Chinese Journal of Oceanology and Limnology Vol. 31 No. 6, P. 1284-1294, 2013 http://dx.doi.org/10.1007/s00343-013-3004-3

Annual variation in sinicus abundance and population structure in the northern boundary area of the Yellow Sea Cold Water Mass*

YIN Jiehui (尹洁慧) 1, 2 , ZHANG Guangtao (张光涛) 1 , * * , ZHAO Zengxia (赵增霞)1 , WANG Shiwei (王世伟) 1 , WAN Aiyong (万艾勇) 1 1 Jiaozhou Bay Marine Ecosystem Research Station, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China 2 University of Chinese Academy of Sciences, Beijing 100049, China

Received Jan. 6, 2013; accepted in principle Mar. 11, 2013; accepted for publication May 9, 2013 © Chinese Society for Oceanology and Limnology, Science Press, and Springer-Verlag Berlin Heidelberg 2013

Abstract The Yellow Sea Cold Water Mass (YSCWM) was suggested as an over-summering site of the dominant species Calanus sinicus in coastal Chinese seas. Population abundance and structure were investigated by monthly sampling along three transects across the northern boundary of the YSCWM during 2009–2010. Results show that thermal stratifi cation existed from June to October and that the vertical thermal difference increased with depth. Generally, total abundance was lowest in October and highest in June, and the female/male sex ratio was highest in February and lowest in August. Evident spatial differences in abundance were observed during the existence of the YSCWM. In June, total abundance averaged 158.8 ind/m3 at well-stratifi ed stations, and 532.1 ind/m3 at other stations. Similarly, high abundances of 322.0 and 324.4 ind/m3 were recorded from July to August inside the YSCWM, while the abundance decreased from 50.4 to 1.9 ind/m3 outside the water mass. C . sinicus distribution tended to even out over the study area in September when the YSCWM disappeared. We believe that the YSCWM may retard population recruitment in spring and preserve abundant cohorts in summer. The summer population was transported to neritic waters in autumn. In addition to low temperatures, stable vertical structure was also an essential condition for preservation of the summer population. C . sinicus can survive the summer in marginal areas in high abundance, but the population structure is completely different in terms of C5 proportion and sex ratio.

Keyword : Calanus sinicus; Yellow Sea Cold Water Mass (YSCWM); over-summer strategy; boundary area; thermal stratifi cation

