Composition of Fish Species in the Bering and Chukchi Seas and Their Responses to Changes in the Ecological Environment

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Acta Oceanol. Sin., 2014, Vol. 33, No. 6, P. 63–73 DOI: 10.1007/s13131-014-0490-x http://www.hyxb.org.cn E-mail: [email protected]

Composition of fish species in the Bering and Chukchi Seas and their responses to changes in the ecological environment LIN Longshan1*, CHEN Yongjun1, LIAO Yunchih2, ZHANG Jing3, SONG Puqing1, YU Xingguang1, WU Risheng1, SHAO Kwang-tsao2 1 Third Institute of Oceanography, State Oceanic Administration, Xiamen 361005, China 2 Biodiversity Research Center, Academia Sinica, Taipei 11529, China 3 Fisheries College of Jimei University, Xiamen 361012, China

Received 12 March 2013; accepted 20 August 2013

©The Chinese Society of Oceanography and Springer-Verlag Berlin Heidelberg 2014

Abstract Based on trawl surveys in the Bering Sea and Chukchi Sea during the 2010 Chinese National Arctic Research Expedition, fish biodiversity characteristics, such as fish composition, dominant species, biodiversity, and faunal characteristics were conducted. We also discussed the responses of fishes to the quick changes in Arctic climate. The results showed that a total of 41 species in 14 families were recorded in these waters. The dominant species were Hippoglossoides robustus, Boreogadus saida, Myoxocephalus scorpius, Lumpenus fabricii, and Artediellus scaber. There were 35 coldwater species, accounting for 85.37%, and six cold temperate species, occupying 14.63%. The habitat types of fish could be grouped as follows: 35 species of demersal fishes, five benthopelagic fishes, and one pelagic fish. The Shannon–Wiener diversity index (H′) (range between 0 and 2.18, 1.21 on average) was not high, and descended from south to north. Climate change has caused some fishes to shift along their latitudinal and longitudinal distribution around the Arctic and Subarctic areas, and this could lead to the decline of Arctic fishery resources. Key words: Arctic, fish fauna, biodiversity, responses to ecological environment Citation: Lin Longshan, Chen Yongjun, Liao Yunchih, Zhang Jing, Song Puqing, Yu Xingguang, Wu Risheng, Shao Kwang-tsao. 2014. Composition of fish species in the Bering and Chukchi Seas and their responses to changes in the ecological environment. Acta Oceanologica Sinica, 33(6): 63–73, doi: 10.1007/s13131-014-0490-x

1 Introduction et al., 2006; Grebmeier, Cooper et al., 2006; Mueter and Litzow, As one of the most sensitive areas responding to global cli- 2008; Mueter et al., 2009). The effect of climate change on Arc- matic changes (Yu, 2011; Zhang et al., 2011), Arctic seawater is tic fish migration has been a hot topic in international research experiencing increasing surface temperature, melting frozen in recent years (Arctic Writing Group, 2011; Mecklenburg et al., zone, decreasing sea ice, and so on, which have a dramatic im- 2011; Reist et al., 2006; Allison et al., 2005). However, scientific pact on the marine environment, organisms, and biosphere investigations and studies for these two seawaters in China are (Lubchenco, 2011; Kedra et al., 2010). The plentiful oil, gas, only about hydrology (Tang et al., 2001; Chen et al., 2011; Gao et and mineral resources, sailing course, and fishery resources of al., 2003), atmosphere (Wang et al., 2008; Ji et al., 2011), plank- the Arctic Ocean have become the focus of different countries ton (Lin, Yang et al., 2009; Yang and Lin, 2006), and nutrients (Zhang, 2009; Shen et al., 1987). The climatic changes may affect and salinity (Gao et al., 2011; Xing et al., 2011). No studies on the the whole Arctic region and have far-reaching influences on the fishery resources have been conducted by Chinese scientists, ecology and even the fishery resources (Arctic Writing Group, except the acoustic investigation of Theragra chalcogramma in 2011). 1999 (Chen and Zhang, 2001). The Bering Sea, located in the northernmost Pacific Ocean, In our study, we analyzed the trawl investigation data of contains a wide continental shelf and rich fishery resources the 4th Chinese National Arctic Research Expedition in the (Wan et al., 2009). The Chukchi Sea, which is the marginal sea of Bering Sea and Chukchi Sea (58°00.00′–75°19.80′N, 176°12.24′– the Arctic Ocean, is an important source of nutrients, heat, and 157°09.53′W) during July 12–19 and September 1, 2010 in the fresh water for the Arctic Ocean. The nutrients support Arctic Bering Sea, and July 21–August 30, 2010 in the Chukchi Sea. The ecosystems and the heat can influence the ice (Shi et al., 2004). species composition, dominant species, ecological type, and The Bering Strait forms its southernmost limit and connects to species diversity of these two seawaters were analyzed. In order the Bering Sea and Pacific Ocean. Previous studies on the Ber- to compare with the composition and distribution of species in ing Sea and Chukchi Sea were mainly about the composition of the marginal sea of the Northwest Pacific and North Atlantic– fish species (Barber et al., 1997; Norcross et al., 2010), fish dis- Eastern Greenland waters, the present study discussed the rap- tribution (Rand and Logerwell, 2011; Mecklenburg et al., 2011; id responses of fishes to Arctic climate changes and would pro- Busby et al., 2005), and responses to changes in the ecological vide essential data for the fishery resources, ecosystem changes, environment (Robertis and Cokelet, 2012; Grebmeier, Overland and relationship between the ecosystem and the environment.

