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Journal of Experimental Marine Biology and Ecology 390 (2010) 134–142
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Journal of Experimental Marine Biology and Ecology
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j e m b e
Diel feeding pattern and prey selection of mesozooplankton on
microplankton community
Chih-Jung Wu a, Kuo-Ping Chiang a,b,c,⁎, Hongbin Liu d
a
Institute of Environmental Biology and Fisheries Science, National Taiwan Ocean University, Keelung 202-24, Taiwan, ROC
Institute of Marine Environmental Chemistry and Ecology, National Taiwan Ocean University, Keelung 202-24, Taiwan, ROC
Center for Marine Bioscience and Biotechnology, National Taiwan Ocean University, Keelung 202-24, Taiwan, ROC
d
Department of Biology, The Hong Kong University of Science and Technology, Clear Water Bay, Hong Kong, China
b
c
a r t i c l e
i n f o
Article history:
Received 23 December 2009
Received in revised form 5 May 2010
Accepted 5 May 2010
Keywords:
Diel feeding pattern
Feeding behavior
Mesozooplankton
Microplankton
a b s t r a c t
Mesozooplankton play an important role in transporting energy from microphytoplankton and microzooplankton to higher trophic levels. However there were few studies on the diel feeding patterns and prey
selectivity of mesozooplankton. We conducted feeding experiments of mesozooplankton in the East China
Sea to determine their respective diel feeding patterns on diatoms, ciliates and dinoflagellates, and to assess
the contribution of these prey items to mesozooplankton diet. The results showed higher mesozooplankton
grazing rates on ciliates and dinoflagellates than on diatoms at the day time, and the opposite pattern at the
night time. A significant prey selection was observed, in which mesozooplankton positively selected ciliates
and dinoflagellates during day and diatoms at night. The different grazing reactions of mesozooplankton
toward each prey item might be related to the mobility of the prey. In all, microzooplankton (ciliates and
dinoflagellates) provided the majority of the mesozooplankton carbon ingestion, even at a station dominated
by small pennate diatoms. In particular, dinoflagellates are an important prey of mesozooplankton in the East
China Sea and their contribution to the diet of mesozooplankton is unproportionate to their abundance.
© 2010 Elsevier B.V. All rights reserved.
1. Introduction
Mesozooplankton are significant consumers of microphytoplankton and microzooplankton, channeling organic carbon and energy to
higher trophic levels in marine pelagic ecosystems. Mesozooplankton
could consume 10–40% primary production in different environment
conditions (Calbet, 2001). The relative contribution of different prey
to mesozooplankton diet depends on the trophic states of the
ecosystems (Calbet, 2001; Calbet and Saiz, 2005). Generally, ciliates
occupy a large proportion of mesozooplankton diet in oligotrophic
ecosystems where primary producers are dominated by picophytoplankton, whereas diatoms are the main food source of mesozooplankton in productive waters (Fessenden and Cowles, 1994; Calbet,
2001). Calbet and Saiz (2005) estimated that ciliates account 22–49%
in copepod diet and their proportion in the diet decreases following
the rise of in situ phytoplankton biomass.
Microzooplankton, which includes mainly ciliates and dinoflagellates, are considered better food based on their high nitrogen to
carbon ratio (Kleppel, 1993). Dietary composition of mesozooplankton would affect egg production, hatching success and subsequent
⁎ Corresponding author. Institute of Environmental Biology and Fisheries Science,
National Taiwan Ocean University, Keelung 202-24, Taiwan, ROC. Tel.: +886 2 2462
2192x5019; fax: + 886 2 2462 1016.
E-mail address: [email protected] (K.-P. Chiang).
0022-0981/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2010.05.003
development because of toxicity or the absence of essential dietary
components. Some previous studies report that the best population
growth efficiency of mesozooplankton is reached in mixed-prey
condition, and this is probably because of the presence of different
fatty acids in each prey species including diatoms, dinoflagellates and
ciliates (Kleppel et al., 1991; Jones and Flynn, 2005). On the other
hand, biotoxin from some algal species has been proven to have
deleterious effects to copepod growth and reproduction (Jones and
Flynn, 2005). For example, mono-species algal blooms of Skeletonema
costatum and Pseudo-nitzschia delicatissima have been reported to
cause reduced hatching success of copepod eggs (Miralto et al., 1999).
