Feeding and egg production of the planktonic copepod Calanus ...

JOURNAL OF PLANKTON RESEARCH

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Feeding and egg production of the planktonic copepod Calanus sinicus in spring and autumn in the Yellow Sea, China YUAN-ZI HUO1,2, SHI-WEI WANG1,2, SONG SUN1*, CHAO-LUN LI1 AND MENG-TAN LIU1,2 1

KEY LABORATORY OF MARINE ECOLOGY AND ENVIRONMENTAL SCIENCES, INSTITUTE OF OCEANOLOGY, CHINESE ACADEMY OF SCIENCES, 266071, CHINA AND 2GRADUATE SCHOOL, CHINESE ACADEMY OF SCIENCES, BEIJING 100049, CHINA

7 NANHAI ROAD,

QINGDAO

*CORRESPONDING AUTHOR: [email protected] Received January 23, 2008; accepted in principle February 25, 2008; accepted for publication February 27, 2008; published online March 4, 2008 Corresponding editor: Roger Harris

Shipboard incubations were conducted in spring (April) and autumn (October/November) 2006 to measure the feeding and egg production rates (EPR) of Calanus sinicus in the Yellow Sea, China. The ingestion rate (2.08 – 11.46 and 0.26– 3.70 mg C female21 day21 in spring and autumn, respectively) was positively correlated with microplankton carbon concentrations. In the northern part of the Yellow Sea, feeding on microplankton easily covers the respiratory and production requirements, whereas in the southern part in spring and in the frontal zone in autumn, C. sinicus must ingest alternative food sources. Low ingestion rates, no egg production and the dominance of the fifth copepodite (CV) stage indicated that C. sinicus was in quiescence inside the Yellow Sea Cold Bottom Water (YSCBW) area in autumn. Calanus sinicus ingested ciliates preferentially over other components of the microplankton. The EPR (0.16 –12.6 eggs female21 day21 in spring and 11.4 eggs female21 day21 at only one station in autumn) increased with ciliate standing stock. Gross growth efficiency (GGE) was 13.4% (3– 39%) in spring, which was correlated with the proportion of ciliates in the diet. These results indicate that ciliates have higher nutrient quality than other food items, but the low GGE indicates that the diet of C. sinicus is nutritionally incomplete.

I N T RO D U C T I O N Copepods dominate the mesozooplankton in the oceans and play a key role in transferring primary production to higher trophic levels in all marine pelagic ecosystems (Verity and Smetacek, 1996). Knowledge about rates of production and grazing is crucial to understanding the flux of carbon and nutrients through the food web (Satapoomin et al., 2004). In the Yellow Sea and East China Sea, Li et al. (Li et al., 2002) reported the grazing rates of planktonic copepods in autumn 2000 and spring 2001. They showed that significant proportions (84 and 67%, respectively) of total carbon ingested by

small copepods (,500 mm) came from phytoplankton, whereas only small proportions of phytoplankton were consumed by large copepods (.1000 mm). In these waters, Zhang et al. (Zhang et al., 2006b) found that 31– 50% of the Chl a stock and 81– 179% of the Chl a production were grazed per day by microzooplankton in spring and summer. These characteristics suggest that an active community of small organisms recycles a great deal of phytoplankton production in microbial food webs (Bradford-Grieve et al., 1999) and that phytoplankton carbon ingested by large copepods (.1000 mm) cannot meet their metabolic and production

doi:10.1093/plankt/fbn034, available online at www.plankt.oxfordjournals.org # The Author 2008. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]


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requirements. This implies that microheterotrophic food sources (mainly ciliates) may be important in sustaining populations of large copepods (Zeldis et al., 2002). The importance of calanoid copepods in marine food webs and in the geochemical transformations that govern the fate of carbon in the upper ocean has stimulated considerable research on the foraging behavior, feeding rates and diets of these animals (Kleppel et al., 1996, and references cited therein). Calanus sinicus is an ecologically important large calanoid copepod species found in shelf waters around China, Japan and Korea, and it accounts for as much as 80% of the total zooplankton biomass in the Yellow and East China Sea (Chen, 1964). In the Yellow Sea, previous studies on C. sinicus were focused mostly on life history strategies in summer (Sun et al., 2002; Wang et al., 2003; Pu et al., 2004a, b) and on seasonal variations of reproduction rates (Zhang et al., 2005; Wang et al., unpublished results). Li et al. (Li et al., 2004) reported that the daily ration of C. sinicus was 2.8% of body C day21 grazing on phytoplankton, which cannot meet their metabolic requirements in summer. Using the herbivore index method, Zhang et al. (Zhang et al., 2006a) showed that 17.5 and 51.2% of non-phytoplankton carbon constituted the diet of C. sinicus in spring and autumn in the Bohai Sea, which is adjacent to the Yellow Sea. In contrast, Uye and Murase (Uye and Murase, 1997) reported that microzooplankton is an unimportant food item for C. sinicus females in spring (from April to June) in the Inland Sea of Japan. Nevertheless, the relative importance of different food items, especially ciliates, within the natural diet of C. sinicus, and the direct contribution of this prey item to egg production remain uncertain. The aims of this study were to investigate the composition of the diet of natural populations of C. sinicus, together with selectivity measurements, to determine the relationship between feeding (especially on ciliates) and egg production. These investigations help provide a greater understanding of the variability of C. sinicus production and the role of this species in transferring material and energy between trophic levels of the Yellow Sea ecosystem.

