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Reduction in size-at-age of black sea bream (Acanthopagrus schlegelii) following intensive releases of cultured juveniles in Hiroshima Bay, Japan
Fisheries Research 99 (2009) 130–133
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Fisheries Research journal homepage: www.elsevier.com/locate/fishres
Short communication
Reduction in size-at-age of black sea bream (Acanthopagrus schlegelii) following intensive releases of cultured juveniles in Hiroshima Bay, Japan Enrique Blanco Gonzalez a , Tomoya Murakami b , Takashi Yoneji b , Kazuya Nagasawa a , Tetsuya Umino a,∗ a b
Laboratory of Aquaculture, Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima 739-8528, Japan Prefectural Technology Research Institute Fisheries and Ocean Technology Center, Kure Hiroshima 737-1207, Japan
a r t i c l e
i n f o
Article history: Received 10 October 2008 Received in revised form 22 April 2009 Accepted 23 April 2009 Keywords: Size-at-age Black sea bream Acanthopagrus schlegelii Stock enhancement Carrying capacity Hiroshima Bay
a b s t r a c t More than 20 million black sea bream (Acanthopagrus schlegelii) juveniles have been released in Hiroshima Bay since stock enhancement of the fishery began in the early 1980s. The majority (90%) of the black sea bream harvest occurs between April and June. Catch per unit effort (CPUE) increased substantially following the most intensive releases (1985–1996). However, the size-at-age in 2000 was significantly lower than in 1983. In addition, by 2000 many of the released fish had matured as females, changing the sex ratio of this protandrous hermaphrodite. These changes are thought to be related to the intensive release of hatchery-reared juveniles in the bay, although there is also evidence to suggest that a lower market price for the species, resulting in reduced fishing effort, also contributed to these effects. Our results highlight the potential negative impact of intensive stock enhancement on the population structure of a local fishery. They also emphasise the importance of assessing the status of the stock, and monitoring the carrying capacity of the habitat for the target species, to determine how many, if any, cultured juveniles should be released to achieve management objectives. © 2009 Elsevier B.V. All rights reserved.
1. Introduction Intensive stock enhancement programs have been implemented throughout the Japanese archipelago to restore and/or increase the harvestable stocks of commercially valuable marine finfish. However, reports of success are limited (Fushimi, 2001; Kitada and Kishano, 2006). One of the target species is the black sea bream (Acanthopagrus schlegelii), which has been stocked into Hiroshima Bay in the western part of the Seto Inland Sea of Japan (Fig. 1) since the early 1980s. Stock enhancement program of black sea bream was initiated when annual landings dropped below 200 tonnes. More than one million juveniles were released each year between 1985 and 1996 (Blanco Gonzalez et al., 2008a). Subsequently, total harvest increased to >200 tonnes per year and Hiroshima Bay is now the primary fishing ground for this species in Japan, accounting for 10% of total domestic landings. The recovery of the black sea bream population is generally attributed to stock enhancement (Umino et al., 1999; Nakagawa et al., 2000; Blanco Gonzalez et al., 2008a): the cultured juveniles appear to acclimatize rapidly to the natural con-
∗ Corresponding author. Tel.: +81 824 24 7989; fax: +81 824 24 7989. E-mail address: [email protected] (T. Umino). 0165-7836/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.fishres.2009.04.013
ditions and grow at the same rate as wild fish within a few months of release (Yamashita et al., 1997; Umino et al., 1999; Nakagawa et al., 2000; Jeong et al., 2007). Despite the apparent success of the stock enhancement program for black sea bream, several key issues remain unclear. In particular, the extent to which survival of released juveniles depends on food availability, the carrying capacity of the ecosystem, oceanographic conditions, and intra- and inter-specific interactions (Gaston et al., 1997; Bevers and Flather, 1999; Shepherd and Litvak, 2004; Hattori et al., 2007). In addition, captive breeding may lead to a reduction of fitness which affects the breeding success and effective population size (Fleming and Pettersson, 2001; Ford, 2002; Araki et al., 2007). Although the contribution of cultured black sea bream to spawning biomass has not resulted in undue deleterious effects on genetic diversity (Blanco Gonzalez et al., 2008b), little is known regarding the effect of releases of hatchery-reared juveniles on the dynamics of the natural population. This needs to be examined because the massive releases of chum salmon (Oncorhynchus keta) juveniles (>2 billion juveniles per year) have truncated the age and size structure of natural populations (Ishida et al., 1993; Kaeriyama, 1998; Morita et al., 2001). A similar phenomenon was reported following the accidental escape of a large number of gilthead sea bream (Sparus aurata) from aquaculture operations (Dimitrou et al., 2007). Recently, the importance of adopting a multi-disciplinary approach to manage stock enhancement programs, integrating