However, since most mesozooplankton are selective feeders, they
would choose the optimal prey composition for survival, except under
some special circumstances (Irigoien et al., 2002).
Many mesozooplankton, especially copepods, are selective feeders,
which can ingest prey non-proportionally to ambient densities (Kleppel,
1993; Castellani et al., 2008). Feeding selectivity of copepods not only is
affected by the trophic state of the environments, but also depends on
prey motility (Atkinson, 1995), size (Frost, 1972) and quality (Berggreen
et al., 1988). Some copepods can switch their feeding mode in response to
the most abundant prey (Gismervik and Andersen, 1997). However, most
feeding experiments do not separate respective feeding preference of
mesozooplankton in the day time and night time.
Diel feeding patterns have been observed in marine zooplankton
(Haney, 1988; Sautour et al., 1996; Christaki et al., 1998), usually with
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C.-J. Wu et al. / Journal of Experimental Marine Biology and Ecology 390 (2010) 134–142
higher ingestion rate at night than at day. Besides the normal pattern
(higher ingestion rate at night) (Saito and Taguchi, 1996), observations of the reverse pattern (Daro, 1985; Kiørboe et al., 1985; Roman
et al., 1988), or no significant difference between day and night (Dagg
and Walser, 1987) was also reported. Gauld (1953) hypothesized that
zooplankton rise to the surface of water column at dusk or night,
where phytoplankton biomass is higher than in the deep layer.
However, some studies demonstrate that diel feeding pattern is
dependent with vertical migration, but had no close relationship with
prey concentration (Stearns, 1986; Dagg et al., 1989; Peterson et al.,
1990). Other studies suggest that mesozooplankton feeding activity is
dependent on the prey concentration which does not always occur at
surface (Boyd et al., 1980; Saito and Taguchi, 1996). Also, Stearns
(1986) reported that Acartia tonsa maintained endogenous feeding
rhythm under constant temperature and darkness. However, for
species with vision ability (e.g. Corycaeus), feeding activity would ease
under darkness (Gophen and Harris, 1981). Thus the causes for the
variation in diel feeding behavior among copepods were complex,
which include vertical migration (Stearns, 1986; Dagg et al., 1989;
Peterson et al., 1990), prey condition change (Gauld, 1953; Boyd et al.,
1980; Saito and Taguchi, 1996), light period (Gophen and Harris,
1981), and endogenous pattern (Sautour et al., 1996).
Generally, gut pigment content is employed to determine
instantaneous grazing rate and diel feeding pattern (Kiørboe et al.,
1985). However, ingestion of heterotrophic prey, such as ciliates and
heterotrophic dinoflagellates, which do not contain chlorophyll,
cannot be estimated by the gut fluorescence measurement. The diel
pattern of mesozooplankton feeding on heterotrophic prey was
unknown. The aim of this study was to investigate the diel feeding
pattern of mesozooplankton on phytoplankton and microzooplankton
and to assess the daily consumption of respective prey items in a
subtropical continental shelf ecosystem.
2. Method
We have conducted a total of 6 grazing experiments at 4 stations in
the East China Sea (ECS) (Fig. 1, Table 1). Two stations in the southern
ECS are located in the oligotrophic continental shelf water (Stn. 1) and
the area under the influence of Kuroshio upwelling (Stn. 2),
respectively. The two northern stations were affected by Changjiang
135
Table 1
In situ mesozooplankton biomass and the amount of biomass added to each experiment.
Station
Exp.
Date
Zooplankton biomass
added (μg C L− 1)
Field zooplankton biomass
(mg C m− 3)
1
1a
1b
2
3
3 dark
4
2002/9/2
2002/9/3
2003/4/25
2004/6/14
2004/6/14
2004/6/14
0.27
0.79
2.1
0.64
0.64
0.28
24.7
37.5
133.7
40.9
40.9
199.8
2
3
4
runoff at Stn. 3 and by Kuroshio at Stn. 4 (Gong et al., 1996). Five
experiments were conducted under normal day–night cycle and 1
was incubated under total darkness to investigate whether light is the
main trigger of the diel feeding difference.