METHOD Experiments were conducted onboard the R.V. “Bei-Dou” during two cruises in the Yellow Sea in spring (11– 29 April) and autumn (17 October– 3 November) 2006. Figure 1 shows the locations of six and five experimental stations in spring and autumn, respectively. At each station, vertical temperature and salinity

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Fig. 1. Map of study area and localities of experimental stations in the Yellow Sea for spring (square) and autumn (circle).

profiles were recorded with a Sea-Bird (SBE 25) CTD. Seawater samples for the measurement of Chlorophyll a (Chl a) were collected from depths of 0, 10, 20, 30 and 50 m and close to the bottom. These samples were filtered onto GF/F glass-fiber filters, extracted using 90% aqueous acetone, and the concentration of Chl a determined fluorometrically (Parsons et al., 1984) using a Turner Designs fluorometer. Zooplankton were sampled with two types of conical plankton net (0.8 m mouth diameter, 500 mm mesh size and 0.5 m mouth diameter, 160 mm mesh size), which were towed vertically from near the bottom to the surface. Samples were preserved in 5% neutralized formalin seawater solution. In the laboratory, the samples were split into 1/2 to 1/5 subsamples with a Folsom splitter and 500– 1000 C. sinicus individuals were counted from each sample under a dissecting microscope.

Feeding experiments The C. sinicus for onboard incubation were collected with the 500 mm plankton net towed vertically from 2 m above the sea bed to the surface. Contents of the cod-end were carefully poured into an insulated container and only healthy adult females were used for experiments. Seawater for experiments was collected from the Chl a maximum (10 m depth in spring and 30 m depth in autumn) with a 59 L steel sampler and was gently transferred to a 20 L polycarbonate bucket through tubing with a 200 mm mesh at one end. The females of C. sinicus for experiments were dispensed into 1.3 L polycarbonate bottles filled with well-mixed seawater. To determine the ingestion rate, 9, 12 or 15

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individuals were incubated in each bottle. The concentration of N and P excreted by copepods in the bottles was higher than the initial nutrient concentrations, which might have helped enhance phytoplankton growth in these bottles (Zhang et al., 2006b). Hence, a nutrient mixture (10 mM NaNO3, 10 mM Na2SiO3, 1 mM NaH2PO4) was added to all bottles to override the difference in C. sinicus excretion among treatments (Calbet and Landry, 1999). Six replicates and six control bottles were incubated in the dark at the same temperature as the water from where they were collected. The bottles were inverted gently every 4 h during incubations. At the end of the experiments, the samples were checked for dead individuals but none were found. Copepods were sieved and then rinsed with distilled water onto pre-weighted, pre-combusted (4508C) glass filters (Whatman GF/F) and dried overnight at 608C to determine C. sinicus DW and body C content which was measured with an Elemental Analyser (P-E 240 C). Three 800 mL seawater samples were taken at the beginning and end of experiments for determination of microplankton abundance. After 12 h, three of six replicates and three of six controls were terminated and 800 mL seawater sample was taken from each bottle and the other incubations were sampled at 24 h. All samples were preserved with acid Lugol’s iodine (1% final concentration) for counting of potential prey items. Identification and counting of the microplankton were conducted after the samples underwent overnight sedimentation. Using a Zeiss microscope, more than 1000 microplankton cells were counted per sample. The microplankton size was expressed as ESD (equivalent sphere diameter). Cell volumes were estimated from linear dimensions using simple volumetric formulae and converted to carbon according to Strathmann (Strathmann, 1967) for diatoms, Menden-Deuer and Lessard (Menden-Deuer and Lessard (2000) for dinoflagellates, Putt and Stoecker (Putt and Stoecker, 1989) for naked ciliates, Verity and Langdon (Verity and Langdon, 1984) for tintinnids and Mullin (Mullin, 1969) for other microplankton groups. Filtration and ingestion rates in the incubations were calculated according to the equation of Frost (Frost, 1972) for the taxa that exhibited a significant difference in abundance between controls and incubation bottles. The “general method” proposed by Nejstgaard et al. (Nejstgaard et al., 2001) was used to correct the bias caused by microzooplankton grazing pressure outweighing the copepod grazing rates on the smaller food items in the incubation bottles. Unfortunately, dilution experiments (Landry and Hassett, 1982) were not run simultaneously with the bottle incubation at each station. In this study, the