E. Blanco Gonzalez et al. / Fisheries Research 99 (2009) 130–133
131
Table 1 Monthly landings (kg) of black sea bream collected in Minou in 1982, 1983, 1999, and 2000. Month January February March April May June July August September October November December Total April–June/total (%)
1982
1983
1999
2000
64 79 43 588 8,661 7,098 137 38 219 338 173 133
68 63 73 971 6,773 5,064 111 61 398 528 247 193
537 993 1,424 15,365 24,848 14,565 1,131 84 340 430 268 324
625 314 347 12,167 39,926 17,358 504 42 308 272 138 308
17,571
14,550
60,309
72,308
93.0
88.0
90.8
96.0
Fig. 1. Map of Hiroshima Bay.
biological, social, economical and institutional arrangements to succeed (Bell et al., 2008; Lorenzen, 2008; Tringali et al., 2008), has been emphasised. Here, we help provide vital biological information for such an integrated approach by describing features of the age structure and sex ratio of black sea beam that are consistent with densitydependent effects due to excessive releases of hatchery-reared juveniles. 2. Materials and methods To evaluate the impact of the releases of cultured juveniles on the age and size structure of black sea bream, we analyzed two sets of data. The first set was collected at the beginning of the stock enhancement program in Hiroshima Bay (1982 and 1983). The second was collected following the largest releases (1999 and 2000). All data were collected at the Hiroshima Prefectural Technology Research Institute Fisheries and Ocean Technologies Center (HPTRIFOTC), Hiroshima, Japan. Catch per unit effort (CPUE) was calculated as kg of black sea bream caught per day. The analysis of the CPUE was based on daily reports of landings provided by the commercial fleet holding a “gochi ami” net license in Minou fish market (see Fig. 1) during the study period. This type of bottom trawl has a mesh size of 91 mm and targets black sea bream accounting for ∼10% of the total commercial catch of the species in Hiroshima Bay. The use of the gochi ami nets occurs between April and June, which overlaps with the black sea bream spawning season in Hiroshima Bay. In contrast to other types of fishing gear, the use of this net requires special permission. A limited number of licenses were issued (34 in 1983 and 24 in 2000) and restricted to Minou, minimizing possible bias due to fishing gear, sampling period, or location among the years studied. In addition, records of age (by scale-reading), fork length (FL), and sex were taken from 153 and 161 specimens collected in Minou in 1983 and 2000, respectively, during sampling surveys conducted by the staff at the HPTRIFOTC on board a commercial fishing vessel. The von Bertalanffy growth curve (VBGC) parameters were estimated using the Microsoft Excel Solver routine (Microsoft Corporation, 2000). Data for male and female fish were pooled. Initially, the parameters were fitted to the data using the non-linear leastsquares approach. Later, the results were used to generate the initial value for the maximum likelihood method (MLM).
Fig. 2. Monthly CPUE for black sea bream collected by gochi ami in Minou in 1982, 1983, 1999 and 2000.
in Table 1. The landings for this species between April and June represent ∼90% of the annual catch. The CPUE values (mean and S.D.) for black sea bream caught by gochi ami in Minou are given in Fig. 2. CPUE was highest in May in all 4 years. In 1982 and 1983, prior to the intensive stocking, the CPUE in Hiroshima Bay remained low. In 1999 and 2000, the CPUE increased 10-fold. Although black sea bream caught in 1983 had a wider size class distribution than that in 2000 (Fig. 3), pairwise comparison of the mean size-at-age of fish collected in 1983 and 2000 revealed significant differences for the most abundant age classes (3–6 years) (Table 2). The VBGC parameter estimates were L∞ = 38.70 and 46.32 cm in 1983 and 2000, respectively. The fish collected in 1983 consisted of 62.1% males and 29.4% females (with 3.9% hermaphrodites and 4.6% individuals of
3. Results Monthly landings of black sea bream before (1982 and 1983) and after (1999 and 2000) intensive stock enhancement are given
Fig. 3. Number of black sea bream by size class collected in Minou in 1983 and 2000. FL = fork length.
