Spatial and Temporal Variations of Pelagic Copepods in the North Yellow Sea

CHEN Hongju, LIU Guangxing, , ZHU Yanzhong, and JIANG Qiang

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Spatial and Temporal Variations of Pelagic Copepods in the North Yellow Sea

CHEN Hongju1), 2), LIU Guangxing1), 2),*, ZHU Yanzhong2), 3), and JIANG Qiang2)

1)Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China,Qingdao 266100, P.R. China?2)College of Environmental Science and Engineering, Ocean University of China, Qingdao266100,P.R. China?3)State Environmental Protection Key Laboratory of Estuary and Coastal Environment, Chinese Research Academy of Environmental Sciences, Beijing100012, P.R. China

This study aims to analyze the spatial and temporal variations of the abundance and biodiversity of pelagic copepods and their relationships with the environmental factors in the North Yellow Sea (NYS). These variations were analyzed on the basis of the survey data of the NYS in four seasons from 2006 to 2007. A total of 31 copepod species that belong to 17 genera, 13 families and 4 orders were identified in the four seasons. Of these copepods, the species belonging to Calanoida is the most abundant component. The dominant species include,,,,, and.is the most important and widely distributed dominant species in all of the seasons. The dominant species have not shown any significant variation for the past 50 years. However, the richness of warm-water species increased. The abundance of copepods significantly varied among different seasons: the average abundance was higher in spring (608.2indm?3) and summer (385.1indm?3) than in winter (186.5indm?3) and autumn (128.0indm?3). Factor analyses showed a high correlation between the spatial distributions of dominant copepods and environmental parameters, and Chl-a was the most important factor that influenced the distribution of copepods. This research can provide the fundamental information related to zooplankton, especially pelagic copepods. This research is also beneficial for the long-term monitoring of zooplankton ecology in the NYS.

copepod; species composition; abundance; community structure; North Yellow Sea

1 Introduction

Copepodsinhabit almost every type of marine environments, and these organisms are considered as the most numerous multi-celled organisms on earth (Turner, 2004). Copepods play an important role in the biological cycling of elements and energy transfer in the oceans and constitute the most abundant and diverse marine communities. The abundance, distribution, and community structure of copepods are evidently influenced by marine environmental conditions (Brugnano., 2012; Temperoni., 2014), and these factors have been suggested as biological indicators of water masses (Wang., 2003; Hsieh., 2004; Wang., 2013).

The North Yellow Sea (NYS), surrounded by the Liaoning and Shandong Provinces of China and the Democratic People’s Republic of Korea, is a semi-closed shallow sea with an area of 7.13×104km2. The NYS is connected to the Bohai Sea through a narrow channel but is relatively open to the South Yellow Sea (SYS) (Fig.1). The well-known Yantai-Weihai mackerel fishing ground is located in NYS. In the mid-1950s, scientists conducted comprehensive surveys in the NYS to study the ecological relationships among zooplankton, hydrological conditions, and mackerel (Cheng., 1965). The ‘Comprehensive Oceanography Expedition in China Seas (1958- 1960)’ (Comprehensive Survey Office of Ocean Group of Committee of Science and Technology of the People’s Republic of China, 1977) was then facilitated. These surveys reported the elementary features of zooplankton and copepods in the NYS. Since then, studies on zooplankton in the NYS have been very limited (Yang., 2012; Franco., 2014), and specialized research on cope- pods has yet to be performed.

This study aims to analyze the spatial and temporal variations of the abundance and biodiversity of pelagic copepods and their relationships with the environmental factors in the NYS. It is based on the zooplankton samples collected from four seasonal cruises from 2006 to 2007. This research can provide fundamental information on pelagic copepods and can be beneficial for the long- term monitoring of zooplankton ecology in the NYS.

