Soma Branch, Fukushima Prefectural Fisheries Experimental Station, Soma, Fukushima , Japan. 2

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Aquaculture Sci. 61 1 39 46 2013 Detection of Fishing Grounds, Fishing Season, and Size Distribution of Stocked Barfin Flounder Verasper moseri in Southern Tohoku, the Pacific Coast of Eastern Japan Toshihiro WADA 1,, Kyoichi KAMIYAMA 1, Shinya SHIMAMURA 2, Tetsuya YOSHIDA 3, Takaaki KAYABA 4 and Masayoshi SASAKI 4 Abstract: Barfin flounder Verasper moseri, a rare pleuronectid flatfish, is a target species for stock enhancement programs in Hokkaido (42 N) and Iwate (39 N) prefectures in northern Japan. To elucidate the fishing grounds, fishing season, and size distribution of stocked barfin flounder in southern Tohoku, on the Pacific coast of eastern Japan, fishery data and daily fishery records of offshore bottom-trawl vessels in Fukushima Prefecture were analyzed during 2000-2006. The size distributions in the largest fish market in Fukushima were investigated in 2006. Annual landings increased from lower levels to the highest 1.1 t in 2006, which probably related to the increase of released seedlings in Hokkaido and Iwate prefectures. The main fishing areas evaluated by quantitative assessment of fishery records were found in southernmost Tohoku (35 40-36 35 N) at depths of around 300 m (mean 278 83.9 m). Remarkable seasonality of the landings was detected: over 92% were caught during January-April, with the peak period during February-March (68% in total). The two size modes detected in the landings presumably comprised males (ca. 43 cm TL, n = 361) and females (ca. 60 cm TL, n = 42). Key words: Fishing ground and season; Size distribution; Southern Tohoku; Verasper moseri Barfin flounder Verasper moseri, a pleuronectid flatfish, are distributed in cold water areas around the northwestern Pacific, including the northern Sea of Japan and the Pacific coast of northern Japan (Amaoka et al. 1995). This flounder, growing to 80 cm standard length (Andoh et al. 1999), was a commercially important flatfish species in Hokkaido, the northernmost prefecture of Japan, in the early mid- 20th century because of its palatability and high commercial price (Andoh et al. 1999; Takaya 2011). However, after the late 1970s, commercial landings decreased drastically in Hokkaido (Sasaki 1997) and putatively in Tohoku (Wada et al. 2011) (Fig. 1), probably because of overfishing for young and matured adults (Sasaki 1997). Subsequently, this species was listed as a rare marine fish species in the 1990s (Minami 1998). To recover their severely depleted stock condition, stock enhancement activities for barfin flounder commenced in Hokkaido and Iwate prefectures (Fig. 1), respectively, from 1987 (Watanabe et al. 2001) and 1990 (Sasaki and Nakai 2006). Results for each locality show a gradual increase of commercial landings (Sasaki and Nakai 2006; Misaka and Sasaki 2008). Since 2006, a large-scale stock enhancement program implemented in southwestern Hokkaido has dramatically augmented commercial landings around the released areas by annually releasing more than one million seedlings (Yoshida et al. 2011). Received 15 May 2012; Accepted 28 November 2012. 1 Soma Branch, Fukushima Prefectural Fisheries Experimental Station, Soma, Fukushima 979-2542, Japan. 2 Fukushima Prefectural Fisheries Experimental Station, Iwaki, Fukushima 970-0316, Japan. 3 Fishery Office of Fukushima Prefectural Government, Iwaki, Fukushima 970-8026, Japan. 4 Hokkaido Research Organization, Kushiro Fisheries Research Institute, Kushiro, Hokkaido 085-0024, Japan. Corresponding author: Tel, (+81) 246-54-3153; Fax, (+81) 246-54-9099; E-mail, wada385@yahoo.co.jp (T. Wada).