microzooplankton grazing coefficient in the Yellow Sea (gmic = 0.66 day21) was used (Zhang et al., 2006b). The ingestion rates were compared with C. sinicus respiration requirements estimated by Ikeda (Ikeda, 1985), after correction for egestion losses (Landry et al., 1984), to compare food intake with metabolic and production requirements. Selection for specific microplankton groups/species was quantified using the selectivity index, E, proposed by Ivlev (Ivlev, 1961) and modified by Cotonnec et al. (Cotonnec et al., 2001): E¼

ri pi ; ri þ pi

where ri is the relative proportion of one microplankton group/species in the diet of C. sinicus and pi is the relative proportion of the same group/species in the environment. Thus, 20.25 , E, + 0.25 indicates nonselective feeding, E . +0.25 indicates a preference, and E , 20.25 indicates discrimination against particular prey items.

Egg production rates The egg production rates (EPR) of C. sinicus were measured synchronously with the feeding experiments at each station. Plastic bottles (350 mL) partitioned with a 330 mm mesh screen at the bottom were used to avoid cannibalism. Five adult females were incubated in one plastic bottle filled with 70 mm filtered seawater and five replicates were used in each experiment. All bottles were incubated in the dark. Eggs spawned during the first 24 h were counted. The temperature in the incubator was set to equal the temperature in the feeding experiments. The diameter of 30 – 50 eggs was measured under the microscope. Egg carbon content was estimated from egg volume assuming a conversion factor of 0.14 pg C mm23 (Kiørboe et al., 1985; Huntley and Lopez, 1992).

Data analysis All statistical analyses were performed using SPSS software (v.13.0 SPSS Inc.). The ingestion rates of C. sinicus and the characteristics of the females and eggs during the periods of the study were compared by one-way ANOVA ( post hoc Scheffe´ test). The relationships between ingestion rates and EPR of C. sinicus were performed by simple regression.

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Feeding environments

R E S U LT S Hydrographic conditions Figure 2 shows vertical profiles of temperature, salinity and Chl a at experimental stations during the spring and autumn cruises. In spring, the water column was vertically mixed except at the shallowest station (B), where the thermocline occurred between 23 and 24 m. The surface temperature ranged from 7.6 to 12.08C and salinity ranged from 31.5 to 34.2. At stations A1 and C1, the highest Chl a concentration occurred at 10 m depth (11.89 mg m23) and in surface water (5.83 mg m23), respectively, and then decreased significantly with depth. The maximum value of Chl a ranged from 1.28 to 2.27 mg m23 at other stations and changed little with depth. During the study period in autumn, the presence of Yellow Sea Cold Bottom Water (YSCBW) resulting from stratification was apparent and the seasonal thermocline located between 30 and 50 m depth. Surface temperatures were in the range of 20.0 – 22.78C, and bottom temperatures were 8.0– 9.68C (except station H, at 14.88C). The Chl a concentration was significantly lower than it was in spring, with maximum values located at 30 m at all stations.

The initial composition and biomass of the microplankton differed substantially both during the two cruises and between stations (Fig. 3). During spring, the biomass of microplankton ranged from 14.0 to 271.8 mg C m23. At station A1, diatoms (Skeletonema costatum 5.8 mm, Thalassiosira spp. 6.5– 15.3 mm) dominated the microplankton community and dinoflagllates and ciliates were less important than at the other stations. At the other stations, despite differences in biomass, the dominant species were similar. Rhizosolenia stolterforthii (17.0 mm), Thalassiosira spp., Guinardia flaccida (7.3 mm), and S. costatum were the dominant diatom species. The dominant dinoflagellates were Prorocentrum minimum (7.1 mm), Gymnodinium spp. (6.75 –7.88 mm), Gonyaulax sp. (19.2 mm), and Alexandrium tamarense (16.4 mm). The most common ciliates were Laboea strobila (27.5 mm), Strombidium sp. (22.8 mm), Mesodinium rubrum (15.5 mm) and two other unidentified ciliate species (6.45 and 14.5 mm). During autumn, the total microplankton biomass exceeded 50 mg C m23 at station H, but was ,10 mg C m23 at the other stations. Dinoflagellates and ciliates dominated the biomass except at station H where

Fig. 2. Depth profiles of physical and biological parameters at different experimental stations in spring and autumn.

