Life history strategies of Calanus sinicus in the southern Yellow Sea in summer

Abstract

Ecological and physiological features of the planktonic copepod Calanus sinicus in the southern Yellow Sea in summer were studied to reveal its life history strategy. From the coastal shallow waters to the central part of the southern Yellow Sea, a shift of the stage composition occurs from being dominated by the egg-nauplius stage to being dominated by the fifth copepodite (CV) stage. Most CVs reside in the Yellow Sea Cold Water Mass (YSCWM), where both temperature and food abundance are low. CVs in the YSCWM have longer body lengths, heavier body weights and higher carbon contents than those outside the YSCWM. Onboard incubations show that the development of CVs in the YSCWM is suspended. Energy conservation, development suspension and lack of diel vertical migration (DVM) behavior suggest a diapause status for the CVs in the YSCWM, although vertical distribution patterns indicate the CV individuals are not fully synchronous in physiology and development. This adaptive oversummering strategy would help C. sinicus to live through the warm and food-limited summer in the central part of the southern Yellow Sea; both low temperature and low food supply are necessary for CV to maintain the resting state in the YSCWM. Calanus sinicus exhibits different life history strategies in different regions of the southern Yellow Sea in summer.

Received January 15, 2004; accepted in principle April 7, 2004; accepted for publication May 26, 2004; published online June 1, 2004

INTRODUCTION

Calanus sinicus is a dominant copepod species in the Yellow Sea (Chen, 1964). Calanus sinicus is part of the diets of many predators of different sizes, for example, sardine and anchovy (Zhu and Iverson, 1990; Meng, 2003), and plays an important role in the marine ecosystem. Calanus sinicus is one of the target species in the China-GLOBEC research program (Sun et al., 2002).

In previous studies on the ecology of C. sinicus in the southern Yellow Sea (Sun et al., 2002; Wang et al., 2003; Pu et al., 2004), the fifth copepodite (CV) stage is the dominant developmental stage in the central part of the Yellow Sea in summer, and most CVs and adults reside in the Yellow Sea Cold Water Mass (YSCWM). Temperature and food concentration play important roles in the development and energy conservation of C. sinicus (Pu et al., 2004). Low temperature and low food availability in the YSCWM cause C. sinicus to slow down its developmental rate at the CV stage, decrease energy consumption and thereby increase the possibility of survival (Li et al., 2004; Pu et al., 2004). Since the environmental conditions, such as temperature and food concentration, in the central part of the Yellow Sea are very different to those in the coastal shallow waters and in the waters near Cheju Island, C. sinicus may have different life history strategies in different regions in order to adapt to the environment. It was Chen who first pointed out that C. sinicus had a comparatively larger body size in the YSCWM during summer (Chen, 1964), but detailed information on, and an explanation for this phenomenon are still lacking. In order to understand and build models of the population dynamics of C. sinicus, it is imperative to learn whether different life history strategies apply to C. sinicus living in different environmental conditions and what the controlling environmental factors are.

The aim of this paper is to compare ecological and physiological features of C. sinicus living in different regions of the southern Yellow Sea. The abundance, stage composition and diel vertical migration (DVM) of C. sinicus along the transect between Qingdao and Cheju Island were investigated; body length, weight, carbon (C) and nitrogen (N) content of the CVs and adults were measured; and the molting rates of CV were measured by onboard incubation. The different life history strategies of C. sinicus in different circumstances and the controlling environmental factors were then discussed.

METHOD

Sampling

During August 16–20, 2002, a cruise was conducted onboard the R.V. ‘Bei-Dou’ in the southern Yellow Sea (Fig. 1). At each station, water samples were taken at different depths (0, 10, 20, 35, 50, 75 m, and 2–5 m from the bottom) with a 59 L steel sampler and were filtered with a 38 μm mesh net. The retentates were preserved in buffered 5% formalin seawater solution. Temperature and salinity from bottom to surface were measured with a SBE-25 CTD. Chlorophyll a (Chl a) concentration at each depth was measured with a Turner Designs Fluorometer after 500 mL seawater was filtered with a Whatman GF/F and pigment extracted with 90% aqueous acetone. Each stage (from egg to adult) of C. sinicus in the samples was identified and counted using a dissecting microscope. The individual depth measurements of population abundance [individuals (ind.) m⁻³] were used to calculate water column abundance (ind. m⁻²) by trapezoidal integration.