Foundation item: The Chinese Polar Environment Comprehensive Investigation and Assessment Programs under contract Nos CHIN- ARE2012-2015-04-03 and CHINARE2012-2015-03-05; the Polar Science Strategic Research Foundation of China under contract No. 20120105; the Public Science and Technology Research Funds Projects of Ocean under contract No. 201105022-2. *Corresponding author, E-mail: [email protected] 64 LIN Longshan et al. Acta Oceanol. Sin., 2014, Vol. 33, No. 6, P. 63–73

2 Materials and methods al. (1993). Furthermore, temperate water species were divided into warm temperate species and cold temperate species, and 2.1 Station design and sampling method coldwater species were divided into subcold zone species and Specimens were collected using a middle-water Isaacs-Kidd cold zone species. The samples also were sorted into continen- midwater trawl (IKMT) net (9 m long, 4 m2 net mouth area, 20 tal shelf demersal fish, continental shelf benthopelagic fish, mm mesh size), a French-type otter trawl net (2.5 m wide, 0.5 continental shelf pelagic-neritic fish, oceanic pelagic-neritic m high, and 9 m long; 10 mm mesh size), an otter trawl net (1.6 fish, and oceanic bathydemersal fish, according to Froese and m wide, 0.5 m high, and 3 m long; 20 mm mesh size), and a tri- Pauly (2012), Wilson (2012), and Liu and Ning (2011). Fishes angular bottom trawl net (2.2 m wide, 0.65 m high, and 6.5 m were judged as economic fish by Froese and Pauly (2012) and as long; 20 mm mesh size). The speed was about 3–4 kn. Every net migratory fish by Wilson (2012). Fish distribution of the inves- was operated for 10–60 min due to the different seabeds. The tigation waters was referred to Froese and Pauly (2012), Wilson research vessel for the present study was Xuelong. The survey (2012), Liu (2008), and Tetsuji (2002). stations were designed according to latitude. Sampling stations Biodiversity was analyzed by three indices: species diversity were distributed from the Bering Sea basin through the conti- index (H′), evenness index (J′), and richness index (D) (Ludwing nental rise, continental shelf of the Bering Sea, and northern and Reynolds, 1998; Ma, 1994). and southern Bering Strait, to the shelf of the Chukchi Sea and Species diversity was calculated by the Shannon–Wiener di- Chukchi slope (Fig. 1). If the total weight of the catch was less versity index (H′): than 20 kg, all samples were analyzed. If the total weight of the catch was more than 20 kg, the large and rare individuals were H′ = −ΣPiln Pi . (1) selected and then 20 kg was chosen from the remaining catch at random. The samples were first classified: photos were taken, Evenness was calculated by Pielou’s index: and then samples were frozen immediately. The classification J′ = H′/lnS. (2) was based on Nelson (2006), Coad et al. (1995), and Mecklen- burg et al. (2002). The sampling and analysis method were ac- Species richness was calculated by Margalef’s index, which cording to the Marine Investigation Standard (Standardization was the number of the species in a certain limit: Administration of the People's Republic of China, 2007).