Seawater for grazing incubation experiments was collected from sea
surface using a plastic bucket and gently transferred into a large
polycarbonate carboy. The seawater was pre-screened by a 202 μm
Nylon net to remove mesozooplankton grazers before being filled into
2.3 L polycarbonate incubation bottles. Mesozooplankton were
obtained at each station using a 202 μm plankton net with a 2 L nonfiltering cod-end to minimize damage to the zooplankton by slow
horizontal hauls (about 1 knot for 10 min) at the surface (1 m). Volume
filtered was measured by a flow-meter mounted at the net mouth.
Mesozooplankton samples were transferred into an insulated container
that filled with surface seawater immediately after collection. Using a
2000 μm sieve to exclude large zooplankton, an aliquot of healthy free
swimming animals was placed into experimental bottles filled with
202 μm pre-screened seawater. Three control bottles without grazers
and 3 bottles with aliquots of mesozooplankton were set up for
incubation. In the lightless experiment, all bottles were wrapped in
aluminum foil to eliminate light effect.
The incubation temperature was controlled by running surface
seawater and a neutral screen was applied to reduce 25% surface light
intensity. The incubation proceeded about 24 h to cover the day/night
period. Samples were taken at the beginning, middle and the end of
the experiments. For estimating the difference of mesozooplankton
grazing during day and night, the middle samples were taken at dawn
or dusk during the incubation period. Microplankton samples were
Fig. 1. The study area of the East China Sea showing locations of the sampling stations.
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taken from each bottle (250 or 500 mL) and preserved with final
concentration of 2% buffered formalin and kept at 4 °C under darkness
conditions.
For the determination of the mesozooplankton biomass that was
added into experimental bottles, the same aliquots of zooplankton
were condensed on 65 μm Nylon mesh and dried in a 60 °C oven. A
portion of the net tow was also used to estimate the total dry weight.
All dry weight measurements were performed with triplicates. The
rest of net tow samples were collected on a sieve, transferred to a
500 mL plastic bottle, and preserved with 10% buffered formalin for
future identification and enumeration. Mesozooplankton dry weight
was converted into carbon biomass by a factor of 0.4 (Parsons et al.,
1984). Mesozooplankton samples for species identification and
enumeration were split with a Folsom Plankton Splitter to obtain a
subsample of approximately 500 animals which were identified and
counted. Copepods were identified to genus and other organisms
identified to group. Among all mesozooplankton, only copepods at
each station were used in Bray Curtis similarity analysis. Although
copepod only accounted for 40–90% of mesozooplankton abundance,
the majority of the individuals added into the incubation bottles were
copepods because the N2000 μm animals were excluded.
Microplankton, including ciliates, dinoflagellates and diatoms, was
counted by placing 100 mL subsamples in sedimentation chambers to
settle for at least 24 h (Utermöhl, 1958). Settled cells were then
counted by using an inverted microscope (Nikon-TMD 300) at 200×
or 400× magnification, with cell size also determined simultaneously
for biovolume calculation. Autotrophic and heterotrophic dinoflagellates were not separated. Cell biomass of ciliates was calculated using
a volume-to-carbon conversion factor of 0.14 pg C μm− 3 (Putt and
Stoecker, 1989). Biomass of diatoms and dinoflagellates were
calculated according to Menden-Deuer and Lessard (2000), the
volume-to-biomass equation log C = − 0.353 + 0.864 log V for
dinoflagellates, log C = − 0.541 + 0.811 log V for b3000 μm3 diatoms
and log C = − 0.933 + 0.881 log V for N3000 μm3 diatoms respectively,
where C is biomass (pg C cell− 1) and V is cell volume (μm3).
Mesozooplankton feeding coefficient and grazing rate were
calculated according to Frost (1972). Before computation of clearance
and ingestion rate, prey growth rates in the control and grazing
bottles were compared (t-test). Grazing rates were computed when
prey growth rate in control bottles was significantly higher than in
grazing bottles. Community grazing rate (μg C m− 3 h− 1) was estimated by converting the prey abundance to biomass and by
multiplying in situ zooplankton biomass (mg C m− 3).