T. Wada, K. Kamiyama, S. Shimamura, T. Yoshida, T. Kayaba and M. Sasaki Nevertheless, to date, the recovery of wild populations through intergenerational effects from stocked populations (indirect contribution by reproducing the next generation) has not been confirmed clearly (Kayaba 2009): Few wild fish have been caught recently even in Hokkaido, the main distribution area of this flatfish (Andoh et al. 1999). Therefore, a wider understanding of life history traits of released barfin flounder is necessary to replenish severely depleted natural stocks efficiently. Recent tag-recapture surveys of cultured barfin flounder have revealed that some tagged fish released in Hokkaido moved to southern Tohoku (Takaya et al. 2009a; Yoshida et al. 2011), where wild fish had been caught at least in the 1980s (Wada et al. 2011). These results suggest that the effects of stock enhancement programs in Hokkaido can extend to southern Tohoku (Wada et al. 2011). Subsequently, recent information related to commercial catches of barfin flounder in southern Tohoku will help in clarifying the migration pattern and detailed life history cycle of this rare flatfish, and will serve as a basis for promoting future efficient stock enhancement programs of barfin flounder. Wada et al. (2011) first described the geographical distribution of fishing grounds of barfin flounder in southern Tohoku. For data of 1986-1991, they analyzed daily fishery records of an offshore bottom-trawl vessel, which revealed that barfin flounder were caught at the upper continental slope in the Joban area (Fig. 1a) at depths of 204-315 m. However, more detailed analyses for larger areas encompassing southern Tohoku are necessary because the results obtained by Wada et al. (2011) reflected only a small quantity of barfin Fig. 1. Map of study area. (a) Hokkaido and six prefectures (Aomori, Iwate, Miyagi, Fukushima, Ibaraki, and Chiba) located at the Pacific coast of eastern-northeastern Japan. Tohoku and Joban areas are indicated by arrows. (b) Map of southern Tohoku. Soma-Haragama (open triangle) and Onahama (open square) fish markets are shown in Fukushima Prefecture. Isolines show depth.

Verasper moseri Caught in Southern Tohoku flounder (4.5 kg) caught within a limited fishing area in southern Tohoku (36 20-37 50 N, 140 50-141 40 E, 43-335 m depth). Moreover, they did not investigate the seasonality of landings and size distribution of barfin flounder. This study elucidates seasonal variation of landings and fishing grounds of barfin flounder landed in Fukushima Prefecture through assessments of fishery statistics and daily fishery records of offshore bottom-trawl vessels during 2000-2006, when larger amounts of stocked barfin flounder were landed than the quantities inferred from an earlier study period of 1986-1999 (Wada et al. 2011). Additionally, the size distribution of barfin flounder landed at the largest fish market in Fukushima Prefecture was investigated in 2006. Offshore bottom-trawl vessels of Fukushima Prefecture analyzed in this study have permission to operate in broader fishing areas from southern Iwate Prefecture to northern Chiba Prefecture (Fig. 1). Therefore, the obtained results reliably reflect the characteristics of commercial catches of barfin flounder throughout southern Tohoku. Materials and Methods Fishery statistics The mean annual landings of barfin flounder during 2000-2006 were calculated for two fish markets (Soma-Haragama, Onahama, Fig. 1) from the market databases, where a species identification code has been assigned for barfin flounder. Almost all barfin flounder landings in Fukushima Prefecture were landed at the two markets. In addition, fishery data in Onahama fish market during 1986-1999 were referred from Wada et al. (2011) to assess the longterm trend of landings. Furthermore, monthly variations of fishery landings achieved using respective fishing methods [offshore trawl ( > 15 t vessel), coastal trawl (< 15 t vessel), gillnet, and others] during 2000-2006 were calculated from fishery data to reveal the seasonal variation of commercial landings of barfin flounder. Sample vessel surveys To determine the fishing grounds of barfin flounder landed in Fukushima Prefecture, daily fishery records of three offshore