Summer Assemblages and Biodiversity of Larval Fish Associated with

Marine and Coastal Fisheries: Dynamics, Management, and Ecosystem Science 10:467–480, 2018 © 2018 The Authors. ISSN: 1942-5120 online DOI: 10.1002/mcf2.10037

ARTICLE

Summer Assemblages and Biodiversity of Larval Fish Associated with Hydrography in the Northern South China Sea Lu-Chi Chen* Penghu Marine Biology Research Center, Fisheries Research Institute, Council of Agriculture, Executive Yuan, Penghu, Taiwan

Kuo-Wei Lan Department of Environmental Biology and Fisheries Science, National Taiwan Ocean University, Keelung, Taiwan

Yi Chang Institute of Ocean Technology and Marine Affairs, National Cheng Kung University, Tainan, Taiwan

Wen-Yu Chen Fisheries Agency, Council of Agriculture, Executive Yuan, Taipei, Taiwan

Abstract

The objective of this study was to investigate the association between larval fish assemblages and the environmental factors in the northern South China Sea based on data collected during summertime. Shipboard measurements (Ocean Researcher 1 [cruise CR866], Fishery Researcher 1 [cruise FR1-2008-07-03]) of temperature and salinity profiles were obtained with a conductivity–temperature–depth profiler, and ichthyoplankton was collected with an Ocean Research Institute net. In total, 3,476 larval fishes and 188 taxa representing 80 families were identified. Myctophidae was the most common and abundant taxon in this area. The CPUE (individuals/1,000 m3) of fish larvae differed among sampling stations, with greater abundances at the shallower stations than at the deeper stations, and the species biodiversity at each station also varied. The results of grouping revealed that the spatial distribution of larval fish was divided into a shelf-based group and a pelagic-based group; these two groups were bounded by the 200-m isobath. Abundance of some larval fish was related to environmental factors, such as temperature, salinity, chlorophyll-a concentration, and mixing layer depth. These results indicated that the larvae of some species were more affected by natural environmental characteristics than by internal biological properties.

The South China Sea (SCS) is the largest marginal sea basin of the western Pacific Ocean, and the hydrographic conditions are influenced by the West Pacific Warm Pool

and East Asian Monsoon. The SCS is bordered by Luzon, Palawan, the Malayan peninsula, the Indo-China peninsula, mainland China, and Taiwan. The semi-enclosed

Subject editor: Milo Adkison, University of Alaska–Fairbanks, Juneau *Corresponding author: [email protected] Received November 20, 2017; accepted May 30, 2018 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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basin extends over an area of 3.5 × 106 km2, with an average water depth of approximately 1,250 m (Higginson et al. 2003). Depths range from the shallowest coastal fringe to 5,377 m in the Manila Trench. The SCS is situated in the area of influence of the monsoon regime. It is affected by both southwest monsoons in summer and northeast monsoons in winter (Morton and Blackmore 2001). The seasonal monsoons and complex topography of the continental shelf considerably affect the circulation system in the northern SCS. The waters in this region become exchanged with those in the East China Sea through the Taiwan Strait under the influence of monsoons and the Kuroshio Current, which enters this area through the Luzon Strait (Dale 1956; Fang et al. 1998; Hu et al. 2000). The survival rate of early life stages is vital for determining the annual recruitment of fish (Shepherd and Cushing 1980; Zhang and Lee 2001; Takahashi and Watanabe 2004). Ichthyoplankton is made up of fish eggs and fish larvae, a planktonic stage that is highly sensitive to environmental changes. Many studies have investigated the changes in the composition and spatiotemporal distribution of larval fish assemblages in relation to many factors, including hydrographic conditions (Boucher et al. 1987; Margalef and Estrada 1987), wind forcing (Voss and Hinrichsen 2003), temperature and light intensity (Rodriguez et al. 2011), water depth (Wang and Tzeng 1997), oceanic fronts (Grioche and Koubbi 1997), tides (Suthers et al. 2004), and sea bottom material (Sabates 1990; Humphries and Potter 1993). Furthermore, some biological factors, such as the abundance of phytoplankton and zooplankton, affect the distribution and abundance of larval fish (Humphries et al. 1992; Hsieh et al. 2005). Larval fish assemblages are considered vital research subjects for understanding the status of marine fishery stocks and can serve as references for future marine fishery stock assessments and fishery management. Many studies have investigated the structure of larval fish communities in the waters around Taiwan, but most of these studies focused on the estuarine and coastal waters around Taiwan, waters of northern Taiwan, or entire waters of the Taiwan Strait. Tzeng and Wang (1993) and Chang et al. (2002) reported that the distribution pattern of larval fish assemblages mostly conforms to local hydrographic conditions in the coastal waters of northern Taiwan. Hsieh et al. (2012) identified a similar situation for larval fish assemblages in the coastal waters of southwestern Taiwan. Wang and Tzeng (1997) found close relationships between clupeoid larvae and spatiotemporal variations in the waters off the Tanshui River estuary. In the waters of northern Taiwan, Chen et al. (2012), Chen et al. (2014) reported that the distribution and species composition of larval fish assemblages were affected by factors such as hydrographic conditions, seasonal