Prey selectivity was calculated using the equation of Manly (1974)
α̂i =
Fig. 2. Initial abundance of microplankton community at each station.
at Stn. 3 was also twice as higher as at other stations. Pennate diatoms
were also dominated in microplankton community at Stn. 4, but the
quantity was one order of magnitude lower than at Stn. 3.
Mesozooplankton biomass in experimental stations ranged from
24.7 to 199.8 mg C m− 3 (Table 1). Copepods, cladocerans, bivalvia
larvae and doliolids were the main components of mesozooplankton;
they occupied N 80% of mesozooplankton abundance (Fig. 3A),
especially copepods that contributed 39–92% to mesozooplankton
community. The cluster analysis of the similarity of the copepod
assemblages between each experimental station (Fig. 3B) revealed
that there were two distinct groups, one was dominated by ambush
omnivorous predators (i.e. Oithona spp., Oncaea spp., Coryceus spp.)
and immature individuals (including Stn. 1, 2 and 3; Table 2), and the
other was dominated by filter grazers such as Paracalanus spp. (Stn. 4;
Table 2). It is noteworthy to point out that Exp. 1a and 1b, which were
conducted at Stn. 1 with grazers and experimental seawater collected
at day and night, respectively, contained similar predators (Fig. 3), but
quite different prey (microplankton) compositions (Fig. 2).
lnððni0 −ri Þ = ni0 Þ
k
∑ lnððnj0 −rj Þ = nj0 Þ
j=1
where i = 1,…, k; ri and ni0 are the number of food items of type i
present in the diet and in the environment at the beginning of
experiment, respectively. The index varies from 0 to 1 for any prey
types and values more than 1/k indicate positive selection.
3. Results
3.1. Microplankton and mesozooplankton composition
The abundance of microplankton, including ciliates, diatoms and
dinoflagellates (in both autotrophic and heterotrophic forms), in the
experimental waters were all b 5000 cells L− 1 except at Stn. 3 where
high diatom abundance was observed (Fig. 2). With the exception of
Exp. 1b, the microplankton community at Stn. 1 and 2 was similar
with high abundance of dinoflagellates (N3000 cells L− 1) and low
abundance of diatoms. Stn. 3, was dominated by pennate diatoms and
the abundance reached about 40 ×103 cells L− 1. The ciliate abundance
Fig. 3. Mesozooplankton composition in each experiment based on 5 major groups (A), and
the cluster analysis of copepod species composition calculated by Bray Curtis similarity (B).
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C.-J. Wu et al. / Journal of Experimental Marine Biology and Ecology 390 (2010) 134–142
137
Table 2
Dominant copepods in each experiment. Only genus that accounted for more than 5% of the total abundance are listed with their percentage of total copepod abundance in
parenthesis.
1a
1b
2
3
4
Paracalanus (27.9)
Copepodid + nauplii (19.2)
Oithona (16.2)
Oncaea (9.8)
Paracalanus (24.1)
Copepodid + nauplii (23.5)
Oithona (14.4)
Oncaea (9.1)
Calocalanus (7.4)
Copepodid + nauplii (69.1)
Acrocalanus (8.1)
Temora (6.8)
Calanus (5.4)
Copepodid + nauplii (56.5)
Coryceus (28.3)
Paracalanus (13.0)
Paracalanus (76.3)
Nannocalanus (9.9)
Copepodid + nauplii (5.2)
Table 3
Average feeding coefficient (h− 1, ± SE, n = 3) of each experiment during day and night time.
Exp.
Day
Night
Ciliate
1a
1b
2
3
4
a
0.017
0.073
0.146
0.064
−0.041
Diatom
(0.002)a
(0.003)a
(0.010)a
(0.015)a
(0.004)
− 0.031
0.117
− 0.198
− 0.008
0.013
Dinoflagellate
(0.002)
(0.030)a
(0.002)
(0.004)
(0.001)a
0.094
0.099
0.272
0.046
− 0.167
Ciliate
(0.007)a
(0.004)a
(0.044)a
(0.009)a
(0.016)
0.006
− 0.021
0.122
− 0.017
− 0.029
Diatom
(0.001)a
(0.003)
(0.017)a
(0.012)
(0.006)a
0.039
0.081
0.210
0.025
0.002
(0.007)a
(0.006)a
(0.018)a
(0.002)a
(0.002)
Dinoflagellate
−0.050
0.029
0.134
−0.012
0.094
(0.003)
(0.004)a
(0.031)a
(0.006)
(0.000)a
Denotes significant difference between grazing and control bottles.