132
E. Blanco Gonzalez et al. / Fisheries Research 99 (2009) 130–133
Fig. 4. Sex composition by age of black sea bream collected in Minou in 1983 and 2000.
Table 2 Size-at-age of black sea bream collected in Minou in 1983 and 2000. n = sample size, FL = fork length. Age
1983 n
3 4* 5* 6* 7*
52 22 22 9 5
Total *
2000 FL (cm) 26.5 30.1 31.8 32.9 35.0
± ± ± ± ±
n 1.8 2.5 2.8 3.2 3.1
110
FL (cm) 15 57 27 35 6
27.1 27.8 29.0 30.8 31.3
± ± ± ± ±
2.3 1.9 2.7 2.4 1.4
140
p < 0.05 (using the Mann–Whitney’s U-test).
undetermined-sex). In 2000, 32.3% were males and 67.7% females. In 1983, males were more abundant than females among age classes 4–6, whereas females comprised 65–70% of the specimens for age classes 4–6 in 2000 (Fig. 3). The small number of 7-year-old fish examined (5 and 6 individuals in 1983 and 2000, respectively) may not be representative of their contribution to the natural stock, thus conclusions cannot be drawn regarding this year class. 4. Discussion The effectiveness of stock enhancement programs has traditionally been assessed based on recoveries of the target species in landings (Masuda and Tsukamoto, 1998; Fushimi, 2001). Using this criterion, the stock enhancement program for black sea bream in Hiroshima Bay has been a success (Umino et al., 1999; Jeong et al., 2003, 2007; Blanco Gonzalez et al., 2008a). Three lines of evidence suggest that the release of >20 million juveniles in the bay since the early 1980 have helped to increase yields. First, 4 years after the initial release, hatchery-reared fish accounted for 13% of the stock in the wild. Second, released juveniles are known to have reached maturity (Blanco Gonzalez et al., 2008b). Third, CPUE increased significantly following releases during a period when CPUE for other major species in the Seto Inland Sea continued to decline (Nagai, 2003). Other factors may also have contributed to the recovery of the fishery. At the beginning of the stock enhancement program, black sea bream were a high-priced species subjected to great fishing pressure. Later, the wholesale price decreased drastically. This resulted in lower fishing pressure which may also have contributed to the recovery of the fishery (Blanco Gonzalez et al., 2008a). Caution is needed about interpreting increases in population size as ‘success’ if the carrying capacity of the habitat for the target species has been exceeded. Our data suggest that the combined effects of releases of cultured juveniles and reduced fishing effort (represented by the reduction in netting licenses and increased CPUE) resulted in reduced size-at-age in black sea bream due to density-dependent processes. This phenomenon was also suggested for stocked chum salmon in Japan (Ishida et al., 1993; Kaeriyama, 1998; Morita et al., 2001).