bottom-trawl vessels (19-42 tons) were analyzed during 2000-2006. The records, written by a chief fisherman, included data reflecting the (1) fishing dates, (2) location of fishing grounds (Loran-A or latitude and longitude, and depth), (3) net-entering and net-hauling times for each operation, and (4) catches (nearest 0.1 kg) of a maximum of 15 species for each operation. The total effort (towing hours for trawling, h) and total catch (kg) of barfin flounder were summed for each 5 minutes of latitude/ longitude (35 30-38 15 N, 140 40-142 00 E). Then the catch per unit effort (CPUE, kg/ 100 h) for each 5 minutes of latitude/longitude was calculated based on a database of the fishery records compiled using spreadsheet software (Excel 2007, Microsoft Corp.) at the Fukushima Prefectural Fisheries Experimental Station. Furthermore, a percent frequency distribution of catches for each 50 m depth was calculated based on barfin flounder data in records during 2000-2006. Measurement in the market In 2006, market surveys were conducted about three times a week at the Soma- Haragama fish market, the largest fish market in Fukushima Prefecture, to reveal the size distribution of barfin flounder. At the market, total length (TL) (nearest cm) and weight of barfin flounder were measured. No commercial size limitation for barfin flounder has been implemented in Fukushima Prefecture. Two clear modes found in the TL frequency distribution (see Fig. 6) were separated by fitting normal distributions using least-squares method (Aizawa and Takiguchi 1999). Results Annual and seasonal variations of landings Annual changes of commercial landings of barfin flounder at the two fish markets during 1986-2006 are presented in Fig. 2. Commercial

T. Wada, K. Kamiyama, S. Shimamura, T. Yoshida, T. Kayaba and M. Sasaki landings were found only in Onahama during 1986-2002 and fluctuated within a low level [5.4-124.7 kg, mean standard deviation (SD) = 52.9 37.9 kg]. The landings in Soma-Haragama were first observed in 2003 when total landings increased sharply to 353.3 kg. Thereafter, the total landings maintained a higher level and reached the highest record of 1,100.9 kg in 2006. Monthly changes of barfin flounder landings at the two markets during 2000-2006 are depicted in Fig. 3. Although the monthly absolute value of the landings (Fig. 3) differed greatly among years depending on the total landings for each year (Fig. 2), the seasonal fluctuation pattern was quite characteristic and similar among years. Almost all catches (92.2% in total) were landed during January- April. Particularly, February (36.1%) and March (31.9%) were the peak months, comprising 68% of the total landings. Almost all landings (99.2%) were caught by trawl fishery. Particularly, offshore trawl fishery operated by larger trawl vessels ( > 15 t) accounted for the highest proportion (94.4%), whereas gillnet fishery (0.6%) and other means (0.1%) comprised a much lower proportion. Fishing grounds of offshore bottom-trawl vessels and depth distributions Geographical distributions of fishing effort (operation hours, h) and CPUEs (kg/100 h) of barfin flounder during 2000-2006 are portrayed in Fig. 4. The total fishing effort during the period was 45,018 h. Total catches in the daily fishery records during 2000-2006 were 123.5 kg (2000, 5.1 kg; 2001, 15.9 kg; 2002, 2.3 kg; 2003, 38.7 kg; 2004, 0 kg; 2005, 8.0 kg; 2006, 53.5 kg). Almost all catches in the records were caught during January-April (92.0% in total) with the peak months of February (50.2%) and March (31.7%). Trawling operations were Fig. 2. Annual changes of commercial landings (kg) of barfin flounder in Onahama (black bar) and Soma- Haragama (hatched bar) fish markets. Fishery data for the Onahama fish market for 1986-1999 were referred from Wada et al. (2011). Fig. 3. Monthly variations of fishery landings for respective fishing methods in Fukushima Prefecture during 2000-2006. J, M, and S on the x-axis respectively represent January, May, and September. Fig. 4. (a) Total operation hours of bottom trawling (h), and (b) catch per unit effort (kg/ 100 h) of barfin flounder by three offshore bottom-trawl vessels during 2000-2006 shown for every five minutes of longitude and latitude. Isolines represent depth.