Fig. 1.

The Yellow Sea. Ten stations (Stns 1–10) were arranged along the transect from Qingdao, China, to Cheju Island, Korea. Contour lines indicate water depth.

From August 20 to 25, 2002, 24 h continuous sampling at 3 h intervals was conducted at four stations: Stns 3, 5, 7 and 8. In addition to the sampling methods mentioned above, vertical stratified zooplankton samples were obtained with a vertically towed 312 μm mesh net (0.8 m diameter). At least three water stratums were investigated with the net, towing above the thermocline, in the thermocline and below the thermocline. Prosome lengths (PL) of the CVs taken from different stratums were measured with a dissecting microscope.

Length, weight, condition factor, C and N content

In order to obtain measurements of length, weight, C and N contents, specimens of C. sinicus were obtained using a vertical towered zooplankton net (0.8 m mouth diameter and 312 μm mesh size) from bottom to surface. The samples were quickly diluted into beakers containing seawater obtained from below the thermocline. CVs, adult females and males of C. sinicus were then sorted, and PLs (from anterior end to the posterior lateral end of the prosome) were measured with a dissecting microscope. Dry weights (DW) were measured according to Omori (Omori, 1978). Proportions of C and N contents to DW were measured with a Perkin-Elmer 240C Element Analyzer using acetanilide as standard. The average C and N contents in individual copepods were calculated as the product of DW and the proportions of C and N, respectively. Condition factor (CF), expressed as weight per unit volume, is a measure of a copepod’s nutritional status (Durbin and Durbin, 1978; Durbin et al., 1983; Campbell et al., 2001). CFDW, CFC, CFN are DW, C content and N content per unit volume, respectively. CF was calculated from Equation (1), where W represents DW, C or N contents (μg).  

\[CF\ =\ W/PL^{3}\]

(1)

Molting rate experiments

The molting rate experiments were conducted according to the method of Shreeve and Ward (Shreeve and Ward, 1998). Specimens were obtained by towing a vertical zooplankton net (312 μm mesh size) slowly from bottom to surface. CVs of C. sinicus were picked out quickly under a dissecting microscope. Seawater was collected with a 59 L sampler at the depth of the same temperature set for the incubation. Seawater was then divided into 1 L glass bottles and 10–15 CVs were transferred into the bottles using a wide bore pipette. Then the CVs were cultured at constant temperatures under constant low illumination. Temperatures were maintained in electric incubators with variation being less than ±0.5°C. After 2–4 days, all individuals were picked out and their developmental stages were identified with a dissecting microscope. Molting rate (MR, day⁻¹) was calculated using Equation (2):  

\[MR\ =\ N_{\mathrm{adult}}/(N_{CV}\ {\times}\ t)\]

(2)

In Equation (2), N_adult represents the number of adults at the end of the incubation and N_CV the number of CVs at the start time. t is the incubation time (day). Stage duration (day) of CV was then calculated as the reciprocal of MR.

To evaluate the bottle effects on the molting rate of CV C. sinicus individuals, two supplementary molting rate experiments were conducted at Stns 6 and 7 on September 17–18, 2002. The method of the experiments was the same as that described previously except that the development stages were checked carefully every 3 days and returned to the bottle to continue incubation. At the time of development stage checking, the water was changed for freshly prepared seawater with the same conditions.

RESULTS

Environmental features

Strong thermocline and the occurrence of the YSCWM (Fig. 2a) are the distinct and relatively constant features of the southern Yellow Sea in summer. The YSCWM is the residual cold water (commonly <10°C) formed in the last winter, so its temperature changes from year to year depending on the atmospheric temperature in the last winter (Guo, 1993). Seawater near Cheju Island is affected by the input of freshwater and Yellow Sea warm current water (Fig. 2b). Chl a concentration is at a low level at the center of the transect, usually <0.5 μg L⁻¹ at Stns 5–7 and <0.2 μg L⁻¹ in the YSCWM (Fig. 2c). High Chl a concentration occurs in the 0–20 m water stratum at Stns 8–10; the highest value being >3 μg L⁻¹.

