Open Access

Water mass transport through the northern Bashi Channel in the northeastern South China Sea affects copepod assemblages of the Luzon Strait

Zoological Studies201453:66

DOI: 10.1186/s40555-014-0066-7

Received: 3 September 2013

Accepted: 4 September 2014

Published: 16 September 2014

Abstract

Background

It is controversial to what extent the intrusion of the Kuroshio Branch Current to the Luzon Strait and the South China Sea circulation can shape copepod assemblages around southern Taiwan. We tested the hypothesis that currents such as the Kuroshio Current bring marine zooplankton and copepods from subtropical and tropical waters to the south of Taiwan. We studied copepod assemblages from the Bashi Channel in the northeastern South China Sea at the coast of southwest Taiwan during early October 1996.

Results

A total of 77 copepod species were identified from 34 genera that included calanoids, cyclopoids, harpacticoids, and poecilostomatoids. Several indicator species suggest that the study area is highly influenced by water masses from the northern South China Sea as well as from the Kuroshio Current. Acrocalanus gracilis (Paracalanidae, Calanoida) was most abundant (with a relative abundance (RA) of 22.07 and an occurrence rate (OR) of 100%), followed by Paracalanus aculeatus (Paracalanidae, Calanoida) and Oncaea venusta (Cyclopoida). The stations close to the Kuroshio Current showed a higher species diversity (H') and a higher species richness with 3.9 to 4.6 at moderate abundance, whereas station 11 showed lowest species diversity (H') with (2.1), accompanied by the far lowest species number (14) and abundance (880 ind./100 m3).

Conclusions

Several indicator species suggest that the study area is highly influenced by water masses from the northern South China Sea as well as from the Kuroshio Current.

Keywords

Marine plankton Community ecology Copepoda Current regimes Kuroshio Branch Current Bashi Channel

1 Background

The complexity of oceanic circulations around the island of Taiwan generated a high diversity of marine life, comprising about 10% of the world's total marine fauna and including a large number of endemic species. Such high diversity is suggested to be enhanced by ocean currents and water movements that also affect the structure of copepod communities at spatial and temporal scales. Along the Taiwan Strait and the southern edge of the East China Sea, water circulations are strongly influenced by monsoon winds. During the NE monsoon period in winter (September to April), the China Coastal Current brings cold water from the Yellow Sea and from the East China Sea to the Taiwan Strait (Liu et al. [2003]; Tseng and Shen [2003]; Hwang and Wong [2005]; Hwang et al. [2006]; Chang et al. [2010]).

Water circulation in this area varies seasonally with changes in wind direction. Physical oceanography indicates that the Kuroshio Current intrudes into both the northern South China Sea and the coastal waters of southern Taiwan via the Luzon Channel, particularly during winter (Tseng and Shen [2003]). The Luzon Channel is an important water way transporting marine fauna from the Kuroshio Current towards the northeastern South China Sea and the coastal waters of southern Taiwan (Hwang et al. [2006]; Hsieh et al. [2011]; Hsieh et al. [2012]).

The objective of this study was to investigate spatial patterns of copepod biodiversity in the northeastern part of the South China Sea. Based on evidence from previous studies, we tested the following two hypotheses in the present paper: (a) are the copepod assemblages characteristic for the northeastern South China Sea? and (b) is the copepod composition in coastal areas of southern Taiwan affected by Luzon Strait waters? We use the data from 15 stations along 3 latitudinal transects in the northern South China Sea to test these questions.

2 Methods

The study was conducted on board the Ocean Researcher III during cruise 244 from 1 to 3 October 1996. Data were collected from 15 sampling stations in the northeastern South China Sea to investigate the copepod composition, abundance, and distribution in the Luzon Strait. Locations of the 15 sampling stations are shown in Figure 1.
Figure 1

Sampling stations and satellite image of seawater surface temperature in the waters southwest of Taiwan. During the cruise of 1 to 3 October 1996.

2.1 Zooplankton sampling

Zooplankton samples were collected on board the Ocean Researcher III along the KC edge, the Luzon Strait, and the NSCS around the southern tip of the island of Taiwan. The map of sampling stations along two main transects is following latitude 21°30′ (°N) and latitude 21°45′ (°N) in the northern South China Sea and the Bashi Channel. At each sampling station, sea surface tows (1 to 5 m) were taken using a 4.5-m-long conical zooplankton net with a 1-m mouth diameter (see Dahms and Hwang [2010]). Each sample was collected by a zooplankton net towing for 15 to 20 min with the vessel speed of 2 nautical miles per hour. The water volume filtered was estimated from records of a flow meter that was mounted in the center of the net opening. Zooplankton was preserved in 5% formalin immediately after collection. In the laboratory, copepod species were counted under a stereomicroscope. We used the Shannon-Wiener index to calculate species diversity of copepods. Sea water temperature and salinity information was obtained from the conductivity-temperature-depth (CTD) instrument before plankton tows were taken.

