Keywords

1 Sea of Japan

The Sea of Japan (also called the Japan Sea) is surrounded by the eastern margin of the Eurasian Continent and the Japanese Archipelago and is connected to the adjacent water bodies (East China–Yellow seas, Pacific Ocean, and Sea of Okhotsk) through shallow narrow straits (Fig. 6.1). The water mass structure of the Sea of Japan is characterized by surface water influenced by the Tsushima Warm Current and the Liman Cold Current, and a deep layer (Japan Sea Proper Water) occurring in depths of approximately 200–300 m and deeper. The Tsushima Warm Current, a combination of a branch of the Kuroshio Current and the Taiwan Current, enters the sea through the Tsushima Strait (situated to the southwest) and flows northward along the Japanese Archipelago and the east coast of the Korean Peninsula. On the other hand, the much weaker Liman Cold Current, fed by the Amur River, flows southward along the Eurasian Continent through the Tatar (Mamiya) Strait. The Japan Sea Proper Water is generated by the subsidence of surface water in winter, spreading evenly through the deep water layers without mixing with adjacent water bodies, due to the shallowness of the connecting straits (Kawamura 1998; Gamo et al. 2014).

Fig. 6.1
figure 1

Map of the Sea of Japan with flatfish species composition by family in the entire sea and each of nine areas (see text)

Because the Sea of Japan is a semi-enclosed water body, the physical environment has been influenced by a number of environmental changes (mostly associated with changing climatic conditions) that have occurred in the past. These have corresponded with changing biocoenosis, with repeated mass mortality and recovery of certain marine fauna over the last 85,000 years. Many marine (especially deep-sea) species became extinct 27,000–20,000 years BP due to closure and isolation of the sea due to declining seawater levels, and the stratification of water layers, including strongly anoxic conditions caused by fresh water inflow from the land. Subsequently, a full-scale recovery of the Sea of Japan marine communities leading to their present condition, began 20,000–10,000 years BP with the inflow of the Oyashio Current from the Pacific Ocean through the Tsugaru Strait. From ca. 10,000–8000 years BP, intermittent inflows of the Tsushima Warm Current began from the southwest, becoming continuous some 8000 years ago, resulting in the present day oceanophysical environment. Details on the physical features and geological history of the Sea of Japan are shown in such as Oba et al. (1991), Tada (1994), and Koizumi (2006).

In general, the species diversity of marine organisms inhabiting the Sea of Japan is considered to be much poorer than that in the adjacent seas (Naganuma 2000; Tyler 2002), due primarily to the short geological history (only 8000 years since formation) and physical structure of the former (e.g., small tidal range and lack of coral reefs). Saburo Nishimura (1930–2001), an eminent Japanese biologist, published many works on the marine biology and zoogeography of the Sea of Japan, the series of publications comprising his doctoral thesis (Nishimura 1965a, b, 1966, 1968, 1969) revealing distributional aspects of marine animals in the Sea of Japan, based on a prodigious amount of data and literature information. Subsequently, zoogeography of the Sea of Japan, particularly with regard to marine fishes, was further explored from an evolutionary perspective (Nishimura 1974). Many of his findings are still considered basic to and important for the zoogeography of the Sea of Japan marine fauna.

2 Fishes of the Sea of Japan

Marine fishes are important food resources for the countries bordering the Sea of Japan, leading to many studies on fish species diversity. The first comprehensive survey of fish species diversity in the Sea of Japan originated from the USS Albatross cruise in 1906 (Nishimura 1974; Dunn 1996), a species checklist published by Snyder (1912) also including the distribution of each species in Japanese waters. A few years earlier, Schmidt (1904) had published a species list for the Russian Far East, based on Russian museum specimens. In subsequent years, researchers in Japan, Korea, and the Russian Far East have played central roles in clarifying the fish fauna of the Sea of Japan (e.g., Tanaka 1931; Kim et al. 2005; Parin et al. 2014; Kawano et al. 2014). However, because most of those studies emphasized the fish fauna of specific areas, species lists covering the entire Sea of Japan have been limited to a series of studies by the Russian Ichthyologist G. U. Lindberg and his colleagues, “Fishes of the Sea of Japan and the Adjacent Areas of the Sea of Okhotsk and the Yellow Sea, Parts 1–7” (Lindberg and Legeza 1959, 1965; Lindberg and Krasyukova 1969, 1975, 1987; Lindberg and Fedorov 1993; Lindberg et al. 1997). Although species commonly found in the sea were listed, it became obvious that the lists were inadequate due to limited materials (old specimens in the Zoological Institute, Russian Academy of Sciences, St. Petersburg, plus literature records).