Fig. 2.

Some environmental features along the transect during August 2001 in the southern Yellow Sea. (a) Temperature (°C); (b) salinity; (c) Chl a concentration (μg L⁻¹).

Abundance and stage composition of C. sinicus

The abundance and stage composition of C. sinicus are shown in Fig. 3. At Stns 1–2, no CV or adult C. sinicus were found. A relatively high abundance of eggs (1.3 × 10⁴ eggs m⁻²) occurred at Stn 2, which probably came from other places by horizontal advection. From Stn 2 to the central part of the transect (Stns 5–7), the proportion of eggs decreased quickly and CV gradually became the dominant developmental stage. The maximum proportion of CV (69%) in the population occurred at Stn 5. There was a high density of CV in the lower depths of Stns 5–7, with the highest density of 424 ind. m⁻³ at the 75 m depth of Stn 7.

Fig. 3.

Calanus sinicus in the southern Yellow Sea in summer. Water column abundance (×10³ ind. m⁻²) and stage composition.

Length, weight, C and N content

Overall, the body sizes of CV and adult females were larger in the central area of YSCWM than in the shallow waters and areas to the southeast. PLs of CVs at Stns 5–7 were significantly longer (t-test, P < 0.05) than those at other stations, being >2.0 mm, whereas the average lengths were <1.9 mm at all other stations (Fig. 4). PLs of adult females were significantly longer (t-test, P < 0.05) at Stns 6–7 than at all the other stations except Stn 5. The differences between average PLs of adult males among stations were not as marked as those of CVs and adult females, with the maximum and minimum values occurring at Stn 6 and Stn 9, respectively.

Fig. 4.

Calanus sinicus. CVs, adult females and males of C. sinicus in the southern Yellow Sea in summer. Prosome lengths (average ± 95% CI), DW, CFDW, C content, CFC, N content, CFN and C:N ratios at each station were shown.

The distribution pattern of DW of CVs was similar to that of the PL (Fig. 4). DWs were larger at Stns 5–7 than at ll other stations, >160 μg ind.⁻¹ compared with <125 μg ind.⁻¹. DWs of adult females and males did not show a trend as distinct as that of CVs. For adult females, the DWs were >180 μg ind.⁻¹ at Stns 4–10, but were only 153 and 158 μg ind.⁻¹at Stns 2 and 3, respectively. No significant trend was found for the DW of adult males (not shown in Fig. 4). The variations in CFDW of female adults were not consistent with those in the CFDW of CV (Fig. 4). The CFDW of CV was higher at Stns 6–7 than at other stations. However, the CFDW for females was lower at Stns 6–7 than at other stations. In contrast, the CFDW at Stn 8 was low for CV but high for adult females.

There was a large difference between the C content per CV at Stns 5–7 and that at other stations (Fig. 4). The average C content of CV was 88.0–93.9 μg ind.⁻¹ at Stns 5–7, but was only 50.8–67.2 μg ind.⁻¹ at other stations. The C content of adult females showed the same trend as that of CV. The average C content of adult females was 88.0–98.6 μg ind.⁻¹ at Stns 5–7, and was 62.9–84.6 μg ind.⁻¹ at other stations. The differences in C content in CV and adult females also varied a great deal between the stations. The average C content of adult females was 15–22, 0–5 and 26–67% larger than that of CV at Stns 3–4, Stns 5–7 and Stns 8–10, respectively. The trend of the variation in CFC was similar to that of CFDW (Fig. 4). No regular trend was found in the variations of C content in adult males (not shown in Fig. 4).

The variations in N content between stations exhibited the same trend as those of C content, but were less marked, both for CVs and adults (Fig. 4). The minimum and maximum values of N content of CV were 9.4 and 14.1 μg ind.⁻¹ at Stn 3 and Stn 5, respectively; and the minimum and maximum values for adult females were 16.7 and 22.3 μg ind.⁻¹ at Stns 2–3 and Stn 5, respectively. The differences in N content between CVs and adult females were larger than those for C. The average N content of adult females was 69–78, 47–68 and 85–104% greater than that of CV at Stns 3–4, Stns 5–7, and Stns 8–10, respectively. For adult females, large CFN values occurred at Stn 5 (1.87 μg N mm⁻³) and at Stns 8–10 (1.82–1.87 μg N mm⁻³).