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Fig. 3. Initial composition and concentration (+SD) of different microplankton groups at different experimental stations in spring and autumn.

diatoms contributed an estimated 24.6 mg C m23 of the microplankton carbon pool. Across all stations, Bacteriastrum hyalinum (10.4 mm), Chaetoceros curvisetus (6.6 mm), Ditylum brightwelli (52.7 mm), Corethron hystrix (26.4 mm), Gyrodinium spp. (4.7 – 14.2 mm), and two small unidentified dinoflagellates (6.6 and 9.1 mm) were the dominant species, contributing most to the diatom and dinoflagellate biomass. Laboea strobila disappeared and the biomass of other ciliate species decreased sharply to 1.2– 9.3 mg C m – 3.

Abundance and stage composition of C. sinicus Figure 4 shows the abundance and stage composition of C. sinicus. Nauplii and copepodites I– IV were the dominant developmental stages at all stations during spring and at station H during autumn. However the fifth copepodite stage (CV) and adult females dominated the populations at the other stations in autumn.

Ingestion and prey selection The ingestion prey carbon (C) of C. sinicus in the 0 –12 h interval and over 24 h at different stations after

Fig. 4. Developmental stage composition of C. sinicus at different experimental stations in spring and autumn.

correction are shown in Fig. 5. At stations A1, B and C1 in spring, after the 24 h incubation, the average decrease in total prey C concentration was 38– 46% (33 – 51% for diatoms, 11– 51% for dinoflagellates and 55– 66% for ciliates) and the biomass of microplankton that remained was 106.7 – 168.6 mg C L21, which is sufficient to supply enough food for C. sinicus. Thus, the ingestion rates of 11.30, 10.06 and 11.46 mg C female21 day21, based on the 24 h incubation, should be close to the true ingestion rates in the natural microplankton assemblages at stations A1, B and C1. The prey C ingested by C. sinicus over 12 and 24 h incubations was 6.74 and 7.58 mg C female21, respectively, at station D1, which means that little net gazing occurred in the 12 –24 h interval; this was probably because little prey biomass remained after 12 h (ca. 30% of initial concentration). The 6.74 mg C female21 in the first 12 h interval was similar to the 6.92– 7.23 mg C female21 ingested by C. sinicus in the 0 – 12 h interval at stations A1, B and C1. Thus, in the constant and relatively high biomass of the natural microplankton assemblages (107.2 mg C m23) of station D1, the ingestion rate of C. sinicus likely would be similar to that

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Fig. 5. Ingestion of prey carbon (mg C female21) by C. sinicus in the 0–12 h interval and over 24 h incubations in spring and autumn.

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whereas in autumn the ingestion rate at station H was significantly higher than that at the other stations (P , 0.01). In general, the C. sinicus ingestion rate of microplankton was higher in spring than in autumn. Ingestion rates were significantly correlated with the initial microplankton, diatom, dinoflagellate and ciliate carbon concentrations for all of the data sets (P , 0.05, data not shown). Overall, ingestion rates of ciliates were positively correlated with initial ciliate carbon concentrations (Fig. 6A). Table II shows the selectivity index of C. sinicus feeding on three main food items. Calanus sinicus females preferentially ingested ciliates at almost every station. At stations B, D1 and H, the contribution of dinoflagellates to the total microplankton biomass was high (41, 66 and 39%, respectively), yet C. sinicus ingested diatoms and ciliates, which were less abundant. Calanus sinicus females ingested other microplankton groups preferentially over diatoms at stations F, A2, and C2 because of the relatively lower abundance of diatoms present. During spring at station E, where the diatoms contributed the largest proportion of microplankton (63%), C. sinicus selectively fed on dinoflagellates and ciliates.

