Received: 27 November 2018 | Revised: 18 February 2019 | Accepted: 20 March 2019 DOI: 10.1111/fog.12432

ORIGINAL ARTICLE

Correlation of changes in seasonal distribution and catch of red bream Pagrus major with winter temperature in the eastern Seto , (1972–2010)

Masayuki Yamamoto1 | Hiroaki Omi2 | Naotaka Yasue3 | Akihide Kasai4

1Kagawa Prefectural Fisheries Experimental Station, Takamatsu, Kagawa, Japan Abstract 2Marine Fisheries Research Center, Research bream Pagrus major is a commercially important fish in Japan. In eastern Institute of Environment, Agriculture and (SIS), the catch has increased from 297 tons in 1972 to 2,039 tons Fisheries, Sennan, , Japan 3Hidaka Promotions Bureau, Gobo, in 2010. We examined the relationship, 1972–2010, between increase in catch and Wakayama, Japan winter temperature, based on the catch in February and March and the lowest water 4 Faculty of Fisheries Sciences, Hokkaido temperature at 10 m depth. In 1972–1986, the lowest water temperatures in the University, Hakodate, Hokkaido, Japan inner SIS areas (, Harima‐nada, and Bisan‐seto) were <8°C, which is physi‐ Correspondence ologically unfavorable for red sea bream. However, in 1987–2010 temperatures were Masayuki Yamamoto, Kagawa Prefectural Fisheries Experimental Station, Takamatsu, generally ≥8°C. In the inner areas, the catch during winter had been minimal until the Kagawa 761–0111, Japan. early 1980s, presumably because most red sea breams moved to the Kuroshio‐in‐ Email: [email protected] fluenced (warmer) area. However, the winter catch in the inner areas of Funding information SIS increased from the late 1980s with warm winters. In addition, the catch between Japan Fisheries Agency April and June, the spawning season, increased in the inner areas from the 1990s, and the catch rate of the inner areas was more than twice higher in the 2000s than in the 1980s. The results suggest that expansion of the distribution area during winter due to warm winter and increase in egg production in the inner areas greatly contributes to the increasing in catch in the eastern SIS.

KEYWORDS distribution expansion, Pagrus major, warm winter

1 | INTRODUCTION Climate change associated with global warming has been reported to affect marine ecosystems and fisheries production (Brander, The distribution of fishes is generally limited by the physical envi‐ 2007; Fortibuoni, Aldighieri, Giovanardi, Pranovi, & Zucchetta, 2015; ronment such as temperature, salinity, and currents (Moyle & Cech, Hare & Able, 2007; Kuwahara et al., 2006; Lacoue‐Labarthe et al., 2000; Shinoda & Tsukamoto, 2010). Fish resources are determined 2016; Tadokoro, Sugimoto, & Kishi, 2008). In addition, the increase by biological and abiotic conditions as well as fishing pressure (Alheit in water temperature has been reported to induce a poleward shift & Hagen, 1997; Craig, 2000; Hamilton & Haedrich, 1999; Shelton & in fish distribution (Barbeaux & Hollowed, 2018; Last et al., 2011; Mangel, 2011; Watanabe, 1998). In particular, resource fluctuations Perry et al., 2005), leading to changes in annual catch (Teixeira et al., and water temperature are closely related (Henderson & Henderson, 2014), fish fauna (Lloyd, Plaganyi, Weeks, Magno‐Canto, & Plaganyi, 2017; Oh, Sakuramoto, & Hasegawa, 2002; Perry, Low, Ellis, & 2012; Masuda, 2008; Mavruk, Bengiil, Yeldan, Mamasorli, & Avsar, Reynolds, 2005; Sabatés, Martín, Llopet, & Raya, 2006; Takasuka, 2017), spawning period (Sims, Wearmouth, Genner, Southward, & Oozeki, & Aoki, 2007). Hawkins, 2004), and spawning ground (Villegas‐Hernández, Lloret,

Fisheries Oceanography. 2019;00:1–9. wileyonlinelibrary.com/journal/fog © 2019 John Wiley & Sons Ltd | 1 2 | YAMAMOTO et al.

FIGURE 1 Map showing the habit of red sea bream Pagrus major in the eastern SeaofJapan Seto Inland Sea (SIS), Japan Japan

Shikoku Eastern Seto Inland Sea Kyushu Pacific Kuroshio

OkayamaPref. HyogoPref. Osaka Pref. ° ′ 34 30 Harima-nada Osaka Bay Bisan-seto Izumisano

Takamatsu Hiketa Kada Kagawa Pref.

34°N KiiChannel Wakayama TokushimaPref. Pref.