Further support for the hypothesis that the carrying capacity for black sea bream was exceeded in 2000 comes from the sex ratio. The black sea bream is a protandrous hermaphrodite, maturing as a male first, and then progressing to a mature female at age 3, around 22 cm in body length in the Seto Inland Sea off Hiroshima (Kinoshita, 1936). It appears that by 2000, many of the released fish, and those no longer as vulnerable to capture due to lower fishing effort, had matured as females (see Fig. 4). We conclude that the large number of hatchery-reared black sea bream juveniles released in Hiroshima Bay appears to have increased the stock biomass. This has caused density-dependent decreases in size-at-age and a shift in the sex ratio. Our findings highlight the potential negative effects of intensive releases of cultured juvenile fish. We emphasise the need to assess the status of the stock, and monitor the carrying capacity of the habitat of the target species, to determine how many, if any, cultured juveniles need to be released to achieve management objectives. Acknowledgements The authors are very grateful to the gochi ami fleet in Hiroshima Bay for the daily records of catches. We also appreciate the suggestions from two anonymous reviewers whose recommendations have substantially contributed to improve the quality of the paper. This study was partly supported by a Grant-in-Aid for Scientific Research (C) from the Japan Society for the Promotion of Science (JSPS) to T.U. (Nos. 14560152 & 19580205). References Araki, H., Cooper, B., Blouin, M.S., 2007. Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318, 100–103. Bell, J.D., Leber, K.M., Blankenship, L., Loneragan, N.R., Masuda, R., 2008. A new era for restocking, stock enhancement and sea ranching of coastal fisheries resources. Rev. Fish. Sci. 16, 1–9. Bevers, M., Flather, C.H., 1999. The distribution and abundance of populations limited at multiple spatial scales. J. Anim. Ecol. 68, 976–987. Blanco Gonzalez, E., Umino, T., Nagasawa, K., 2008a. Stock enhancement program for black sea bream, Acanthopagrus schlegelii (Bleeker), in Hiroshima Bay, Japan: a review. Aquacult. Res. 39, 1307–1315. Blanco Gonzalez, E., Nagasawa, K., Umino, T., 2008b. Stock enhancement program for black sea bream (Acanthopagrus schlegelii) in Hiroshima Bay: monitoring the genetic effects. Aquaculture 276, 36–43. Dimitrou, E., Katselis, G., Moutopoulos, D.K., Akovitiotis, C., Koutsikopoulos, C., 2007. Possible influence of reared gilthead sea bream (Sparua aurata, L.) on wild stocks in the area of the Messolonghi lagoon. Aquacult. Res. 38, 398–408. Fleming, I.A., Pettersson, E., 2001. The ability of released, hatchery salmonids to breed and contribute to the natural productivity of wild populations. Nordic J. Freshwater Res. 75, 71–98. Ford, M.J., 2002. Selection in captivity during supportive breeding may reduce fitness in the wild. Conserv. Biol. 16, 815–825. Fushimi, H., 2001. Production of juvenile marine finfish for stock enhancement in Japan. Aquaculture 200, 33–53. Gaston, K.J., Blackburn, T.M., Lawton, J.H., 1997. Inter-specific abundance–range size relationships: an appraisal of mechanisms. J. Anim. Ecol. 66, 579–601. Hattori, T., Narimatsu, Y., Ito, M., Ueda, Y., Fujiwara, K., Kitagawa, D., 2007. Growth changes in bighand thornyhead Sebastolobus macrochir off the Pacific coast of northern Honshu, Japan. Fish. Sci. 73, 341–347.
E. Blanco Gonzalez et al. / Fisheries Research 99 (2009) 130–133 Ishida, Y., Ito, S., Kaeriyama, M., McKinnell, S., Nagasawa, K., 1993. Recent changes in age and size of chum salmon (Onchorhynchus keta) in the North Pacific Ocean and possible causes. Can. J. Fish. Aquat. Sci. 50, 290–295. Jeong, D.S., Blanco Gonzalez, E., Morishima, K., Arai, K., Umino, T., 2007. Parentage assignment of stocked black sea bream Acanthopagrus schlegelii in Hiroshima Bay using microsatellite DNA markers. Fish. Sci. 73, 823–830. Jeong, D.S., Umino, T., Kuroda, K., Hayashi, M., Nakagawa, H., Kang, J.C., Morishima, K., Arai, K., 2003. Genetic divergence and population structure of black sea bream Acanthopagrus schlegeli inferred from microsatellite analysis. Fish. Sci. 69, 896–902. Kaeriyama, M., 1998. Dynamics of a chum salmon, Oncorhynchus keta, population released from Hokkaido in Japan. N. Pac. Anadr. Fish Comm. Bull. No. 1, 90–102. Kinoshita, Y., 1936. On the conversion of sex in Sparus longispinis (Temminck & Schlegel), J. Sc. Hiroshima Univ. Ser. B. Div. 1. 4, Art. 5. Kitada, S., Kishano, H., 2006. Lessons learned from Japanese marine finfish stock enhancement programmes. Fish. Res. 80, 101–112. Lorenzen, K., 2008. Understanding and managing enhancement fisheries systems. Rev. Fish. Sci. 16, 10–23. Masuda, R., Tsukamoto, K., 1998. Stock enhancement in Japan: review and perspective. Bull. Mar. Sci. 62, 337–358.