Carbon budget of C. sinicus 21

of the other three stations. The 9.98 mg C female day21 ingestion rate (average of ingestion rates at stations A1, B and C1) was assumed to be the true ingestion rate of C. sinicus at station D1. For the other stations in spring and all stations in autumn with low initial microplankton biomass (5.40 – 54.69 mg C m23), the prey C ingestion determined in the 12 – 24 h interval was very low, or even negative, indicating that little net grazing occurred in the second 12 h interval; this suggests that there was appreciable bias related to the time of sampling or to relatively high stocking density of copepods in the bottles (see Discussion). Because of this, ingestion rates were estimated using the 0 – 12 h incubation results for C. sinicus at these stations (Table I). Ingestion by C. sinicus was very low for three of the six microplankton groups (haptophytes, cryptophytes and chlorophytes; Fig. 5), probably due to small particle size and low biomass compared with other groups. At station E in spring, the ingestion rate of diatoms was statistically negative, indicating that little net grazing occurred over 24 h and that a cascade effect existed (Fig. 5; see Discussion). Across all stations, ciliates contributed 1.55 – 36.17 and 15.10 – 33.09% to the carbon intake of C. sinicus during spring and autumn, respectively. The C. sinicus ingestion rate was significantly higher at the northern stations (A1– D1) than that at the southern stations (E and F) in spring (P , 0.01),

Daily ingestion was 9.2– 13.0% of body carbon at stations A1, B, C1 and D1, which easily covered the respiratory requirements and supplied substantial carbon for reproduction (Table I). For C. sinicus at station E, ingestion of microplankton almost balanced respiratory demands (93%) but supplied nothing for reproduction. For C. sinicus at other stations, only 6 – 53% of respiratory requirements were met and hence animals still had a deficit, equivalent to 4.6 – 5.7% of body C, in carbon for reproduction.

Egg production and its relation to ciliate ingestion During spring except at station D1 (no eggs), the mean EPR of C. sinicus ranged from 0.16 to 12.6 eggs female21 day21, and during autumn except at station H (11.4 eggs female21 day21), no reproduction by C. sinicus was observed over 24 h incubations (Table III). In spring, the mean body carbon of C. sinicus females at station B1 was 109.9 + 5.6 mg C, which was significantly higher than that at stations A1 and D1 (P , 0.05) but not statistically different from that at stations C1, E and F. The mean C contents of C. sinicus females at the experimental stations during autumn were not statistically different from each other but were significantly lower than the values in spring (Table III,

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Table I: Ingestion, respiration and ingested carbon available for reproduction of C. sinicus that feed on microplankton at different stations in spring and autumn Ingestion Time

Station

mC female21day21

% body C day21

Respiration (% body C day21)

% Respiratory demands meta

C for reproduction (% body C)b

11 –29 April 2006

A1 B C1 D1 E F A2 G C2 D2 H

11.30 10.06 11.46 9.98 2.08 5.30 0.33 0.56 0.26 0.43 3.70

13.0 9.2 11.6 11.2 2.0 5.8 0.4 0.7 0.3 0.6 4.9

5.0 4.6 5.9 6.0 6.2 6.2 6.0 5.6 5.9 6.0 9.1

261 200 195 187 33 93 7 13 6 10 53

5.4 2.7 3.3 3.0 24.6 21.6 25.7 25.0 25.6 25.6 25.2

17 October– 3 November 2006

a

“% respiration demands met” is ingestion (as % body C day21)/respiration (as % body C day21) 100. “C for growth” is ingestion (as % body C day21) 0.82respiration (as % body C day21), where 0.8 scales for non-egested proportion.

b

P , 0.01). The C content of eggs was significantly higher at stations A1, E and F than the values at stations B and C1 (Table III, P , 0.01).

Overall, no significant relationship existed between EPR and total microplankton, diatom and dinoflagellate carbon ingested, whereas a nearly positive correlation (P = 0.053) occurred between EPR and total ciliates ingested at all stations. The estimated gross growth efficiency (i.e. GGE = EPR/ingestion rate 100) ranged from 3 to 39% (average = 13.4%) in spring and 92% at station H in autumn. A positive relationship was observed between GGE and the percentage of ciliates in the diet (except at station A1, which had a low initial ciliate carbon concentration) in spring (Fig. 6B), indicating that ciliates had higher nutritional quality for C. sinicus than the other components of the microplankton. The high GGE at station H in autumn may have resulted from the low ingestion rate on microplankton and this indicated that C. sinicus must ingest other food resources (e.g. nauplii and copepodites of copepods and small copepods) which were not examined in the present study.

DISCUSSION Ingestion and food selection

Fig. 6. (A) Calanus sinicus ingestion rates of ciliates (+ SD) as a function of initial ciliate carbon concentration (+SD): spring (circle) and autumn (square). (B) Relationship between GGE and percentage ciliate carbon in the diet of females at different stations (except station A1) in spring.