Fish species lists for Japanese waters overall in the Sea of Japan were compiled by Kato (1956), Yoshida and Ito (1957), Tsuda (1990), Nakabo (2013), and Kawano et al. (2014). Additionally, many other species lists compiled over the same period focused on specific regions, habitats or taxa: e.g., Maeda and Tsutsui (2003) (Hokkaido); Shiogaki et al. (2004) (Aomori); Honma (2013) (Niigata); Nambu (2013) (Toyama); Sakai et al. (1991) and Yamamoto et al. (1995) (Ishikawa); Takegawa and Morino (1970), Minami et al. (1977), and Uchino et al. (1982) (Kyoto); Watanabe and Ito (1958) and Suzuki et al. (2000) (Hyogo); Moriwaki et al. (2007) (Shimane); Kawano et al. (2011), Fujiwara et al. (2018), and Sonoyama et al. (2020) (Yamaguchi); Yogo et al. (1986) and Nishida et al. (2004, 2005) (Fukuoka); Takeuchi et al. (2015) (Tsushima Island); Shinohara et al. (2011, 2014) (deep-water species in the entire sea); Tashiro et al. (2015) [Pseudorhombus (Paralichthyidae) of the coast of Japan]; Matsui et al. (2014) (gobioid species in Wakasa Bay); Matsunuma et al. (2019) (carangid species in Wakasa Bay and adjacent waters). Many more local lists were included in Kawano et al. (2014). In Korean waters, for example, Jordan and Metz (1913), Mori (1952), Chyung (1977), Kim et al. (2005), Kim and Ryu (2016), and Kim et al. (2020) compiled comprehensive species lists, with several additional lists compiled for Jeju Island, off the southern Korean Peninsula (e.g., Kim et al. 2009; Kim and Nakaya 2013; Kwun et al. 2017). Additionally, Ik-Soo Kim and his colleagues reviewed the taxonomy of several groups in Korean waters: e.g., Tetraodontoidei by Kim and Lee (1990); Blennioidei and Zoarcoidei by Kim and Kang (1991); Cottidae by Kim and Youn (1992); Cynoglossidae by Kim and Choi (1994); Pleuronectiformes by Kim and Youn (1994); and Percoidei by Kim et al. (2001). A considerable amount of additional information on Korean marine fishes was included in Kim et al. (2005) and Kim (2009). For Russian waters, an almost complete species list supported by a huge amount of literature information was published by Parin et al. (2014).

Clearly, despite a comprehensive list of fish species overall in the Sea of Japan having been limited to the studies of G. U. Lindberg and his colleagues, information on regional species diversity is vast. However, the compilation of a complete species list (with distributional ranges for each species) based on representative regional lists [Kawano et al. 2014 (Japanese), Kim et al. 2005 and Kim et al. 2020 (Korean), and Parin et al. 2014 (Russia)] is hampered by the existence of many unreliable records. Even now, some species identifications and distribution in the Sea of Japan are unclear.

3 Review of the Flatfish Fauna in the Sea of Japan

Flatfishes of the order Pleuronectiformes include many commercially important species for fishery activities in Japan, including several targeted for recreational angling. Significantly, these fishes comprise a principal catch component on the Japanese coast of the Sea of Japan (MAFF 2021). Accordingly, Japanese fisheries research institutions located along the Sea of Japan coast have actively engaged in various ecological (e.g., growth, population dynamics, and biomass) and aquacultural studies.