D = (S−1)/lnN. (3) 2.2 Data analysis

The fishes were divided into warmwater species, temper- Pi was the ratio of number of ith and total individuals. S was ate water species, and coldwater species, according to Tian et the number of species. N was the total number of individuals of

80° N 50 100 M06 250 75° SR12 M07 SR11 500 SR10 SR09 Co-10 750 R08 Co-01 1 000 SR07 C05 70° 1 250 R06 C02 1 500 SR03 CC8 2 000 BS05 2 500 65° BS08 Depth/ m BS02 NB09–NB10B 3 000 BB06 NB08B BB05 NB08 3 500 BB02 NB09–NB10 4 000 60° SL01–SL09 B14 4 500 B07 5 000 5 500 55° 6 000 6 500

170° E 180° W 170° 160° 150° French-type otter trawl otter trawl French-type otter trawl and otter trawl triangular bottom trawl middle water IKMT net

Fig.1. Stations of the 2010 Arctic Expedition in the Bering Sea and Chukchi Sea. LIN Longshan et al. Acta Oceanol. Sin., 2014, Vol. 33, No. 6, P. 63–73 65

different stations. 36 stations in the present study, which belonged to seven or- The dominant species were determined by the ratio of the ders, 14 families, and 31 genera. Among them, just one species number of certain species/total individuals and occurrence rate was Chondrichthyes, while the remaining six orders, 13 fami- at different stations. lies, and 30 genera belonged to Osteichthyes. The number of Scorpaeniformes species was the most, which was 17 (34.8%). 3 Results The number of Perciformes species was 14 (27.0%), Pleuronec- tiformes was five (22.3%), Gadiformes was two (15.4%), and 3.1 Species composition and spatial distribution Stomiiformes and Clupeiformes were each one (0.5%). The only Forty-one species (1 226 individuals) were obtained from one Chondrichthyes species belonged to Rajiformes (Table 1).

Table 1. Fish composition of the Bering Sea and Chukchi Sea Appearance Class Order Species Bering Sea Chukchi Sea Bering Strait Chondrichthyes Rajiformes Rajidae Bathyraja parmifera ○ Osteichthyes Stomiiformes Stomiidae Chauliodus macouni ○ Clupeiformes Clupeidae Clupea pallasii ○ Gadiformes Gadidae Arctogadus glacialis ○ Boreogadus saida ○ ○ ○ Perciformes Ammodytidae Ammodytes hexapterus ○ ○ Zoarcidae Gymnelus hemifasciatus ○ ○ Lycodes adolfi ○ Lycodes mucosus ○ ○ Lycodes palearis ○ Lycodes polaris ○ ○ Lycodes raridens ○ ○ ○ Lycodes Sagittarius ○ Lycodes seminudus ○ Stichaeidae Anisarchus medius ○ ○ Eumesogrammus praecisus ○ ○ Leptoclinus maculatus ○ Lumpenus fabricii ○ ○ ○ Stichaeus punctatus ○ Scorpaeniformes Agonidae Ulcina olrikii ○ ○ ○ Cottidae Artediellus atlanticus ○ Artediellus scaber ○ Enophrys diceraus ○ ○ Gymnocanthus tricuspis ○ ○ ○ Hemilepidotus papilio ○ ○ Icelus spatula ○ ○ Myoxocephalus scorpius ○ ○ ○ Triglops pingeli ○ Cyclopteridae Eumicrotremus orbis ○ ○ Hemitripteridae Nautichthys pribilovius ○ Liparidae Careproctus reinhardti ○ ○ Liparis fabricii ○ ○ ○ Liparis gibbus ○ Liparis ochotensis ○ Liparis tunicata ○ ○ Psychrolutidae Cottunculus microps ○ Pleuronectiformes Pleuronectidae Hippoglossoides robustus ○ ○ ○ Lepidopsetta polyxystra ○ ○ Limanda aspera ○ ○ Pleuronectes quadrituberculatus ○ Reinhardtius hippoglossoides ○ Notes: ○ means occurrence. 66 LIN Longshan et al. Acta Oceanol. Sin., 2014, Vol. 33, No. 6, P. 63–73