The average decrease in total prey C concentration was 38– 46% after 24 h incubation at stations A1, B and C1, which is similar to the ca. 30– 40% decrease needed to yield significant difference between cell counts from grazer and control bottles in incubation experiments (Gifford, 1993; Ba˚mstedt et al., 2000). For C. sinicus at other stations, little or even negative ingestion of microplankton occurred in the 12– 24 h interval compared with the first 12 h interval (Fig. 5).

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The linear relationship between ingestion rates and Table II: Selective index of C. sinicus feeding microplankton standing stock for the whole data set on three main food items at different stations indicated that non-saturated feeding behavior of C. in spring and autumn Selective index Time

Station

Diatoms

Dinoflagellates

Ciliates

11 –29 April 2006


20.02 0.15 0.06 0.19 20.61 21.00 21.00 0.21 21.00 20.10 0.12

0.19 20.53 20.16 20.32 0.06 0.02 0.18 20.19 20.13 20.07 20.40

0.23 0.29 0.34 0.51 0.43 0.13 20.05 0.19 0.51 0.25 0.25


One possible explanation is that the initial microplankton concentrations were low and that the predation was so intense that prey stocks became very dilute after 12 h in these incubations; this explanation is consistent with a sub-threshold feeding functional response (Frost, 1975; Landry and Lehner-Fournier, 1988; Zeldis et al., 2002). The stocking density of C. sinicus in the bottles could have led to another experimental bias. The biomass of C. sinicus incubated per bottle (714 – 952 mg C L21) at these stations was sufficient to clear the 1.3 L seawater nearly 70% during the experiments, based on the maximum clearance rates at station C1 (data not shown). Thus, ingestion rates determined for phytoplankton and ciliates based on 24 h incubation results may be greatly underestimated at these stations due to prey depletion. Therefore, the 0 – 12 h ingestion rates are considered to be more accurate representations of true ingestion rates for microplankton at these stations.

sinicus occurred (Irigoien et al., 2000; Dam and Lopes, 2003). During spring at the four northern stations, the daily ration (R) of C. sinicus was 9.2– 13.0% of body C day21, whereas the R was 2.0 and 5.8% of body C day21 at two southern stations (E and F, respectively). During autumn at four stations inside the YSCBW area (Wang and Zuo, 2004), the R was only 0.3– 0.7% of body C day21, which is consistent with the data reported by Li et al. (Li et al., 2004) for summer. At station H, which was located in the frontal zone and had a relatively high Chl a concentration, the R was 4.9% body C day21. Based on these results, we conclude that C. sinicus is in the active feeding mode in the northern part of the Yellow Sea in spring and in a quiescent feeding mode inside the YSCBW area in autumn. The presence of diatoms, dinoflagellates, ciliates and other nanoplankton groups in the diet is indicative of the omnivorous character of C. sinicus feeding, which is consistent with the results from a number of previous studies (Yang, 1997; Zhang et al., 2006a). Gut content examination (Yang, 1997) and the gut pigment method (Zhang et al., 2006a), however, may substantially underestimate ingestion rates and bias prey-selectivity estimates. Different methodologies preclude a detailed inter-study comparison of ingestion and food selection. In the current study, particle sizes of diatoms, dinoflagellates, and ciliates ranged from ca. 6 to 53 mm, and C. sinicus could capture them efficiently. The other three nanoplankton items were represented by small cells (e.g. Chromulina sp. 3.3 mm, Isochrysis sp. 3.7 mm, Chroomonas sp. 2.7 mm and Cryptomonas sp. 3.6 mm) and likely were

Table III: Dry weight (+SD), egg weight (+SD), EPR (+SD) and GGE of C. sinicus at different stations in spring and autumn EPR Time

Station

Dry weight (mC female21)a

11 –29 April 2006


87.0 (10.4) 109.9 (5.6) 98.8 (7.8) 88.7 (3.1) 103.2 (8.1) 91.9 (4.6) 82.5 (2.8) 77.9 (2.4) 75.6 (3.6) 73.1 (1.0) 76.1 (1.6)


Egg weight (mC egg21)

Egg day21

mg C day21

Gross growth efficiency (%)b

0.35 0.31 0.30 — 0.37 0.39 — — — — 0.30

3.96 (5.08) 12.6 (7.25) 2.24 (5.01) — 0.16 (0.36) 0.96 (0.70) — — — — 11.4 (5.01)

1.40 3.89 0.68 — 0.06 0.38 — — — — 3.42

12.4 38.7 5.9 — 2.9 7.2 — — — — 92.4

a

Dry weight of females is given in terms of carbon content. GGE (%) was calculated as EPR/ingestion rate100.