1 INTRODUCTION sinicus (Wang et al., 2003). C . sinicus is a dominant planktonic copepod widely The spatial distribution of zooplankton is distributed in shelf waters of the Northwest Pacifi c determined by interactions between their behavior (Hulsemann, 1994), which provides food for many and physical oceanographic structure and processes commercially important fi sh stocks (Zhu and Iverson, (Daly and Smith, 1993; McManus and Woodson, 1990; Uye and Shimazu, 1997; Uye et al., 1999). 2012). The Yellow Sea Cold Water Mass (YSCWM) Over its geographical distribution range, its tempo- is a bottom water mass with a temperature below spatial pattern is determined by its thermal adaptation 10 C under the thermocline in central areas of the Yellow Sea in China (He et al., 1959). Its existence exerts vital impacts on the spatial distribution of both * Supported by the Knowledge Innovation Program of Chinese Academy bacterioplankton and zooplankton (Wang and Zuo, of Sciences, the National Basic Research Program of China (973 Program) (No. 2011CB403604), and the IOCAS-Zhangzidao Fishery Eco- 2004; Li et al., 2006; Zuo et al., 2006). It has been Mariculture Joint Laboratory suggested as an over-summering site for Calanus ** Corresponding author: [email protected] No.6 YIN et al.: Annual variation of Calanus sinicus in the Yellow Sea Cold Water Mass 1285 and various temperature regimes. The upper thermal 1989) or a part of the YSCWM (Yu et al., 2006). limit of C . sinicus was estimated to be ~23°C in the According to geographical variation of the bottom inland Sea of Japan (Huang et al., 1993), whereas, temperature in summer, the boundary area of the according to previous fi eldwork in Chinese waters, it YSCWM was narrowest in the Northern Yellow Sea, was no longer present when the temperature exceeded and the highest bottom temperature gradient was 25–27°C (Huang and Chen, 1985; Zhang and Wong, expected (Naimie et al., 2001). Hence, the Zhangzi 2012). In summer, water temperatures increased Island area, 40 nautical miles from the north coast of beyond its thermal tolerance in the surface layer the Yellow Sea, was selected for our study. Abundance throughout the Yellow Sea and the East China Sea. and population structure of C . sinicus, as well as Correspondingly, C . sinicus abundance decreased physical environments and Chlorophyll a (Chl- a ) signifi cantly in neritic areas and concentrated in the concentrations, were investigated monthly along YSCWM area, although bottom temperatures lower three transects across the north boundary of the than its upper thermal limit were recorded in regions YSCWM during the period July 2009–June 2010. other than the YSCWM (Wang et al., 2003). The Our goals are to illustrate the annual variation of the YSCWM originates from cold winter water and exists C . sinicus population in the boundary waters of the until the following autumn, but its impacts on YSCWM and evaluate the impacts of the YSCWM by population recruitment of C . sinicus were investigated comparing C . sinicus abundance and population in summer through geographical comparisons in structure between well stratifi ed and less stratifi ed previous studies. Though it was hypothesized that the areas. autumn population in neritic waters was recruited by the over-summered population (Sun, 2005), no direct 2 METHOD evidence was available on cross boundary transport 2.1 Field investigation and sample treatment until now. Different development and diel vertical migration Monthly surveys were carried out by the R/V (DVM) patterns were observed in the over-summering Keyan 19 from July 2009 to June 2010 except in population inside the YSCWM, in association with January and May, when ferryboats to Zhangzi Island environmental conditions including low bottom were held up by bad weather. Thirteen stations along temperature, low food availability and stable vertical three zonal transects were covered (Fig.1). physical structure (Wang et al., 2003; Zhang et al., Zooplankton samples were collected at each station 2007). In addition to higher abundance, the population with a conical plankton net (mouth opening 0.5 m2 , of C . sinicus in the YSCWM was characterized by a mesh size 500 μm), vertically towed from 2 m above higher proportion of adults and copepodites in the the bottom to the surface. The volume of water fi ltered fi fth stage (C5), and adult female abundance was was measured by a fl ow meter mounted in the center more than 10 times higher than that of males. of the net mouth. Samples were preserved in a 5% According to continuous observation during a diel neutralized formalin seawater solution. C . sinicus cycle, females inside the YSCWM underwent DVM were sorted and classifi ed under a dissecting although they rarely entered the surface layer, but microscope as female, male, C5 and early stages C1– DVM was not observed outside the YSCWM. The C5 4. Nauplii were insuffi ciently sampled, and were not stage was much more abundant inside the YSCWM, included in the population analysis. where most of them remained in the bottom layer Temperature and salinity in the water column were throughout the day. To defi ne the essential conditions measured with an AAQ1183-1F CTD (Alec for successful over-summering, it is necessary to look Electronics Co., Japan). Water samples were collected at continuous population recruitment in the boundary with Niskin bottles every 10 m from the surface to areas of the YSCWM, where signifi cant gradients of 2 m above the bottom. 500-mL natural seawater for temperature and food concentration were expected. total Chl-a measurements were fi ltered through The location of the YSCWM varies signifi cantly 0.45 μm cellulose acetate membranes. The membranes from year to year, and it is hard to predict its boundary, were wrapped with aluminum foil and immediately particularly in the East China Sea. Cold bottom water frozen at -20 C. After extracting the membranes in with similar physical characters and temporal duration 90% acetone solution (v/v) in a refrigerator (≤0°C) was also observed in the northern East China Sea, for 24 h, the Chl-a concentrations were measured recognized as an independent water mass (Su et al., with a Turner Designs Model 7200 fl uorometer. 1286 CHIN. J. OCEANOL. LIMNOL., 31(6), 2013 Vol.31

Bohai Sea Northern Yellow Sea

Southern Yellow Sea

39.5° N

39.3° East China Sea

39.1° A1 B1 C1 Zhangzi Island B2 A3 B3 C3

A5 B5 C5 38.9° South China Sea

A6 B6 C6

122.4° 122.6° 122.8° 123° E Fig.1 Location of the northern marginal area of the Yellow Sea Cold Water Mass (shown in the large map) and sampling sites in this study (marked in the small map)

30 2.2 Data analysis 25 Surface 20 Bottom Abundance of adult, C5 and C1-4 stages was 15 calculated at each station. Less than 10 individuals were captured at some stations, so they were calculated 10

Temperature (°C) as total numbers from all stations in each month. 5 Contour maps were generated in Golden Software 0 Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May Jun. Surfer 9.0. 33 3 RESULT

32 3.1 Physical environments

Salinity In the study area, different annual trends were 31 observed in surface and bottom layers, with thermal stratifi cation present mainly from June to September 30 Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May Jun. (Fig.2). On average, the lowest water temperature presented in March. It was 2.62°C in the surface layer Fig.2 Annual variation of temperature and salinity in surface and bottom layers during 2009–2010, with and 2.22°C on the bottom. The highest surface error bars showing the standard deviation temperature of 23.54°C was recorded in August, but No.6 YIN et al.: Annual variation of Calanus sinicus in the Yellow Sea Cold Water Mass 1287