monsoon-driven currents, and geographical features. The composition and abundances of larval fish were closely associated with hydrographic variables during monsoons in the Taiwan Strait (Hsieh et al. 2005). Moreover, Hsieh et al. (2010) and Lo et al. (2010) revealed that the distribution patterns of larval fish assemblages were closely linked to the dynamic nature of water currents, and a high abundance of larval fish was typically restricted to a topographic upwelling area and matched the abundance of phytoplankton and zooplankton in the Taiwan Strait. Because the coastal waters of southwestern Taiwan are important fishing grounds, the distribution of larval fish assemblages in the northern SCS must be elucidated. Some studies have described the species composition of larval fish in the SCS. Huang and Chiu (1994) and Chamchang and Chayakul (1999) reported that larval fish communities were mainly composed of myctophids and gonostomatids. This study was designed to gain a further understanding of the structure of larval fish communities and the relationship between fish larvae and environmental conditions in the SCS. Therefore, we collected biological samples by trawling with plankton nets, and we obtained environmental data by shipboard measurements, remote sensing, and model-based calculations. Cluster analysis was used to determine the distribution of larval fish assemblages, and the relationships between larval fish and environmental factors were examined using canonical correspondence analysis. In brief, the study aimed to (1) determine the species composition, abundances, and biodiversity of larval fish; (2) examine the spatial distribution patterns of larval fish assemblages; and (3) investigate the relationships between larval fish and hydrography.

METHODS Data collection.— Field sampling was performed during the Ocean Researcher 1 cruise from May 28 to June 6, 2008, and the Fishery Researcher 1 cruise from July 3 to July 16, 2008 (Table 1). Overall, 19 sampling events were carried out at 12 stations (Figure 1). Vertical profiles of conductivity and temperature were obtained at each station from 5 m above the ocean floor to the surface with the Sea-Bird SBE 911 Plus conductivity–temperature– depth profiler. Ichthyoplankton was collected using an Ocean Research Institute (ORI) net with a mouth diameter of 1.6 m and a stretch mesh size of 330 μm. A flow meter was attached to the center of the ORI net to calculate the volume of water filtered. The net was towed obliquely from a depth of 200 m to the surface at deep (>200m) stations or from 10 m above the ocean floor to the surface at shallow (2%) were the lanternfishes Diaphus A group (11.48%), Oceanic Lightfish Vinciguerria nimbaria (10.51%), Bristlemouth Cyclothone alba (8.39%), Bleekeria mitsukurii (6.52%), Gobiidae type 1 (3.55%), mackerels Scomber spp. (3.45%), Scaly Paperbone Scopelosaurus harryi (2.62%), Warming’s Lanternfish Ceratoscopelus warmingii (2.51%), Clupeidae spp. (2.42%), lanternfishes Lampanyctus spp. (2.30%), Longfin Lanternfish Diogenichthys atlanticus (2.28%), Diaphus B group (2.22%), ponyfishes Leiognathus spp. (2.20%), and Asian seabasses Lateolabrax spp. (2.10%). Over 50% of the species belonged to the Myctophidae, Phosichthyidae, and Gonostomatidae families, indicating that the main larval fish species in the northern SCS are deep-sea fish. Table 1 shows the larval abundance and biodiversity index at each station. Overall, the abundance of larval fish varied from 18.97 individuals/1,000 m3 (at FR28) to 960.08 individuals/1,000 m3 (at OR28), with an average value of 267.73 ± 255 (mean ± SD) individuals/1,000 m3. Larval fish abundance was higher at shallower stations than at deeper stations. The diversity index at individual stations varied from 2.13 to 4.72; the average value was 3.66 ± 0.73. Stations OR4 and OR11 had the highest diversity values, and FR26 had the lowest value. The evenness index varied from 0.62 to 0.97 among stations, with an average value of 0.81 ± 0.10. Station FR27 had the highest evenness value, and SEATS-3 had the lowest. The richness index calculated for the stations varied from 1.30 to 11.20 (5.40 ± 2.69); OR11 had the highest richness value, and FR26 had the lowest value. Figure 4 shows the spatial distribution of the abundance and percent composition for the 10 dominant taxa at each station. Station OR27 mainly contained gobiid