2.2 Identification and enumeration

In the laboratory, each sample was split with a Folsom splitter to a subsample of less than 500 individuals for taxonomic identification and counting. Species composition of each sample was determined by counting all mature animals in the subsamples. The following keys and taxonomic references were used for copepod identification: Chen and Zhang ([1965]); Chen et al. ([1974]); Huys and Boxshall ([1992]); Chen ([1992]), and Chihara and Murano ([1997]). Other monographs were consulted for the identification of particular species (Frost and Fleminger [1968]; Nishida [1985]; Bradford-Grieve [1994]; Markhaseva [1996]).

2.3 Spatial similarity analysis

In order to elucidate the relative importance of spatial and temporal scales in this study, we compared the similarity of species composition among stations for each sampling date. It is suggested in the literature that the hydrographic situation of the study area is influenced by the surrounding ocean currents and that water sources will affect the structure of copepod communities at spatial and temporal scales.

We analyzed copepod community structures between each station by applying the Plymouth Routines In Multivariate Ecology Research (PRIMER) computer package. To compare differences in copepod groups with station samples, the logarithmic abundances of the most common species (those with occurrence rates of >20%) were standardized; then, cluster analysis (CA) was used to place species with similar distributions into groups or clusters using minimum variance (or Ward) linkages. To identify groups of copepod species that covaried in logarithmic abundance, the data matrix was transposed so that samples became variables, and then, cluster analysis was used to determine the covarying species groups. The numerical abundances of all copepod species in each group were integrated and averaged to display their distribution patterns.

3 Results

3.1 Temperature versus salinity

Sea surface temperatures to the east and southeast of Taiwan averaged 25°C throughout the year due to the influence of the warmer KC and tropical SCS waters. In contrast, surface salinity varied widely among sampling stations and did not show a clear pattern. The characteristic of the T/S diagram in the upper waters at station 1 was between the South China Sea Surface Current and the Kuroshio Current, while deeper zones were influenced by the warmer Kuroshio Current (Figure 2).
Figure 2

Temperature-salinity diagram from the sampling station 1 in the waters southwest of Taiwan. During the cruise of 1 to 3 October 1996. SCSSC refers to the South China Sea Surface Current and KC to the Kuroshio Current.

3.2 Systematic inventory

Copepods were the most dominant component of the zooplankton in the study area in terms of species richness and numerical abundance. The distribution of copepods was relatively patchy. A total of 77 copepod species were identified from 34 genera that include calanoids, cyclopoids, harpacticoids, and poecilostomatoids (Table 1).
Table 1

List of copepod species from all sampling stations of the present study

CALANOIDA

Pontellopsis strenua (Dana 1849)

ACARTIIDAE

L. detruncata (Dana 1849)

Acartia danae Giesbrecht 1889

L. minuta Giesbrecht 1889

A. negligens Dana 1849

Pontella fera Dana 1849

CALANIDAE

Pontellina plumata (Dana 1849)

Canthocalanus pauper (Giesbrecht 1888)

SCOLECITRICHIDAE

Cosmocalanus darwinii (Lubbock 1860)

Scolecithricella emarginata (Farran 1905)

Nannocalanus minor (Claus 1863)

Scolecithrix nicobarica Sewell 1929

Neocalanus gracilis (Dana 1849)

TEMORIDAE

Undinula vulgaris (Dana 1849)

Temora discaudata (Giesbrecht 1889)

CALOCALANIDAE

T. turbinata (Dana 1849)

Calocalanus pavo (Dana 1849)

CYCLOPOIDA

C. plumulosus (Claus 1863)

OITHONIDAE

CANDACIIDAE

Oithona setigera Dana 1849

Candacia catula (Giesbrecht 1892)

O. similis Claus 1866

C. curta (Dana 1849)

O. tenuis Rosendorn 1917

C. pachydactyla (Dana 1849)

HARPACTICOIDA

Paracandacia truncata Dana 1849

MIRACIIDAE

P. simplex (Giesbrecht 1888)

Macrosetella gracilis (Dana 1847)

CENTROPAGIDAE

POECILOSTOMATOIDA

Centropages calaninus (Dana 1849)