The C:N ratios of CVs were significantly higher than those of adult females (Fig. 4). The highest and lowest C:N ratios for CVs were 6.8 at Stn 7 and 5.1 at Stn 8, respectively. C:N ratios of adult females and males were around 4. The highest and lowest C:N ratios for adult females were 4.7 at Stn 6 and 3.8 at Stn 2, respectively.

Molting rates of CV C. sinicus

The results of molting rate experiments are listed in Table I and Fig. 5. Experiments were conducted at temperatures in the range of 9–12°C, representative of the temperatures in the YSCWM and at the lower boundary of the thermocline. At 9°C, none of the 48 CVs molted in the 3.3 days of incubation. At 11–12°C, the molting rate varied between 1.6 and 3.1 × 10⁻² day⁻¹ for short incubations. In the long incubation, 85% CVs molted into adults in 25 days. In the experiments conducted in September, molting rates changed with the incubation time (Fig. 5). The molting rates were 1.3, 0.9 and 2.4 × 10⁻² day⁻¹ at 10°C; and 1.1, 7.4 and 13.8 × 10⁻² day⁻¹ at 15°C, in the three successive periods, respectively.

Table I:

Molting rates of C. sinicus CV in August in the southern Yellow Sea measured using shipboard incubations

Stations	Stn 8	Stn 7	Stn 5	Stn 3	Stn 5
Date	August 21	August 23	August 24	August 25	August 24
Temperature (°C)	12	9	11–12	11	12
Total no. CVs reared	30	48	78	59	109
Length of incubation (days)	4.2	3.3	2.9	2.7	25
Total no. adults	2	0	7	3	93
Number dead	0	0	1	1	9
Molting rate (day−1)	0.016	0 (0)	0.031 (0.016)	0.019 (0.002)	0.034 (0.004)

Mean values for duplicate measurements and mean values (with standard deviations in parentheses) for triplicate measurements shown.

Fig. 5.

Molting rates of C. sinicus CV in September at Stn 6 (10°C) and Stn 7 (15°C) measured by shipboard incubations. Experiments were conducted in three successive periods. The maximum molting rates were obtained from laboratory incubation results under excess food conditions at 10.3 and 15°C, respectively (Uye, 1988).

Vertical distribution and diel vertical migration

CV individuals tended to reside in the YSCWM (Fig. 6); there was a clear upward migration at Stn 8 during the night. At the four diel stations, most CVs and adults resided below the thermocline in the daytime. But a proportion of them migrated upward into or through the thermocline during the night, and reached the highest water layers at 21:00 (Fig. 7). The migration ranges of females were significantly larger than those of CVs. CVs did not occur at 20 m and above at Stns 3 and 5. However, a few CV individuals passed through the thermocline during the night at Stn 7, and a significant proportion of CVs reached 20 m at Stn 8. According to the water column integral abundance, the proportion of CVs residing in the water at >15°C at 21:00 was 10 and 43% at Stns 7 and 8, respectively.

Fig. 6.

Vertical distribution of C. sinicus CV (ind. m⁻³) in the southern Yellow Sea during August 2002. The black and white bars indicate day (05:00–19:00) and night (19:00–05:00), respectively.

Fig. 7.

Vertical distribution of CVs (left) and adult females (right) of C. sinicus at 9:00 and 21:00 at the four diel stations in the southern Yellow Sea during August, 2002 (ind. m⁻³). Both CVs and adult females resided near the bottom during the day and reached the highest position in the water column at 21:00. Contour lines indicate temperature (°C).

CVs that migrated upward during the night were not distributed randomly within the population. CVs with different body sizes and possibly different physiological features had different DVM patterns. At the four diel stations, PLs of CVs in different water strata were measured at 21:00 (Fig. 8). At Stns 8, 7 and 5, the prosome lengths beneath the thermocline were always significantly longer than those in water strata above or at the thermocline (t-test, P < 0.05). CVs with PLs of >2.1 mm were never found in the upper two water strata at Stns 8, 7 and 5.