Oceanic Water 134° 135°E

& Muñoz, 2015). However, there is not sufficient published informa‐ trawl net and set net (Sakaji & Yamamoto, 2017). The catch size of tion on the relationship between increase in water temperature and this species varies from approximately 15–70 cm in total length, and stock variation (Alheit et al., 2012; Eriksen, Ingvaldsen, Nedreaas, the longevity is 15–20 years old (Shimamoto, 2006). & Prozorkevich, 2015; Hermant, Lobry, Bonhommeau, Poulard, & In Japan, red sea breams are evaluated on three stocks (Fisheries Pape, 2010; Sabatés et al., 2006) in order to predict the dynamics of Agency & Fisheries Research & Education Agency of Japan, 2017). fisheries resources caused by global warming. The SIS is one of the main fishing grounds, as the catch was 4,410 The Seto Inland Sea (SIS) is located in western Japan and is a tons in SIS in 2010, accounting for approximately 30% of the total semi‐enclosed coastal sea surrounded by the islands of Honshu, catch in Japan (Yamamoto et al., 2013). The SIS has two stocks, the , and Kyushu (Figure 1). It has a length of 500 km and an eastern SIS stock (Sakaji & Yamamoto, 2017) and the central and average depth of approximately 30 m. The SIS is one of the most western SIS stock (Yamamoto & Sakaji, 2017). In this study, we ex‐ productive waters globally (Takeoka, 2002). The warm Kuroshio cur‐ amined the eastern SIS stock, composed of Kii Channel, Bisan‐seto, rent flows toward the east of Shikoku, so that the southern part of Haraima‐nada, and Osaka Bay (Figure 1). the SIS, the Kii Channel area, is directly influenced by these warmer The catch of the eastern SIS stock decreased from the 1950s to waters. Based on monthly oceanographic observations at ≥150 sites early 1970s; however, by the mid‐2010s the catch recovered from from 1973 to 2013, the annual water temperature in the surface, the late 1970s (Sakaji & Yamamoto, 2017). In the eastern SIS stock, 10 m, and bottom layers in the SIS has been reported to have in‐ the cause of the increase in the catch has been suggested to be the creased by approximately 1°C during the monitoring period (Abo et improvement of fishing efficiency of small trawl nets in the 1970s al., 2015). and conservation of small fish caused by decreasing effort of small Red sea bream Pagrus major (family: Sparidae) is distributed from trawl nets from the 1980s (Shimamoto, 2006). However, since the the coastal water of northern Japan to the East China Sea (Hayashi, late 1980s the catch of flatfishes and shrimps caught by small trawl 2002) supporting commercially important fisheries in Japan (Masuda nets has not similarly increased (Yamamoto, 2012; Yamashita, 2007). & Tsukamoto, 1998; Nagai, 1995; Shimamoto, 2006; Yamamoto, Omi, The contribution of the seeding production to the enhancement has & Miyahara, 2013). Red sea bream spawn in spring and consume var‐ reported to be limited for the eastern SIS stock (Sakaji & Yamamoto, ious prey items such as crustaceans, polychaetes, fishes, and squids 2017). Based on previous reports, other factors excluding the fish‐ (Shimamoto, 2006). In the SIS, this species is caught mainly by small ery and the release of artificial seeds are expected to be related to YAMAMOTO et al. | 3 the increase in catch. Zenitani, Onishi, and Obata (2014) implied that Office, Kinki Regional Agricultural Administration Office, Ministry there was an association between the increase in the catch and in‐ of Agriculture, Forestry, and Fisheries (1974), and Izumisano Fishery crease in water temperature in the eastern SIS. It is suggested that Cooperative (Research Institute of Environment, Agriclture and the fish migrated to the Kii Channel and overwinter in the warm wa‐ Fisheries, ), respectively. In Harima‐nada, the ters (Shimamoto, 2006), because red sea bream die due to low water water temperature at seven sites of was mea‐ temperature of <3–8°C (Takeda, Tsuji, & Itazawa, 1989; Woo & Fung, sured by Kagawa Prefectural Fisheries Experimental Station (Masui, 1980). In recent years, the annual water temperature increased in 2015). The monthly catch in 1972–2010 was calculated based on the SIS due to global warming, and the water temperature has grad‐ the catch data of Kagawa Branch Office, Chugoku, and Shikoku ually increased especially during winter (Abo et al., 2015; Yamamoto, Regional Agricultural Administration Office, Ministry of Agriculture, 2003). The increasing resource might be due to the expansion of dis‐ Forestry and Fisheries (1974), and Hiketa Fishery Cooperative tribution during winter by increased water temperature. (Kagawa Prefctural Fisheries Station). In Bisan‐seto, the water tem‐ In this study, to examine the hypothesis that warm winter con‐ perature at 14 sites was measured by Kagawa Prefectural Fisheries tributes to spreading red sea bream during winter, we examined the Experimental Station (Masui, 2015). The monthly catch in 1972– annual change in the spatial distribution during winter and lowest 2010 was calculated based on the catch data of Kagawa Branch water temperature using the catch and water temperature in the Office, Chugoku, and Shikoku Regional Agricultural Administration four areas of eastern SIS from 1972 to 2010. In addition, the an‐ Office, Ministry of Agriculture, Forestry and Fisheries (1974), and nual change in the spawning stock biomass and spawning ground Takamatsu Fish Market (Takamatsu Municipal Wholesale Market, was clarified. 1984), respectively.