Verasper moseri Caught in Southern Tohoku found throughout southern Tohoku with depths of less than 900 m (Fig. 4a). Higher effort was detected from northern Fukushima to southern Miyagi (37 10-38 00 N) at depth of less than 100 m. In addition, higher effort was also found for the area off southern Ibaraki (35 40-36 30 N) at depths of less than 300 m. In contrast, higher CPUEs of barfin flounder were observed only off Ibaraki (35 40-36 35 N) at depths of around 300 m (Fig. 4b). Lower CPUEs were observed off Fukushima (37 00 N, 37 20 N). Much smaller values were observed off Fukushima at depths of less than 100 m. Percent catches for every 50 m depth are presented in Fig. 5. Although the catches were observed within wide ranges of 40.3-500 m depth, higher percentages were found at 250-400 m depth (86.1% in total), with the peak at 300 m (28.2%). A small peak was found at 100 m depth (4.5%). Mean depth ( SD) was calculated as 278.6 83.9 m. Size frequency distribution in the market The size frequency distribution of barfin flounder landed on Soma-Haragama fish market in 2006 is depicted in Fig. 6. In all, 403 individuals of landed barfin flounder were measured, corresponding to 56.7% (by weight) of total landings in the market in 2006. Two clear modes were detected from the size distribution: one large mode around 43 cm TL and another smaller mode around 60 cm TL. These two modes were clearly separated by fitting normal distributions. The peak ( SD) of each distribution was calculated as 42.7 2.95 cm TL and 59.9 4.67 cm TL. The quantity of fish assigned for each mode was estimated respectively as 361 and 42. All the measured barfin flounder have abnormal pigmentation in the blind side. These results indicated that cultured barfin flounder released from Hokkaido or Iwate occupied a much higher proportion among landings because few wild flatfishes show abnormal pigmentation in the blindside (Tomiyama et al. 2008a), and few wild barfin flounder have been caught recently (Andoh et al. 1999). Discussion Our study revealed the geographical distribution of barfin flounder catches throughout southern Tohoku quantitatively (Fig. 4). The geographical distribution can be analyzed because many fishery data of barfin flounder were recorded in the daily fishery records, probably because of the increase of catches (Fig. 2). Almost all the barfin flounder landed on Fukushima were judged as stocked fish according to their abnormal pigmentation in the blind side. Therefore, the increase of commercial landings was unquestionably related to the increase of released seedlings in Hokkaido and Iwate prefectures (Fig. 7). Landings and fishing grounds in southern Tohoku Our study elucidated the fishing season, the geographical distribution of fishing grounds, and Fig. 5. Percent frequency distribution of catches of barfin flounder for every 50 m depth, caught by three offshore bottom-trawl vessels during 2000-2006. Fig. 6. Size frequency distribution of barfin flounder landed at the Soma-Haragama fish market in 2006 (grey columns). Two normal distributions fitted to the size distribution are presented with black lines.