C6 C6

22 C5 C5 12 12 17 (°C) 7 7 27 C3 C3 24 C1 C1 17 21

B6 B6 18 12 15 B5 22 B5

7 7

17 12 B3 12 B3 12

2 9 Stations B2 B2 17 6

2 22 B1 2 B1 3 0 A6 A6 -3 7 12 7

12

A5 17 A5

12

2 2 A3 A3 17

A1 A1 Jul. Aug. Sep. Oct. Nov. Dec. Feb. Mar. Apr. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Feb. Mar. Apr. Jun. Fig.3 Temporal and spatial variation of surface (left) and bottom (right) temperature (°C) in this investigation the bottom temperature reached its highest (15.70°C) In the surface layer, spatial differences between in September. Thermal differences between surface water temperatures were detected in both summer and and bottom layers were highest in July, when winter, but temperatures were higher at southern temperatures averaged 22.49°C in the surface layer stations in both seasons. The surface temperature and only 12.82°C on the bottom. Vertical thermal difference among stations was less than 5°C in all difference decreased to only 1.75°C in October, and months. In summer, the spatial difference was largest disappeared until next March. in July, when surface temperatures averaged 24.48°C Spatial variation in bottom temperatures was at the southernmost stations and 22.67°C at the others. observed mainly in summer, due to the existence of The largest difference in winter appeared in February, the YSCWM (Fig.3). Generally, bottom temperature with averages of 4.31 and 2.60°C. decreased with water depth increase along each A seasonal variation in salinity was observed transect during June-October. Bottom temperatures at mainly in the surface layer (Fig.2). Surface dilution the southernmost stations (A6, B6, and C6) were appeared mainly in the rainy season, i.e. from June to lower than 10°C in July, and increased to 10.54– August. During this period, salinity in the surface 12.35°C in August and 10.67–11.82 °C in September. layer averaged 32.19, 31.16, and 31.49 at the At the other stations, water temperature varied southernmost stations, and 30.78, 30.65 and 30.72 at between 9.95–17.42°C in July, 13.11–20.51°C in the other stations. The lowest salinity in these three August, and 12.59–20.01°C in September. In October, months was recorded at stations C1, B1, and C3, the bottom temperature varied between 11.96 and indicating infl uences from the Yalu River located 12.78°C at the southernmost stations, and between northeast of the investigation area. 14.48 and 17.60°C at other stations. The spatial 3.2 Chl- a concentration difference disappeared completely in November. During the cooling period from December to March, According to the column integrated average, Chl-a lower bottom temperatures were observed at shallow concentration was highest at 1.10 μg/L in August, stations, and the spatial difference was less than 3°C. followed by 0.85 μg/L in March (Fig.4). It was lowest When the YSCWM became detectable in June, in February at 0.19 μg/L, with the least spatial temperature gradients appeared again along each variation. A comparatively high Chl-a concentration transect. of 0.57 μg/L was observed in October. A phytoplankton 1288 CHIN. J. OCEANOL. LIMNOL., 31(6), 2013 Vol.31 bloom appeared in August mainly at shallow stations varied between 0.05 and 2.81 μg/L in the bottom layer (Fig.5), with the highest value (7.32 μg/L) observed at the other stations. In April, Chl-a concentration in in the surface layer at station B3. In March, Chl-a the bottom layer was 3.78, 3.60, and 0.61 at the concentration increased at all stations except A1, southernmost stations, but varied between 0.04 and where water temperature was also the lowest. 1.57 μg/L in the bottom layer at the other stations. According to geographical distribution, another minor Chl- a concentration peak was observed in October, 3.3 Seasonal variation of abundance and sex ratio with the highest values at stations A3, B3, and C5. of C. sinicus According to Chl-a concentration in bottom layers, The abundance of C . sinicus was highest at extremely high values were observed at the 446.0 ind/m3 in June, followed by 113.1 ind/m3 in southernmost stations in March and April. In March, July (Fig.6). It decreased signifi cantly to 18.6 ind/m3 Chl- a concentration was highest on the bottom layer in August. Though it increased to 38.2 ind/m3 in (1.06, 6.53 and 2.51 μg/L at stations A6, B6 and C6. It September, the total abundance reached the lowest of 11.9 ind/m3 in October. A minor abundance peak presented in December, but the abundance of 73.6 ind/ 2.0 m3 was still much lower than that in June and July.

1.5 800 9 Total abundance 8 ) 3 Sex ratio 7 1.0 600 6 5 400 0.5 4 Sex ratio

Chl- a concentration (μg/L) 3

Abundance (ind/m 200 2 0.0 1 Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May Jun. 0 0 Fig.4 Annual variation of Chl- a concentration (μg/L) Jul. Aug.Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May Jun. during 2009–2010, with error bars showing the Fig.6 Annual variation of total abundance and sex ratio standard deviation (female/male) of Calanus sinicus during 2009–2010

C6 C6 6.4 C5 2.8 C5 1 1 5.6 0.5 0.5 2.4 C3 0.5 C3 4.8

1 0.5 2 C1 C1 4

1.6 4 B6 B6 3.2 0 2 3 B5 0.5 1.2 0.5 B5 1 2.4 1 Station 1.5 0.8 B3 Chl- a concentration (μg/L) B3 Chl- a concentration (μg/L) 1.6