SR12 was the station that had the most species: 12 species. 3.3 Ecological type and ecosystem characteristics Station BS08 had 11 species; NB08, NB09–NB10, and BS05 had 10 species each. Only one species was obtained from each B07 3.3.1 Adaptability to temperature and habitat type and BB05. Thirty-one species were found in the Bering Sea and Coldwater species and cold temperate species were domi- 24 fish species were identified in the Chukchi Sea. Fourteen nant in the investigation areas. The number of coldwater spe- species were found in both seas: Boreogadus saida, Gymnelus cies was 35 (85.4%), which was the most of all species. Among hemifasciatus, Lycodes polaris, Lycodes raridens, Anisarchus them, there were 31 subcold zone species and four cold zone medius, Lumpenus fabricii, Ulcina olrikii, Enophrys diceraus, species. There were six temperate water species (14.6%), which Gymnocanthus tricuspid, Myoxocephalus scorpius, Careproctus were all warm temperate species. The results showed that these reinhardti, Liparis fabricii, Hippoglossoides robustus, and Li- two sea waters were typically cold zone and cold temperate manda aspera. zone. According to the habitat type, there were 35 species of demersal fish (85.4%), which was the most. Among them, 29 3.2 Dominant species and spatial distribution were shallow water fish of continental shelf and six were ocean The dominant species were determined by the ratio of the deepwater. There were five species of near demersal fish, of number of certain species/total individuals and occurrence which three were near shallow water fish of continental shelf, rate at different stations. B. saida was identified at 23 stations two were near ocean deepwater fish, and one was a pelagic fish. (63.9%), H. robustus 20 stations (55.6%), G. tricuspis 15 stations Clupea pallasii, B. saida, Ammodytes hexapterus, H. robustus, (41.7%), L. fabricii 15 stations (41.7%), U. olrikii 13 stations and Reinhardtius hippoglossoides were migratory fish. C. pal- (36.1%), and L. aspera and Pleuronectes quadrituberculatus lasii, Arctogadus glacialis, B. saida, A. hexapterus, L. aspera, P. each at 10 stations (27.8%). The occurrence rate of the other quadrituberculatus, and R. hippoglossoides were economic spe- species was less than 25%. cies (Appendix I). H. robustus, B. saida, M. scorpius, L. fabricii, and Artediellus scaber were dominant, comprising 15.6%, 14.6%, 11.7%, 8.2%, 3.3.2 Ecosystem characteristics and 5.2% of the total, respectively. In the Bering Sea, H. robustus, The common fish species were obtained by comparison of M. scorpius, B. saida, Lycodes palearis, L. fabricii, and L. aspera the species in the Bering Sea, Chukchi Sea, Yellow Sea, Bohai were dominant, while M. scorpius, B. saida, A. scaber, Lycodes Sea, North Atlantic Ocean–Eastern Greenland waters, and mar- seminude, and G. tricuspis were dominant species in the Chuk- ginal sea of the Northwest Pacific Ocean (Fig. 2). The results chi Sea (Table 2). showed that 37 fish species were only found in the Chukchi Sea, The dominant species in different areas were significantly and 33 fish species were only found in the Bering Sea. The com- different. Boreogadus saida was the most dominant species in mon species in the Yellow Sea and Bohai Sea were C. pallasii, A. the whole investigation region. The dominant species in the hexapterus, L. aspera, and Chauliodus macouni. The number of Bering Sea were H. robustus and L. fabricii, in the Bering Strait common species in other waters decreased with the latitudinal were H. robustus and M. scorpius, while M. scorpius and A. scab- distances, while the number of common species in North Atlan- er were the dominant species in the Chukchi Sea. tic Ocean–Eastern Greenland waters was 26. The results showed

Table 2. Dominant species of the Bering Sea and Chukchi Sea Area Dominant species Individual rate/% (>5%) Occurrence rate/% All stations Hippoglossoides robustus 15.6 55.6 Boreogadus saida 14.6 63.9 Myoxocephalus scorpius 11.7 22.2 Lumpenus fabricii 8.2 16.7 Artediellus scaber 5.2 8.3 Bering Sea Hippoglossoides robustus 25.5 76.2 Lumpenus fabricii 13.5 23.8 Boreogadus saida 11.5 47.6 Lycodes palearis 7.3 19.1 Limanda aspera 7.0 42.9 Liparis fabricii 6.0 57.1 Chukchi Sea Myoxocephalus scorpius 23.5 26.7 Boreogadus saida 18.7 86.7 Artediellus scaber 12.2 26.7 Lycodes seminudus 10.5 13.3 Gymnocanthus tricuspis 7.3 53.3 Bering Strait Hippoglossoides robustus 20.6 66.7 Myoxocephalus scorpius 19.1 66.7 Gymnocanthus tricuspis 17.6 66.7 Ulcina olrikii 10.3 66.7 Lycodes mucosus 5.9 33.3 LIN Longshan et al. Acta Oceanol. Sin., 2014, Vol. 33, No. 6, P. 63–73 67

40 37 that similarity of cold temperate-cold ecosystem between the 35 33 North Pacific–North Arctic and North Atlantic–North Arctic was higher than other comparisons.