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Morita, S.H., Morita, K., Sakano, H., 2001. Growth of chum salmon (Oncorhynchus keta) correlated with sea-surface salinity in the North Pacific. ICES J. Mar. Sci. 58, 1335–1339. Nagai, T., 2003. Recovery of fish stocks in the Seto Inland Sea. Mar. Pollut. Bull. 47, 126–131. Nakagawa, H., Umino, T., Hayashi, M., Sasaki, T., Okada, K., 2000. Changes in biochemical composition of black sea bream released at 20 mm size in Daio Bay, Hiroshima. Suisanzoshoku 48, 643–648. Shepherd, T.D., Litvak, M.K., 2004. Density-dependent habitat selection and the ideal free distribution in marine fish spatial dynamics: considerations and cautions. Fish Fish. 5, 141–152. Tringali, M.D., Leber, K.M., Halstead, W.G., McMichael, R., O’Hop, J., Winner, B., Cody, R., Young, C., Neidig, C., Wolfe, H., Forstchen, A., Barbieri, L., 2008. Marine stock enhancement in Florida: a multi-disciplinary, stakeholder-supported, accountability-based approach. Rev. Fish. Sci. 16, 51–57. Umino, T., Hayashi, M., Miyatake, J., Nakayama, K., Sasaki, T., Okada, K., Nakagawa, H., 1999. Significance of release of black sea bream at 20-mm size on stock enhancement in Daiô Bay, Hiroshima. Suisanzoshoku 47, 337–342. Yamashita, H., Umino, T., Nakahara, S., Okada, K., Nakagawa, H., 1997. Changes in some properties of black sea bream released into the Daio Bay. Fish. Sci. 63, 267–271.
Contents lists available at ScienceDirect
Fisheries Research journal homepage: www.elsevier.com/locate/fishres
Short communication
Reduction in size-at-age of black sea bream (Acanthopagrus schlegelii) following intensive releases of cultured juveniles in Hiroshima Bay, Japan Enrique Blanco Gonzalez a , Tomoya Murakami b , Takashi Yoneji b , Kazuya Nagasawa a , Tetsuya Umino a,∗ a b
Laboratory of Aquaculture, Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima 739-8528, Japan Prefectural Technology Research Institute Fisheries and Ocean Technology Center, Kure Hiroshima 737-1207, Japan
a r t i c l e
i n f o
Article history: Received 10 October 2008 Received in revised form 22 April 2009 Accepted 23 April 2009 Keywords: Size-at-age Black sea bream Acanthopagrus schlegelii Stock enhancement Carrying capacity Hiroshima Bay
a b s t r a c t More than 20 million black sea bream (Acanthopagrus schlegelii) juveniles have been released in Hiroshima Bay since stock enhancement of the fishery began in the early 1980s. The majority (90%) of the black sea bream harvest occurs between April and June. Catch per unit effort (CPUE) increased substantially following the most intensive releases (1985–1996). However, the size-at-age in 2000 was significantly lower than in 1983. In addition, by 2000 many of the released fish had matured as females, changing the sex ratio of this protandrous hermaphrodite. These changes are thought to be related to the intensive release of hatchery-reared juveniles in the bay, although there is also evidence to suggest that a lower market price for the species, resulting in reduced fishing effort, also contributed to these effects. Our results highlight the potential negative impact of intensive stock enhancement on the population structure of a local fishery. They also emphasise the importance of assessing the status of the stock, and monitoring the carrying capacity of the habitat for the target species, to determine how many, if any, cultured juveniles should be released to achieve management objectives. © 2009 Elsevier B.V. All rights reserved.