To date, a total of 88 valid flatfish species plus one species complex, representing eight families, have been recorded from the Sea of Japan (Table 6.1; Kawano et al. 2014; Parin et al. 2014; Kim et al. 2020; Sonoyama et al. 2020). However, records for many of these are not supported by vouchers, such as museum specimens. It is anticipated that flatfishes will be an important group for studying the evolution (including biogeography) of fishes inhabiting the Sea of Japan, since the former is one of the few groups distributed throughout the entire sea. Therefore, a clear understanding of flatfish species diversity may provide significant insight for our understanding of overall fish species diversity in the sea. Notwithstanding, our knowledge of flatfish species diversity—the most fundamental biological information—remains poor, with even the distribution of each species being poorly understood [see Nakabo 2013].

Table 6.1 Species list of flatfishes in the Sea of Japan

In this chapter, the flatfish fauna of the entire Sea of Japan is reviewed as a first step toward accurately understanding the process and drivers of species diversity of fishes in the Sea of Japan.

3.1 Species Checklist: What Species and Where?

A reconstructed species list based on museum specimens and photographic records is shown in Table 6.1 and Appendix. A total of 72 species plus one species-complex, all after metamorphosis, are recognized from the Sea of Japan, as follows: 27 species plus one species-complex in Pleuronectidae (37.5%), 16 species in Bothidae (22.2%), 10 species in Cynoglossidae (13.9%), eight species in Paralichthyidae (11.1%), six species in Soleidae (8.3%), three species in Samaridae (4.2%), and one species each in Citharidae and Poecilopsettidae (each 1.4%). At this time, no evidence has been found to support the occurrence of the following 17 species: Lepidoblepharon ophthalmolepis (Citharidae); Pseudorhombus dupliciocellatus (Paralichthyidae); Arnoglossus japonicus, Bothus myriaster, Bothus pantherinus, Engyprosopon macroptera, and Parabothus coarctatus (all Bothidae); Pleuronectes bilineatus, Limanda proboscidea, and Reinhardtius hippoglossoides (all Pleuronectidae); Samariscus latus (Samaridae); Aesopia cornuta, Liachirus melanospilus, and Soleichthys heterorhinos (all Soleidae); and Cynoglossus arel, Cynoglossus bilineatus, and Cynoglossus nigropinnatus (all Cynoglossidae) (Table 6.1). The Sea of Japan is divided into nine areas, together with the characteristics of each.

The “Tatar” area, located in the northernmost part of the sea, is connected to the Sea of Okhotsk, to the north via the Tatar Strait, and to the south via the Soya (La Pérouse) Strait (Fig. 6.1). A total of only 16 flatfish species are recognized (Table 6.1; Appendix), all being pleuronectids. On the other hand, no reliable records exist for the following species, all included in this area by Parin et al. (2014): Atheresthes evermanni, Eopsetta grigorjewi, Hippoglossus stenolepis, Limanda aspera, Microstomus achne, Platichthys bicoloratus, Reinhardtius hippoglossoides, Verasper moseri, and Verasper variegatus (all Pleuronectidae).

The “Hokkaido” area, located in the northeastern part of the sea, is connected to the Sea of Okhotsk in the north via the Soya Strait and to the Pacific Ocean in the south via the Tsugaru Strait (Fig. 6.1). A total of 19 species in three families are recognized (Table 6.1; Appendix), 17 in Pleuronectidae (90%), and one each in Paralichthyidae and Cynoglossidae (each 5%). Despite being included in Kawano et al. (2014), records for the following species could not be confirmed: Pseudorhombus pentophthalmus and Tarphops oligolepis (Paralichthyidae); Atheresthes evermanni, Dexistes rikuzenius, Glyptocephalus kitaharae, Lepidopsetta billineata, Liopsetta pinnifasciata, Pleuronectes quadrituberculatus, Pseudopleuronectes obscurus, Reinhardtius hippoglossoides, Verasper moseri, and Verasper variegatus (all Pleuronectidae); and Pseudaesopis japonica (Soleidae).

The “Tohoku-Hokuriku” area, the eastern to southern part of the sea, is connected to the Pacific Ocean in the north via the Tsugaru Strait (Fig. 6.1). A total of 37 species in six families (about half of all species) are recognized herein (Table 6.1; Appendix): 18 species in Pleuronectidae (48.6%), five species each in Cynoglossidae and Paralichthyidae (each 13.5%), four species each in Bothidae and Soleidae (each 10.8%), and one species in Poecilopsettidae (2.7%). Records of the following species, included in Kawano et al. (2014), could not be confirmed: Lepidoblepharon ophthalmolepis (Citharidae); Tarphops elegans (Paralichthyidae); Arnoglossus tenuis, Crossorhombus kobensis, Engyprosopon grandisquama, and Psettina tosana (all Bothidae); Atheresthes evermanni, Hippoglossoides elassodon species complex, Hippoglossus stenolepis, Lepidopsetta billineata, Liopsetta pinnifasciata, Reinhardtius hippoglossoides, and Verasper moseri (all Pleuronectidae); Samariscus japonicus (Samaridae); Aesopia cornuta (Soleidae); and Cynoglossus robustus (Cynoglossidae).

The “Kinki-San’in” area, located in the south to southwestern part of the sea, is connected to the Seto Inland Sea in the west via the Kanmon Strait (Fig. 6.1). A total of 55 species in six families (about three-fourths of all species) are recognized herein (Table 6.1; Appendix): 19 species in Pleuronectidae (34.5%), 11 species in Bothidae (20.0%), eight species each in Cynoglossidae and Paralichthyidae (each 14.5%), four species in Soleidae (7.3%), three species in Samaridae (5.5%), and one species each in Citharidae and Poecilopsettidae (each 1.8%). Records of the following species included in Kawano et al. (2014) could not be confirmed: Lepidoblepharon ophthalmolepis (Citharidae); Pseudorhombus dupliciocellatus (Paralichthyidae); Arnoglossus japonicus, Bothus pantherinus, Bothus myriaster, Engyprosopon macroptera, and Parabothus coarctatus (all Bothidae); Lepidopsetta bilineata, Pseudopleuronectes schrenki, and Reinhardtius hippoglossoides (all Pleuronectidae); Samariscus latus (Samaridae); Aesopia cornuta, Aseraggodes kaianus, Liachirus melanospilus, and Soleichthys heterorhinos (all Soleidae); and Cynoglossus arel, Cynoglossus bilineatus, and Cynoglossus nigropinnatus (all Cynoglossidae).

The “Kyushu” area, located in the southernmost part of the sea, is connected to the Seto Inland Sea in the east via the Kanmon Strait (Fig. 6.1). Because specimens examined by the author and voucher specimens supporting published lists were much fewer than for the other Japanese areas, the present species list for this area includes many presumptive species (Table 6.1). A total of 47 species (including 23 presumptive) in eight families are included, as follows: 13 species in Pleuronectidae (27.7%), 10 species in Bothidae (21.3%), eight species in Paralichthyidae (17.0%), seven species in Cynoglossidae (14.9%), four species in Soleidae (8.5%), three species in Samaridae (6.4%), and one species each in Citharidae and Poecilopsettidae (each 2.1%) (Table 6.1; Appendix). Despite being listed by Kawano et al. (2014) and Takeuchi et al. (2015), records of the following species could not be confirmed: Arnoglossus japonicus (Bothidae), Aesopia cornuta and Aseraggodes kaianus (Soleidae), and Cynoglossus arel (Cynoglossidae).

The “Southern Korea” area, forming the southernmost part of the sea together with the Kyushu area, is connected to both the East China and Yellow seas (Fig. 6.1). Based on published lists supported by voucher specimens (e.g., Lindberg and Fedorov 1993; Kim and Youn 1994; Kim and Ryu 2016), a total of 43 species in eight families are recognized herein (Table 6.1; Appendix): 16 species in Pleuronectidae (37.2%), eight species in Bothidae (18.6%), six species in Cynoglossidae and (14.0%), five species in Soleidae (11.6%), four species in Paralichthyidae (9.3%), two species in Samaridae (4.7%), and one species each in Citharidae and Poecilopsettidae (each 2.3%). Records could not be confirmed for the following species: Pseudorhombus oculocirris and Tarphops elegans (Paralichthyidae); Arnoglossus japonicus, Bothus myriaster, Crossorhombus kobensis, and Psettina iijimae (all Bothidae); Lepidopsetta mochigarei, Pseudopleuronectes obscurus, and Verasper moseri (all Pleuronectidae); Aesopia cornuta and Heteromycteris japonica (Soleidae); and Cynoglossus gracilis (Cynoglossidae).

