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Striking taxonomic differences in summer zooplankton in the northern South China Sea: implication of an extreme cold anomaly
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Xiping LIAN1, Yehui TAN1, *, Liangmin HUANG1, Linbin ZHOU1
Acta Oceanologica Sinica | 2017, 36(10) : 87 - 96
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Acta Oceanologica Sinica | 2017, 36(10): 87-96
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Striking taxonomic differences in summer zooplankton in the northern South China Sea: implication of an extreme cold anomaly
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Xiping LIAN1, Yehui TAN1, *, Liangmin HUANG1, Linbin ZHOU1
Affiliations
  • 1 Key Laboratory of Marine Bio-resource Sustainable Utilization (LMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
Published: 2017-10-01 doi: 10.1007/s13131-017-0975-5
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An extreme persistent cold anomaly was prevailing in the South China Sea in February 2008. In order to understand the effect of the cold anomaly on zooplankton community, the zooplankton composition, abundance and biomass were analyzed in the northern South China Sea in August 2007 and August 2008. A total of 467 zooplankton species representing 16 groups were identified, with 275 species in August 2007 and 351 in August 2008. Copepods were the most dominant zooplankton group in the study area. Compared with 2007, a dramatic decline was observed in the abundance of four dominant copepod species: Subeucalanus subcrassus, Temora discaudata, Nannocalanus minor and Temora turbinata in 2008. Moreover, zooplankton abundance declined from 133.37 ind./m3 in August 2007 to 75.49 ind./m3 in August 2008. In contrast, the abundance of medusa, such as Diphyes chamissonis, and tunicate, such as Doliolum denticulatum and Dolioletta gegenbauri, increased during the same season. Cluster analysis showed that there was a difference in zooplankton community structure between the two years. These variations in zooplankton communities were indicative of an anomalous oceanographic condition along with the extreme cold event in 2008.

zooplankton  /  community  /  cold anomaly  /  northern South China Sea
Xiping LIAN, Yehui TAN, Liangmin HUANG, Linbin ZHOU. Striking taxonomic differences in summer zooplankton in the northern South China Sea: implication of an extreme cold anomaly[J]. Acta Oceanologica Sinica, 2017 , 36 (10) : 87 -96 . DOI: 10.1007/s13131-017-0975-5
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1 Introduction
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Zooplankton plays an important role in the biological cycling of carbon and other elements in the ocean (Roemmich and McGowan, 1995), and is the main trophic link that connects phytoplankton and microzooplankton with larger vertebrate and invertebrate predators (Mackas and Beaugrand, 2010). Zooplankton serves also as excellent indicators of changes in ocean and climate conditions because of their short life cycles and free floating feature (Hays et al., 2005; Hooff and Peterson, 2006; Zhang and Wong, 2011). Interannual changes in zooplankton species assemblages often reflect an integrated response of the ecosystem to hydro-climatic forcing (Dippner et al., 2001; Beaugrand and Ibanez, 2004; Wiafe et al., 2008). For instance, dramatic changes in zooplankton community observed in eastern Pacific were attributed to the abnormal temperatures during El Niño/La Niña in 1997–1999 (Jiménez-Pérez and Lavaniegos, 2004; McKinnon et al., 2008). The utility of zooplankton as indicators of such changes in oceanographic conditions is based on a solid understanding of the ecology of dominant species (McKinnon et al., 2008).
The South China Sea (SCS) is the largest semi-enclosed sea in the western tropical Pacific Ocean (Su, 2004; Qiu, 2011). In the northern SCS (NSCS), the bottom topography is characterized by a steep continental slope between a shallow continental shelf (150–250 km in width) in the northwest, and a wide deep basin in the southeast (Zhang et al., 2009). The summer monsoon is typically southwesterly, which peaks in July and gradually decay in September. The SCS is a haven for oceanographers and climate researchers because it is a crossroads for currents that influence the climate of the entire globe (Qiu, 2011).
In February 2008, an extreme persistent cold anomaly is accompanied by a long-persisting northerly anomaly and a sequence of cold advection occurring in Southeast Asia. The extreme cold anomaly not only broke the lowest temperature record for the past 50 year but also caused numerous agriculture and fishery losses over Southeast Asia (Hong and Li, 2009). It was reported that nearly 90% of fishes around the coastline of Penghu, a small island west of Taiwan, died during this cold event (Xian et al., 2008). These geological and oceanographic features were expected to have greatly affected zooplankton communities in the NSCS.
Our present knowledge of zooplankton in the NSCS is mainly derived from previous studies (Li et al., 2004, 2006; Tan et al., 2004; Hwang et al., 2007, 2010; Tseng et al., 2008; Zhang et al., 2009; Chertoprud et al., 2011). However, these studies either focused on special groups, such as copepod communities, or conducted in the Zhujiang (Pearl River) Estuary. Moreover, research on the structure of zooplankton community in the NSCS and the impact of hydro-climatic events on zooplankton community is limited.
We have monitored and analyzed zooplankton composition, abundance and biomass in the NSCS in August 2007 and 2008. The results indicated a significant difference in zooplankton community between August 2008 and August 2007. What were the causes of such differences? We try to use the two years data to illustrate the structure of zooplankton community in the NSCS, demonstrate the difference in zooplankton community in August 2007 and August 2008, and present possible reasons for this difference.
2 Materials and methods
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2.1 Field sampling
The investigations were conducted in the NSCS in 2007 and 2008, from August 10 to 30. Zooplankton samples were collected at 21 sites in 2007 and at 23 sites in 2008 (Table 1), and were obtained by a vertical tow net (505 μm mesh size, 0.8 m diameter at a pulling speed of 0.5 m/s) from 2 m above the bottom with depths less than 200 m, or from 200 m to the surface with depths more than 200 m. The samples were fixed immediately in 5% formaldehyde. Temperature and salinity were measured using a SBE-19 CTD. Sea water for chlorophyll a (Chl a) analysis was collected by 5-L Niskin bottles. A 500 mL subsample was gently filtered through a GF/F filter, which was then stored at –20°C for laboratory analysis. Size fractionated Chl a was measured by sequential filtrating the water samples onto 25 mm polycarbonate filters (20 μm, 3 μm, and 0.7 μm) by steps.
2.2 Laboratory procedures
Zooplankton samples were identified to the species level when possible and counted (Chen and Zhang, 1965, 1974a, b; Chen et al., 1974; Liu, 2008). Wet biomass was measured with an electronic balance after removing large detrital particles, jellyfishes and tunicates under a microscope, and eliminating excess interstitial water by vacuum extraction technique. Zooplankton abundance and wet biomass were expressed as ind./m3 and mg/m3, respectively. For the determination of total Chl a concentration, Chl a samples were extracted in 90% acetone and preserved in a refrigerator (dark, –20°C) for 24 h. Chl a concentration was then measured fluorometrically (Turner designs 10 AU fluorometer) before and after acidification.
2.3 Data analysis
2.3.1 Sea surface temperature (SST)
Monthly averaged satellite-derived SST images for August 2007 and 2008 were obtained from the advanced very high resolution radiometer (AVHRR) (http://data.nodc.noaa.gov/pathfinder/Version5.0). Interannual variations of the SST in the SCS (0°–25°N, 99°–130°E) were calculated from January 2006 to December 2008. The SST data were obtained from the TMI (http://www.remss.com/tmi/tmibrowse.html). Monthly climatology of the SST at each grid point was calculated by averaging the SSTs for the individual calendar months during the three years, and then monthly anomalies of the SSTs were calculated by subtracting the monthly climatology from the individual SSTs. In this study, positive (negative) SST anomaly means that ocean SST was higher (lower) than the average SST.
2.3.2 Dominant species
Y is the dominance indicator, and a species is considered as dominant when Y≥0.02 (Xu and Chen, 1989). Y index was calculated as
$Y = \frac{{{N_i}}}{N} \cdot {f_i},$
where Ni is the abundance of the ith species, N is the total species abundance, and fi is the occurring frequency of species ith at all sites.