r 30 26 25 21 3.4 Diversity characteristics 20 16 The Shannon–Wiener diversity index of different stations ac- 15 12 cording to the individual composition was 1.21, with a range of Species numbe 10 0–2.18. Margalef’s species richness index was 1.48, with a range 5 4 of 0–3.11, and Pielou’s evenness index was 0.76, with a range of 0 0–1.00. The Shannon–Wiener diversity index and species rich- BYSJES JS OS BS CS NAG ness index of the Bering Sea were higher than those of Chukchi Sea area Sea, and the Bering Sea showed greater fluctuation. The evenness index of the Chukchi Sea was higher than the Bering Sea Fig.2. Comparison of common fish numbers in differ- (Table 3). The diversity and richness index showed a trend of ent seas. BYS represents Bohai Sea and Yellow Sea, JES high in the south and low in the north, and the distribution was Sea of East Japan, JS Sea of Japan, OS Sea of Okhotsk, positively correlated (R2 = 0.889, P < 0.01, n = 36). BS Bering Sea, CS Chukchi Sea, and NAG North Atlantic Comparison of the Shannon–Wiener diversity index, species Ocean and Greenland water. richness index, and evenness index of different stations (Fig. 3)

Table 3. Diversity index of the Bering Sea and Chukchi Sea Shannon–Wiener (H′) Margalef’s (D) Pielou’s (J′) Area Range Average Range Average Range Average All stations 0–2.18 1.21 0–3.11 1.48 0–1.00 0.76 Bering Sea 0–2.18 1.32 0–3.11 1.65 0–1.00 0.74 Chukchi Sea 0.16–1.87 1.07 0.30–1.92 1.25 0.23–1.00 0.78

M06 M06 M06 M07 M07 M07 SR12 SR12 SR12 SR11 SR11 SR11 SR10 SR10 SR10 SR09 SR09 SR09 Co-10 Co-10 Co-10 Co-01 Co-01 Co-01 R08 R08 R08 C05 C05 C05 SR07 SR07 SR07 R06 R06 R06 C02 C02 C02 CC8 CC8 CC8 SR03 SR03 SR03 BS02 BS02 BS02 Statio n

BS05 Statio n BS05 Statio n BS05 BS08 BS08 BS08 BB06 BB06 BB06 NB09–NB10B NB09–NB10B NB09–NB10B NB09–NB10 NB09–NB10 NB09–NB10 NB08B NB08B NB08B NB08 NB08 NB08 SL09 SL09 SL09 SL08 SL08 SL08 SL07 SL07 SL07 SL06 SL06 SL06 SL05 SL05 SL05 SL04 SL04 SL04 SL03 SL03 SL03 SL02 SL02 SL02 SL01 SL01 SL01 BB05 BB05 BB05 BB02 BB02 BB02 B14 B14 B14 B07 B07 B07 0 0.5 1.0 1.5 2.0 2.5 3.0 0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 0 0.2 0.4 0.6 0.8 1.0 H' D J′

Fig.3. Comparison of the diversity index for each station. 68 LIN Longshan et al. Acta Oceanol. Sin., 2014, Vol. 33, No. 6, P. 63–73