1. Introduction Intensive stock enhancement programs have been implemented throughout the Japanese archipelago to restore and/or increase the harvestable stocks of commercially valuable marine finfish. However, reports of success are limited (Fushimi, 2001; Kitada and Kishano, 2006). One of the target species is the black sea bream (Acanthopagrus schlegelii), which has been stocked into Hiroshima Bay in the western part of the Seto Inland Sea of Japan (Fig. 1) since the early 1980s. Stock enhancement program of black sea bream was initiated when annual landings dropped below 200 tonnes. More than one million juveniles were released each year between 1985 and 1996 (Blanco Gonzalez et al., 2008a). Subsequently, total harvest increased to >200 tonnes per year and Hiroshima Bay is now the primary fishing ground for this species in Japan, accounting for 10% of total domestic landings. The recovery of the black sea bream population is generally attributed to stock enhancement (Umino et al., 1999; Nakagawa et al., 2000; Blanco Gonzalez et al., 2008a): the cultured juveniles appear to acclimatize rapidly to the natural con-
∗ Corresponding author. Tel.: +81 824 24 7989; fax: +81 824 24 7989. E-mail address: [email protected] (T. Umino). 0165-7836/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.fishres.2009.04.013
ditions and grow at the same rate as wild fish within a few months of release (Yamashita et al., 1997; Umino et al., 1999; Nakagawa et al., 2000; Jeong et al., 2007). Despite the apparent success of the stock enhancement program for black sea bream, several key issues remain unclear. In particular, the extent to which survival of released juveniles depends on food availability, the carrying capacity of the ecosystem, oceanographic conditions, and intra- and inter-specific interactions (Gaston et al., 1997; Bevers and Flather, 1999; Shepherd and Litvak, 2004; Hattori et al., 2007). In addition, captive breeding may lead to a reduction of fitness which affects the breeding success and effective population size (Fleming and Pettersson, 2001; Ford, 2002; Araki et al., 2007). Although the contribution of cultured black sea bream to spawning biomass has not resulted in undue deleterious effects on genetic diversity (Blanco Gonzalez et al., 2008b), little is known regarding the effect of releases of hatchery-reared juveniles on the dynamics of the natural population. This needs to be examined because the massive releases of chum salmon (Oncorhynchus keta) juveniles (>2 billion juveniles per year) have truncated the age and size structure of natural populations (Ishida et al., 1993; Kaeriyama, 1998; Morita et al., 2001). A similar phenomenon was reported following the accidental escape of a large number of gilthead sea bream (Sparus aurata) from aquaculture operations (Dimitrou et al., 2007). Recently, the importance of adopting a multi-disciplinary approach to manage stock enhancement programs, integrating
E. Blanco Gonzalez et al. / Fisheries Research 99 (2009) 130–133
131
Table 1 Monthly landings (kg) of black sea bream collected in Minou in 1982, 1983, 1999, and 2000. Month January February March April May June July August September October November December Total April–June/total (%)
1982
1983
1999
2000
64 79 43 588 8,661 7,098 137 38 219 338 173 133
68 63 73 971 6,773 5,064 111 61 398 528 247 193
537 993 1,424 15,365 24,848 14,565 1,131 84 340 430 268 324
625 314 347 12,167 39,926 17,358 504 42 308 272 138 308
17,571
14,550
60,309
72,308
93.0
88.0
90.8
96.0
Fig. 1. Map of Hiroshima Bay.