2 | MATERIALS AND METHODS 2.2 | Data analysis

The survey areas were divided into the Kuroshio‐influenced Kii 2.1 | Data source Channel area and the inner areas (Osaka Bay, Harima‐nada, Bisan‐ Eastern SIS consists of four areas: Kii Channel (average depth: seto). To clarify whether the increase in water temperature affects 46 m), Osaka Bay (30 m), Harima‐nada (26 m), and Bisan‐seto (16 m; the distribution of red sea bream during winter, we examined the Figure 1). The water temperature in the Kii Channel is greatly af‐ relationship between the lowest water temperature and the catch fected by the with warm Kuroshio water, because the in February and March, the coldest season, from 1972 to 2010 in Kii Channel is located in the southern end of the eastern SIS. On each area by Spearman rank statistic. In addition, to estimate the the other hand, Osaka Bay, Harima‐nada, and Bisan‐seto are inner relative spawning biomass in each area, we examined the catch waters with less influence of the Pacific Ocean. The water tempera‐ between April and June, when red sea bream spawn (Shimamoto, tures in the all areas are lowest in February and/or March (Tarutani, 2006). Pearson's correlation coefficient determined the significance 2005). During winter, the water temperature at 10 m depth in the Kii of the association of catch in the inner areas between winter and Channel is almost ≥10°C, while the water temperature in the inner spawning season. areas is almost <10°C (Tarutani, 2005). Because the water is well mixed associating with similar temperatures in the all layers during winter (Abo et al., 2015) and red sea bream ranges from the middle 3 | RESULTS to bottom layers (Shimamoto, 2006), we used water temperature at 10 m depth in this study. The catch of the eastern SIS stock of red sea bream increased Annual catch of red sea bream in each area between 1972 gradually from 1972 to 2010, reaching 297 tons in 1972, 636 tons and 2010 was used from Japanese fisheries statistics (Fisheries in 1980, 996 tons in 1990, 1,601 tons in 2000, and 2,039 tons in Development Council of the Seto Inland Sea, 1996; Japan Fisheries 2010 (Figure 2). The catch was 6.7 times higher in 2010 than in 1972. Agency, 2016). The data sources of the water temperature at 10 m Annual variation in the catch was geographically different. In the Kii depth and the monthly catch in the four areas between 1972 and Channel, the catch increased in the late 1970s and early 1980s and 2010 are shown below. In the Kii Channel, the water temperature remained at a high level of approximately 500 tons between the late at 15 sites of was measured by Wakayama 1980s and 2000s. In Osaka Bay and Harima‐nada, the catches were Prefectural Fisheries Experimental Station (Nakachi, 2015). The <100 tons in the early 1970s, however, gradually increased from the monthly catch was calculated based on the catch data of Kada mid‐1980s to early 1990s. The catch did not increase in Osaka Bay Fishery Cooperative (Wakayama Prefectural Fisheries Station). in the 2000s and remained at a high level of approximately 370 tons, The catch data between 1990 and 1992 were not available. In while the catch increased in the 2000s in Harima‐nada and reached Osaka Bay, the water temperature at 20 sites was measured by 679 tons in 2010. The catch in Bisan‐seto gradually increased from Research Institute of Environment, Agriculture and Fisheries, Osaka the late 1980s to 2000s. Prefecture (Akiyama, 2015). The monthly catch in 1972–1983 and The lowest water temperature was often below <8°C from 1972 1984–2010 was calculated based on the catch data of Osaka Branch to 1986 in the inner areas, Osaka Bay, Harima‐nada, and Bisan‐seto, 4 | YAMAMOTO et al.

FIGURE 2 Annual change in catch of red sea bream in each water area (symbols) and total catch (bar) in the eastern SIS from 1972 to 2010. KIC, OSB, HAN, and BIS indicate Kii Channel, Osaka Bay, Harima‐nada, and Bisan‐seto, respectively

and the lowest water temperature was <6.5°C in 1977 and 1984 (Figure 5; rs = –0.09, p = 0.27). The catch varied between 1 and 8 tons (Figures 3 and 4). However, the lowest water temperatures were in the early 1970s; however, it increased from the late 1970s to the ≥8°C from 1987 to 2010, except in 1996. The lowest water tem‐ early 1990s and has remained at a high level of approximately 100 perature significantly increased in Harima‐nada (rs = 0.28, p = 0.046) tons between the late 1990s and 2000s. and Bisan‐seto (rs = 0.66, p < 0.01), although there was no signif‐ The catch during the spawning season increased from the icant trend toward increasing lowest water temperature in Osaka 1980s to 1990s and greatly increased from the 2000s (Figure 6).

Bay (rs = 0.10, p = 0.27). The catch in February and March varied Annual variation in the catch was geographically different. The from 0 to 5 tons between 1972 and 1987, expect in 1977 with 8 tons catch increased in the Kii Channel in 1980s; however, it decreased and in 1984 with 33 tons. The catch clearly increased from 1988 in the 1990s and the 2000s. In contrast, the catch greatly in‐ to 2010, reaching 6 tons in 1990, 14 tons in 2000, and 45 tons in creased in the inner areas from the 1990s, especially Bisan‐seto 2010 (Figure 4). The relationship between the lowest temperature and Harima‐nada from the 2000s. The catch rate in the inner areas and catch clearly shows that the catch was abundant in the 2000s was <40% in the 1970s and 1980s, but increased in the 1990s and in relation to the temperature rise in each inner water (Figure 4). was >70% from the 2000s. There was a significant positive cor‐ On the other hand, the lowest water temperature varied between relation of catch in the inner areas between winter and spawning 9.3 and 14.3°C and did not significantly increase in the Kii Channel season (r = 0.86, p ≪ 0.01).

12

10

8

Lowest WT (°C) 6 OSBHAN BIS

4 80 BIS 60 HAN

on ) OSB 40 FIGURE 3 Annual changes in the lowest water temperature (top) and catch Catch (t 20 in February and March (bottom) in the inner areas; Osaka Bay, Harima‐nada, and 0 Bisan‐seto, from 1972 to 2010. A dashed 1972 1977 1982 19871992199720022007 line in the top panel indicates 8°C YAMAMOTO et al. | 5

FIGURE 4 Relationships between the 35 Bisan-seto lowest water temperature and catch in Osaka Bay Harima-nada 30 February and March in the inner areas; Osaka Bay (OSB), Harima‐nada (HAN), 25 1984 n

and Bisan‐seto (BIS), from 1972 to 2010. o t 20 Open, shadowed, and solid symbols ( h c indicate data from 1972 to 1987, from t 15 a 1988 to 1999, and from 2000 to 2010, C) 10 respectively 5 1984 1977 1984 0 5811 5811 5811 Lowest water temperature (°C)

FIGURE 5 Annual changes in the 16 lowest water temperature (top) and catch 14 in February and March (bottom) in the Kii Channel area from 1972 to 2010, except 12 for 1990–1992. A dashed line in the top 10 panel indicates 8°C WT (°C) 8 Low 6 4

200

150 on)

h (t 100 c t a C 50

ND 0 1972 1977 1982 1987 1992 1997 2002 2007

FIGURE 6 Annual change in catch between April and June (spawning season) in the four areas of the eastern Seto Inland Sea (bar chart) and catch rate of the inner water areas (line chart) from 1972 to 2010, except for 1990–1992 6 | YAMAMOTO et al.