T. Wada, K. Kamiyama, S. Shimamura, T. Yoshida, T. Kayaba and M. Sasaki Fig. 7. Quantities of release of barfin flounder seedlings in Hokkaido and Iwate prefectures during 1994-2005. Data are from the general report published in March 2011 by the National Association for the Promotion of Productive Seas. size distribution of stocked barfin flounder in southern Tohoku. Their specific characteristics were (1) remarkable seasonality of the landings with the peak period during January-April, (2) limited main fishing grounds (35 40-36 35 N) at depths of around 300 m, and (3) two size distributions of the landings at around ca. 43 cm and 60 cm TL. We discuss these characteristics in the following paragraphs. The seasonality of landings was striking (Fig. 3). Over 92% of catches were landed during January-April in 2000-2006. Although seasonality of landings in Fukushima Prefecture has been observed for some flatfish species (e.g., the congeneric species Verasper variegatus, Wada et al. 2012), no flatfish species except for barfin flounder has shown such remarkable seasonality. Many flatfish species are caught throughout the year, except for the trawl fisheries closed season of July and August (Hirakawa 1978; Shimamura and Igarashi 1999, 2000; Yamada et al. 2006; Yamanobe 2007; Tomiyama et al. 2008b; Chiyokubo 2010). The geographical distribution of fishing grounds and depth distributions are also quite characteristic. Although trawl fisheries operate throughout southern Tohoku (Fig. 4a), the higher CPUEs were only found off Ibaraki Prefecture (35 40-36 35 N) at depths of around 300 m (Figs. 4b, 5), corresponding to the upper continental slope near the southernmost part of the First Oyashio Intrusion (Shimizu et al. 2001). The catches also occurred off Fukushima, but the CPUEs were much lower (Fig. 4b). These results indicate that some fish released in Hokkaido or Iwate prefectures congregated to deeper waters around southernmost Tohoku mainly during January- April. These specific geographical and depth distributions were quite different from those of other flatfishes in southern Tohoku. Many flatfish species were caught from broader latitudes in southern Tohoku with wider depth ranges in accordance with their seasonal migration cycles (e.g., feeding migration and spawning migration). Furthermore, the depth distribution pattern in southern Tohoku differed greatly from those of young barfin flounder around the release areas in Hokkaido and Iwate prefectures. Cultured seedlings were released mainly at shallower areas at depths less than 10 m, and younger fish (age-0 to age-2 fish) remained in coastal areas to achieve high growth performance by feeding mainly on abundant epifaunal crustaceans and fish of several kinds (Watanabe et al. 2001; Watanabe and Minami 2003; Yoshida et al. 2007a). The size distribution of landings was also characteristic (Fig. 6). Two clear modes separated at around 50 cm TL were detected. Furthermore, fish smaller than 30 cm TL, which is the target size for fishing around the release areas (Watanabe et al. 2001; Sasaki and Nakai 2006), was not found irrespective of high-frequency market surveys in the Soma- Haragama fish market. Reportedly, females of released barfin flounder grew faster than males, became larger at age-2 or older, and reached over 50 cm TL at age 4 (Mori et al. 1999; Yoshida et al. 2007b). In contrast, few males grew to over 50 cm TL in Hokkaido (Yoshida et al. 2007b, 2008). In addition, sex discrimination of released barfin flounder based on the skin coloration in the blind side (male, yellow; female, white) was proved with probability of greater than 90% (Misaka and Sasaki 2008). At the Onahama fish market, two descriptive trading names were assigned for barfin flounder: ki-matsukawa (literal translation: yellow barfin flounder, having