b

730

(0.005) (0.03) (0.02) (0.01) (0.03)

(0.02)

(1.79) (2.24) (1.51) (0.13) (0.26)

(1.50)

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not efficiently captured (Paffenho¨fer, 1988; Kleppel et al., 1998).The selective index for ciliates, as well as the relationship between ingestion rates of ciliates and initial ciliate concentrations, indicated that C. sinicus clearly preferred ciliates over phytoplankton, which is consistent with the data from a number of previous studies (Zeldis et al., 2002; Castellani et al., 2005). Laboea strobila, Strombidium sp. and M. rubrum, the dominant species of ciliates in these experiments, also are preferentially ingested by other copepod species (Nejstgaard et al., 2001; Castellani et al., 2005; Liu et al., 2005). Although dinoflagellates contributed most to the biomass of microplankton, the selectivity indices indicated that C. sinicus discriminated against this prey item at stations B, D1 and H. Gonyaulax sp., P. minimum and Gyrodinium spp. were the dominant species at these stations, contributing 66, 83 and 82% of the dinoflagellate biomass, respectively. The lack of feeding on these species by C. sinicus may indicate that they are nutritionally insufficient or toxic (Delgado and Alcaraz, 1999; Albuquerque et al., 2005; Dam and Colin, 2005). However, C. helgolandicus and Temora stylifera exhibited high egg production and hatching rates when feed on P. minimum compared with diatoms (Laabir et al., 1999; Turner et al., 2001; Poulet et al., 2007). These results suggest that feeding interactions between copepods and dinoflagellates may be species-specific. Copepods might also diversify their diet depending on conditions, with higher selectivity indices for diatoms or ciliates when dinoflagellates are dominant, as already established by Kleppel (Kleppel, 1993). Low rates of ingestion of diatoms at stations F, A2 and C2 might have been due to their lower biomass (0.73, 0.41 and 0.16 mg C m23, respectively) compared with other items. Statistically negative feeding at station F indicated that a cascade effect occurred at this site: as the incubations proceeded, diatom growth in treatments was higher than diatom growth in controls, because diatoms in treatments were released from ciliate grazing pressure as the ciliates were consumed by C. sinicus, as indicated by Nejstgaard et al. (Nejstgaard et al., 2001) and Zeldis et al. (Zeldis et al., 2002). At station E, C. sinicus preferentially ingested dinoflagellates and ciliates over diatoms even though diatoms accounted for 63% of the microplankton biomass, which also emphasizes the importance of diversity in the diet. Diatoms contain abundant amounts of eicosapentaenoic acid (EPA), but the content of docosahexaenoic acid (DHA) is lower than that in dinoflagellates (Sargent et al., 1987 and references therein; Brown et al., 1997), and some amino acids may be scarce or lacking (Kleppel, 1993). Bonnet and Carlotti (Bonnet and Carlotti, 2001) reported that the daily specific growth rate for Centropages typicus was

significantly lower when it grazed on Thalassiosira weissfloggi, a cosmopolitan species of diatoms, compared with diets composed of other taxa. Thus, a diverse diet might increase the probability that copepods will obtain a nutritionally complete ration (Kleppel, 1993).

Carbon budget In spring, daily ingestion of microplankton by C. sinicus at stations A1, B, C1 and D1 easily covered respiratory requirements and supplied substantial carbon for production, but daily ingestion of carbon at stations E and F and in autumn at station H could not meet the copepods’ metabolic requirements, let alone acquire carbon for production. However, egg production experiments showed that 0.2, 1.0 and 11.4 eggs were produced per female at these three stations, respectively. This conflicting result suggests that other food resources may be very important for C. sinicus to sustain reproduction. Eggs and nauplii of copepods are very important food resources for adult copepods, and their ingestion could represent ca. .20% of the total daily egg production (Kang and Poulet, 2000; Harris et al., 2007). Zeldis et al. (Zeldis et al., 2002) reported that the total carbon flow to the large size fraction of copepods from small cyclopoid and calanoid copepods was 30 mg C m22 day21 in the New Zealand Subtropical Frontal Zone, which easily exceeded the daily growth requirements of large copepods. A high abundance of C. sinicus nauplli was observed at stations E, F and H (12 775, 3575 and 38 500 ind. m22, respectively). If eggs and nauplii of other copepods and small copepods (mainly 200– 500 mm) were also considered, C. sinicus could meet their respiratory and reproduction requirements by grazing on these food resources. During autumn at stations A2, G, C2 and D2, the daily carbon ration was only 0.3– 0.7% body C day21, indicating that there were large deficits between carbon ingested and carbon required for respiration and reproduction. These four stations were located inside the YSCBW area, where low temperatures and food concentrations (Fig. 2) resulted in the suspension of C. sinicus development and stage CV dominated the populations (Fig. 4). This finding is consistent with the results of previous studies showing that C. sinicus was in quiescence in autumn (Li et al., 2004; Pu et al., 2004a).