B2 0.5 0.4 B2 0.8

0.5 B1 0 B1 0

A6 A6 2 0.5

1 A5 0.5 A5

A3 A3

A1 A1 Jul. Aug. Sep. Oct. Nov. Dec. Feb. Mar. Apr. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Feb. Mar. Apr. Jun. Fig.5 Temporal and spatial variation of Chl-a concentration (μg/L) expressed as water column average (left) and in bottom layer (right) in this investigation No.6 YIN et al.: Annual variation of Calanus sinicus in the Yellow Sea Cold Water Mass 1289

From February to April, average abundance varied August, from October to November, and in April. between 37.5 and 49.0 ind/m3 . Dominance of C5 was observed in June, with a Bimodal annual variation was observed in the sex signifi cant spatial difference. ratio (Fig.6). Female/male ratio was highest in When total abundance peaked in June, proportions February (7.8 females/males). The sex ratio in the of these groups were similar at 0.33, 0.43 and 0.24. In available months decreased thereafter, and an the other months with a relatively low abundance, extremely low ratio was observed in August, when proportions also differed among groups. Proportion 384 males were captured from all stations but only of adults was the lowest at 0.02 in July, and increased 310 females were sampled. The sex ratio increased to thereafter until the highest (0.73) was reached in 4.8 in October, and then decreased to 2.2 in November. March. Relatively low proportions of 0.36 and 0.38 were observed in October and November compared 3.4 Population structure of C. sinicus with 0.48 in September. The proportion of C5 was All three developmental groups, C1-4, C5 and comparatively high in August (0.33) and September adults, were recorded in each month, with different (0.36), and lowest (0.09) in April. The proportion of proportions (Fig.7). Adults dominated in the over- early stages fl uctuated between 0.06 in March and wintering population (December to March), and a 0.79 in July. Relatively high proportions of 0.47 and high proportion was also observed in September. 0.60 appeared in October and April, and it was Early stages C1-4 dominated separately from July to comparatively low in September (0.17). 3.5 Geographical distribution of C. sinicus

600 0.9 Geographical variation in abundance was observed C1-4 C5 Adults 0.8 mainly in summer and spring (Fig.8). In June, total 500 C1-4-P C5-P Adults-P ) 3 3 0.7 abundance averaged 158.8 ind/m at the southernmost 400 0.6 stations and 532.1 at the other stations. Abundance of 0.5 300 all three groups was higher at inshore stations than at 0.4 Proportion the southernmost stations, with the highest value at 200 0.3

Abundance (ind/m station B5. From July to August, C . sinicus abundance 0.2 3 100 decreased from 50.4 to 1.9 ind/m at inshore stations, 0.1 but at the southernmost stations similarly high 0 0 3 Jul. Aug.Sep. Oct. Nov.Dec. Jan. Feb. Mar. Apr.May Jun. abundance of 322.0 and 324.4 ind/m were recorded. Fig.7 Annual variation of abundance and proportion of Along transects A and C, early stages concentrated at different developmental stages of Calanus sinicus in the southernmost stations, but the spatial difference 2009–2010 was not signifi cant along Transect B. C5s tended to

C6 C6 C6 (ind/m3) C5 C5 C5 700 C3 C3 C3 600 C1 C1 C1 500 B6 B6 B6 400 B5 B5 B5 300 B3 B3 B3 200 Station B2 B2 B2 100 B1 B1 B1 0 A6 A6 A6 A5 A5 A5 A3 A3 A3 A1 A1 A1 Jul. Aug.Sep.Oct.Nov.Dec.Feb.Mar.Apr. Jun. Jul. Aug.Sep.Oct.Nov.Dec.Feb.Mar.Apr. Jun. Jul. Aug.Sep.Oct.Nov.Dec.Feb.Mar.Apr. Jun. Fig.8 Temporal and spatial variation of abundance (ind/m3 ) of C1-4, C5 and adult life stages of Calanus sinicus (from left to right) in 2009–2010 1290 CHIN. J. OCEANOL. LIMNOL., 31(6), 2013 Vol.31

600 concentrate at the southernmost stations in August, July 500 whereas in July this spatial pattern was evident only August

) along Transect A. Higher C5 abundance was also 3 400 September observed at Station C3, and no obvious gradient was observed along Transect B. Higher abundance in 300 adults appeared only at Station C3 in July. 200 Abundance (ind/m 4 DISCUSSION 100

0 4.1 Annual variation of C . sinicus populations in 8 1114172023the boundary area of the YSCWM Bottom temperature (°C) Fig.9 Relationship between total abundance of Calanus Monthly sampling in our study revealed that spatial sinicus and bottom temperature at each station in differences in C . sinicus abundance presented mainly summer (July–September) in 2009 during the existence of the YSCWM, and different

0 500 impacts were observed on population recruitment in 22 various phases. When the YSCWM became detectable a 22 10 400 ) in June, bottom temperature was less than 5°C at the 3 southernmost stations and varied from 5 to 9°C at 16 20 17 300 20 19 other stations. Chl-a concentration varied from 0.33– 0.54 μg/L inside the YSCWM and 0.22–0.52 μg/L 30 200 15 12 outside. The thermal range was suggested as between

13 Abundance (ind/m 1 and 27°C for C . sinicus survival and 5–23°C for 40 100 population reproduction (Wang et al., 2003).