biological, social, economical and institutional arrangements to succeed (Bell et al., 2008; Lorenzen, 2008; Tringali et al., 2008), has been emphasised. Here, we help provide vital biological information for such an integrated approach by describing features of the age structure and sex ratio of black sea beam that are consistent with densitydependent effects due to excessive releases of hatchery-reared juveniles. 2. Materials and methods To evaluate the impact of the releases of cultured juveniles on the age and size structure of black sea bream, we analyzed two sets of data. The first set was collected at the beginning of the stock enhancement program in Hiroshima Bay (1982 and 1983). The second was collected following the largest releases (1999 and 2000). All data were collected at the Hiroshima Prefectural Technology Research Institute Fisheries and Ocean Technologies Center (HPTRIFOTC), Hiroshima, Japan. Catch per unit effort (CPUE) was calculated as kg of black sea bream caught per day. The analysis of the CPUE was based on daily reports of landings provided by the commercial fleet holding a “gochi ami” net license in Minou fish market (see Fig. 1) during the study period. This type of bottom trawl has a mesh size of 91 mm and targets black sea bream accounting for ∼10% of the total commercial catch of the species in Hiroshima Bay. The use of the gochi ami nets occurs between April and June, which overlaps with the black sea bream spawning season in Hiroshima Bay. In contrast to other types of fishing gear, the use of this net requires special permission. A limited number of licenses were issued (34 in 1983 and 24 in 2000) and restricted to Minou, minimizing possible bias due to fishing gear, sampling period, or location among the years studied. In addition, records of age (by scale-reading), fork length (FL), and sex were taken from 153 and 161 specimens collected in Minou in 1983 and 2000, respectively, during sampling surveys conducted by the staff at the HPTRIFOTC on board a commercial fishing vessel. The von Bertalanffy growth curve (VBGC) parameters were estimated using the Microsoft Excel Solver routine (Microsoft Corporation, 2000). Data for male and female fish were pooled. Initially, the parameters were fitted to the data using the non-linear leastsquares approach. Later, the results were used to generate the initial value for the maximum likelihood method (MLM).
Fig. 2. Monthly CPUE for black sea bream collected by gochi ami in Minou in 1982, 1983, 1999 and 2000.
in Table 1. The landings for this species between April and June represent ∼90% of the annual catch. The CPUE values (mean and S.D.) for black sea bream caught by gochi ami in Minou are given in Fig. 2. CPUE was highest in May in all 4 years. In 1982 and 1983, prior to the intensive stocking, the CPUE in Hiroshima Bay remained low. In 1999 and 2000, the CPUE increased 10-fold. Although black sea bream caught in 1983 had a wider size class distribution than that in 2000 (Fig. 3), pairwise comparison of the mean size-at-age of fish collected in 1983 and 2000 revealed significant differences for the most abundant age classes (3–6 years) (Table 2). The VBGC parameter estimates were L∞ = 38.70 and 46.32 cm in 1983 and 2000, respectively. The fish collected in 1983 consisted of 62.1% males and 29.4% females (with 3.9% hermaphrodites and 4.6% individuals of
3. Results Monthly landings of black sea bream before (1982 and 1983) and after (1999 and 2000) intensive stock enhancement are given
Fig. 3. Number of black sea bream by size class collected in Minou in 1983 and 2000. FL = fork length.
132
E. Blanco Gonzalez et al. / Fisheries Research 99 (2009) 130–133
Fig. 4. Sex composition by age of black sea bream collected in Minou in 1983 and 2000.
Table 2 Size-at-age of black sea bream collected in Minou in 1983 and 2000. n = sample size, FL = fork length. Age
1983 n
3 4* 5* 6* 7*
52 22 22 9 5
Total *
2000 FL (cm) 26.5 30.1 31.8 32.9 35.0
± ± ± ± ±
n 1.8 2.5 2.8 3.2 3.1
110
FL (cm) 15 57 27 35 6
27.1 27.8 29.0 30.8 31.3
± ± ± ± ±
2.3 1.9 2.7 2.4 1.4
140
p < 0.05 (using the Mann–Whitney’s U-test).