showed that the diversity index and species index of BS08, BS05, only be found in Keelung coastal waters of Taiwan (Froese and NB09–NB10, and R08 were higher, all of which were located in Pauly, 2012). The results of the present study showed that the the continental shelf. BS08 and BS05 were located in the Bering North Atlantic Ocean to Eastern Greenland waters and Bering Strait, which was the only channel of the Bering Sea and Chuk- Sea to Chukchi Sea had the most common species compared chi Sea. Only one species was found in each B07 and BB05. with the Sea of Okhotsk and Sea of Japan. The common species with Sea of Okhotsk were 21, and with Sea of Japan were 12. The 4 Discussion result showed that the species composition of the survey area was similar with the North Atlantic Ocean to Eastern Greenland 4.1 Species composition, faunal characteristics, and diversity waters. The break of the Bering Sea basin may be the major reason for the distribution pattern. The demersal fish can just live 4.1.1 Species composition in the east and north shelf of the Bering Sea, while the Chukchi Species composition was formed by the relationship of dif- Sea is connected with the North Atlantic waters by a wide sea- ferent fish populations and environmental factors, of which bed of the Arctic Ocean. In the present study, all stations were temperature, salinity, and water system were the most influen- located in the continental shelf except B07, which was located tial factors (Liu and Ning, 2011; Song et al., 2012). In the present in the Bering Sea basin. study, the investigation area was located in the Arctic and Sub- arctic region. The Bering Sea is connected with the Pacific Ocean 4.1.3 Diversity characteristics and the surface temperature in summer is under 8°C (Gao et al., The Shannon–Wiener diversity index and species richness 2003). The core space temperature of the north shelf in summer index of the Bering Sea were higher than that of the Chukchi is −1.61°C on average (Wang and Zhao, 2011). The Chukchi Sea Sea, and showed a trend of high in the south while low in the is connected with the Bering Sea by the Bering Strait and the north. The results were in accordance with Wang et al. (2012) hydrological characteristics are affected by the Pacific Ocean. and Chen et al. (2007). In the present study, these two indices The North Chukchi Sea is affected by low-temperature water of were lower than San Juan Island (Fleischer, 2007), East Gulf the Arctic ice, and is connected with the North Atlantic Ocean of Alaska (Johnson et al., 2003), and the Yellow Sea (Liu et al., by the Fram Strait and channels of the Canadian Archipelago 2006), but higher than the northeastern waters of Japan (Toshi- (Steele et al., 2004). Therefore, composition of the Bering Sea hiko et al., 1993). The Shannon–Wiener diversity index (1.60) of and Chukchi Sea combine the characteristics of the North Pa- the Bering Strait was lower than Taiwan Strait (2.47), which was cific fauna, North Arctic fauna, and North Atlantic fauna, and the same type of strait (Song et al., 2012). Therefore, the results showed unique faunal composition. indicated a low level of diversity for the survey area. The dominant species in the present study belonged to two The geographical position was not the only factor that af- orders, Scorpaeniformes and Perciformes, and nine families of fected fish diversity: overfishing might play an important role these two orders were obtained. The number of Cottidae and in the diversity index (Lin, Miao et al., 2009; Liu and Ning, 2011; Zoarcidae species were eight each, then Stichaeidae, Liparidae, Song et al., 2012). For example, the diversity index and catch per and Pleuronectidae species were five each. The study showed unit effort (CPUE) decreased with the inappropriate develop- similar results with the long-term investigation results from ment of fishery resources. Superior economic fishes were re- Russia and USA (Mecklenburg et al., 2007). The coldwater fishes placed by low quality species. The three Gadidae fish were also were dominant in the survey area and grew in number with the in the state of overfishing and resource decline (Saitoh et al., increase in latitude. Based on the ecological type, the dominant 2008). Recently, changes in the environment and climate have species in the survey area were continental shelf demersal fish. become the most important factors for the resource situation. One reason was most of the stations used bottom trawls, but it As one of the sea areas with maximum catches (Mueter and Lit- did not affect the reliability of results. Most were not migratory zow, 2008), the shelf of the East Bering Sea was rich in Theragra fish. However, migratory species mostly were economic fish, chalcogramma and Gadus macrocephalus resources. The open such as C. pallasii, B. saida, Ammodytes hexapterus, L. aspera, P. water of the Bering Sea was one of the ocean fisheries in China quadrituberculatus, R. hippoglossoides, and so on. The propor- (Song and Chen, 1998). The National Marine Fisheries Service tion of the catch that were B. saida, L. aspera, and P. quadritu- (NMFS) began to investigate and make a total allowable catch berculatus was higher, and economic species were 21.6% of the (TAC) plan for the East Bering Sea from the 1960s. The North total catch. Pacific Fishery Management Council (NPFMC) also began to do fishery investigations annually for the Chukchi Sea and Beau- 4.1.2 Faunal characteristics fort Sea since 2008. There were only four common species in the survey area of the Yellow Sea and Bohai Sea: 9.76% of the total fish species. The 4.2 Changes of fish distribution and responses to changes in result was in accordance with Liu and Ning (8.1%) (2011). All the ecological environment four fish species were coldwater species, and C. pallasii (Liu, In the present study, some fish species were obtained from 2008), A. hexapterus (Froese and Pauly, 2012), and L. aspera (Fro- the undistributed seawater according to former documents and ese and Pauly, 2012) were important economic fish in the North materials. C. reinhardti and L. fabricii (Wilson, 2012) were spe- Pacific Ocean. The survey area was the Sea of Okhotsk to Bering cies distributed in the North Atlantic to North Arctic, while one Sea, which originates from cold seawater of the North Pacific C. reinhardti individual was caught from B14 and 42 L. fabricii (Liu and Ning, 2011; Liu, 2008). Three of these species also could individuals were caught from 12 stations, such as B14. The dis- be found in the Yellow Sea because the center-deep water of the tribution range of these two species greatly deviated from their Yellow Sea was controlled by the Yellow Sea Cold Water Mass. C. original region. B. parmifera (IUCN, 2011; Mecklenburg et al., macouni is an oceanic bathydemersal fish, and in China it can 2002) was distributed in the North Pacific Ocean, but was ob- LIN Longshan et al. Acta Oceanol. Sin., 2014, Vol. 33, No. 6, P. 63–73 69