3.2. Mesozooplankton grazing
Noticeable diel feeding patterns of mesozooplankton on different
prey items were observed. Except Exp. 4, high mesozooplankton
clearance and ingestion rates on ciliates or dinoflagellates usually
occurred during the day (Table 3, Fig. 4), and in contrary significant
mesozooplankton grazing on diatoms were usually observed at night
time. Exp. 4, which contained a different mesozooplankton assemblage
to other experiments, displayed an opposite diel grazing pattern.
The preference of prey items by mesozooplankton (selectivity index)
also displayed a significant difference between the day and night (Fig. 5).
Positive selections on ciliates and dinoflagellates at day and on diatoms at
night were evident, except in Exp. 4 which showed an opposite pattern.
The different selectivity towards different prey during day and night
indicated that the mesozooplankton assemblages in the experimental
sites exhibited prey switching between the day and night time.
We conducted a parallel experiment at Stn. 3 with a set of bottles
incubated under natural condition and another set of bottles kept at
Fig. 4. Mesozooplankton clearance and ingestion rates on ciliates, diatoms and dinoflagellates during day and night time.
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biomass varied dramatically among stations (Fig. 8). Mesozooplankton
carbon intake from microzooplankton (ciliates and dinoflagellates) was
always higher than that from phytoplankton (diatoms), even for Stn. 3
with abundance of diatoms more than one order of magnitude higher
than that of ciliates and dinoflagellates (Table 4). The contribution of
microzooplankton to mesozooplankton diet ranged from 51.4 to 99% in
the daily carbon intake and the contribution of dinoflagellates was
higher than ciliates.
4. Discussion
4.1. Diel feeding pattern
Fig. 5. Selectivity index calculated for mesozooplankton with respect to 3 microplankton prey types at day time (A) and night time (B), respectively.
complete darkness. The dark incubation resulted in a higher total
ingestion caused by higher ingestion rate on dinoflagellates with the
proportions from ciliates and diatoms remained the same (Fig. 6).
We analyzed the mesozooplankton clearance and ingestion rates on
preys of difference sizes. Since most diatoms and dinoflagellates were
b 20 µm ESD, only ciliate data were presented (Fig. 7). Except Exp. 4,
which observed no ingestion of ciliates, the general pattern that
mesozooplankton ingested more ciliates during day than during night
was held for ciliate in all sizes. Mesozooplankton clearance rate on ciliates
increased with ciliate sizes and reached a maximum at 30–40 µm ESD in
Exp. 1a, 1b and 2, while in Exp. 3, the clearance rates remained
approximately the same over the size range of ciliates (Fig. 7).
Total in situ grazing rate of mesozooplankton community extrapolated from measured ingestion rate and in situ mesozooplankton
Fig. 6. Ingestion rate of mesozooplankton on each type of microplankton in bottles
incubated under natural light–dark cycle and those wrapped in total darkness.