50 0 Population recruitment in the spring can be reduced in A1 A3 A5 A6 the YSCWM by low bottom temperatures, as total 0 500 abundance was twice as high at inshore stations as it 24 b was inside the YSCWM. 23 400 10 21 ) 3 In summer, C . sinicus concentrated at stations

20 300 inside the YSCWM, especially in early life stages 19 17 (Fig.9). In August, it was present almost exclusively 13 17 30 200 inside the YSCWM, where the bottom temperature 15 was lower than 13°C (Fig.10). Since the YSCWM is Abundance (ind/m 40 12 100 composed of preserved cold winter water, it was suggested that an independent cohort that was 50 0 B1B2 B3 B5 B6 developed inside the YSCWM survived the summer. 0 500 The copepodites outside the water mass may have suffered from a high loss rate even though the surface c 24 25 ) 10 22 400 3 temperature was lower than the suggested thermal 22 21 tolerance at some stations. In our study, the lowest 19 20 300 recorded surface temperature in July and August was

Depth (m) Depth (m) Depth (m) 20.17°C and the highest was 26.14°C. Based on fi eld 17 30 200 15 observations, peak abundance of eggs and nauplii Abundance (ind/m occurred when the water temperature was between 13 31 100 40 and 18°C (Chen, 1964). Population size, determined by both recruitment and loss processes, decreased 50 0 C1 C3 C5 C6 before its upper thermal limit was reached. Station Cross boundary transportation of the over- Fig.10 Vertical structure of water temperature (shown summered population occurred in September, when with contour map in units of centigrade) and spatial variation of total abundance of Calanus sinicus the surface temperature decreased below its upper (shown with histogram) along three transects in thermal tolerance but thermal stratifi cation had not August in 2009 completely disappeared. Total abundance at the No.6 YIN et al.: Annual variation of Calanus sinicus in the Yellow Sea Cold Water Mass 1291