Fig. 8.

Prosome lengths (mm, average ± 95% CI) of C. sinicus CV individuals in water strata of different depths at 21:00 at the four diel stations in the southern Yellow Sea during August 22–26, 2002.

DISCUSSION

In this paper, abundance, stage composition and DVM of C. sinicus in the southern Yellow Sea in summer were investigated. PL, DW, and elemental C and N content of CVs and adults were measured, and the molting rate of CV was measured using onboard incubation.

Methodology for measuring molting rate of CV

The shipboard incubation method is based on the assumption that immediate, post-capture behavior accurately reflects the same processes in nature (Runge et al., 1985). This method may be affected by bottle effects, and might be flawed when age within stage is not uniformly distributed (Miller et al., 1984; Runge et al., 1985; Shreeve and Ward, 1998). Souissi et al. hypothesized that with low food levels and low temperature, copepod populations would display a stable structure (Souissi et al., 1997). Calanus sinicus also has a relatively stable age structure in the Yellow Sea in summer. When reared in a similar temperature and food environment to that in the field, the development rate of CVs supposedly should not change much within several days, although longer incubation would affect the development rate considerably (Fig. 5). Considering these facts, the measured molting rates in the first several days should represent the real molting rate but with a tendency for higher values.

Different characteristics of C. sinicus in different regions

There were significant variations among the 10 stations in the transect, both in physical environment and in the ecological and physiological features of C. sinicus. According to these differences, the investigated transect could be divided into three sections: (1) the coastal shallow waters to the northwest of the southern Yellow Sea consisting of Stns 1–4. In this region, the water depth was <60 m and temperature was >15°C except in the bottom layers of Stns 3–4. Population abundance was low, and egg and nauplii were the dominant developmental stages. CVs and females had smaller body size, low DW and hence appeared to be in poor condition. (2) The central part of the southern Yellow Sea consisting of Stns 5–7. Water depth was 73–80 m with a prominent thermocline and low Chl a concentration. The population was dominated by CV, which had larger body size, higher weight and better condition than CV in other sections. (3) The southeast region of the Yellow Sea consisting of Stns 8–10. Chl a concentrations were much higher in the upper layers, and the bottom temperature increased gradually from 10 to 15°C (Fig. 2a). The population was dominated by egg and nauplii. The body size and weight of CV was smaller than that in the central section. CVs and adult females displayed obvious DVM patterns.

DVM patterns of CVs and differentiation among individuals

At the four diel stations, most CVs and adult females resided below the thermocline and a component of them migrated upward into or through the thermocline. Their mean vertical depths reached the highest position in the water column at 21:00. At Stns 5, 7 and 8, the PLs of CVs in the water column below the thermocline were always significantly longer than those in or above the thermocline (Fig. 8). This result implies that physiological status plays an important role in the DVM patterns of CV C. sinicus. Huang et al. indicated that predator avoidance and feeding were major driving forces inducing vertical migration of CV and adult female C. sinicus (Huang et al., 1993b). Moreover, DVM avoids potential egg cannibalism (Huang et al., 1992), and Enright suggested that greater energetic benefit is achieved by feeding in the warm, phytoplankton-rich surface layer during the night, and by enhancing utilization of ingested food in the cool deep layer during the day (Enright, 1977). In this study, feeding or achieving energetic benefit is also likely to be an important outcome of the DVM pattern of CV. Besides the environmental factors, physiological status also plays an important role in the DVM patterns of CV C. sinicus. This study is the first time that the effect of physiological status on the DVM of C. sinicus has been considered.

CVs with different physiological status exhibit different DVM patterns. The differentiation among the CV individuals would have significant effects on the population dynamics of C. sinicus. CVs with larger body size stay in the cold water throughout the day. Their development is suspended in this environment with low temperature and low food supply. However, CVs with smaller body size (PL <2.0 mm) exhibit long-distance DVM patterns. They reside in the cold waters during the day and migrate to the upper warmer layers with greater food supply at night. The higher temperature and greater food supply in the upper water layers are likely to promote their development to adults, and thus the population dynamics of C. sinicus is affected.