EPR and GGE The mean EPR was 3.98 (0 – 12.6) eggs female21 day21 during April, which was within the scope of monthly average EPRs reported by Zhang et al. (Zhang et al., 2005), whereas eggs were only produced at one

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experimental station during autumn. The EPR of C. sinicus was related to, but not quite significantly correlated with, total ciliates ingested, but not with total microplankton carbon. The GGE of C. sinicus also was positively correlated with the proportion of ciliates in the diet. These results suggest that for C. sinicus, ciliates provide better nutrition than other food particles (Kleppel, 1993) and result in enhanced egg production (Kleppel et al., 1991). This observation is consistent with the results of a number of other studies (Bonnet and Carlotti, 2001; Zeldis et al., 2002; Arendt et al., 2005; Castellani et al., 2005). Stoecker and Capuzzo (Stoecker and Capuzzo, 1990) noted that protozoa contain high amounts of essential nutrients, especially polyunsaturated fatty acids (e.g. EPA and DHA), sterols and amino acids. However, findings from the present study contrast with the results of Jońasdo´ttir et al. (Jońasdo´ttir et al., 1995), Dam and Lopes (Dam and Lopes, 2003) and Broglio et al. (Broglio et al., 2003), who found no evidence of the nutritional superiority of ciliates over phytoplankton. Strombidium sulcatum, one member of the dominant genus Strombidium sp. in the current study, was not considered to be nutritionally superior for copepods (Broglio et al., 2003) and no evidence was found for trophic upgrading of food quality by S. sulcatum cultured using either bacteria or the green alga Dunaliella sp. as a food source (Klein Breteler et al., 2004). However, in the present study and in others (Nejstgaard et al., 2001; Castellani et al., 2005; Liu et al., 2005), copepods ingested this ciliate at high rates, and high nutritional quality and trophic upgrading of food quality by Strombidium sp. might occur when fed on different phytoplankton taxa (Tang and Taal, 2005). The other dominant ciliates were ingested by C. sinicus at high rates as well, as also observed by Nejstgaard et al. (Nejstgaard et al., 2001), indicating that these ciliate species may contain high amounts of essential nutrients. However, the mean GGE (13.4%, range = 3 – 39%) estimated in the present study in spring is lower than the often used value of 30% (Ikeda and Motoda, 1978) and the mean and median values for copepods of 26% and 22% (Straile, 1997). The relatively low GGE in the present study may have resulted from the low egg production which might be affected by the nutrient composition of the diets of C. sinicus. The diets may be nutritionally inadequate to support high EPR; i.e. the diets lacked, or had insufficient concentrations of, specific nutrients essential, such as sterols and polyunsaturated fatty acids, for egg production (Dam and Lopes, 2003). In addition, the low egg production might be due to insufficient levels of nitrogen in the diet, as indicated by Tang and Dam (Tang and Dam, 1999) and Dam and Lopes (Dam and Lopes, 2003).

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CONCLUSION The results of this study have shown that in spring, the daily ration of microplankton ingested by C. sinicus can easily cover its basic metabolic and production requirements in the northern part of the Yellow Sea, whereas C. sinicus in the southern part must consume alternative food sources to sustain its respiratory and production needs. Low feeding rates and egg production and the dominance of stage CV in the population indicated that C. sinicus was in quiescence inside YSCBW area in autumn. Ciliates have higher nutritional qualities and were selectively removed by C. sinicus, but the low GGE that resulted from low egg production might be due to insufficient concentrations of specific nutrients in the diet. Future research will be required to elucidate the roles of alternative food sources in the diet and to discover which nutritional factors determine seasonal variability in the fecundity and egg viability of C. sinicus in the Yellow Sea.

AC K N OW L E D G E M E N T S We would like to thank crew on R.V. “Bei-Dou” for their assistance in the field and thank Prof. Da-Ji Huang and Xiu-Ren Ning for providing CTD and Chlorophyll a profiles. Thanks are due also to anonymous reviewers for their valuable comments and suggestions on the manuscript.

FUNDING Support from the NSFC (No.40631008) and the MOST (PN: 2006CB400606) to S. S. and the CAS (KZCX2-YW-213) to C.-L. L. is acknowledged.

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