FIGURE 7 Annual change in biomass of the eastern Seto Inland Sea (SIS) stock (Sakaji & Yamamoto, 2017) and central and western SIS stock (Yamamoto & Sakaji, 2017) from 1977 to 2010

4 | DISCUSSION Yoshida, & Hamaguchi, 2007). These suggest that the shift to the main spawning ground to the inner areas with wide seaweed bed The annual variation in the catch in February and March indicates increases the survival rate of the juveniles. Since the catch in the that the biomass of red sea bream in the inner areas during winter inner areas during winter and spawning season was synchronized, increased from the late 1980s when the lowest water temperature the distribution in the inner areas during winter may contribute to increased to ≥8°C (Figure 3). It was reported that red sea bream increase in the survival rate. migrate to the Kii Channel from late autumn to early winter to According to Sakaji and Yamamoto (2017) and Yamamoto and avoid cold water and overwinter in warm waters (Shimamoto, Sakaji (2017), the biomass of the eastern SIS stock increased, while 2006). The lower limit of water temperature in the habitat is 5.5°C the biomass of the central and western SIS stock did not increase (Woo & Fung, 1980). However, low temperature of <8°C physi‐ from 1977 to 2010 (Figure 7). The annual water temperature in‐ ologically damages red sea bream (Sakaguchi & Hamaguchi, 1979), creased in the both areas from 1973 to 2013 (Abo et al., 2015). In the and deaths of cultured fish begin to be observed in approximately central and western SIS, the distribution of red sea bream is not lim‐ 8°C (Sakaguchi & Hamaguchi, 1979; Takeda et al., 1989). Moreover, ited to any specific areas during winter (Yamamoto & Sakaji, 2017), abnormal behavior of wild red sea bream is observed in <8°C because the area with <8°C is small in this water area (Tarutani, (Ueta, 2011). These suggest <8°C is physiologically unfavorable 2005). Therefore, warmer winter would not contribute to the ex‐ for red sea bream. Since the lowest water temperature was ≥8°C pansion of distribution area during winter and change in spawning in the inner areas from the late 1980s, the fish did not have to mi‐ ground. The recruitment of the eastern SIS stock has been main‐ grate to the southern area and would be able to overwinter in the tained at a high level since the mid‐1990s (Sakaji & Yamamoto, 2017), inner areas. The annual catch of red sea bream increased with the while that of the central and western SIS stock has decreased since increase in the catch in the inner waters during winter, although mid‐1990s (Yamamoto & Sakaji, 2017). According to fisheries stock the fishing effort of the small trawl nets (total number of fishing assessment, the eastern SIS stock is predicted to increase the catch days) decreased to approximately 0.7 times in the eastern SIS from and biomass in the future under the current fishing pressure (Sakaji the 1970s to 2000s (Sakaji & Yamamoto, 2017). In addition, the & Yamamoto, 2017), whereas the central and western SIS stock is biomass of the eastern SIS stock increased with the annual catch predicted to slightly decrease the catch and biomass under the cur‐ (Sakaji & Yamamoto, 2017). These suggest that one of the factors rent fishing pressure (Yamamoto & Sakaji, 2017). These suggest that of the biomass increase in the eastern SIS stock was the expansion high fishing rate and low recruitment are the factors leading to the of the overwinter water due to the increase in water temperature decrease in biomass of the central and western SIS stock. in the inner waters during winter. Since the catch during the spawning season was limited in the The annual variation in the catch in the four areas during the Bisan‐seto in the 1970s and 1980s (Figure 6), the egg production spawning season suggests that the spawning stock biomass greatly should also have been minimal. However, the catch was high in increased and the main spawning grounds shifted from the Kii Bisan‐seto in the 2000s. In addition, Zenitani et al. (2014) have re‐ Channel to the inner areas (Figure 6). Red sea bream juveniles gen‐ ported that Bisan‐seto was a spawning ground for red sea bream in erally distribute in shallow areas such as seaweed beds and reefs the late 2000s based on the counting of red sea bream eggs using a (Azeta, Ikemoto, & Azuma, 1980; Sakaji & Yamamoto, 2017). The monoclonal antibody assay. The report indicates that the spawning seaweed bed in the inner areas (31.2 km2) was 3.9 times larger ground disappeared in the 1960s and 1970s and had revived in the than that in the Kii Channel (8.0 km2) (Ministry of the Environment, 2000s. Since the catch in winter and the spawning season in the 2000). The experiments in a mesocosm indicated that seagrass inner areas was synchronized, the expansion of the distribution in Zostera marina habitat reduces vulnerability of red sea bream juve‐ the inner areas during winter might contribute to the revival of the nile from the predation by piscivorous fish (Shoji, Sakiyama, Hori, spawning ground in Bisan‐seto. YAMAMOTO et al. | 7