CORYCAEIDAE

C. furcatus (Dana 1849)

Corycaeus (Agestus) flaccus Giesbrecht 1891

C. gracilis (Dana 1849)

C. (Corycaeus) crassiusculus Dana 1849

C. orsini Giesbrecht 1889

C. (C.) speciosus Dana 1849

CLAUSOCALANIDAE

C. (C.) vitreus Dana 1849

Clausocalanus furcatus (Brady 1883)

C. (Ditrichocorycaeus) affinis McMurrich 1916

EUCALANIDAE

C. (D.) dahli Tanaka 1957

Pareucalanus attenuatus (Dana 1849)

C. (D.) erythraeus Cleve 1901

Rhincalanus rostrifrons (Dana 1852)

C. (D.) lubbocki Giesbrecht 1891

Subeucalanus crassus (Giesbrecht 1888)

C. (D.) subtilis M. Dahl 1912

Subeucalanus subcrassus (Giesbrecht 1888)

C. (Monocorycaeus) robustus Giesbrecht 1891

EUCHAETIDAE

C. (Onychocorycaeus) catus F. Dahl 1894

Euchaeta indica Wolfenden 1905

C. (O.) pacificus M. Dahl 1912

E. rimana Bradford 1974

C. (O.) pumilus M. Dahl 1912

LUCICUTIIDAE

C. (Urocorycaeus) lautus Dana 1849

Lucicutia flavicornis (Claus 1863)

C. (U.) longistylis Dana 1849

L. ovalis (Giesbrecht 1889)

Farranula gibbula Giesbrecht 1891

METRIDINIDAE

ONCAEIDAE

Pleuromamma borealis (Dahl 1893)

Oncaea venusta Philippi, 1843

P. gracilis (Claus 1863)

SAPPHIRINIDAE

P. xiphias (Giesbrecht 1889)

Copilia mirabilis Dana 1849

PARACALANIDAE

C. quadrata Dana 1852

Acrocalanus gibber Giesbrecht 1888

Sapphirina angusta Dana 1849

A. gracilis Giesbrecht 1888

S. darwini Haeckel 1864

A. monachus Giesbrecht 1888

S. intestinata Giesbrecht 1891

Paracalanus aculeatus Giesbrecht 1888

S. iris Dana 1849

PONTELLIDAE

S. nigromaculata Claus 1849

Calanopia elliptica (Dana 1849)

S. scarlata Giesbrecht 1891

C. minor A. Scott 1902

S. sinuicauda Brady 1883

Labidocera acuta (Dana 1849)

 

3.3 Comparison of stations: copepod abundance, relative abundance, and occurrence

High copepod abundances in the study area are shown to be caused by both a year-round Kuroshio Current intrusion and the SW monsoon, prevailing in the South China Sea during summer that brings plankton from subtropical and tropical regions. Several indicator species suggest that the study area is highly influenced by water masses from the northern South China Sea as well as from the Kuroshio Current. Among them was Acrocalanus gracilis, the most abundant (with a relative abundance (RA) of 22.07 and an occurrence rate (OR) of 100%), followed by Paracalanus aculeatus and Oncaea venusta (Table 2). The stations close to the Kuroshio Current showed a higher Shannon-Wiener index as species diversity (H′) and a higher species richness with 4.0 to 4.3 at a moderate abundance (mean abundance was 14,950 ind./100 m3), whereas station 11 showed lowest species diversity (2.1), accompanied by the far lowest species number (14) and abundance (880 ind./100 m3).
Table 2

Average abundance, relative abundance, and occurrence of the 20 most common copepod species in the waters southwest of Taiwan

Species

Abundance

RA

OR

Acrocalanus gracilis

3,300 ± 1,215

22.07

100

Paracalanus aculeatus

2,073 ± 716

13.87

93

Oncaea venusta

1,638 ± 441

10.96

80

Undinula vulgaris

894 ± 378

5.98

73

Clausocalanus paululus

787 ± 262

5.26

73

Acartia negligens

540 ± 166

3.61

87

Farranula gibbula

423 ± 120

2.83

87

Lucicutia flavicornis

391 ± 224

2.62

33

Cosmocalanus darwinii

374 ± 216

2.50

40

Temora discaudata

354 ± 118

2.37

80

Acrocalanus gibber

325 ± 104

2.17

73

Clausocalanus furcatus

306 ± 100

2.05

73

Canthocalanus pauper

305 ± 220

2.04

53

Eucalanus subcrassus

253 ± 91

1.69

67

Calanopia elliptica

203 ± 60

1.36

80

Sapphirina intestinata

182 ± 182

1.22

7

Corycaeus (D.) erythraeus

155 ± 51

1.04

67

Calanopia minor

154 ± 74

1.03

47

Copilia mirabilis

152 ± 67

1.02

60

Temora turbinata

146 ± 108

0.98

27

Other copepods (58)

1,993 ± 1,034

13.35

-

Total

14,950 ± 2,947

100

-

Taiwan average abundance (mean ± SE, ind./100m3), relative abundance (RA, %), and occurrence (OR, %) of the 20 most common copepod species in the waters southwest of Taiwan during the cruise of 1 to 3 October 1996.