Dormancy and life history strategy

Previous studies have shown that condition of copepod is positively related to food concentration but is not affected by temperature (Durbin et al., 1983; Wang et al., 1988; Campbell et al., 2001; Pu et al., 2004). In the YSCWM where food is scarce, however, CV individuals have comparatively higher condition factors. This discrepancy implies that CVs in the YSCWM have reserved energy beforehand and slow down their energy consumption to a much lower level. According to the molting experiments, the molting rate was 0 day⁻¹ at Stn 7 at 9°C, and 0.013 day⁻¹ at Stn 6 at 10°C. However, the duration of the CV stage was only 6.7 days at 10.3°C (equivalent to a molting rate of 0.15 day⁻¹) under excess food conditions (Uye, 1988). This means that the development of CV in the YSCWM is suspended. Energy conservation, development suspension and lack of DVM behavior suggest a resting or dormant status for the CVs in the YSCWM. By definition, dormancy consists of diapause and quiescence, and diapause differs from quiescence in that the former, which is ultimately genetically determined, is a response to predictable, cyclic changes in the habitat and is initiated by fixed ontogenetic instars (Dahms, 1995; Hirche, 1996). Since the existence of YSCWM is a constant and predictable feature in the Yellow Sea in summer (Guo, 1993), and dormancy occurs exclusively in CV but not in other developmental stages, we believe this is a genetically related adaptation to this predictable environment. It can therefore be argued that diapause, rather than quiescence, is occurring.

However, low levels of gut pigment and oxygen consumption have been detected for the CVs in this region (Li et al., 2004), and the development of CVs resumed at a higher rate after 1-week incubation at 15°C. Hence, the dormant CV may have passed or, indeed lack, the refractory phase of a programmed diapause in which the resting animals would not be aroused after a short time, but information from the whole season is required before firm conclusions can be drawn. According to Alekseev and Fryer, great variation exists in the degrees of diapause among Crustaceans (Alekseev and Fryer, 1996). So the resting CVs in YSCWM could represent a shallow degree of diapause. This kind of situation is quite similar to the CV stage of Calanus finmarchicus in the southern Gulf of Maine, which feeds but is not ready to molt (Durbin et al., 1997). It should also be noted that CV individuals in the YSCWM section are not fully synchronous in their physiological and ecological behavior. The CV individuals with smaller body size who migrated upwards to the warmer waters with more food supply should surely molt faster to reach the adult stage. The non-synchrony phenomenon also occurs for other Calanus species (Herman et al., 1991; Miller et al., 1991; Pedersen et al., 1995), making it too complex to describe the population as a whole.

The dormancy status of C. sinicus is closely related to the low temperature and low food supply in the YSCWM. Stabilization of seawater in the YSCWM is also helpful in maintaining the copepod there. No dormant features occur in populations out of the YSCWM in the southern Yellow Sea and in the Inland Sea of Japan (Huang et al., 1993a). Based on incubation results (Pu et al., 2004), and the relationships between population features and in situ environments; temperature and food availability are the two major environmental factors controlling physiological and ecological features of C. sinicus. Calanus sinicus maintains its population at the resting CV in the YSCWM under conditions of food scarcity, but reproduces actively at Stn 8–10, where there are phytoplankton-rich water strata. These adaptive, over-summering strategies ensure the survival of C. sinicus in adverse environments and allow its population to spread quickly in favorable conditions. Data on the year-round variations in the abundance, stage composition, length, weight, development and reproduction are needed to give us a full picture of the population dynamics and life history strategy of C. sinicus.

We thank the crew of the R.V. ‘Bei-dou’ for their great assistance. We would also like to thank Professor D.-J. Huang for providing CTD data, and Professor R.-H. Li for measuring Chl a concentration. Thanks are due also to two anonymous reviewers for their valuable comments and suggestions on the manuscript. This work was supported by the Ministry of Science and Technology, People’s Republic of China (project no. G19990437-08).

Author notes

¹Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China and ²Graduate School, Chinese Academy of Sciences, Beijing 100093, China