YSCWM station was high in July and August, but bloom was observed in October and November, so the from August to September, it decreased inside the predicted autumn abundance peak might have been YSCWM and increased outside (Fig.9). C . sinicus depressed by high predation pressure (Zhang, was distributed evenly at all stations in September, unpublished data). with abundances ranging between 2.6 and 51.8 ind/m3 Compared with water temperature, phytoplankton and the highest abundance present at station C3. biomass was not a limiting factor in spatial and According to population structure, both juveniles and seasonal patterns of C . sinicus abundance. In August, adults were observed at inshore stations in September, C . sinicus disappeared from coastal stations, where a indicating a low possibility of local recruitment. signifi cant phytoplankton bloom was observed in Increased C . sinicus abundance in autumn was upper water layers. Its abundance peak in spring also reported in mainly neritic waters, such as Jiaozhou lagged at least two months behind the Chl-a Bay (Huang et al., 2009). In a previous investigation concentration peak. The highest Chl-a concentration covering the entire Chinese coastal area, different presented in March, but the highest C . sinicus annual patterns were obtained in different geographical abundance appeared in June, although the proportion ranges. Two peaks with similar abundances were of early developmental stages increased signifi cantly recorded in June and December in the Bohai Sea and as early as April. Low feeding pressure on the standing the northern Yellow Sea (Chen, 1964), whereas no stock of phytoplankton was expected through the obvious autumn peak was detected in the entire water column in this month, as high Chl-a Yellow Sea in re-analysis of the same data set (Wang concentration was observed in the bottom layer. et al., 2003). As the YSCWM occupies a large area in Higher abundance was observed in coastal areas with the central Yellow Sea, a higher percentage of coastal higher primary production in June, but no correlation stations were included in the Bohai Sea and northern was observed between total abundance and Chl-a Yellow Sea compared with the entire Yellow Sea. concentration. The abundance increase in neritic waters may be 4.2 Essential conditions for summer population resulted from local reproduction after horizontal preservation in the YSCWM transportation, as the reproduction rate increased in the southern Yellow Sea in autumn when temperature Our investigation was carried out in a limited area, fell into its ideal range again (Zhang et al., 2005). In a but a signifi cant spatial difference was observed in previous report, three generations per year were association with the YSCWM. The over-summering suggested for the C . sinicus population in the Yellow population was preserved only in well-stratifi ed areas. Sea, with the autumn generation appearing during When surface temperature reached its highest in October-November (Chen, 1964). A high proportion August, C . sinicus distributed at deep stations with of early stages was recorded in autumn in both shelf signifi cant thermoclines (Fig.10). At vertically mixed and neritic waters. However, the contribution of a stations, where surface temperatures were sometimes newly developed cohort to total abundance was not lower than the proposed upper thermal limit of 23°C detected in autumn in our study. In our study, the at transect A and B and bottom temperature was in its proportion of early developmental stages increased favored range of 10–20°C, total abundance decreased from September to October, but the total abundance to less than 6.0 ind/m 3 , and reached zero at some decreased simultaneously. A signifi cant increase of stations. In a previous report, female C . sinicus total abundance was observed until December, when avoided hot surface layers through limited diel water temperatures were only 5–9°C, but it accounted vertical migration and C5s stayed in the cold bottom for only 16% of that in June. Water temperatures in layer throughout the day in central YSCWM areas, our results fell into its favored thermal range in the whereas both of them were observed in the lethal same period, but increased total abundance was surface layer at the station with less stable vertical observed until December. Population abundance in structure (Zhang et al., 2007). our study increased from August to September, but Active horizontal transportation can also induce decreased in October and November, despite the signifi cant loss of the population preserved in well- increased Chl-a concentration in October. The average stratifi ed areas. Lower surface temperatures were abundance in October was lower than that of 74.3 ind/ observed on transect B in July and August, so more m3 recorded in the same month in the entire Northern active horizontal water exchange was inferred Yellow Sea (Jiang, 2010). A ctenophore (Beroe sp.) compared with the other two transects, possibly 1292 CHIN. J. OCEANOL. LIMNOL., 31(6), 2013 Vol.31 owing to tidal currents and topographic features. areas of the YSCWM. In August 1999, adults Correspondingly, total abundance at inshore stations accounted for 47% and C5s accounted for 37% of was higher on this transect than the others, and was total abundance inside the YSCWM (Wang et al., lower at offshore stations. Cross boundary water 2003). The highest proportion of the C5 stage was exchange might carry more C . sinicus outside the observed in August 2001 (Zhang et al., 2007). In our YSCWM area and increase population loss under study, the proportion of early stages (C1-4) was higher high temperature conditions. than both adults and C5 in July and August, and lower More population loss was expected in subtropical in September. It is suggested that over-summering areas with less stable vertical structure and a longer populations may exist widely in the YSCWM areas period of lethally high surface temperatures. Such but various developmental patterns are expected. transportation might occur in coastal waters of the Similar population structure was also observed in the Taiwan Strait, where cold bottom water also exists in Taiwan Strait, where the abundance of older stages far deep areas. In summer, C . sinicus was recorded at exceeded that of early stages in November but was inshore stations in this area, with relatively high evenly split in summer months (Hwang and Wong, abundance within the well-recognized upwelling 2005). regions (Guo et al., 2011). In shelf waters of the South Another character of the over-summering China Sea, C . sinicus was observed in considerable population in the central YSCWM area was a high sex abundance in summer, but almost disappeared in ratio (female:male=11.39), indicating a low autumn (Yin et al., 2011). Winter populations may be reproduction rate due to the low temperature and food sustained under cold water conditions but cannot concentration (Wang et al., 2003). The sex ratio in our survive the warm season in areas with active water study showed a similar bimodal annual variation with exchange. that in 1959 (Chen, 1964), but differed in its value Food availability was not essential for a successful range. In 1959, the sex ratio peaked in March (14.0) over-summering strategy. Decreased food availability and September (6.5). The lowest value of 1.6 was has been documented in the YSCWM area, as the observed in May. It peaked in October and February upwelling of regenerated nutrients in the bottom layer in our study, whereas males outnumbered females in was blocked by strong thermal stratifi cation (Wang, August. Female-skewed adult sex ratios are common 2000; Wang et al., 2003). In previous studies, low in copepod species in both wild and cultured Chl- a concentration was observed in the YSCWM populations. It was explained by both intrinsic factors area in the Southern Yellow Sea (Wang et al., 2003; (sex-specifi c longevity, mortality, and develop rate, Zhang et al., 2007). In our study, relatively high Chl-a etc.) and environmental conditions (food availability, concentration was recorded in summer, probably temperature) (Kiørboe, 2006; Gusmão and McKinnon, owing to exchange with nutrient-rich coastal water. 2009). Highest percentages of males were High Chl-a concentration was recorded at inshore hypothesized to be present during the periods of fast stations in July and August, because of nutrient growth of the cohort, usually coinciding with enrichment induced by freshwater input (Yin et al., phytoplankton blooms (Irigoien et al., 2000). A forthcoming). According to low abundance at these decreasing sex ratio was recorded during increasing stations, it was suggested that deleterious effects of copepod abundance from October to December and high temperature could not be ameliorated by an from February to June, but the extremely low sex increased food supply. ratio in August remains unexplained. This is the fi rst report on different copepod over- 4.3 Over-summering strategy in the boundary summering strategies under various environmental area of the YSCWM regimes. Food availability was suggested as a more Different population structure was observed in the important regulating factor than water temperature boundary area of YSCWM. Similar abundance was for the population structure in boundary areas of the documented in the boundary area of YSCWM in our YSCWM, since relatively high Chl-a concentration study and in the central areas in previous studies was recorded in the boundary areas. It is commonly (Wang et al., 2003; Zhang et al., 2007), but observed that marine can survive characteristics of the over-summering population unfavorable environments in a state of diapause. were not recorded in our study. Individuals of older Another Calanus species in the Northern Atlantic stages were observed in high abundance in central Ocean, C . fi nmarchicus , is known to over-winter by No.6 YIN et al.: Annual variation of Calanus sinicus in the Yellow Sea Cold Water Mass 1293 undergoing a facultative diapause in juvenile stages Daly K L, Smith W O. 1993. Physical-biological interactions (Hirche, 1996). Compared with deep pelagic ocean infl uencing marine plankton production. Annu . Rev . Ecol . areas, more variable environments were observed in Sysl ., 24 : 555-585. shelf regions of the Yellow Sea and East China Sea. Guo D H, Huang J Q, Li J. 2011. Planktonic copepod compositions and their relationships with water masses in Even in the YSCWM area, environmental conditions the southern Taiwan Strait during the summer upwelling varied between the central and boundary areas. period. Con t . Shelf Res ., 31 (6 ) : S67-S76. Accordingly, developmental patterns differed with Gusmão L F M, McKinnon A D. 2009. Sex ratios, intersexuality geographical locations and with seasonal changes. and sex change in copepods. J . Plankton Res ., 31 (9): Therefore, quiescence, defi ned as a phase of retarded 1 101-1 117. development allowing a fast response to changing He C B, Wang Y X, Xu S. 1959. A preliminary study of the environmental conditions (Seebens et al., 2009), was formation of Yellow Sea Cold Water Mass and its expected for the over-summering population of C. properties. Oceanol . Limnol . Sin ., 2(1): 11-15. (in Chinese sinicus in the central YSCWM area, because of the with English abstract) Hirche H J. 1996. Diapause in the marine copepod, Calanus combined effects of low temperature and food fi nmarchicus - a review. Ophelia , 44 (1-3): 129-143. availability (Pu et al., 2004). Meanwhile, normal Huang C, Uye S, Onbe T. 1993. Geographic distribution, population structure was observed in boundary areas seasonal life cycle, biomass and production of a planktonic with relatively high food concentrations, indicating a copepod Calanus sinicus in the Inland Sea of Japan and low need for quiescence. its neighboring Pacifi c Ocean. J . Plankton Res ., 15 (11): 1 229-1 246. 5 CONCLUSION Huang F P, Huang J Z, Yang Y L, Li Y, Wang Z L. 2009. Spatial temporal distribution of planktonic copepod in the Low bottom temperatures in the YSCWM retarded Jiaozhou Bay. Acta Ecologica Sinica , 29(8): 4 045-4 052. recruitment during the onset of population (in Chinese with English abstract) amplifi cation in spring, and protected the inside Huang J, Chen B. 1985. Species composition and distribution cohort from deleterious high temperatures in summer. of planktonic copepods in the Jiulongjiang estuarine. The autumn population of C . sinicus in neritic areas Taiwan Strait, 4: 79-88. (in Chinese with English abstract) originated from the over-summered population in the Hulsemann K. 1994. Calanus sinicus Brodsky and C . jashnovi , nom. nov. (Copepoda: ) of the North-west YSCWM area through cross boundary transportation. Pacifi c Ocean: a comparison, with notes on the In summer, high abundance was observed only at integumental pore pattern in Calanus s. str. Invertebr . stations with strong thermal stratifi cation. Stable Taxon ., 8 (6): 1 461-1 482. vertical structure and weak horizontal water exchange Hwang J S, Wong C K. 2005. The China Coastal Current as a were suggested as essential conditions for a successful driving force for transporting Calanus sinicus (Copepoda: over-summering population. In the boundary area of Calanoida) from its population centers to waters off the YSCWM with a less stable physical structure and Taiwan and Hong Kong during the winter northeast higher food availability, a different over-summering monsoon period. J . Plankton Res ., 27 (2): 205-210. strategy was developed compared with the central Irigoien X, Obermüller B, RHead N, Harris R P, Rey C, Hansen B W, Hygum B H, Heath M R, Durbin E G. 2000. The area. A lower sex ratio and a higher percentage of effect of food on the determination of sex ratio in Calanus early life stages were recorded in the boundary area. spp.: evidence from experimental studies and fi eld data. ICES J . Mar . SCI ., 57 (6): 1 752-1 763. 6 ACKNOWLEDGEMENT Jiang Q. 2010. Study on the Macro-Zooplankton and Meso- Zooplankton Community Ecology in the North Yellow We thank Mr. ZANG Y. C. and all the crew on the Sea in Spring and Autumn. Master thesis. Ocean research vessel of Dalian Zhangzidao Fishery Group University of China, Qingdao. Co. Ltd. for their support with fi eld sampling. We also Kiørboe T. 2006. Sex, sex-ratios, and the dynamics of pelagic thank the Open Cruise of Chinese Offshore copepod populations. Oecologia , 148 (1): 40-50. Oceanography Research by IOCAS for giving us the Li H, Xiao T, Ding T, Lü R. 2006. Effect of the Yellow Sea sampling opportunity in December 2010. Cold Water Mass (YSCWM) on distribution of bacterioplankton. Acta Ecologica Sinica , 26 (4): 1 012- References 1 020. McManus M A, Woodson C B. 2012. Plankton distribution and Chen Q C. 1964. Study on the reproduction, sex ratio and body ocean dispersal. J . Exp . Biol ., 215 : 1 008-1 016. size of Calanus sinicus . Oceanol . Limnol . Sin ., 6 : 272- Naimie C E, Blain C A, Lynch D R. 2001. Seasonal mean 287. (in Chinese with English abstract) circulation in the Yellow Sea—a model-generated 1294 CHIN. J. OCEANOL. LIMNOL., 31(6), 2013 Vol.31