FIGURE 2. Temperature–salinity diagram of (A) cruise CR866 (sites sampled by the vessel Ocean Researcher 1) and (B) cruise FR1-2008-07-03 (sites sampled by Fishery Researcher 1) for South China Sea water (SCSW) and Kuroshio Branch water (KBW). The SCSW and KBW data were obtained from Jan et al. (2006).

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(A)

(B)

(C)

(D)

FIGURE 3. Horizontal distributions of (A) sea surface chlorophyll a, (B) surface layer wind speed, (C) current speed at 35 m, and (D) mixing layer depth in the northern South China Sea during summertime.

larvae and clupeoid larvae, which can typically be caught in shallow waters. Bleekeria mitsukurii, Scomber spp., and Scaly Paperbones were observed at OR28. Only one dominant species was caught at FR27 and FR28; the Diaphus A group was found at FR27, whereas Oceanic Lightfish were caught at F28. The composition proportion among the dominant taxa was equal at FR26, which contained Bristlemouths and Lampanyctus spp. The Diaphus A group was the most represented taxon at FR25 and OR4; the Oceanic Lightfish was the most represented taxon at

OR1. The composition of dominant taxa at OR6 was the same as the composition at OR11 and included Diaphus A group, Oceanic Lightfish, Bristlemouths, Warming’s Lanternfish, and Lampanyctus spp. The dominant taxa at the SEATS station were Diaphus A group and Oceanic Lightfish; the dominant species at FR36 were the Bristlemouth and Bleekeria mitsukurii. In general, the dominant taxa at the deeper stations mostly comprised deep-sea fish, such as myctophid, gonostomatid, and phosichthyid larvae, but the composition of dominant taxa at the shallower

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LARVAL FISH ASSEMBLAGES IN THE SOUTH CHINA SEA TABLE 2. Quantitative data for main larval fish family abundances (individuals/1,000 m3) and species abundances.

Family

Abundance

Percentage

1,408.28

27.68

Myctophidae

Gonostomatidae

660.52

12.98

Phosichthyidae

Phosichthyidae

563.58

11.08

Gonostomatidae

Ammodytidae Scombridae Gobiidae Carangidae

331.63 311.39 244.94 164.69

6.52 6.12 4.82 3.24

Ammodytidae Gobiidae Scombridae Notosudidae

Notosudidae

133.34

2.62

Myctophidae

Clupeidae Percichthyidae

123.21 115.00

2.42 2.26

Clupeidae Myctophidae

Leiognathidae

111.81

2.20

Myctophidae

Others (100-m isobaths and revealed significantly different species compositions. The species composition of each group identified in the present study is discussed in detail below. Group A, comprising stations OR27, OR28, and FR36, was characterized by shallow water. The five leading taxa were Bleekeria mitsukurii, Scomber spp., Gobiidae spp., Clupeidae spp., and the Scaly Paperbone. Sand lances such as Bleekeria mitsukurii occur in estuarine, open coastal, and offshore habitats. Some evidence indicated that spawning occurs principally inshore from November to March (Norcross et al. 1961; Sherman et al. 1984). Larvae are most abundant off the mouths of major estuaries but are common out to the edge of the continental shelf (Norcross et al. 1961; Richards and Kendall 1973). Hsieh et al. (2011) also found that Bleekeria mitsukurii was a common species in the southwest of Taiwan and Penghu. We supposed that this species might be spawned at inshore areas and be transported by the current; as a result, Bleekeria mitsukurii larvae were plentiful at the shelf stations in this study. Scombridae is a common commercial fish species worldwide, and our results concerning scombrid larvae resemble those

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LARVAL FISH ASSEMBLAGES IN THE SOUTH CHINA SEA TABLE 5. Canonical correspondence analysis summary (canonical R = 0.99; P = 0.00000) for environmental and biological variances (enviro-variance and bio-variance, respectively; SWT = seawater temperature; SWS = seawater salinity; SSC = sea surface chlorophyll a; SLWS = wind speed of the surface layer; −35 m CS = current speed at 35 m; MLD = mixed layer depth; LC = light cycle).