3.4 Spatial similarity analysis

In order to elucidate the relative importance of spatial and temporal scales in this analysis, we compared the similarity of species composition among stations for each sampling date. It is suggested in the literature that the hydrographic situation of the study area is influenced by the surrounding ocean currents and that water sources will affect the structure of copepod communities at spatial and temporal scales.

The numerical abundance, species number, and Shannon-Wiener diversity of copepods in the waters southwest of Taiwan during the cruise of 1 to 3 October 1996 are provided in Table 3. The most abundant two species are by far A. gracilis and P. aculeatus (Figure 3). Most dominant copepods exhibited higher abundance in the waters closer to the southwestern coast of Taiwan, with the exception of Lucicutia flavicornis, Cosmocalanus darwinii, and Temora discaudata, having higher numbers in the waters near the Kuroshio Current. All dominant copepod species showed lowest abundance in the northeastern South China Sea at station 10 and station 11 (Figure 3).
Table 3

Species diversity (H′), species number, and abundance (×10 3 ind./100m 3 ) of copepod species in the waters southwest of Taiwan

Station

1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

Mean

H'

3.2

3.5

3.6

3.7

4.6

4.4

3.9

3.9

4.1

3.5

2.1

3.4

2.4

2.8

3.2

3.5 ± 0.2

Species number

26

28

22

27

43

38

29

30

32

22

14

26

31

22

23

28 ± 2

Abundance

17.1

13. 6

15.0

15.4

13.0

21.2

3.6

16.8

9.5

2.1

0.9

13.5

27.1

8.1

47.4

14.9 ± 2.9

During the cruise of 1 to 3 October 1996.

Figure 3

Numerical abundance of the 12 most common copepod species in the waters southwest of Taiwan. During the cruise of 1 to 3 October 1996.

Four station groups were defined from the results of a cluster analysis using the 48 most dominant copepod species that are delineated on the map (Figure 4): group I contains stations mostly in the northern SCS and KC, group II contains three stations located in the transition zone of the three station groups (coastal waters, Kuroshio Current, and northeastern South China Sea), group III contains two stations in the northeastern South China Sea, and group IV contains five stations in or near the Kuroshio Current.
Figure 4

Station groups delineated from the result of cluster analysis using 48 most dominant copepod species.

Four copepod assemblages were also distinguished using covarying copepod species groups and their distribution patterns in the waters southwest of Taiwan during the cruise of 1 to 3 October 1996 (Figure 5). Group I contains stations with the most dominant species with higher abundances in the coastal waters of southwestern Taiwan and lower numbers in the waters near the northern SCS and KC. Group II contains stations in the waters near KC. Group II contains stations characterized by low abundance at all stations during the present study. The species in group IV have higher abundances in the coastal waters of southwestern Taiwan and lower abundances in the waters near the SCSSC and KC, but most species of this group were not dominant.
Figure 5

Covarying copepod species groups and their distribution patterns in the waters southwest of Taiwan. During the cruise of 1 to 3 October 1996.

4 Discussion

The zooplankton communities in the boundary waters of the northeastern South China Sea are unique and complex as a result of the collective impacts of these three water circulations (Hwang et al. [1998]; Shih and Chiu [1998]; Hwang and Wong [2005]; Hwang et al. [2006]). This notion could be substantiated by our present investigation. According to Shih and Young ([1995]), there are 431 planktonic copepod species recorded from the marginal seas of China, including the waters surrounding Taiwan. The number of recorded species of planktonic copepods in the Kuroshio edge exchange processes (KEEP) sector of the western North Pacific was estimated as 53 by Tan ([1967]), 113 by Shih and Chiu ([1998]), 144 by Hsiao et al. ([2004]), 174 by Hsiao et al. ([2011]), and 78 copepod species in the study by Tseng et al. ([2008a]). Comparing the species list of the present study with that of Shih and Chiu ([1998]), there are 13 species that are reported in the latter study but are absent from the present study. Surface currents are supposed to have a major impact on the abundance and diversity of planktonic communities in the region studied here (Shih and Chiu [1998]).