2.3.3 Cluster analysis
Cluster analysis was performed using PRIMER ν6 (PRIMER-E Ltd.) software. Similarity matrices were constructed using Bray-Curtis similarity because it does not derive similarity from conjoint absences (Clarke and Warwick, 1994). Species abundance data, which were square root transformed, were used for the analysis. Relationships between the sites were visualized using non-metric multidimensional scaling (nMDS) ordination, which was further supplemented by cluster analysis. Following a cluster analysis, the species that had a major contribution to the dissimilarities of site groups were determined using SIMPER dissimilarity percentage program (Clarke and Warwick, 1994).
3 Results
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3.1 Variation of environmental factors
The monthly SST anomalies demonstrated that a long-persisting cold anomaly prevailed in the SCS in early 2008 (Fig. 1) (Hong and Li, 2009). The SST in the NSCS was higher in August 2007 than that in August 2008 (Fig. 2), while the average sea surface salinity in 2007 (33.13) was very similar to that in 2008 (33.08), and increased from onshore to offshore (Fig. 3).
The average sea surface Chl a was 0.64 mg/m3 in August 2007 with values ranging from 0.05 to 3.73 mg/m3. However, the average sea surface Chl a decreased to 0.33 mg/m3 in August 2008 with values ranging from 0.04 to 2.32 mg/m3 (Fig. 4). We also found that the largest size fraction of phytoplankton (>20 μm) took a bigger percentage of total sea surface Chl a in August 2007 than that in August 2008 (Fig. 5).
3.2 Changes in zooplankton biomass and abundance
The average zooplankton biomass in the NSCS was 207.68 mg/m3 in 2007, and sharply decreased to 52.98 mg/m3 in 2008 (Fig. 6). In addition, a remarkable change in zooplankton abundance was also recorded (Table 2). The average zooplankton abundance was 133.37 ind./m3 in 2007, with copepods being the most abundant group (69.40 ind./m3), which accounted for 52.04% of the total zooplankton abundance. Other abundant groups included planktonic larvae (including copepod nauplii, polychaete larvae, echinopluteus larvae, etc.) and chaetognatha, with mean abundance of 21.00 ind./m3 and 12.99 ind./m3, respectively, in 2007.
The average zooplankton abundance decreased to 75.49 ind./m3 in 2008, exhibiting a sharp decrease in the abundance of copepods and larva decreased sharply. Copepods abundance was 30.35 ind./m3 in 2008, less than half of that in 2007. The abundance of larvae decreased from 21.00 ind./m3 in 2007 to 3.74 ind./m3 in 2008.
The abundance of medusae and tunicates also showed great fluctuations between 2007 and 2008. The average abundance of medusae was 8.63 ind./m3 in 2007 with values ranging from 0 to 32.91 ind./m3, but increased to 13.99 ind./m3 in 2008 with values ranging from 1.36 to 72.86 ind./m3 (Fig. 7). Medusae became the second most abundance group in 2008, but not in 2007. The same trend was also observed in tunicates (Fig. 8). The average abundance of tunicates was higher in 2008 (10.27 ind./m3) than in 2007 (4.97 ind./m3).
Multiple regression analysis between zooplankton and environmental variables showed that zooplankton abundance and biomass increased with increasing Chl a concentration in 2007. However, there was no correlation between zooplankton abundance and Chl a concentration in 2008 (Table 3).
3.3 Succession in taxonomic composition
Sixteen groups representing 275 species, including 118 species of copepods and 157 other zooplankton species, were identified in 2007 (Table 2), copepods were the most important group followed by medusae (43), chaetognatha (18), amphipoda (18), and zooplankton larvae (17).
In 2008, 351 species were recorded, including 121 species of copepods and 230 species of other zooplanktons that represented 14 groups. Copepods were also the most dominant zooplankton group. Major copepod species in both years are listed in Appendix (Table A1). Besides copepods, medusae were the second important group in 2008. The species richness of medusae increased from 43 species in 2007 to 88 species in 2008 (Table 2).