A notable diel prey switch of mesozooplankton assemblages was
observed in this study. The general pattern suggests active grazing of
mesozooplankton on ciliates or dinoflagellates during day time, but
switching to diatoms at night time (Fig. 4). Many previous studies
reported similar diel feeding patterns of mesozooplankton on phytoplankton (night N day) determined via gut chlorophyll content (Boyd
et al., 1980; Stearns, 1986; Dagg et al., 1989, 1997; Peterson et al., 1990;
Atkinson et al., 1996; Saito and Taguchi, 1996). However, there was no
study measuring the diel feeding pattern of mesozooplankton on the
other prey. A number of studies have explored the mechanisms of diel
feeding pattern (active grazing in night time) of mesozooplankton on
phytoplankton in the field (Boyd et al., 1980; Stearns, 1986; Dagg et al.,
1989, 1997; Peterson et al., 1990; Atkinson et al., 1996; Saito and
Taguchi, 1996) or in laboratory (Calbet et al., 1999). The majority of
existing literatures attribute the diel feeding pattern on phytoplankton
to the nocturnal upward vertical migration into the food-rich surface
layer (Gauld, 1953; Peterson et al., 1990; Atkinson et al., 1996; Saito and
Taguchi, 1996). However, a competing hypothesis suggests that diel
feeding pattern and vertical migration of mesozooplankton are
controlled independently. The high grazing rate occurred in night
time because during the day the feeding copepods might attract visual
predators by their foraging movements and by enhanced visibility of
their fully packed guts (Stearns, 1986). Therefore, feeding in day time
would increase the risk of being detected by visual planktivores. The diel
grazing pattern switch not only occurred in the migration species, the
phenomenon was also observed in the non-migration species (Peterson
et al., 1990). These species did not perform diel vertical migrations, but
the grazing behavior was also controlled by diel change in the light
rhythm (Peterson et al., 1990). In our study, the main copepod taxa
included Paracalanus, Oithona and Oncaea, which exhibited no vertical
migration (Peterson et al., 1990; Tang et al., 1994) or just small scale
migration (Tanimura et al., 2008), therefore the variation in zooplankton composition between day time and night time were insignificant
(Exp. 1a and 1b; paired t-test, p N 0.05). Thus the different grazing
response of mesozooplankton on each prey between day and night
might be a responsive behavior of mesozooplankton to the diel variation
of environmental parameters or an endogenous behavior.
A comparison between normal (Exp. 3) and darkness (Exp. 3 dark)
experiments resulted a similar diel feeding pattern (Fig. 6), although a
higher ingestion rate in dark incubation due to enhanced ingestion of
dinoflagellates, which suggested that light rhythm was not the main
controlling factor of diel feeding pattern of mesozooplankton. Instead,
the change in mesozooplankton feeding behavior over day and night
time may follow their endogenous feeding rhythm. Several previous
studies support this hypothesis; they found that copepods maintain
endogenous feeding rhythm under constant darkness (Stearns, 1986;
Calbet et al., 1999).
Light might also affect on the activity of protist prey, including
movement (Tomaru et al., 2001), feeding, digestion and growth (Strom,
2001). These activities may affect the quality of the protist prey and the
detection and interception by mesozooplankton. The mechanisms
regulating the shifting of feeding behavior of mesozooplankton between
day and night remain unclear and further study is needed.
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C.-J. Wu et al. / Journal of Experimental Marine Biology and Ecology 390 (2010) 134–142
139
Fig. 7. Size-specific clearance and ingestion rates of mesozooplankton assemblages on ciliates of different sizes.
4.2. Prey preference
Many studies show that the prey compositions in the diet of
copepods and in the ambient seawater are different, demonstrating
selectivity in the feeding processes (Wiadnyana and Rassoulzadegan,
1989; Kleppel, 1993; Kiørboe et al., 1996). It is well known that many
copepod species tend to positively select ciliates and dinoflagellates
over phytoplankton (Wiadnyana and Rassoulzadegan, 1989; Castellani
et al., 2008; Yang et al., 2009; Jing et al., 2010). The selectivity index
calculated from our results revealed a significant different prey
preference between day and night time (Fig. 5); the mesozooplankton
assemblages preferred ciliates and dinoflagellates at day time, but
switched to prefer diatoms at night time.
The different feeding behavior among copepod species might be the
cause of prey switch between day and night. Greene (1988) summarized the interaction between swimming and feeding behaviors and
the resulting dietary habit of calanoid copepods. There are two types
of swimming and feeding modes of copepod; one is the stationary
Table 4
Estimates of mesozooplankton community grazing rate on microzooplankton (microzoo) and phytoplankton (phyto) and the proportion of daily intake from different prey
items.
Exp.
Fig. 8. In situ daily ingestion rates of mesozooplankton assemblages on ciliates, diatoms
and dinoflagellates.
