and von
Bodungen showed that copepods ingested diatoms
according to their abundance in the field (Meyer-Harms
and von Bodungen, 1997). Although copepods are able to
dismember colonies of diatoms, in our study the vast proportion of diatoms recorded formed long chains
(>200 µm) which are not suitable as a food for copepods
due to their size. Only diatoms as solitary cells could have
been ingested by copepods. Schnack found that copepods
were unable to feed on the entire colonies of diatoms, but
consumed them once they had disintegrated (Schnack,
1983).
In contrast to the other two copepod species considered
in this study, T. longicornis selectively grazed on the cryptophytes. As often observed in previous studies (Curl and
McLeod, 1961) and noted in our study, food concentration is not the deciding factor for selection by T. longicornis. According to Tackx et al., (1989), particle size can be
an important selection factor. T. longicornis predominantly
grazes on particles >20 µm (Tackx et al., 1990). In our
study, the cryptophytes were under this size limit (7 µm).
Therefore, we suggest that the nutritive value of this algal
group is the determining factor for selection of cryptophytes by T. longicornis. The presence of the C18:3 fatty
acid in the cryptophytes and its role as processor in the
biosynthesis of the lipid reserves (i.e. the C20:53 and
C22:63) could explain this selection. Meyer-Harms and
von Bodungen suggested that food quality was the determining factor for selection of cryptophytes by Acartia
bifilosa in the Baltic Sea (Meyer-Harms and von Bodungen, 1997).
During our study, dinoflagellates were also found in low
concentration similar to the cryptophytes. They presented
a more adequate size for copepods (>20 µm). But, in contrast to the cryptophytes, dinoflagellates were apparently
avoided by all copepods. Nevertheless, as the peridinin
was not detected in the POM although the dinoflagellates
were present, the ingestion of these food particles by copepods cannot be excluded. Dinoflagellates are known to be
sometimes a major component of the copepod diet
(Kleppel et al., 1991). However, Kleppel observed
(Kleppel, 1993) that some dinoflagellate species are
ingested and others are rejected. The nutritive value of
dinoflagellates, in terms of egg production of copepods, is
known to vary with species (Razouls et al., 1991). Huntley
et al. found that dinoflagellates offered limited nutritional
value (Huntley et al., 1986). In our work, the nutritive value
of dinoflagellates was high and it cannot explain the
avoidance of dinoflagellates by copepods. Some dinoflagellates are known to produce toxic substances which
may be responsible for their avoidance or rejection by
copepods (Huntley et al., 1986). The presence of such
dinoflagellate species could explain our observations.
Unfortunately, the dinoflagellate species were not identified in our study. As the dinoflagellates were apparently
avoided by copepods, the C22:63 found in copepods did
not result from the ingestion of phytoplankton or from a
selective incorporation of dietary fatty acids (Weers et al.,
1997). Our results corroborate the possibility that the
C22:63 is biosynthesized by copepods using some fatty
acids from their diet. Nevertheless, the level of this fatty
acid can also result from long-term storage.
Selection of food particles by copepods has been
described by numerous authors (Cowles et al., 1988; Tackx
et al., 1989, 1990). Regarding our results, all copepod
species were selective during our study, with T. longicornis
the most selective of the three species. However, our findings about the selectivity index concerning A. clausi and P.
elongatus suggested a similar discriminating behaviour.
DeMott has reported that T. longicornis was weakly selective, P. elongatus highly selective and A. clausi intermediate
(DeMott, 1988). However, this was in a restrictive feeding
medium containing only algae and detritus. The selection
of phytoplankton cells depended on the algal group and
the species of grazer. The similar proportions of Chl c3
and Chl c in the three copepod species suggest a similar
feeding behaviour concerning both Phaeocystis sp. and

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JOURNAL OF PLANKTON RESEARCH
VOLUME
diatoms. The deciding factors for the feeding behaviour
were the high concentration for Phaeocystis sp. and the size
of the diatom colonies. By contrast, the selection of
cryptophytes by T. longicornis was linked to the high nutritional value of these algal cells. It was noted that copepods
would feed on the more nutritious foods when it was
efficient to do so (Cowles et al., 1988). This species-specific
selection could be linked to different physiological requirements of T. longicornis in comparison to A. clausi and P. elongatus. Pseudocalanus sp. is usually considered to be more
herbivorous (Marshall, 1973), and Temora and Acartia more
omnivorous (Marshall, 1973). Our results with respect to
the lipid composition (i.e. pigments and fatty acids) of T.
longicornis and P. elongatus were consistent with those of
Fraser et al., who considered the total lipid content (Fraser
et al., (1989). Comparing the results of this study with
those of Fraser et al., our findings suggest a more herbivorous diet for P. elongatus (similar proportions of
C18:19, C20:53 and C22:63), and a more omnivorous diet for T. longicornis and A. clausi (low level of
C18:19 in contrast to C20:53 and C22:63). In
addition, T. longicornis showed a more selective feeding
activity in comparison with A. clausi during a bloom of
Phaeocystis sp. as solitary cells, although they are both
omnivorous. We suggest that T. longicornis would be less
opportunistic than A. clausi concerning its diet. These
differences highlighted the importance and utility of
analysing a combination of two specific natural markers.

NUMBER
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PAGES
‒
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AC K N O W L E D G E M E N T S
This research was supported by the programme Interreg
II-Kent. Thanks are due to the crews of the RV ‘Côte de
la Manche’, to P. Koubbi, X. Harlay, E. Charley and T.
Deleye for their contributions during the survey, to L.
Fraga-Lago, V. Gentilhomme and G. Bourcier for their
help with the analysis, and to P. D. Eastwood for his
English corrections. We wish to thank two anonymous
reviewers for comments on the manuscript.
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Received on July 21, 2000; accepted on February 27, 2001
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