Some copepod species can be used as indicator species of water masses. Such copepods can provide suitable indicators for water mass movements such as the intrusion of Kuroshio Current waters that are otherwise characterized by different temperature and salinities (Hsieh et al. [2004]; Hsiao et al. [2004]; Hwang et al. [2007]; Hsiao et al. [2011]). It has to be emphasized that most common copepod species found during the present study do not belong to temperate water species according to the proposed ecological classifications by some researchers (Takahashi and Hirakawa [2001]). We suggest here in accordance with previous studies that copepods have been transported from the Kuroshio Current into southwest Taiwan through the Luzon Strait based on similarity analyses (Lo et al. [2004]; Hwang et al. [2007]). This intrusion has been evidenced by physical data before (Liu et al. [2003]). The Kuroshio Current intrusion through the Luzon Strait into the northern South China Sea and southwest Taiwan may also in part explain why copepods show a very high diversity in adjacent waters of the intrusion areas (Hwang et al. [2007]).

Similarly, Hwang and Wong ([2005]) showed that Calanus sinicus is transported by the China Coastal Current along the west coast of Taiwan even as far south as Hong Kong. However, in the present study, C. sinicus and Euchaeta concinna, two species with higher index values for winter (see Hwang et al. [2006]), originate from the East China Sea (Chen [1992]) and were lacking altogether in the present inventory. Under the influence of the SW monsoon, the South China Sea Surface Current moves northwards during summer in the area of the Kuroshio Branch Current (Tseng and Shen [2003]). From late autumn to early spring (November to March), the NE monsoon drives water masses from the East China Sea along the China coast line towards the Taiwan Strait, resulting in the obstruction of the north-flowing Kuroshio Current at the Changyun Ridge. The Kuroshio Current can flow over the Changyun Ridge and affects the northern part of the Taiwan Strait only when the NE monsoon begins to subside in spring.

Several species were found in comparatively low numbers in the present study. One possible explanation for this could be the unequal distribution of copepods vertically in the water column. A recent study from an upwelling system in the southeastern TS showed that most copepod species stay in deeper waters (Kao [2003]). Similarly, a study of copepods in the coral reef ecosystem of Ken-tin, southern Taiwan, demonstrated that several species never migrate to the surface (Lo et al. [2004]).

According to the present study, the dominant ten copepod species were similar at all stations considered during the present study. The similarity of dominant copepod species in these regions indicate a long-term water mixing. However, the dominant copepod species in the present study were very different from northern Taiwan (Tseng et al. [2008b],[c],[d]), indicating a separation of northern and southern water masses. Influenced by the SW monsoon, the South China Sea surface current moves northwards during summer to the area of the Kuroshio Branch Current (Tseng and Shen [2003]). The zooplankton communities in the boundary waters are unique and diverse as a result of the collective impacts of these three water circulations (Shih and Chiu [1998]). According to the present study, it is suggested that sampling stations in the NSCS have higher copepod densities as well as species numbers than those of the KC. Furthermore, lower latitudes show generally higher copepod species richness than higher latitudes, confirming a higher tropical diversity. In terms of the vertical profile of the water column, copepod abundances are generally higher in the upper 50 m than in deeper strata of the water column. Several species have been suggested to be associated with water masses in that region.

5 Conclusions

High copepod abundances in the northeastern South China Sea during summer are caused by both a year-round Kuroshio Current intrusion and the South China Sea surface current driven by the SW monsoon. Both currents bring plankton from subtropical and tropical regions. The stations close to the Kuroshio Current show a higher species diversity H′ and a higher species richness. Several indicator species suggest that the study area is highly influenced by water masses from the northern South China Sea as well as from the Kuroshio Current.

Declarations

Acknowledgements

We thank the members of JS Hwang's laboratory for their assistance in field sampling and the provision of data. Special thanks are dedicated to the Taiwan Ocean Research Institute in providing us with weather information from the data bank for atmospheric research. We thank the captain and crew of Ocean Researcher III, Taiwan. This research was supported by grants from the Ministry of Science and Technology of the ROC to J.S. Hwang (NSC86-2611-M-019-009-OS and NSC102-2611-M-019-003) and to W.T. Lo (NSC96-2611-M-110-006 and 97C030200 (Kuroshio Project)). This study was supported by a NRF Collaboration Project (2012-R1A2A2A02012617).

Authors’ Affiliations

(1)
Department of Marine Biotechnology and Resources, National Sun Yat-Sen University
(2)
Department of Biomedical Science and Environmental Biology, Kaohsiung Medical University
(3)
Institute of Marine Biology, National Taiwan Ocean University

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© Lo et al.; licensee Springer. 2014

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited.