Okamejei Kenojei

24 Abstract—The population structure Population structure of the ocellate spot skate of the ocellate spot skate (Okamejei kenojei), distributed in the western (Okamejei kenojei) inferred from variations in North Pacific, was assessed on the basis of genetic variations in the mitochondrial DNA (mtDNA) sequences and from mitochondrial DNA control region morphological characters of regional populations (mtCR) and differences in morphological characters and features. Sig- nificant genetic differentiation in Ryo Misawa (contact author)1 mtCR was observed among 6 region- Yoji Narimatsu2 al populations along the Japanese Hiromitsu Endo3 Archipelago and Korean Peninsula. 1 Unique haplotypes found in Osaka Yoshiaki Kai Bay and off the east coast of Kyushu Island suggested an absence of gene Email address for contact author: [email protected] flow from the other 5 regions. In addition, comparisons of morphological 1 Maizuru Fisheries Research Station characters and features, including Field Science Education and Research Center measurements, nuchal thorn counts, Kyoto University, Nagahama, Maizuru, differences in maturity size, and col- Kyoto 625-0086, Japan oration, indicated that populations 2 Tohoku National Fisheries Research Institute of ocellate spot skate from Osaka Fisheries Research and Education Agency Bay and from off the Pacific coast of 25-259 Same-machi, Hachinohe, northern Japan were clearly distin- Aomori 031-0841, Japan guishable from 4 other regional pop- 3 ulations. Together with molecular Laboratory of Marine Biology differentiation among the regional Faculty of Science and Technology populations, they suggest that the Kochi University, straits, ocean currents, and limited 2-5-1 Akebono-cho, migrations are significant barriers Kochi 780-8520, Japan to gene flow between populations. Future fisheries management of the species is discussed on the basis of the present findings. Many elasmobranch fishes (sharks, are being discussed on a global scale rays, and skates) are particularly (e.g., Dulvy et al., 2014; Davidson vulnerable to overfishing because of et al., 2016). Shallow-water elasmo- their large size, slow growth, late branchs particularly have a higher maturity, and low fecundity (Brand- risk of extinction or decrease in er, 1981; Dulvy et al., 2000; Griffiths population because of their constant et al., 2010; Griffiths et al., 2011). exposure to coastal fisheries (Dulvy These life-history traits translate et al., 2014). The ocellate spot (or into low rates of reproduction and spiny) skate Okamejei kenojei (fam- low potential rates of population in- ily Rajidae) is widely distributed 1) crease (Walker and Hislop, 1998). in shallow coastal waters of 20–230 Elasmobranch fishes are also target- m depth (mainly 30–100 m) in the ed by fisheries because their meat, western North Pacific: 2) from the fins, and liver oil are commercially coastal waters off southern Hokkai- Manuscript submitted 6 July 2018. valuable (Dulvy et al., 2014; David- do, Japan, southward to waters off Manuscript accepted 26 November 2018. son et al., 2016). In addition, elasmo- northern Taiwan, including 3) along Fish. Bull. 117:24–36 (2019). branch fishes are often caught as by- the Pacific coast of Japan; 4) within Online publication date: 4 December 2018. catch of fisheries that focus on more the Sea of Japan; 5) the East China doi: 10.7755/FB.117.1.4 commercially valuable teleost fish Sea; and 6) the Yellow Sea (Ishihara, species, such as tunas and demersal 1987; Hatooka et al., 2013; Last et The views and opinions expressed or implied in this article are those of the fishes (Dulvy et al., 2014). The fish- al., 2016). The age at maturity of author (or authors) and do not necessarily ing pressure on elasmobranchs is in- the species has been estimated to reflect the position of the National creasing and therefore their extinc- be about 3 years, and females pro- Marine Fisheries Service, NOAA. tion risk and conservation interest duce at least 300 egg capsules during Misawa et al.: Population structure of Okamejei kenojei 25 previously recognized as R. fusca, i.e., as the “northern form.” Ishihara (1987) suggested that the “northern form” differed from forms in other areas in having a bluntly angled and extremely translucent snout, numerous nuchal thorns, and black spots or reticulated patterns scattered over the entire dorsal surface of the disc. Such morphological divergence among local populations has suggested the existence of a complex population structure within the species. Okamejei kenojei has considerable economic value in Korea and Japan (Ishihara, 1990; Ishihara et al., 2009; Baeck et al., 2011). Domingues et al (2018) suggested that management and conservation policies for shark and ray fisheries should include information on genetic diversity. However, despite the potential population structur- ing and high economic value of O. kenojei, there have been no studies of genetic structure at the population level for this species—information that is crucial for fish- Figure 1 eries management and conservation