tained from the Bering Sea shelf near the St. Lawrence Islands Arctic species was 2–4 times lower than that of low latitude wa- and eggs were found at M06 and M07 of the Chukchi Sea shelf. ters and fishes were more sensitive to climate changes (Cheung The main distribution region of R. hippoglossoides is the east- et al., 2009). Sustained global warming will have an irreversible ern Bering Sea shelf and St. Lawrence Gulf (Rand and Loger- effect on the biodiversity and fishery resources. The result of well, 2011; Allen et al., 1988), but it was caught only at M07 of this study could not statistically calculate the migratory level the Chukchi Sea. The results indicated that some native species of fish habitat due to the limited investigation data and limited may start to enlarge their habitat range due to changes in the sampling methods. In conclusion, the monitoring of marine environment and climate. In addition, catch locations of C. ma- organisms and resources in Arctic and Subarctic seawaters will couni, L. ochotensis, and L. polyxystra, which belonged to North be helpful for understanding the influencing mechanism and Pacific fauna, and L. raridens and H. robustus, which belonged integrated management. to the North Pacific–North Atlantic fauna were close to the northernmost distribution area (Appendix II). Acknowledgements The previous research showed that 15 fish species, such as We thank all the teammates and crew of R/V Xuelong for col- Gadus morhua and Solea solea, had dispersed in the latitudinal lecting the samples during the fourth Arctic scientific investiga- direction about 48–403 km in the Subarctic region and North tion. Sea, and 13 went northward (Perry et al., 2005). However, Dulvy et al. (2008) found that many economic species, such as Lepi- References dorhombus whifftagonis, were moving to deeper seawaters by 5.5 m per year, and appeared to disperse along depth. Studies Allen M J, Smith G B. 1988. Atlas and zoogeography of common fishes on the nektons of the shelf in Bering Sea showed that H. robus- in the Bering Sea and Northeastern Pacific. NOAA Technical Re- tus and R. hippoglossoides moved significantly northward by port NMFS, 66: 115–116 Allison L P, Low P J, Ellis J R, et al. 2005. Climate change and distribution about 76 m and 98 m, respectively, during 1983–2006. These two shifts in marine fishes. Science, 308(5730): 1912–1915 species were also found in our study. The larger dispersal spe- Arctic Writing Group. 2011. Arctic Problem Research (in Chinese). Bei- cies was Bathymaster signatus, and its dispersal distance was jing: China Ocean Press 237 km (Mueter and Litzow, 2008). In addition, six species, in- Barber W E, Smith R L, Vallarino M, et al. 1997. Demersal fish assem- cluding Chionoecetes opilio and R. hippoglossoides, are impor- blages of the northeastern Chukchi Sea, Alaska. 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Appendix I. Temperature adaptability, habitat type, economic value, migration, and distribution of each fish