The “Eastern Korea” area is defined herein as the east coast of the Korean Peninsula, north of Pohang (Fig. 6.1). On the basis of literature covering the Southern Korea area, a total of 24 species (including two presumptive) in eight families are recognized (Table 6.1; Appendix): 19 species in Pleuronectidae (79.2%), two species each in Cynoglossidae and Paralichthyidae (8.3%), and one species in Soleidae (4.2%). A fauna of flatfishes in this area is characterized by mostly pleuronectids with a small number of other families. Records could not be confirmed for the following species: Bothus myriaster (Bothidae); Lepidopsetta billineata, Liopsetta pinnifasciata, and Verasper moseri (all Pleuronectidae); and Aseraggodes kobensis (Soleidae).

The “Primorsky Krai” area, in the northwestern part of the sea (Fig. 6.1), is characterized by a relatively low flatfish diversity, comprising only 15 species (all in Pleuronectidae) (Table 6.1; Appendix). Despite being included in the comprehensive list given by Parin et al. (2014), records could not be confirmed for the following species: Paralichthys olivaceus (Paralichthyidae); Eopsetta grigorjewi, Hippoglossus stenolepis, Microstomus achne, Platichthys bicoloratus, Pleuronectes quadrituberculatus, Pleuronichthys spp., Pseudopleuronectes yokohamae (all Pleuronectidae); and Cynoglossus itinus and Symphurus orientalis (Cynoglossidae).

The “Yamato Bank” area, located in the central Sea of Japan, is an underwater mountain range (236 m depth at its shallowest) comprising the Yamato Bank and seamounts scattered in deep water off the southern Yamato Bank (Fig. 6.1). Only three pleuronectid species, also listed in Shinohara et al. (2011) on the basis of museum specimens, are recognized herein (Table 6.1; Appendix).

3.2 Faunal Characteristics

It is well established that the community structures of shallow-water fishes in the Sea of Japan change drastically between southern Hokkaido and northern Tohoku, and off the east coast of the Korean Peninsula (e.g., Nishimura 1965a; Kafanov et al. 2000), due to the influence of environmental factors, such as the path of the Tsushima Warm Current flowing from the south, the path of the North Korean Cold Current flowing along the continental coast, and different climatic conditions. Additionally, these and other environmental factors have also resulted in a wide transition zone of warm- and cold-water fishes, especially along the coast of Honshu Island, Japan. There are various theories about a zoozeographic boundary for fishes in the Sea of Japan [see Nishimura 1965a; Kafanov et al. 2000].

Similar patterns can be seen in the species diversity of flatfishes. Warm-water species (e.g., Bothidae, Cynoglossidae, Paralichyidae, and a few species of Pleuronectidae) are dominant in the Kyushu, Kinki-San’in, Tohoku-Hokuriku, and Southern Korea areas, which are strongly influenced by the Tsushima Warm Current, whereas a less diverse fauna, comprising mostly cold-water species (Pleuronectidae), dominate the Eastern Korea, Primorsky Krai, and Tatar areas (all strongly influenced by cold water currents), and the Hokkaido area (Tsushima Warm Current flows along the coast but exposed to a cold climate). In addition, a gradual shift in fauna from warm- to cold-water species, and vice versa, has been observed in the waters between the Kinki-San’in (20% and 80%, respectively) and Tohoku-Hokuriku (27% and 73%, respectively) areas (Fig. 6.1). A comparison of the fauna of these areas based on more fine-scaled data should result in clearer transition patterns being observed.