Statistic Number of variables Variance extracted (%) Total redundancy (%) 1 2 3 4 5 6 7 8 9 10

Enviro-variance

Bio-variance

7

10

100.00

88.45

86.56

72.32

SWT SWS SSC SLWS −35 m CS MLD LC

Oceanic Lightfish Lanternfishes Diaphus A group Bristlemouth Longfin Lanternfish Warming’s Lanternfish Diaphus B group Slender Fangjaw Gobiidae spp. Smallfin Lanternfish Lanternfishes Lampanyctus spp.

reported by Hsieh et al. (2010) and Chen et al. (2012), who found that the distribution of Auxis spp. was related to Kuroshio. As common coastal fish around Taiwan, Auxis spp. were abundant at the shelf stations. Gobiid larvae were distributed widely, inhabiting places such as reefs, estuaries, sandy bottoms, and continental shelves and could be caught easily in the nearshore area. This species typically spawns during spring to fall (Ken and Katsunori 2010), resulting in its abundance at nearshore shelf areas during the summertime, as confirmed in our study. The Scaly Paperbone is a bathypelagic fish with a regular distribution in the North Pacific region. It is interesting that the larvae of this species were caught at a shelf station. Chen et al. (2012) also found that some deep-sea fish larvae, such as the Diaphus A group, belonged to the shelf group. Therefore, we guessed that some of the deep-sea fish larvae also occurred in the shallow area. Clupeids are pelagic migratory fish that can live in many habitats. Garrido et al. (2009) and Ooi and Chong (2011) found that clupeid larvae were highly abundant in shelf areas, which could explain their abundance at the shelf stations in our study. Concerning group B, subgroup B1 comprised stations OR1 and OR11, and its five leading taxa were the

TABLE 6. Results of chi-square tests with successive roots removed. Values in bold italics are significant at the 0.05 level.

Root removed 0 1 2 3 4 5 6

Canonical R

Canonical R2

χ2

df

P

0.9999 0.9974 0.9824 0.8769 0.8120 0.6185 0.3384

0.9999 0.9948 0.9652 0.7690 0.6594 0.3826 0.1145

185.98 105.79 58.53 28.31 15.13 5.43 1.09

70 54 40 28 18 10 4

0.000 0.000 0.029 0.448 0.653 0.860 0.895

Diaphus A group, Slender Fangjaw, Oceanic Lightfish, Bristlemouth, and Diaphus B group. Subgroup B2 comprised stations OR4, OR6, SEATS, FR25, FR26, FR27, and FR28, and its five leading taxa were the Diaphus A group, Oceanic Lightfish, Bristlemouth, Warming’s Lanternfish, and Diaphus B group. The Diaphus A group accounted for the highest number of myctophid larvae, which were widely distributed in the waters around Taiwan. Sassa et al. (2002) indicated that this group was more abundant at the offshore oceanic station around Kuroshio, in accordance with our results. According to Hsieh et al. (2011), Oceanic Lightfish could pass north by Kuroshio and northwest by its branch, resulting in this species’ high abundance at the oceanic stations in our study. The Bristlemouth is distributed widely in the IndoPacific Ocean, the western Pacific Ocean, and the SCS and was easily sampled at the oceanic stations. The Slender Fangjaw and the Diaphus B group were similarly abundant. Okazaki and Nakata (2007) reported their abundance in Kuroshio and offshore sea, as did Sassa et al. (2002). In our study, Warming’s Lanternfish was abundant at the oceanic stations. This species belongs to the Myctophidae and is mainly distributed in the southwest and west of Taiwan as well as Dongsha Island. Sassa et al. (2002, 2004) reported that myctophid larvae are affected by the current, and these species were distributed relative to the passage of the Kuroshio Current. This could explain the abundance of Warming’s Lanternfish at the oceanic stations. In summary, the shelf stations were mainly affected by the SCSW, and the oceanic stations were primarily affected by the KBW. In addition to the influence of water mass, these stations had varied topography, causing different distributions among dominant species in different stations. Boehlert and Mundy (1993) and Genin (2004) reported that larval fish assemblages are affected by topography and circulation; accordingly, our study could distinguish a shelf group from an oceanic group.