1a
1b
2
3
4
Ingestion (μg C m− 3 day−1)
Daily proportion (%)
Microzoo
Phyto
Microzoo
Phyto
67.9
16.1
433.0
67.8
397.7
0.6
1.8
1.8
64.1
28.6
99.1
89.9
99.6
51.4
93.3
0.9
10.1
0.4
48.6
6.7
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swimming mode, in which the copepod creates a suspension feeding
current, and the other is the ‘cruise and sink’ or continuously cruising
mode, which is more closely related to the predatory-feeding mode.
Tiselius and Jonsson (1990) made a detailed analysis of swimming
behavior and divided copepods into slow-moving or stationary
suspension feeder, fast swimming with periods of sinking, and sinking
with short jumps. The different swimming behavior reflects the
difference in feeding strategies. The stationary suspension feeding was
mostly efficient for capture of non-motile prey, while the fast swimming
or sinking mode is better for capture of moving, rheotactic prey (Tiselius
and Jonsson, 1990).
The mesozooplankton grazers in our study sites were not completely
composed of suspension feeders (such as Paracalanus); copepods with
the capability of prey switching and selective feeding to obtain the
essential nutrition were also abundant (Table 2). Suspension feeders,
including Paracalanus, Temora (Tiselius and Jonsson, 1990), Calanus
(Eiane and Ohman, 2004), Nannocalanus, Acrocalanus and Calocalanus
(Timonin, 1971), accounted for less than 30% of the copepod
communities, except at Exp. 4. Omnivorous ambush feeders that have
the foraging strategy of prey selectivity toward motile prey (Tiselius and
Jonsson, 1990), including Oithona (Paffenhöfer, 1998), Oncaea and
Coryceus (Timonin, 1971), were also abundant in our study. Moreover,
most nauplii and the copepodid of some species cannot create feeding
current because of the incomplete development of appendages; instead
they encounter food by active swimming (Gauld, 1958; Uchima and
Hirano, 1988; Paffenhöfer et al., 1996). A general trend between the
feeding selection pattern and the composition of mesozooplankton
community was observed in our results. There was a positive
relationship between the percentage of omnivorous ambush feeder
Fig. 9. Relationships between the proportion of mesozooplankton that belongs to
ambush omnivores and the clearance rate on specific prey items. Open circle represents
the day time rate and filled circle the night time rate.
and the mesozooplankton clearance rate on ciliates (r2 = 0.25, p = 0.03;
Fig. 9). An opposite, but less robust trend appeared on diatoms and
dinoflagellates, indicating the uncertainty of feeding preference of
grazers. The mesozooplankton community at Stn. 4 was dominated by
Paracalanus spp., which is considered suspension feeding species.
However, our results suggest that they prefer dinoflagellates rather
than diatoms, which may be attributed to the better nutritional value of
dinoflagellates over diatoms (Kleppel, 1993; Liu et al., 2010).
Our results also showed that mesozooplankton cleared large
particles more efficiently, which agreed with other studies of copepod
dominated mesozooplankton assemblages (Liu et al., 2005). A number
of studies have reported higher clearance rates on larger-sized prey for a
number of copepod species (Paffenhöfer, 1988; Rollwagen Bollens and
Penry, 2003). On the other hand, relative steady clearance rates over the
prey size ranges observed in Exp. 3 (Fig. 7) can be related to the high
abundance of doliolids and cladoceran, which are efficient at feeding on
small particles (Kremer and Madin, 1992; Katechakis and Stibor, 2004).
4.3. Dietary composition
A number of previous studies in the ECS focused on the spatial and
temporal variation of zooplankton biomass and composition and their
relationship with environmental parameters (e.g., Shih and Chiu,
1998; Zuo et al., 2006), but only few reports on copepod grazing using
gut pigment analysis (e.g. Hwang et al., 1998). Our data present the
first study to discuss the mesozooplankton dietary composition in the
ECS.