Ecological characteristics Species Temperature Habitat type Economic value Migration Distribution adaptability Rajidae Bathyraja parmifera SCW CSD 0 0 BS, OS, JS, JES Stomiidae Chauliodus macouni CT OBP 0 0 BS, OS, JS, BYS, JES Clupeidae Clupea pallasi CT CSP 1 1 BS, CS, OS, JS, BYS, JES Gadidae Arctogadus glacialis CW OBP 1 0 CS, NAG Boreogadus saida SCW CSD 1 1 BS, CS, NAG Ammodytidae Ammodytes hexapterus CT CSB 1 1 BS, CS, OS, JS, BYS, NAG, JES Zoarcidae Gymnelus hemifasciatus SCW CSD OBD 0 0 BS, CS Lycodes adolfi SCW CSD 0 0 CS, NAG Lycodes mucosus CW CSD 0 0 BS, CS, OS, NAG Lycodes palearis SCW CSD 0 0 BS, CS, OS, JS Lycodes polaris SCW CSD 0 0 BS, CS, NAG Lycodes raridens SCW OBD 0 0 BS, CS, OS Lycodes Sagittarius CW OBD 0 0 CS, NAG Lycodes seminudus CW 0 0 CS, NAG Stichaeidae Anisarchus medius SCW CSD 0 0 BS, CS, NAG, JES Eumesogrammus praecisus SCW CSB 0 0 BS, CS, NAG Leptoclinus maculatus SCW CSD 0 0 BS, CS, OS, NAG Lumpenus fabricii SCW CSD 0 0 BS, CS, NAG Stichaeus punctatus SCW CSD 0 0 BS, CS, NAG Agonidae Ulcina olrikii SCW CSD 0 0 BS, CS, NAG Cottidae Artediellus atlanticus SCW CSD 0 0 CS, NAG Artediellus scaber SCW CSD 0 0 BS, CS, NAG Enophrys diceraus SCW CSD 0 0 BS, CS, OS, JS, JES Gymnocanthus tricuspis SCW CSD 0 0 BS, CS, NAG Hemilepidotus papilio SCW CSD 0 0 BS, CS, OS, JES Icelus spatula SCW CSD 0 0 BS, CS, OS, NAG Myoxocephalus scorpius SCW CSD 0 0 BS, CS, OS, NAG Triglops pingeli SCW CSD 0 0 BS, CS, OS, NAG, JES Cyclopteridae Eumicrotremus orbis SCW CSD 0 0 BS, CS, OS, JES Hemitripteridae Nautichthys pribilovius SCW CSD 0 0 BS, CS, OS, JS, JES Liparidae Careproctus reinhardti SCW OBD 0 0 CS, NAG Liparis fabricii SCW OBD 0 0 CS, NAG Liparis gibbus SCW CSD 0 0 BS, CS, NAG Liparis ochotensis CT CSD 0 0 BS, OS, JS, JES Liparis tunicata SCW CSD 0 0 BS, CS, NAG Psychrolutidae Cottunculus microps CT OBD 0 0 CS, NAG Pleuronectidae Hippoglossoides robustus SCW CSD 0 1 BS, CS, OS, JS, JES Lepidopsetta polyxystra SCW CSD 0 0 BS, OS, JES Limanda aspera CT CSD 1 0 BS, CS, OS, JS, BYS, JES Pleuronectes quadrituberculatus SCW CSD 1 0 BS, CS, OS, JS, JES Reinhardtius hippoglossoides SCW CSB 1 1 BS, CS, OS, JS, NAG, JES Notes: Temperature adaptability: cold temperate (CT), subcold zone (SCW), cold zone (CW); habitat type: continental shelf demersal (CSD), oceanic bathydemersal (OBD), continental shelf benthopelagic (CSB), oceanic benthopelagic (OBP), continental shelf pelagic- neritic (CSP); economic value, migration: yes (1), no (0); and distribution: Bering Sea (BS), Chukchi Sea (CS), Sea of Okhotsk (OS), Sea of Japan (JS), Sea of East Japan (JES), Bohai Sea and Yellow Sea (BYS), North Atlantic Ocean and Greenland water (NAG). LIN Longshan et al. Acta Oceanol. Sin., 2014, Vol. 33, No. 6, P. 63–73 73

Appendix II. Species that respond to ecological environment changes and their distributional changes Species Distribution range Occurrence in survey Distribution in survey

Rajidae North Pacific: Sea of Okhotsk to SL01, SL02, SL03 adults close to the northernmost Bathyraja parmifera Alaska Bay (M6, M7) distribution range, eggs beyond distribution range Stomiidae widely distributed in North B07 North Pacific fauna species, close to Chauliodus macouni Pacific temperate areas the northernmost distribution range Zoarcidae Sea of Okhotsk, Bering Sea, and BB06, BS05, NB09–NB10, close to the northernmost Lycodes raridens Northwest Arctic NB09–NB10B, SR09 distribution range Liparidae North Pacific: Sea of Japan to NB08 North Pacific fauna species, close to Liparis ochotensis Bering Sea the northernmost distribution range Pleuronectidae North Pacific: Sea of Japan to B14, BB02, BB06, BS05, BS08, North Pacific to Northwest Hippoglossoides robustus Bering Sea, Northwest Arctic NB08, NB08B, NB09–NB10, R06, Arctic fauna species, close to the R08, SL01–SL06, SL09, SR03, SR09 northernmost distribution range Pleuronectidae North Pacific: Sea of Okhotsk to BS02, BS05, SL06 North Pacific fauna species, close to Lepidopsetta polyxystra Alaska Bay the northernmost distribution range Pleuronectidae Subpolar region: North Atlantic M07 mainly distributed in Bering Sea, Reinhardtius and North Pacific only discovered in shelf of Chukchi hippoglossoides Sea in this survey Liparidae North Atlantic and North Arctic B14, BB06, BS05, BS08, M06, Arctic and Atlantic fauna species, Liparis fabricii NB08, NB08B, NB09–NB10, discovered in 12 stations in Bering NB09–NB10B, SL01, SL02, SL04, Sea SL05, SR11, SR12 Liparidae North Atlantic and North Arctic B14, M07, SR11 Arctic and Atlantic fauna species, Careproctus reinhardti discovered at Sta. B14 Notes: Stations in parentheses are where eggs occurred.