Mechanisms of resource increase by water temperature rise can AUTHOR CONTRIBUTION be explained as follows: (a) expansion of optimum water temperature All authors contributed extensively to the work presented in this area (Landa, Ottersen, Sundby, Dingør, & Stiansen, 2014; Last et al., paper. M. Yamamoto and A. Kasai designed the study. M. Yamamoto, 2011), (b) expansion of spawning area and period (Sabatés et al., 2006; H. Omi, and N. Yasue analyzed the data. M. Yamamoto interpreted Villegas‐Hernández et al., 2015), and (c) increase in prey availability the data and wrote the paper. A. Kasai, H. Omi, and N. Yasue gave (Mueter, Peterman, & Pyper, 2002). The increase in the biomass of beneficial advice and edited the manuscript. the eastern SIS stock might be greatly influenced by the expansion of warm water temperature in winter and spawning area. Increases in catch and abundance of subtropical/tropical species due to increase DATA AVAILABILITY STATEMENT in water temperature have been reported in coastal waters in the The catch data of sea bream at Kada, Izumisano and Hiketa (Masuda, 2008), Portugal (Teixeira et al., 2014) and the Fishery Cooperative belongs to Wakayama Prefectural Fisheries northern (Fodrie, Heck, Powers, Graham, & Robinson, Station, Research Institute of Environment, Agriculture and 2010). Catches of pike conger Muraenesox cinereus (Watari et al., 2014) Fisheries, Osaka Prefecture and Kagawa Prefectural Fisheries and red spotted grouper Epinephelus akaara (Takashima, 2016), which Station, respectively. These research institutes permitted the use were originally distributed from the tropics to subtropical water, have of the data. increased in SIS in recent years. However, these two species have increased since the 2000s, whereas the eastern SIS stock of red sea bream has increased since the 1980s. In addition, pike conger does not ORCID distribute in the inner areas of SIS in winter (Okazaki, Ueta, & Hamano, Masayuki Yamamoto https://orcid.org/0000-0002-9302-5623 2012), and red spotted grouper does not migrate seasonally (Sekiya, 1994). Therefore, the mechanisms of resource increase for the two species might differ from that for the red sea bream. REFERENCES The catch in February and March was abnormally high in the low water temperature year of 1977 and 1984 (Figure 4). Red sea bream Abo, K., Akiyama, S., Harada, K., Nakachi, Y., Hayashi, K., Murata, K., … Tokumitsu, S. (2015). Long‐term variations of sea conditions in the has reported to become lethargic and almost immobile floating on Seto Inland Sea. In K. Abo, K. Abe, M. Nakagawa, & M. Tsujino (Eds.), water surface in very low temperature of <8°C (Ueta, 2011). It is The results of oceanographic observation research during the period reported that in 1984, many floating red sea bream were observed of 40 years in the Seto Inland Sea, Japan (pp. 242–256). Hatsukaichi, in Akashi Straight and Naruto Straight (Shimamoto, 2006). In the Japan: National Research Institute of Fisheries and Environmental of Inland Sea. (in Japanese). , large catches of sole Solea solea were observed in early Akiyama, S. (2015). Costal water off Osaka Prefecture: Osaka Bay. In 1963 (Woodhead, 1964) and 1996 (Horwood & Miller, 1998) when K. Abo, K. Abe, M. Nakagawa, & M. Tsujino (Eds.), The results of there was an exceptionally cold winter. Woodhead (1964) consid‐ oceanographic observation research during the period of 40 years in ered that these abnormal catches at low water temperatures were the Seto Inland Sea, Japan (pp. 45–61). Hatsukaichi, Japan: National Research Institute of Fisheries and Environmental of Inland Sea. due to increased vulnerability of the fish to fishing. The large catches (in Japanese). in February and March of 1977 and 1984 can also be explained by Alheit, J., & Hagen, E. (1997). Long‐term climate forcing of European abnormal cold water temperature. herring and sardine populations. Fisheries Oceanography, 6, 130–139. Our study suggests that expansion of the distribution area of the https://doi.org/10.1111/j.1365​ -2419.2007.00435.x Alheit, J., Pohlmann, T., Casini, M., Greve, W., Hinrichs, R., Mathis, M., eastern SIS stock for red sea bream during winter and subsequently … Wagner, C. (2012). Climate variability drives anchovies and sar‐ expansion of spawning grounds by warm winter since the late 1980s dines into the North and Baltic . Progress in Oceanography, 96, greatly contributed to the catch and biomass. The increase in water 128–139. https://doi.org/10.1016/j.pocean.2011.11.015​ temperature due to global warming is greatly related not only to the Azeta, M., Ikemoto, R., & Azuma, M. (1980). Distribution and growth of distribution of fishes but also to the fluctuation of biomass. Such demersal 0‐group red sea bream, Pagrus major, in Shijiki Bay. Bulletin of the Seikai Regional Fisheries Research Laboratory, 54, 259–278. (in information will be useful for understanding the mechanisms of fish‐ Japanese with English abstract). eries resource change caused by global warming. Barbeaux, S. J., & Hollowed, A. B. (2018). Ontogeny matters: Climate variability and effects on fish distribution in the eastern . Fisheries Oceanography, 27, 1–15. https​://doi.org/10.1111/ ACKNOWLEDGEMENTS fog.12229​ Brander, K. M. (2007). Global fish production and climate change. The authors would like to thank all of those who have measured water Proceedings of the National Academy of Sciences of the USA, 104, temperature and gathered catch data in SIS between 1972 and 2010. 19709–19714. https://doi.org/10.1073/pnas.07020​ 59104​ ​ This research was conducted by a grant from Japan Fisheries Agency. Craig, J. F. (2000). Percid fishes, systematics ecology and exploitation. Oxford, UK: Blackwell, 370 pp. Eriksen, E., Ingvaldsen, R. B., Nedreaas, K., & Prozorkevich, D. (2015). The effect of recent warming on polar cod and beaked redfish juveniles in CONFLICT OF INTEREST the . Regional Studies in Marine Science, 2, 105–112. https​ The authors have no conflict of interest to declare. ://doi.org/10.1016/j.rsma.2015.09.001 8 | YAMAMOTO et al.