There are also remarkable changes in dominant species. Subeucalanus subcrassus was the most dominant copepod in the NSCS in August 2007, followed by Temora discaudata, Nannocalanus minor and T. turbinata. Other dominant species were Echinoplutes larvae, Macruran larvae, Flaccisagitta enflata, Lestrigonus schizogeneios, and Lucifer typus. However, in August 2008, the dominant species changed into Doliolum denticulatum, F. enflata, Diphyes chamissonis, S. subcrassus, T. turbinata, Euchaeta concinna and Dolioletta gegenbauri. Among these, D. denticulatum and F. enflata contributed substantially to the total zooplankton abundance.
The decline in abundance of the dominant copepod species Subeucalanus subcrassus, Temora discaudata, Nannocalanus minor, and T. turbinate in 2008 indicated a major change in zooplankton composition. For instance, the mean abundance of S. subcrassus decreased from 6.04 ind./m3 in August 2007 to 2.29 ind./m3 in August 2008. The other two dominant species, T. discaudata and N. minor in 2007, were replaced by Euchaeta concinna, which usually dominated in winter (Zhang et al., 2009) (Fig. 9a).
In addition to the change in dominant copepod species, other tropical water copepod species, such as Subeucalanus pileatus, Undinula vulgaris, Cosmocalanus darwinii, S. subtenuis, Paraeuchaeta russelli, Euchaeta rimana, E. plana, Labidocera acuta and Scolecithrix danae recorded in 2007 also showed a relatively lower abundance or absence in August 2008 (Fig. 9b), which coincided with the occurrence of the low temperature period. In contrast, Clausocalanus arcuicornis and C. furcatus, usually dominant in winter (Zhang et al., 2009), were recorded only in August 2008.
3.4 Variation of zooplankton community structure by cluster classification and nMDS ordination
Zooplankton communities from the collection stations were classified into four groups (I–IV) according to the cluster analysis (Fig. 10). The dissimilarities between these stations were also visualized by non-metric multidimensional scaling (nMDS) ordination (Fig. 11). The relative distance between these stations reflected their relative dissimilarity in species composition and abundance. For example, samples collected from the onshore sites in 2007 clustered together, indicating that samples from those sites were similar in zooplankton composition. A similar phenomenon was observed in the offshore sites in 2007. However, they were far apart from the samples in 2008 (Fig. 11). SIMPER analysis demonstrated that Echinoplutes larvae, Macruran larvae, Subeucalanus subcrassus, Flaccisagitta enflata, Temora discaudata, Doliolum denticulatum, T. turbinata and Diphyes chamissonis, etc. contributed much to the difference between zooplankton in 2007 and 2008 (Table 4).
4 Discussion
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The composition of copepod dominant species in the northern South China Sea in summer 2007 was similar to that observed in previous years, such as, in the summer of 2004 (Zhang et al., 2009). Moreover, copepod abundance in the summer of 2007 (69.40 ind./m3) was very similar to that in the summer of 2004 (70.27 ind./m3), whereas the copepod community structure between summer 2007 and summer 2008 was strikingly different. The decrease in total zooplankton biomass, abundance, abundance of dominant copepod species and abundance of tropical copepod species correlated with the influence of cold water in early 2008. It is also coincided with the increase in warm temperature species, which are usually dominant in winter.
The anomaly in ocean and climate conditions was also demonstrated by Wheeler (2008), Perlwitz et al. (2009), Trenberth and Fasullo (2010), and Kaufmann et al. (2011), who illustrated a strong La Niña event that dominated the tropical Pacific and nearby in 2008. Affected by La Niña, the long-persisting cold anomaly was prevailed in the SCS in early 2008 (Fig. 1) (Hong and Li, 2009; Wang and Guo, 2009), causing interannual variations of many oceanographic features. For example, the integrated primary productivity in the euphotic zone in NSCS was 745 mg/(m2·d) in August 2007 (Liu et al., 2009), and sharply decreased to 225.39 mg/(m2·d) in August 2008 (Song et al., 2010).