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TABLE 7. Canonical weights of environmental and biological variances (enviro-variance and bio-variance, respectively; SWT = seawater temperature; SWS = seawater salinity; SSC = sea surface chlorophyll a; −35 m CS = current speed at 35 m; SLWS = wind speed of the surface layer; MLD = mixed layer depth; LC = light cycle). Bold italics indicate values >0.60.

Enviro-variance

Root 1

Root 2

Root 3

Bio-variance

Root 1

Root 2

Root 3

SWT SWS SSC −35 m CS SLWS MLD LC

0.0001 0.0743 −1.1075 −0.0780 −0.0086 −0.2287 0.0268

0.0582 −0.6871 0.7633 0.5590 0.1145 1.6856 −0.2556

0.9918 −0.2099 0.3605 −0.0249 0.0055 −0.5270 0.0059

Lanternfishes Diaphus A group Oceanic Lightfish Bristlemouth Bleekeria mitsukurii Gobiidae type 1 Mackerels Scomber spp. Scaly Paperbone Warming’s Lanternfish Clupeidae spp. Lanternfishes Lampanyctus spp.

−0.1882 −0.0206 0.1932 −0.0710 0.0205 −1.7741 1.5139 −0.0393 −0.8642 −0.0534

1.0950 0.2805 −1.2888 −0.1045 0.0486 1.9549 −2.2535 0.3277 0.0422 0.3280

−0.5909 −1.0025 0.5832 −0.0827 −0.3323 −0.1295 −0.4996 0.1080 −0.1163 −0.0819

Relationship Between Larval Fish and Environmental Factors The CCA results of the first canonical axes indicated that Scomber spp. and Clupeidae spp. prefer an environment of relatively high SSC. By contrast, the Scaly Paperbone was abundant in areas with relatively low SSC. The results of the second canonical axes revealed that the Diaphus A group and Scomber spp. were more abundant with relatively low SWS but relatively high SSC when the MLD was greater, whereas the Bristlemouth and Scaly Paperbone were more abundant with relatively high SWS but relatively low SSC when the MLD was shallower. The results of the third canonical axes indicated that Oceanic Lightfish prefer an environment of relatively low SWT. Many studies have indicated close associations between the composition of larval fish and environmental factors, such as water temperature, salinity, chlorophyll a, and upwelling; consequently, we assumed that because the study area was affected by the southwestern monsoon in summer, this would influence the abundance of some larval fish. According to Chia and Wu (2007), the MLD in the SCS exhibits diel variations; Wang and Chen (2001) and Kendall et al. (1994) confirmed that the larval fish of several species engage in diel migration. Although these species might be influenced by natural stimulation, we argue that environmental factors, such as SWT, SWS, or MLD, constitute a more likely explanation because of the varying distributions at different sea areas observed in our results. CONCLUSIONS In our study, we found that the composition of larval fish was primarily dominated by deep-sea taxa. Moreover, the abundance of larval fish was higher in shallower areas than in deeper areas, and biodiversity also varied with the

situation of the grouping; thus, high diversity occurred in the shelf group, and lower diversity occurred in the oceanic group. Larval fishes were affected by hydrography and topography, which resulted in different groupings, clearly identifying that larval fish were closely associated with some environmental factors. However, the field sampling in our study was carried out from May to July rather than throughout an entire year. As a result, the temporal variation of larval fish and its relationship to environment variability are not fully understood. In addition, several previous studies have reported that the abundance and distribution of fish larvae are closely connected with food sources (Humphries et al. 1992; Hsieh et al. 2010; Chen et al. 2012). We recommend a longer study period and the consideration of some biological factors in future work, which would further elucidate the spatiotemporal variations of larval fish and the influence of biological factors in the study area.

ACKNOWLEDGMENTS We thank the captain, officers, and crews of the Ocean Researcher 1 and Fishery Researcher 1 for providing information and assistance for the field experiment. We extend our deepest respect and gratitude to Ming-An Lee, DonChung Liu, Yu-Tzu Wang, Yu-Kai Chen, and Jia-Yi Pan for providing samples and guidance. There is no conflict of interest declared in this article.

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