Fisheries Agency and Fisheries Research and Education Agency of Japan Lloyd, P., Plaganyi, E. E., Weeks, S. J., Magno‐Canto, M., & Plaganyi, (2017). Marine fisheries stock assessment and evaluation for Japanese G. (2012). Ocean warming alters species abundance patterns waters (fiscal year 2016/2107), 2054 pp. (in Japanese). and increases species diversity in an African sub‐tropical reef‐ Fisheries Development Council of the Seto Inland Sea (1996). Annual fish community. Fisheries Oceanography, 21, 78–94. https​://doi. variation in catch of major stock in each water of Seto Inland Sea, 107 org/10.1111/j.1365-2419.2011.00610.x pp. (in Japanese). Masuda, R. (2008). Seasonal and interannual variation of subtidal fish Fodrie, F. J., Heck, K., Powers, S., Graham, W. G., & Robinson, K. L. (2010). assemblages in Wakasa Bay with reference to the warming trend in Climate‐related, decadal‐scale assemblage changes of seagrass‐as‐ the Sea of Japan. Environmental Biology of Fishes, 82, 387–399. https​ sociated fishes in the northern Gulf of Mexico. Global Change Biology, ://doi.org/10.1007/s10641-007-9300-z 16, 48–59. https​://doi.org/10.1111/j.1365-2486.2009.01889.x Masuda, R., & Tsukamoto, K. (1998). Stock enhancement in Japan: Review Fortibuoni, T., Aldighieri, F., Giovanardi, O., Pranovi, F., & Zucchetta, and perspective. Bulletin of Marine Science, 62, 337–358. M. (2015). Climate impact on Italian fisheries (). Masui, T. (2015). Coastal water off Kagawa Prefecture: Harima‐nada, Regional Environmental Change, 15, 931–937. https​://doi.org/10.1007/ Bisan‐seto and Hiuchi‐nada. In K. Abo, K. Abe, M. Nakagawa, & s10113-015-0781-6 M. Tsujino (Eds.), The results of oceanographic observation research Hamilton, L. C., & Haedrich, R. L. (1999). Ecological and population during the period of 40 years in the Seto Inland Sea, Japan (pp. 95–131). changes in fishing communities of the North Atlantic arc. Polar Hatsukaichi, Japan: National Research Institute of Fisheries and Research, 18, 383–388. https​://doi.org/10.1111/j.1751-8369.1999. Environmental of Inland Sea. (in Japanese). tb003​18.x Mavruk, S., Bengiil, F., Yeldan, H., Mamasorli, M., & Avsar, D. (2017). The Hare, J. A., & Able, K. W. (2007). Mechanistic links between cli‐ trend of lessepsian fish populations with an emphasis on tempera‐ mate and fisheries along the east coast of the United States: ture variations in Iskenderun Bay, the Northeastern Mediterranean. Explaining population outbursts of Atlantic croaker (Micropogonias Fisheries Oceanography, 26, 542–554. https​://doi.org/10.1111/ undulatus). Fisheries Oceanography, 16, 31–45. https​://doi. fog.12215​ org/10.1111/j.1365-2419.2006.00407.x Ministry of the Environment (2016). Study on distribution of algae and Hayashi, M. (2002). Sparidae. In T. Nakabo (Ed.), Fishes of Japan with tidal flats in the Seto Inland Sea (eastern waters). Retrieved from http:// pictorial keys to the species, English ed. (pp. 856–859). , Japan: www.env.go.jp/press/​files/​jp/104209.pdf. Tokai Univ. Press. Moyle, P. B., & Cech, J. J. Jr (2000). Fishes, an introduction to ichthyology, Henderson, P. A., & Henderson, R. C. (2017). Population regulation in 4th ed. Upper Saddle River, NJ: Prentice Hall, 612 pp. a changing environment: Long‐term changes in growth, condition Mueter, F. J., Peterman, R. M., & Pyper, B. J. (2002). Opposite effects of and survival of sprat, Sprattus sprattus L. in the Bristol Channel, ocean temperature on survival rates of 120 stocks of Pacific salmon UK. Journal of Sea Research, 120, 24–34. https​://doi.org/10.1016/j. (Oncorhynchus spp.) in northern and southern areas. Canadian seares.2016.11.003 Journal of Fisheries and Aquatic Sciences, 59, 456–463. https​://doi. Hermant, M., Lobry, J., Bonhommeau, S., Poulard, J., & Le Pape, O. org/10.1139/F02-020 (2010). Impact of warming on abundance and occurrence of flatfish Nagai, T. (1995). Stock status of the red sea bream in the Seto Inland populations in the (France). Journal of Sea Research, 64, Sea. Nippon Suisan Gakkaishi, 61, 679–683. https​://doi.org/10.2331/ 45–53. https://doi.org/10.1016/j.seares.2009.07.001​ suisan.61.679. (in Japanese with English abstract). Horwood, J. W., & Miller, R. S. (1998). Cold induced abnormal catches of Nakachi, Y. (2015). Coastal water off Wakayama Prefecture: Kii Channel. sole. Journal of the Marine Biological Association of the United Kingdom, In K. Abo, K. Abe, M. Nakagawa, & M. Tsujino (Eds.), The results of 78, 345–347. https​://doi.org/10.1017/S0025​31540​0040133 oceanographic observation research during the period of 40 years in Japan Fisheries Agency (2016). Annual statistics of fishery and aquaculture the Seto Inland Sea, Japan (pp. 1–15). Hatsukaichi, Japan: National production in Japan. Retrieved from http://www.e-stat.go.jp/SG1/ Research Institute of Fisheries and Environmental of Inland Sea. (in estat/​GL080​20101.do?_toGL0​80201​01_&tstat​Code=00000​10151​ Japanese). 74&reque​stSen​der=dsearch. (in Japanese). Oh, T., Sakuramoto, K., & Hasegawa, S. (2002). On the relationship be‐ Kagawa Branch Office, Chugoku and Shikoku Regional Agricultural tween water temperature and catch fluctuations of walleye pollock Administration Office, Ministry of Agriculture, Forestry and Fisheries Theragra chalcogramma in the northern waters of the Japan Sea. (1974–1984). Annual Statistics of Fishery and Aquaculture Production in Nippon Suisan Gakkaishi, 68, 866–873. https​://doi.org/10.2331/su‐ Kagawa Prefecture. (in Japanese). isan.68.866. (in Japanese with English abstract). Kuwahara, H., Akeda, S., Kobayashi, S., Takeshita, A., Yamashita, Y., & Okazaki, T., Ueta, Y., & Hamano, T. (2012). Distribution and migration Kido, K. (2006). Predicted changes on the distribution areas of ma‐ of daggertooth pike‐conger Muraenesox cinereus in the eastern rine organisms around Japan caused by the global warming. Global Seto Inland Sea, Japan estimated by mark and recapture experiment. Environmental Research, 10, 189–199. Nippon Suisan Gakkaishi, 78, 913–921. https​://doi.org/10.2331/su‐ Lacoue‐Labarthe, T., Nunes, P. A. L. D., Ziveri, P., Cinar, M., Gazeau, F., isan.78.913. (in Japanese with English abstract). Hall‐Spencer, J. M., … Turley, C. (2016). Impacts of ocean acidification Osaka Branch Office, Kinki Regional Agricultural Administration Office, in a warming Mediterranean Sea: An overview. Regional Studies in Ministry of Agriculture, Forestry and Fisheries (1974–1985). Annual Marine Science, 5, 1–11. https​://doi.org/10.1016/j.rsma.2015.12.005 statistics of fishery and aquaculture production in Osaka Prefecture. (in Landa, C. S., Ottersen, G., Sundby, S., Dingør, G. E., & Stiansen, J. (2014). Japanese). Recruitment, distribution boundary and habitat temperature of an Perry, A. L., Low, P. J., Ellis, J. R., & Reynolds, J. D. (2005). Climate change arcto‐boreal gadoid in a climatically changing environment: A case and distribution shifts in marine fishes. Science, 308, 1912–1915. study on Northeast haddock (Melanogrammus aeglefinus). https://doi.org/10.1126/scien​ ce.1111322​ Fisheries Oceanography, 23, 506–520. https​://doi.org/10.1111/ Sabatés, A., Martín, P., Llopet, J., & Raya, V. (2006). Sea warming and fish fog.12085​ distribution: The case of the small pelagic fish, Sardinella aurita, in the Last, P. R., White, W. T., Gledhill, D. C., Hobday, A. J., Brown, R., Edgar, G. western Mediterranean. Global Change Biology, 12, 2209–2219. https​ J., & Pecl, G. (2011). Long‐term shifts in abundance and distribution ://doi.org/10.1111/j.1365-2486.2006.01246.x of a temperature fish fauna: A response to climate change and fish‐ Sakaguchi, H., & Hamaguchi, A. (1979). Physiological studies on cultured ing practices. Global Ecology and Biogeography, 20, 58–72. https​://doi. red sea bream–I, Seasonal variation of chemical constituents in org/10.1111/j.1466-8238.2010.00575.x plasma, hepatopancreas and other viscera. Nippon Suisan Gakkaishi, YAMAMOTO et al. | 9

45, 443–448. https​://doi.org/10.2331/suisan.45.443. (in Japanese Ueta, Y. (2011). An appearance of floating red sea bream under low water with English abstract). temperature in Naruto channel in winter. News of Tokushima Fisheries Sakaji, H., & Yamamoto, K. (2017). Stock assessment of red sea bream in Research Center, 78, 9–10. (in Japanese). the eastern Seto Inland Sea. In Fisheries Agency and Japan Fisheries Villegas‐Hernández, H., Lloret, J., & Muñoz, M. (2015). Reproduction, Research Agency (Eds.), Fishery resource assessment in waters off condition and abundance of the Mediterranean bluefish (Pomatomus Japan (pp. 1299–1330). Yokohama, Japan: Japan Fisheries Research saltatrix) in the context of sea warming. Fisheries Oceanography, 24, Agency. (in Japanese). 42–56. https://doi.org/10.1111/fog.12091​ ​ Sekiya, Y. (1994). Results of release of tagging red spotted grouper Watanabe, Y. (1998). Resurgence and decline of the Japanese sardine Epinephelus akaara and future issues. Saibai, 70, 13–17. (in Japanese). population. In L. A. Fuiman, & R. G. Werner (Eds.), Fishery science (pp. Shelton, A. O., & Mangel, M. (2011). Fluctuations of fish populations and 243–257). Oxford, UK: Blackwell. the magnifying effects of fishing. Proceedings of the National Academy Watari, S., Murata, M., Baba, T., Ishitani, M., Mishiro, K., & Uchida, Y. of Sciences of the USA, 108, 7075–7080. https​://doi.org/10.1073/ (2014). Fisheries resource management of the daggertooth pike con‐ pnas.1100334108​ ​ ger, Muraenesox cinereus, using exiting limited datasets in the west‐ Shimamoto, N. (2006). Stock management of red sea bream in the Eastern ern Seto Inland Sea, Japan. Fisheries Management and Ecology, 21, Seto Inland Sea, Japan. Tokyo, Japan: Japan Fisheries Resource 470–479. abs/10.1111/fme.12096​ Conservation Association, 1330 pp. (in Japanese). Woo, N. Y. S., & Fung, A. C. Y. (1980). Studies on the biology of the red Shinoda, A., & Tsukamoto, K. (2010). Environment. In K. Tsukamoto (Ed.), sea bream Chysophrys major. I. temperature tolerance. Marine Ecology An introduction to fish ecology (pp. 1–11). Tokyo, Japan: Koseisha‐ko‐ Progress Serious, 3, 121–124. seikaku. (in Japanese). Woodhead, P. M. J. (1964). Changes in the behavior of the sole, Solea vul- Shoji, J., Sakiyama, K., Hori, M., Yoshida, G., & Hamaguchi, M. (2007). garis, during cold winters, and the relation between the winter catch Seagrass habitat reduces vulnerability of red sea bream Pagrus major and sea temperatures. Helgoland Marine Research, 10, 328–342. juveniles to piscivorous fish predator. Fisheries Science, 73, 1281– Yamamoto, K., & Sakaji, H. (2017). Stock assessment of red sea bream 1285. https://doi.org/10.1111/j.1444​ -2906.2007.01466.x in the central and western Seto Inland Sea. In Fisheries Agency and Sims, D. W., Wearmouth, V. J., Genner, M. J., Southward, A. J., & Hawkins, Japan Fisheries Research Agency (Eds.), Fishery resource assess- S. J. (2004). Low‐temperature‐driven early spawning migration of a ment in waters off Japan (pp. 1331–1367). Yokohama, Japan: Japan temperate marine fish. Journal of Animal Ecology, 73, 333–341. https​ Fisheries Research Agency. (in Japanese). ://doi.org/10.1111/j.0021-8790.2004.00810.x Yamamoto, M. (2003). The long-term variations in water temperature Tadokoro, K., Sugimoto, T., & Kishi, M. (2008). The effects of anthropo‐ and salinity in Bisan-Seto, central Seto Inland Sea. Bulletin of the genic global warming on the marine ecosystem. Umi no Kenkyu, 17, Japan Society of Fisheries Oceanogrphy, 67, 163–167. (in Japanese with 404–420. (in Japanese with English abstract). Englishe abstract). Takamatsu Municipal Wholesale Market (1984–2011). Annual report of Yamamoto, M. (2012). Annual changes in catch and unit price of major Takamatsu Municipal Wholesale Markets. (in Japanese). fishes and shellfish in the Seto Inland Sea off Kagawa Prefecture, Takashima, K. (2016). Stock enhancement of redspotted grouper from 1970 to 2006. Bulletin Kagawa Prefectural Fisheries Experimental Epinephelus akaara called “Akoh” in . News of Ehime Station, 13, 19–26. (in Japanese). Research Institute of Agriculture, Forest and Fisheries, 9, 9. (in Japanese). Yamamoto, M., Omi, H., & Miyahara, K. (2013). Long‐term variation in Takasuka, A., Oozeki, Y., & Aoki, I. (2007). Optimal growth temperature catch of important stocks in the Seto Inland Sea, Japan. Bulletin of the hypothesis: Why do anchovy flourish and sardine collapse or vice Japan Society of Fisheries Oceanography, 77, 308–311. (in Japanese versa under the same ocean regime? Canadian Journal of Fisheries with English abstract). and Aquatic Sciences, 64, 768–776. https​://doi.org/10.1139/ Yamashita, Y. (2007). Discussion of revival of fishery resources in the f07-052 Seto Inland Sea. In Research Institute for Seto Inland Sea (Ed.), The Takeda, T., Tsuji, T., & Itazawa, Y. (1989) Facilitation of housing capac‐ Seto Inland Sea to “Satoumi” (pp. 17–28). Tokyo, Japan: Koseisha‐ko‐ ity for red porgy by drop in water temperature. Nippon Suisan seikaku. (in Japanese). Gakkaishi, 55, 1011–1015. https​://doi.org/10.2331/suisan.55.1011. Zenitani, H., Onishi, Y., & Obata, Y. (2014). Spawning grounds of red sea (in Japanese with English abstract). bream in the east Seto Inland Sea. Fisheries Science, 80, 499–504. Takeoka, H. (2002). Progress in Seto Inland sea research. Journal https​://doi.org/10.1007/s12562-014-0710-5 of Oceanography, 58, 93–107. https​://doi.org/10.1023/A:10158​ 28818202 Tarutani, K. (2005). Seasonal variations and long‐term variation charac‐ How to cite this article: Yamamoto M, Omi H, Yasue N, Kasai teristic of environmental factor in the Seto Inland Sea. In S. Oka, & A. Correlation of changes in seasonal distribution and catch K. Tarutani (Eds.), The results of oceanographic observation research during the period of 30 years in the Seto Inland Sea, Japan (pp. 179– of red sea bream Pagrus major with winter temperature in the 190). Hatsukaichi, Japan: National Research Institute of Fisheries and eastern Seto Inland Sea, Japan (1972–2010). Fish Oceanogr. Environmental of Inland Sea. (in Japanese). 2019;00:1–9. https://doi.org/10.1111/fog.12432​ ​ Teixeira, C. M., Gamito, R., Leitao, F., Cabrãl, H. N., Erzini, K., & Costa, M. J. (2014). Trends in landings of fish species potentially affected by cli‐ mate change in Portuguese fisheries. Regional Environmental Change, 14, 657–669. https​://doi.org/10.1007/s10113-013-0524-5