2 Materials and Methods

2.1 Study Area and Sampling Methods

Four surveys were conducted at 78, 81, 82 and 82 stations in July-August 2006 (summer), January 2007 (winter), April-May 2007 (spring), and October 2007 (autumn), respectively, in the NYS onboard R/V ‘2’ (Fig.1). Zooplankton were sampled with a 505μm mesh ring net (diameter = 0.8m) hauled vertically from the bottom of the sea to the sea surface at a rate between 0.8 and 1ms?1. The volume of the filtered water was determined using a flow meter (Hydrobios, 438110) placed in the net. After each tow was completed, the nets were washed and the samples were preserved in 5% formalin (in seawater) for further analyses. The temperature, conductivity, and depth of the water were obtained using a CTD profiler (Sea-Bird SBE 911). The spatial and vertical distribution characteristics of the temperature and salinity were all published by Bao. (2009); and chl-concentration values were all provided by Professor LI Zhengyan from the Ocean University of China.

Fig.1 Map of the study area and sampling stations in the North Yellow Sea.

.2 Laboratory Procedures

The zooplankton taxa presenting in the samples were identified to the species level when possible; the number of zooplankton was counted under a stereomicroscope (Leica, S8APO). Data were standardized to abundance per cubic meter.

2.3 Data Analysis

The dominance () of each species was calculated using the following equation (Xu and Chen, 1989):

=,

wherenis the abundance of species,fis the occurrence frequency of species, andis the copepod abundance. The species with a dominance of ≥0.02 were defined as dominant species (Xu and Chen, 1989).

The correlation between biotic and environmental data was determined using the routine RELATE of the statistical package Plymouth Routines In Multivariate Ecological Research (v6.1.10, PRIMER-E Ltd., 2006) (Clarke and Warwick, 2001). The relationships between the abundance of dominant species and the environmental parameters were analyzed through principal component analysis (PCA) on the basis of the correlation coefficients between the parameters by using SPSS 11.5. Surface temperature (SST), bottom temperature (SBT), surface salinity (SSS), bottom salinity (SBS), surface chlorophyll(Surface Chl-), bottom chlorophyll a (Bottom Chl-a), and depth were considered as the possible controlling factors affecting the distributional pattern of the dominant copepod species. The contours of temperature and salinity were obtained from the gridded data by using Kriging method.

3 Results

3.1 Species Composition

Copepod was the most abundant component among the identified groups. A total of 31 copepod species belonging to 17 genera, 13 families and 4 orders were identified in four seasons. Table 1 shows the number and abundance of copepod species in each season. The species belonging to Calanoida and Cyclopoida were dominant; by contrast, the pelagic species belonging to Harpacticoida and Monstrilloida were very limited. The species belonging to Calanoida was the most abundant and diverse component, accounting for more than 95% of the total abundance (the proportion reached up to 99.2% in spring). In autumn, the richness and abundance of the species belonging to Cyclopoida attained the peak and accounted for 9.8% of the total abundance.

Most of the copepod species recorded in this study belong to a temperate eurythermal low-saline group. However, several warm-water copepod species, such as,,,,and, were also detected in autumn and winter.

Table 1 Number and abundance of the copepod species in the NYS in four seasons.

3.2 Seasonal Variation and Horizontal Distributions of the Total Abundance

The copepod abundance significantly varied among different seasons (One-way ANOVA,= 16.872,= 0.000). The average abundance was higher in spring (608.2indm?3) and summer (385.1indm?3) than in winter (186.5indm?3) and autumn (128.0indm?3). Fig.2 shows the distribution pattern of the abundance in the NYS. The spatial distribution of the total abundance substantially varied in different seasons. In spring, the copepod abundance varied from 41.5indm?3to 5863.7indm?3. The high value occurred in the coastal area of Liaoning Province, followed by the coastal area of Yantai and Weihai cities; by contrast, the low value was distributed in the central part of the NYS. In summer, the abundance varied from 2.7indm?3to 1899.5indm?3, and approximately showed a northeastwardly declining gradient. The highest abundance occurred in the coastal area of the Shandong Peninsula. The copepod abundance sharply decreased during autumn, and the distribution was relatively uniform. The abundance varied from 8.3indm?3to 988.6indm?3. The high values occurred in the east part of the Liaodong Peninsula coastal area. The low-abundance area was located near the Weihai shore. In winter, the abundance slightly increased to an average of 186.5indm?3, ranging from 11.0indm?3to 1937.0indm?3. The distribution pattern showed an approximate opposite tendency to that of summer. The high-abundance area was located in the coastal area of the Liaodong Peninsula. Two low-abun- dance areas were also found, one in the coastal area of Yantai and the other in the eastern middle part of the surveyed area (38.1?-39.0?N, 123.3?-124.0?E).

Fig.2. Horizontal distribution of the total abundance of pelagic copepods in NYS (indm?3). a) spring; b) summer; c) autumn; d) winter.

3.3 Dominant Species

Six dominant species were recorded in four respective seasons (Table 2):in the four seasons;in autumn and winter;in spring and summer;in spring, summer, and winter;in winter;in autumn and winter.

was the most important and widely distri- buted dominant species, accounting for 49.2%, 85.0%, 58.0%, and 35.5% of the total abundance in spring,summer,autumn, andwinter, respectively. The abundance ofshowed a clear seasonal variation (Fig.3). The abundance was higher in summer (327.3indm?3) and spring (299.5indm?3) than in autumn (74.3 indm?3) and winter (66.2indm?3).almost occurred at every station in all of the seasons. In spring,was concentrated in the offshore area of LiaodongPeninsula. With the formation of the Yellow Sea Cold Water Mass (YSCWM), the species gradually drifted to the central part of the NYS in summer. In autumn, the abundance sharply decreased, and the distribution pattern was relatively uniform. In winter, the abundance slightly decreased, with the peak value area drifting to the Liaodong Peninsula offshore.

was dominant in autumn (38.8indm?3) and winter (48.2indm?3), with similar spatial distribution patterns. The high-abundance areas were located in the southern offshore of LiaodongPeninsula (Fig.4). In spring, the species was mainly distributed in the coastal area but rarely found in the central part of the surveyed area. The abundance distribution was quite even in summer (7.7indm?3), and a relatively high-abundance area was found in the offshore area of Weihai City.

Table 2 Dominance and average abundance of dominant species. The dominant species in each season are in boldface

Fig.3 Spatial distribution of C. sinicus abundance in the NYS (indm?3). a) spring; b) summer; c) autumn; d) winter.

was dominant in spring and summer, and the distribution pattern remarkably varied in different seasons (Fig.5). In spring,was the second most abundant dominant species (136.8indm?3). The low-abundance areas were located in the southeast part of the surveyed area along approximately 38.5?N. The abundance sharply decreased in summer (25.3indm?3), and the peak value area drifted to the central region of the surveyed sea area. In autumn, this species was only detected in Changshan Archipelago sea area with a low abundance. A slight increase in the abundance (3.0indm?3) occurred in winter, and the distribution areas extended to both Shandong and Liaodong Peninsula coastal areas.

Fig.4 Spatial distribution of P. parvus abundance in the NYS (indm?3). a) spring; b) summer; c) autumn; d) winter.

Fig.5 Spatial distribution of C. abdominalis abundance in the NYS (indm?3). a) spring; b) summer; c) autumn; d) winter.

The highest abundance of, which was quite scattered in patches, was recorded in spring (157.5 indm?3) and found in the southern offshore area of LiaodongPeninsula, whereas another peak value area was located in the Yantai coastal area. In summer, the distribution pattern ofwas similar to that of, the average abundance being 16.8indm?3. In autumn, the abundance of this species was low, and this species was detected in the shore area near Liaodong Peninsula and in the southeast part of the surveyed area. In winter, the abundance dramatically increased (59.4indm?3); the high-abundance area was located in the southern offshore of LiaodongPeninsula (Fig.6).

was dominant in autumn (10.7 indm?3) and winter (3.9indm?3), with similar distribution patterns. The area with the highest abundance was in the southern offshore of LiaodongPeninsula (Figs.7a, b).was dominant in winter (5.3indm?3), with a distribution pattern in contrast to that of. The peak value area was located in the southeast corner of the surveyed area(Fig.7d).

Fig.7 Spatial distribution of Corycaeus affinis (a, b) and Oithona plumifera (c, d) in the NYS (indm?3). a) spring; b) summer; c) autumn; d) winter.

3.4 Relationship with Environmental Factors

We initially hypothesized that biotic data were not related to environmental data, but we rejected this hypothesis on the basis of the results of routine RELATE, and the different ρ values of 0.431, 0.328, 0.295, and 0.482 in spring, summer, autumn, and winter, respectively (< 0.001).

Factor analysis was conducted to determine the bio- logical and environmental parameters that showed a high degree of correlation between the spatial distributions of dominant copepods and environmental factors.

In spring, the first principal component accounted for 34.3% of the variation in dominant copepods; this result showed a positive factor loading for SST, SBT, surface Chl-, and bottom Chl-. It also yielded a negative factor loading for SSS, SBS, and depth. By contrast, the second principal component, which explained 19.8% of the variation in dominant copepods, showed a positive factor loading for SST, SBT, SSS, SBS and bottom Chl-and a negative factor loading for depth. In the distribution of the factor loading illustrated in the scatter diagram, all of the dominant copepod species were associated with Chl-(Fig.8a).

In summer, the first principal component explained 38.5% of the variation in dominant copepods, and showed a positive factor loading for SST, SSS, SBS, and depth and a negative factor loading for SBT, surface Chl-, and bottom Chl-. The second principal component, which explained 20.5% of the variation in dominant copepods, showed a positive factor loading for depth, surface Chl-, and bottom Chl-and a negative factor loading for SST, SBT, SSS, and SBS. In the distribution of the factor loading illustrated in the scatter diagram, all of the dominant copepod species were associated with water depth (Fig.8b).

In autumn, the first principal component explained 45.1% of the variation in dominant copepods, and showed a positive factor loading for bottom Chl-and SBT and a negative factor loading for SSS, SBS, SST, and depth. By contrast, the second principal component, which explained 18.4% of the variation in dominant copepods, showed a positive factor loading for surface Chl-, SBS, and depth and a negative factor loading for SST and SBT. In the distribution of the factor loading illustrated in the scatter diagram, all of the dominant copepod species were associated with surface Chl-and bottom Chl-(Fig.8c).

Fig.8 Factor loading results of the first and second principal components on the basis of the environmental factors and the dominant copepods in the NYS in each season. a) spring; b) summer; c) autumn; d) winter.

In winter, the first principal component explained 52.1% of the variation in dominant copepods, which showed a positive factor loading for SST, SBT, SSS, SBS, and depth and a negative factor loading for surface Chl-and bottom Chl-. Conversely, the second principal component, which explained 12.8% of the variation in dominant copepods, showed a positive factor loading for SST, SBT, SBS, and depth and a negative factor loading for SSS, surface Chl-, and bottom Chl-. In the scatter diagram, the factor loadings of the two components were considered as basis to divide dominant copepods into two types: (1) copepods whose abundance was associated with Chl-and (2) species whose abundance was related to water depth, salinity and temperature (Fig.8d).

4 Discussion

4.1 Species Richness

The Lubei Coastal Current, Liaonan Coastal Current, YSCWM and Yellow Sea Warm Current (YSWC) are mixed in the NYS (Su, 1989). The complex hydrological environment brings zooplankton in NYS a characteristic feature. A total of 31 copepod species/taxa have been found in the NYS, close to the number recorded in the Bohai Sea (30) (Bi., 2000) but much lower than that in the South Yellow Sea (92) (Xiau, 1979) and East China Sea (226) (Xu., 2004). From Xiau’s record (1979), no significant changes are found in total species number compared with that found 30 years ago. The richness of species is higher in summer and autumn than that in winter and spring, similar to the previous studies in NYS (Cheng., 1965; Xiau, 1979; Wang., 2005), SYS (Xiau, 1979) and East China Sea (Xu., 2004).

Most of the copepod species that inhabit the semi- closed NYS belong to temperate eurythermal low-saline species. However, warm-water species were detected in this study, which reflects the influence of warm current. The high-temperature and high-salinity water from East China Sea-Yellow Sea warm current system driven by Kuroshio not only alters the marine environment and atmospheric circulation pattern but also changes the composition of zooplankton species. In autumn, a good number of warm-water copepod species appear with low abundance in the NYS, and such appearance has not been reported before. However, the northward expansion of other warm-water species (and) in the NYS had been reported (Yang., 2012). Climate change might result in YSWC reinforcement and then increase both abundance and species richness of warm-temperate species in the NYS. In winter, the strong north wind drives the southward surface flow along the coast; correspondingly, the YSWC is compensated northward along the Yellow Sea Trough. The water coming from the East China Sea changes the NYS zooplankton community structure.is considered to be a good bio-indicator of YSWC (Wang., 2003). In winter,appeared in 22 stations in the middle and southern part of the surveyed area, with C602 (N38?46.8′, E120?0.6′) being the northernmost station. The result shows that the northward penetrating YSWC could spread to this sea area. In Contrast to the the deep winter penetration, the YSWC becomes much less intrusive in summer (Xu., 2009), hence the absence of warm-water species.

4.2 Seasonal Succession of Dominant Species

The main dominant species recorded in this study were,,and, and no significant difference was found between the dominant species of the present study and those in the surveys during 1955-1958 (Cheng., 1965). The distribution of each species showed its respective characteristics in different seasons. Zooplankton distributions are controlled not only by the hydrological environment but also by the interaction among other creatures sharing the same habitat, namely prey, predator and competitor. Temperature and food availability govern the marine copepods growth and productivity (Hirst and Bunker, 2003; Maar., 2013). Species-specific distributions presented in this study might result from the influence of temperature and food availability on the copepods.

In spring, dominant species include,and, which showed similar distribution patterns. The abundance peak value appeared in the areas near the shore. According to PCA, the species distribution were associated with Chl-(Fig.8a). During the survey period, the hydrological environment condition (see Bao. 2009) was in the favorable temperature ranges for(8.7-25.9℃, Huang., 1993),(8.9-21.1℃, Liang., 1996) and(8-24℃, Sun., 2009). Therefore, the food availability might be an important factor for the growth and distribution of copepods. According to the simultaneous Chl-data, during spring bloom, the phytoplankton abundance is higher in the areas near the shore. Even the nutrient structure and limitations in the onshore area are greatly changed by the rapid consumption of phytoplankton in spring (Zhang., 2009). Accordingly, the mushroom proliferation of phytoplankton supports the rise in copepod dominant species.

In summer, the distribution center ofmoved to the middle part of the surveyed area. The YSCWM, a bottom pool of the remnant Yellow Sea Winter Water resulting from summer stratification, plays a sheltering role forin summer (Pu., 2004). Accordingly, the present study recorded a high abundance of(>250.0indm?3, Fig.3) occurring in this area (<12℃, Bao., 2009). In addition, the peak value areas ofandwere also shifted to the middle part of NYS (Figs.5b and 6b). According to PCA, these three dominant species distinctly have negative correlation with SBT (Fig.8b). During the survey period, high SST (>21℃, Bao., 2009) exceeded the optimal temperature range, which drove the copepod to migrate downwards to the deep.

The dominant species changed during autumn. The abundance ofandsharply declined and were sporadically distributed. However,was considered to be an important dominant species. Synchronously,was also significantly increased, whereaswas still the most abundant. According to PCA, the species distribution was associated with Chl-(Fig.8c).andshowed a similar distribution pattern abundant in the Liaoning coastal area (Figs.4c and 7a).

androse to be the dominant species in winter. The scatter diagram showed two types of dominant species (Fig.8d). Except, other copepods were associated with Chl-a and mainly abun- dant in the area near the shore, especially in the Liaodong Peninsula sea area.

was the most important copepod species in the NYS. Chen and Zhang (1965) indicated thatis a warm-temperate coastal species, with a wide tolerance range of temperature and salinity (Huang., 1993). As seen in the year-round variation (Fig.3), the abundance and distribution significantly varied in different seasons, andwas always the most abundant copepod in the NYS. According to Cheng. (1965), the abundanceofwas low in March, sharply increased in May, and reached its peak in July. In August, the abundance acutely decreased, whereas in September and October, the abundance raised appreciably. In December, the abundance reached the bottommost value and lasted until the next early spring. Compared with the present study, the year-round variation was quite similar to that in 50 years ago (Cheng., 1965). The highest value presenting in summer indicated that the YSBCW serves as an over-summering shelter for(Pu., 2004).

The spatial distribution patterns ofandwere quite similar, but the abundance variation throughout the year differed. The peaks occurred in spring, but the secondary peaks ofandwere present in winter and summer, respectively (Table 2, Fig.5, and Fig.6). The variation of YSBCW and temperature are the main factors affectingin the NYS (Wu, 1991). Cheng. (1965) reported thatfaded away after September. According to PCA, the abundance was greatly associated with SST (Fig.8). In winter and spring,wasmainly distributed in the area near the shore, especially in the Liaoning Peninsula coastal area, whereas in summer, the distribution center moved to the middle part of the NYS. The variation pattern was similar to that in 50 years ago (, Cheng., 1965).

According to Gallienne and Robins (2001),might be the most important copepod in the ocean worldwide and occur in almost any marine environment (Paffenh?fer, 1993).has never been recorded as a dominant species in the NYS before. The species of genushas a wide range of diets, being fed on phytoplankton and faecal pellets. Coprophagy helps explaining the wide distribution of, as faecal pellets are the universal source of food (González and Smetacek, 1994; Porri., 2007). PCA showed that the abundance ofis not related with Chl-a (Fig.8). During this survey, the distribution offollowed the salinity isopleths well (Bao., 2009).

is highly abundant in winter in the Inland Sea of Japan; therefore, this species has been categorized as a cold-water species (Liang and Uye, 1996). According to Cheng. (1965),showed two peaks in the NYS annually. In July,reached the first peak (171indm?3) and subsequently declined in August. The other peak appeared in October (321indm?3) and maintained more than 200indm?3in November and December (Cheng., 1965). In the present study,was dominant in winter and autumn, with an abundance of 48.2 and 38.8indm?3, respectively.is a small- sized copepod that shows characteristics analogous to,, and. The abundance may be underestimated as a result of the mesh size selection (the samples in our study were collected with a 505 μm mesh plankton net).

Acknowledgements

This study was supported by the National Natural Science Foundation of China (31101875, 41210008). We extend our gratitude to the captain and crew of the R/V ‘2’. We also acknowledge Mr. Xu, D. H., Mr. Lin, J., Mr. Chen, X. F., and Mr. Huang, Y. S., for helping with the sampling work on board.Thanks are also to Professor Li, Z. Y. of CESE, OUC, for the data of Chl-in the North Yellow Sea.

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(Edited by Ji Dechun)

DOI 10.1007/s11802-015-2787-6

ISSN 1672-5182, 2015 14 (6): 1003-1012

? Ocean University of China, Science Press and Springer-Verlag Berlin Heidelberg 2015

(October 20, 2014; revised August 3, 2015; accepted August 14, 2015)

* Corresponding author. Tel: 0086-532-66782672 E-mail:gxliu@ouc.edu.cn