Verasper moseri Caught in Southern Tohoku yellow body coloration in the blind side) and matsukawa (barfin flounder, having white body coloration in the blind side) (Wada et al. 2011). In association with these pieces of information, the fact that the body coloration on the blind side was mainly white in fish over 50 cm TL and yellow in fish less than 50 cm (S. Shimamura, personal observation, 2006) strongly suggests that the one mode around 43 cm TL comprised males and the other mode around 60 cm TL comprised females. The vastly different quantities of fish assigned for each mode (361 vs. 42) are attributable to the following two reasons. One possibility is that the sex ratio of released cohorts was already biased to males. Actually, the sex ratio of released seedlings and recaptured fish during 1998-2003 was reportedly biased to males (ca. 68% in total) in Hokkaido (Takaya et al. 2009b). Another possibility and/or synergetic effect is that initial ages for migration from the waters near the release area to southern Tohoku were older in females, resulting in the male-biased sex ratio because of the longer fishing mortality for remaining females than for migratory males. A large share of the landings (Fig. 6) exceeded the estimated smallest size at maturation (male, > 33.8 cm TL; female, > 45.3 cm TL) (Yoshida et al. 2008). The main fishing season (Fig. 3) accorded well with the spawning season in captivity (mainly March-April) (Kayaba 2005) and also with the season when commercial landings had decreased drastically in Hokkaido (Yoshida et al. 2011), where no specific spawning area of stocked barfin flounder has yet been detected (Kayaba 2009). These results suggest that the congregation of barfin flounder around southernmost Tohoku at depths of around 300 m (Figs. 4, 5) might be related to spawning events. Detailed assessments of the maturation status of the landings in southern Tohoku are necessary as a next step for this research. Acknowledgments This study was conducted as part of a research project Research and Development Projects for Application in Promoting New Policy of Agriculture, Forestry, and Fisheries, funded by the Ministry of Agriculture, Forestry, and Fisheries, Japan. We are grateful to Dr. T. Matsubara and to the members of this project for their help in promoting this study. References Aizawa, Y. and N. Takiguchi (1999) Consideration of the methods for estimating the age-composition from the length frequency data with MS-Excel. Bull. Jpn. Soc. Fish. Oceanogr., 63, 205-214 (in Japanese). Amaoka, K., K. Nakaya and M. Yabe (1995) Barfin flounder Verasper moseri Jordan et Gilbert. In The Fishes of Northern Japan (ed. By K. Amaoka, K. Nakaya and M. Yabe), Kita-Nihon Kaiyo Center, p. 306 (in Japanese). Andoh, T., K. Watanabe and T. Matsubara (1999) Problems and perspectives in stock enhancement of barfin flounder (review). Bull. Hokkaido Natl. Fish. Res. Inst., 63, 19-33 (in Japanese with English abstract). Chiyokubo, T. (2010) Recent catch of the shotted halibut Eopsetta grigorjewi off Fukushima. Bull. Fukushima Pref. Fish. Exp. Stn., 15, 1-9 (in Japanese). Hirakawa, H. (1978) Studies on the fishing ground of small trawl nets in Fukushima. Bull. Fukushima Pref. Fish. Exp. Stn., 5, 43-51 (in Japanese). Kayaba, T. (2005) Studies on techniques of reliable production of seed of barfin flounder Verasper moseri. Sci. Rep. Hokkaido Fish. Exp. Stn., 69, 1-116 (in Japanese with English abstract). Kayaba, T. (2009) Estimation of spawning ecology of a rare flatfish, barfin flounder. Kushirosuishi-dayori, 90, 3-5 (in Japanese). Minami, T. (1998) Barfin flounder. In Data Book for Rare Wild Aquatic Organisms in Japan (ed. By Fishery Agency of Japan), Japan Fisheries Resource Conservation Association, pp. 102-103 (in Japanese). Misaka, T. and M. Sasaki (2008) Sex discrimination of landed barfin flounder from the body coloration in the blind side. Kushirosuishi-dayori, 89, 8-11 (in Japanese). Mori, T., S. Saito, T. Sugimoto and T. Kayaba (1999) Differences in growth rate among sexes of barfin flounder (Verasper moseri). Sci. Rep. Hokkaido Fish. Exp. Stn., 56, 137-141 (in Japanese with English abstract). Sasaki, M. (1997) Fishery status and ecology of barfin flounder in the waters of Hidaka and Iburi areas, southwestern Hokkaido. Hokusuishi-dayori, 38, 7-12 (in Japanese). Sasaki, R. and K. Nakai (2006) Mark-recapture experiment using barfin flounder, Verasper moseri on the coast of Iwate Prefecture. Saibai Giken, 34, 1-6 (in Japanese with English abstract). Shimamura, S. and S. Igarashi (1999) Flatfish, Dexistes rikuzenius ( Jordan et Starks), caught in the coast of Fukushima region. Bull. Fukushima Pref. Fish. Exp. Stn., 8, 17-27 (in Japanese). Shimamura, S. and S. Igarashi (2000) Flatfish, Tanakius

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