prac- Sampling area and number of examined specimens of Okamejei tices. In some skate species, molecular ge- kenojei. Each symbol represents a sampling site. n=number of speci- netic studies have revealed both population mens used in mtCR analysis and numbers in parentheses=number of specimens used in morphological comparisons. EC=East China structure and demographic history, as well Sea; YS=Yellow Sea; SJ=Sea of Japan; EK=East coast of Kyushu Is.; as the existence of cryptic species based OS=Osaka Bay; NP=Pacific coast of northern Japan. on mitochondrial DNA (mtDNA) sequences (e.g., Valsecchi et al., 2005; Chevolot et al., 2006; Griffiths et al., 2010; Griffiths et al., their lifetime, although some may produce up to 600 2011; Spies et al., 2011; Dudgeon et al., 2012; Frodella over 4 years (Ishihara et al., 2009). The egg capsules et al., 2016; Im et al., 2017; Vargas-Caro et al., 2017). (43–59 mm length) have tendrils on each corner, which The mtDNA control region (mtCR) has been frequently anchor the capsules to the seafloor (Ishiyama, 1958). used to infer population structures within species be- Skates generally have a low dispersal ability (Var- cause of the high levels of nucleotide polymorphism gas-Caro et al., 2017). In fact, previous tagging studies evident in several skate species (Valsecchi et al., 2005). have suggested that some skates have relatively small In this context, we examined the population structure home ranges (e.g., Walker et al., 1997), and population of O. kenojei by analyzing mtCR sequences and mor- genetics have also revealed evidence of a local popu- phological variations and present an outline of population structure of skates (e.g., Chevolot et al., 2006). lation boundaries and their connectivity for fisheries Similarly, O. kenojei was formerly recognized as two management. allopatric species, Raja porosa, known from the East China Sea, Yellow Sea, Sea of Japan, and the Pacific coast of southern Japan, and R. fusca, known from the Materials and methods Pacific coast of northern Japan (Ishiyama, 1967). Ac- cording to Ishiyama (1967), the nominal forms could Samples be distinguished by differences in external characters, such as snout length, interorbital width, and cranium For the mtCR analysis and morphological comparisons, shape. Later, Boeseman (1979) suggested that R. po- a total of 293 individuals of Okamejei kenojei were col- rosa was a junior synonym of R. kenojei (=Okamejei lected from six regions along the Japanese Archipelago kenojei), and was followed by Ishihara (1987), who con- (regional populations abbreviated as EC (East China sidered both R. porosa and R. fusca to be junior syn- Sea); SJ (Sea of Japan); EK (East coast of Kyushu Is.); onyms of O. kenojei owing to similarities in the distri- OS (Osaka Bay); NP (Pacific coast of northern Japan); butional pattern of ventral sensory pores and similari- and YS (Yellow Sea) (Fig. 1; Suppl. Table). Of these, ties in clasper structure. Nevertheless, Ishihara (1987) 194 individuals (EC=31; YS=10; SJ=74; EK=1; OS=24; recognized several morphological variants among local NP=54) were used for mtCR sequence analysis, 212 in- populations, in particular in reference to individuals dividuals (EC=29; YS=7; SJ =72; EK=8; OS=27; NP=69) from the Pacific coast of northern Japan, which were for morphological comparisons, and 113 individuals 26 Fishery Bulletin 117(1–2) (EC=22; YS=0; SJ=44; EK=1; OS=20; NP=26) for both genetic differentiation. The null hypothesis of genetic mtCR analysis and morphological comparisons. The homogeneity was assessed by 10,000 replications with individuals for both mtCR analysis and morphological Arlequin and sequential Bonferroni corrections (Rice, comparisons only partly overlapped because some of 1989). the individuals were in poor condition and could not be used for either of the mtCR analysis or morphologi- Morphological comparisons cal comparisons. Morphological characters were examined after fixa- mtCR analysis tion in 10% formalin and preservation in 70% ethanol or 50% isopropanol. For comparisons of coloration Total DNA was extracted from muscle tissue preserved among regional populations, photographs of the fresh in 99.5% ethanol by using the DNeasy Tissue Kit color of most specimens (before fixation) were taken (Qiagen, Japan) or Wizard Genomic DNA Purification by digital photography, except for specimens from YS Kit (Promega Corp., Madison, WI1), according to the and EK. For morphological comparisons, 13 measure- manufacturer’s protocols. Polymerase chain reaction ments, those of Last et al. (2008) and Ishiyama (1958), (PCR) was performed with the primers ElDloopF (5′- were taken: 1) total length (TL); 2) disc length; 3) disc TCC CAA AGC CAA GAT TCT GC-3′) and RajinaeP7r width; 4) tail length; 5) head length; 6) dorsal snout (5′-AAA CTG GGA GGG CTG GAA ATC TTG A-3′) length; 7) eye diameter; 8) distance between orbits; (Valsecchi et al., 2005), which amplified 597 base pairs 9) ventral head length; 10) ventral snout length; 11) (bp) of mtCR.

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