climatology. Cont . Shelf Res ., 21 (6-7): 667-695. spatial variation of nutrient and Chlorophyll-a Pu X M, Sun S, Yang B, Ji P, Zhang Y S, Zhang F. 2004. The concentrations during summer and autumn in the Zhangzi combined effects of temperature and food supply on Island area (Northern Yellow Sea). J . Ocean Univ . China Calanus sinicus in the southern Yellow Sea in summer. J . ( Oceanic and Coastal Sea Research ), accepted. Plankton Res ., 26 (9): 1 049-1 057. Yin J Q, Huang L M, Li K Z, Lian S M, Li C L, Lin Q. 2011. Seebens H, Einsle U, Straile D. 2009. Copepod life cycle Abundance distribution and seasonal variations of adaptations and success in response to phytoplankton Calanus sinicus (Copepoda: Calanoida) in the northwest spring bloom phenology. Global Change Biol ., 15 (6): continental shelf of South China Sea. Cont . Shelf Res ., 1 394-1 404. 31 (14): 1 447-1 456. Su Y, Li F,Ma H, Qian Q. 1989. Formation and seasonal Yu F, Zhang Z, Diao X, Gou J, Tang Y. 2006. Analysis of variation of bottom cold water mass in northern area of evolution of the Huanghai Sea Cold Water Mass and its the East China Sea. Journal of Ocean University of relationship with adjacent water masses. ACTA Qingdao , 19 (1): 1-14. (in Chinese with English abstract) Oceanologica Sinica , 28 (5): 26-34. (in Chinese with Sun S. 2005. Over-summering Strategy of Calanus sinicus . English abstract) GLOBEC International Newsletter , 11 (1): 34. Zhang G T, Sun S, Yang B. 2007. Summer reproduction of the Uye S, Shimazu T. 1997. Geographical and seasonal variations planktonic copepod Calanus sinicus in the Yellow Sea: in abundance, biomass and estimated production rates of infl uences of high surface temperature and cold bottom meso- and macrozooplankton in the Inland Sea of Japan. water. J . Plankton Res ., 29 (2): 179-186. J . Oceanogr ., 53 (6): 529-538. Zhang G T, Sun S, Zhang F. 2005. Seasonal variation of Uye S, Iwamoto N, Ueda T, Tamaki H, Nakahira K. 1999. reproduction rates and body size of Calanus sinicus in the Geographical variations in the trophic structure of the Southern Yellow Sea, China. J . Plankton Res ., 27 (2): 135- plankton community along a eutrophic–mesotrophic– 143. oligotrophic transect. Fish . Oceanogr ., 8 (3): 227-237. Zhang G T, Wong C K. 2012. Population abundance and body Wang B D. 2000. Characteristics of variations and interrelations size of Calanus sinicus in marginal habitats in the coastal of biogenic elements in the Huanghai Sea Cold Water seas of southeastern Hong Kong. J . Mar . Bio . Assoc . UK , Mass. Acta Oceanologica Sinica , 22(6): 47-54. (in 93 (1): 135-142. Chinese with English abstract) Zhu D, Iverson A. 1990. and other fi sh resources in Wang R, Zuo T. 2004. The Yellow Sea Warm Current and the the Yellow Sea and East China Sea November 1984-April Yellow Sea Cold Bottom Water, their impact on the 1988. Mar . Fish . Res ., (11): 1-143. (in Chinese with distribution of zooplankton in the southern Yellow Sea. J . English abstract) Soc . Oceanogr . Korean , 39: 1-13. Zuo T, Rong W, Chen Y Q, Gao S W, Wang K. 2006. Autumn Wang R, Zuo T, Wang K. 2003. The Yellow Sea Cold Bottom net copepod abundance and assemblages in relation to Water—an oversummering site for Calanus sinicus water masses on the continental shelf of the Yellow Sea (Copepoda, Crustacea). J . Plankton Res ., 25 (2): 169-183. and East China Sea. Journal of Marine Systems , 59 (1-2): Yin J H, Zhao Z X, Zhang G T, Wang S W, Wan A Y. Tempo- 159-172.