The decline of copepod abundance in August 2008 could also be attributed to the decrease in number of larger phytoplankton preferred by copepods (Fig. 5). Copepods have a preference for larger particles (>20 μm) such as microphytoplankton and ciliates (Kleppel, 1993; Sommer et al., 2000; Stibor et al., 2004; Vargas and González, 2004). The decline of large size phytoplankton in August 2008 could have affected the zooplankton community structure (Lavaniegos et al., 2002), which was further corroborated by the lack of correlation between Chl a and zooplankton abundance in August 2008.
In contrast, the increase in tunicate abundance during the same period may be due to their ability to remove particles at high filtration rates and their preference for small particles (<20 μm) (Alldredge and Madin, 1982; Flood et al., 1992; Sommer et al., 2000). Furthermore, their life histories permit rapid, exponential population increases to take immediate advantage of increased food supply and to exist without reproduction during periods of low food supply (Alldredge and Madin, 1982). Although the numerical increase in tunicates contribution was lower in comparison to the decrease in copepod abundance, differences in typical body sizes of both groups would mean a much larger change in ecosystem functioning (González et al., 2000; Lavaniegos et al., 2002).
Medusa was usually used as indicator of environmental changes, such as temperature change (Purcell et al., 2007). The increase in medusa was probably due to the extremely cold anomaly event in early 2008. The medusa distribution and abundance patterns have also been correlated with climate change, such as the southern-oscillation and the North Pacific Decadal Oscillation (Hays, 2006). On the other hand, many fish compete for the same prey as medusa (Purcell and Arai, 2001). Many fish stocks are in decline in some regions, and there is strong evidence for coincident rises in jellyfish abundance (Graham et al., 2001; Lynam et al., 2006). Xian et al. (2008) investigated the catch rate and diversity in waters near the Penghu Island from March 2008 to May 2008, and found that both the catch rate and diversity decreased significantly, and nearly 90% of fishes died during the cold event. Their findings support our results that the death of fish caused by extremely low temperatures and climatic changes may have led to the increase of medusa.
5 Conclusions
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A total of 467 zooplankton species, representing 16 groups, were identified in the two cruises in the NSCS, with 275 species being identified in August 2007 and 351 in August 2008. Compared with the summer of 2007, the zooplankton abundance and biomass decreased in the summer of 2008. There are also remarkable changes in dominant species and tropical species in 2008. For example, a dramatic decline was revealed in the abundance of four dominant copepod species: Subeucalanus subcrassus, Temora discaudata, Nannocalanus minor and Temora turbinata in 2008. A decrease in total zooplankton abundance and abundance of dominant species, especially abundance of tropical species were correlated with the influence of cold water in the early of 2008, and coincided with the increase in warm temperature species that are usually dominant in winter. Zooplankton species composition showed a change from tropical and subtropical species to warm temperate species. The decline of copepod abundance in 2008 could also be attributed to a decrease in larger phytoplankton (>20 μm), which is preferred by copepods. In contrast, the increase of tunicate abundance may be attributed to an increase in small particles (<20 μm) preferred by tunicates. The variation in zooplankton communities during the two years indicated an anomaly in oceanographic conditions along with the occurrence of a strong La Niña event.
Funding
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  • The National Natural Science Foundation of China under contract Nos 41506161 and 41276162; the National Basic Research Program (973 Program) of China under contract No. 2015CB452903; the Strategic Priority Research Program of the Chinese Academy of Sciences under contract No. XDA11020305; the Special Fund for Agro-scientific Research in the Public Interest under contract No. 201403008.
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doi: 10.1007/s13131-017-0975-5
  • Receive Date：2016-06-27
  • Online Date：2026-04-16
  • Published：2017-10-01
Article Data
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History
  • Received：2016-06-27
  • Accepted：2016-09-12
Funding
The National Natural Science Foundation of China under contract Nos 41506161 and 41276162; the National Basic Research Program (973 Program) of China under contract No. 2015CB452903; the Strategic Priority Research Program of the Chinese Academy of Sciences under contract No. XDA11020305; the Special Fund for Agro-scientific Research in the Public Interest under contract No. 201403008.
Affiliations
    1 Key Laboratory of Marine Bio-resource Sustainable Utilization (LMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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