Our results showed that microzooplankton (ciliates and dinoflagellates) contributed more than phytoplankton (diatoms) to total
mesozooplankton carbon ingestion at all experiments, including
experiment at Stn. 3 where diatom abundance was one order of
magnitude higher than that of ciliates and dinoflagellates (Table 4,
Fig. 8). The results were consistent with the result of Calbet and Saiz
(2005) and were on line with studies conducted in other geographic
locations (Table 5). Results in Table 5 suggest that contribution of
microzooplankton to the diet of mesozooplankton could vary in a
wide range with different prey composition. Tiselius (1989) reported
that under low concentration of aloricate ciliates, the contribution of
ciliates to the diet of copepod was negligible. Fessenden and Cowles
(1994) reported that ciliates contributed 16–100% of the carbon
ingested by copepods during non-upwelling months and between
diatom blooms in Oregon coastal water. On the other hand, the
contribution of ciliates was insignificant during diatom bloom.
Microzooplankton also occupied low percentages (7–14%) of copepod
diet in an upwelling filament off Spain coast (Batten et al., 2001;
Halvorsen et al., 2001). Kleppel et al. (1998) reported that the
contribution of microzooplankton to the diet of A. tonsa ranged from
16% to 70%. At Mississippi River plume, where pennate diatoms
dominated, microzooplankton in the diet of mesozooplankton
increased with ciliate abundance; but under diatom bloom condition,
ciliate contributed more than 30% carbon ingest (Liu et al., 2005). In
our study, the contribution of microzooplankton in the diet is
significant and unproportionate to ambient abundance, indicating
clear prey selections of mesozooplankton in the ECS.
In conclusion, a diel feeding pattern of mesozooplankton presenting higher grazing rate and selection on diatoms at night time and the
contrary reaction on ciliates and dinoflagellates was revealed in this
study. The remarked diurnal switching in prey selectivity might be an
endogenous behavior rather than a reaction to the light–dark cycle,
and could be influenced by the composition of mesozooplankton
species with different feeding modes. Results from our study also
showed higher carbon intake from ciliates and dinoflagellates than
from diatoms even under high diatom abundance, confirming the
importance of microzooplankton as an important food source for
mesozooplankton in subtropical shelf waters.
Author's Personal Copy
C.-J. Wu et al. / Journal of Experimental Marine Biology and Ecology 390 (2010) 134–142
141
Table 5
Mesozooplankton community grazing on microzooplankton and the contribution of microzooplankton to mesozooplankton diet in this and other studies.
Area
Grazer
Prey
Community grazing rate Microzooplankton
Reference
contribution to diet
on microzooplankton
(%)
(mg C m− 3 day− 1)
East China Sea
Mesozooplankton
Natural assemblages
(diatoms, ciliates, dinoflagellates)
Natural assemblages
(chlorophyll a, ciliates)
Natural assemblages
(chlorophyll a, ciliates, dinoflagellates)
Natural assemblages
(chlorophyll a, ciliates, nanoflagellates)
Natural assemblage
(ciliates, dinoflagellates, nanoflagellates,
diatoms, picoeukaryotes)
Natural assemblages (diatoms,
ciliates, dinoflagellates, nanoplankton,
microflagellates)
Natural assemblage (chlorophyll a, ciliates)
0.02–0.6
51.4–99.6
This study
0.14–3.2
0.9–38.4
Liu et al. (2005)
0.01–0.03
7–15
0.08
21.3
Halvorsen et al. (2001); Batten et al.
(2001)
Zeldis et al. (2002)
Mississippi River plume Mesozooplankton
NW coast of Spain
Mesozooplankton
Subantarctic water off Copepod
New Zealand
Sea of Japan
Calanus sinicus
Neocalanus
plumchrus
Florida Bay
Acartia tonsa
Swedish coastal waters Acartia sp.
Centropages
hamatus
Oregon coastal waters Calanus paificus
Pseudocalanus sp.
Centropages
abdominalis
Acartia longiremis
Calanus pacificus
Natural assemblage (chlorophyll a, ciliates)
Acknowledgements
We are grateful to Dr. C.-T. Shih of National Taiwan Ocean University
for his constructive comments on this work. We also thank the officers
and crew members of the R.V. ‘Ocean Research I’ and R.V. ‘Ocean
Research II’. This study was supported by grants from the National
Science Council, ROC (NSC 94-2611-M-019-003) to K.-P. Chiang, and
Hong Kong RGC (661809) to H. Liu.[SS]
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