Although some pleuronectid species, such as Cleisthenes pinetorum, Clidoderma asperrimum, Glyptocephalus stelleri, and Pseudopleuronectes herzensteini, are distributed throughout the Sea of Japan (Table 6.1), most have a more or less limited distribution, toward to the north (warm-water species) or south (cold-water species). Interestingly, the distributional limits vary among species, even if closely related. For example, the abundant bothid Engyprosopon multisquama is widely distributed from Kyushu to Tohoku on the Japanese coast, whereas the congeners E. grandisquama and E. longipelvis are less common and have a northern limit not extending beyond the Noto Peninsula (Appendix). Such small but significant differences in distribution patterns may provide clues to understanding the evolution of fishes in the Sea of Japan.

The reconstructed flatfish faunal list resulting from this most recent assessment of species has a certain similarity to the lists proposed by previous studies, notwithstanding the unsupported records for 17 species (see above). The occurrence of such species in the Sea of Japan should remain questionable until confirmed by voucher specimens—which treatment should also apply to the distributional ranges for each of the recognized species.

3.3 Temporal Changes in Flatfish Community Structures in Wakasa Bay

Minami et al. (1977) conducted a benthic sledge survey from June 1971 to October 1972 to investigate the benthic fish community in the western part of Wakasa Bay (also called Tango Sea), located on the southern coast of the Sea of Japan (Kinki-San’in area) (Fig. 6.1). Recently, the author and colleagues conducted a similar survey (from April 2014 to March 2018) in approximately the same areas as those previously surveyed (off the mouth of the Yura River in depths of 5–60 m). A comparison of the overall results of the two survey programs found an increase in the number of flatfish species from 14 in 1971–1972 to 18 in 2014–2018 (Table 6.2). Among the new records, the paralichthyid Pseudorhombus oligodon was particularly notable, having been commonly collected during the later surveys. Additionally, significant fluctuations in abundance were also noted for the cynoglossid Cynoglossus joyneri (ca. 100 individuals in 1971–1972 vs. <5 in 2014–2018) and the soleid Aseraggodes kobensis (1 in 1971–1972 vs. >50 in 2014–2018).

Table 6.2 Flatfishes collected during benthic sledge surveys in western Wakasa Bay in 1971–1972 and 2014–2018

The paralichthyid Tarphops oligolepis is small-sized species mainly inhabiting sandy coastal shores. Because of its abundance, some fundamental biological studies on the species had been undertaken in the Tango Sea [e.g., Minami 1983 (early life history); Kamisaka et al. 1999 (reproductive biology)]. However, the species inexplicably disappeared from the sandy beach (<10 m depth) off the Yura River during 2013–2015 (Tashiro et al. 2017). Although a small number of individuals have been recorded from that area since summer 2016, the cause of this phenomenon is still unclear.

4 Conclusion

In recent years, there has been a shift in the community structure of fishes in the Sea of Japan, with an increase in numbers of southern species (warm-water species). Although a causal relationship with global warming has sometimes been suggested (Nishida et al. 2005; Kawano et al. 2014), dispersal linked to expanded distribution may be a natural consequence of evolving species, and most neritic fishes inhabiting adjacent seas can actively or passively enter the Sea of Japan without difficulty. In fact, many incidental cases of warm-water species in the Sea of Japan have been recorded over the years (e.g., Nishimura 1965a; Tashiro et al. 2017; Matsunuma et al. 2019). Because of the young age of the Sea of Japan, thereby resulting in “unexplored” waters, it is likely that some species have been trying to establish viable populations in the sea for a long time. Accordingly, there may be little meaning in discussing changes in community structure and species diversity related to global warming, based on simple comparisons of species numbers. However, the community structure of fishes in the Sea of Japan may have changed over the past few decades as a result of human activities, including not only direct causes such as overfishing and coastal development but also land-based activities. In order to maintain fish species diversity in the Sea of Japan and continue with associated applied research, the overall fish fauna needs to be identified and confirmed as soon as possible.

This review has adopted a relatively negative view of published fish species lists unsupported by voucher specimens, due to the necessity for scientific research to be “reproducible”. On the other hand, such studies have summarized a very large amount of information from a wide range of sources and have stimulated an interest in species diversity among many subsequent researchers, including myself.