undetermined-sex). In 2000, 32.3% were males and 67.7% females. In 1983, males were more abundant than females among age classes 4–6, whereas females comprised 65–70% of the specimens for age classes 4–6 in 2000 (Fig. 3). The small number of 7-year-old fish examined (5 and 6 individuals in 1983 and 2000, respectively) may not be representative of their contribution to the natural stock, thus conclusions cannot be drawn regarding this year class. 4. Discussion The effectiveness of stock enhancement programs has traditionally been assessed based on recoveries of the target species in landings (Masuda and Tsukamoto, 1998; Fushimi, 2001). Using this criterion, the stock enhancement program for black sea bream in Hiroshima Bay has been a success (Umino et al., 1999; Jeong et al., 2003, 2007; Blanco Gonzalez et al., 2008a). Three lines of evidence suggest that the release of >20 million juveniles in the bay since the early 1980 have helped to increase yields. First, 4 years after the initial release, hatchery-reared fish accounted for 13% of the stock in the wild. Second, released juveniles are known to have reached maturity (Blanco Gonzalez et al., 2008b). Third, CPUE increased significantly following releases during a period when CPUE for other major species in the Seto Inland Sea continued to decline (Nagai, 2003). Other factors may also have contributed to the recovery of the fishery. At the beginning of the stock enhancement program, black sea bream were a high-priced species subjected to great fishing pressure. Later, the wholesale price decreased drastically. This resulted in lower fishing pressure which may also have contributed to the recovery of the fishery (Blanco Gonzalez et al., 2008a). Caution is needed about interpreting increases in population size as ‘success’ if the carrying capacity of the habitat for the target species has been exceeded. Our data suggest that the combined effects of releases of cultured juveniles and reduced fishing effort (represented by the reduction in netting licenses and increased CPUE) resulted in reduced size-at-age in black sea bream due to density-dependent processes. This phenomenon was also suggested for stocked chum salmon in Japan (Ishida et al., 1993; Kaeriyama, 1998; Morita et al., 2001).
Further support for the hypothesis that the carrying capacity for black sea bream was exceeded in 2000 comes from the sex ratio. The black sea bream is a protandrous hermaphrodite, maturing as a male first, and then progressing to a mature female at age 3, around 22 cm in body length in the Seto Inland Sea off Hiroshima (Kinoshita, 1936). It appears that by 2000, many of the released fish, and those no longer as vulnerable to capture due to lower fishing effort, had matured as females (see Fig. 4). We conclude that the large number of hatchery-reared black sea bream juveniles released in Hiroshima Bay appears to have increased the stock biomass. This has caused density-dependent decreases in size-at-age and a shift in the sex ratio. Our findings highlight the potential negative effects of intensive releases of cultured juvenile fish. We emphasise the need to assess the status of the stock, and monitor the carrying capacity of the habitat of the target species, to determine how many, if any, cultured juveniles need to be released to achieve management objectives. Acknowledgements The authors are very grateful to the gochi ami fleet in Hiroshima Bay for the daily records of catches. We also appreciate the suggestions from two anonymous reviewers whose recommendations have substantially contributed to improve the quality of the paper. This study was partly supported by a Grant-in-Aid for Scientific Research (C) from the Japan Society for the Promotion of Science (JSPS) to T.U. (Nos. 14560152 & 19580205). References Araki, H., Cooper, B., Blouin, M.S., 2007. Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318, 100–103. Bell, J.D., Leber, K.M., Blankenship, L., Loneragan, N.R., Masuda, R., 2008. A new era for restocking, stock enhancement and sea ranching of coastal fisheries resources. Rev. Fish. Sci. 16, 1–9. Bevers, M., Flather, C.H., 1999. The distribution and abundance of populations limited at multiple spatial scales. J. Anim. Ecol. 68, 976–987. Blanco Gonzalez, E., Umino, T., Nagasawa, K., 2008a. Stock enhancement program for black sea bream, Acanthopagrus schlegelii (Bleeker), in Hiroshima Bay, Japan: a review. Aquacult. Res. 39, 1307–1315. Blanco Gonzalez, E., Nagasawa, K., Umino, T., 2008b. Stock enhancement program for black sea bream (Acanthopagrus schlegelii) in Hiroshima Bay: monitoring the genetic effects. Aquaculture 276, 36–43. Dimitrou, E., Katselis, G., Moutopoulos, D.K., Akovitiotis, C., Koutsikopoulos, C., 2007. Possible influence of reared gilthead sea bream (Sparua aurata, L.) on wild stocks in the area of the Messolonghi lagoon. Aquacult. Res. 38, 398–408. Fleming, I.A., Pettersson, E., 2001. The ability of released, hatchery salmonids to breed and contribute to the natural productivity of wild populations. Nordic J. Freshwater Res. 75, 71–98. Ford, M.J., 2002. Selection in captivity during supportive breeding may reduce fitness in the wild. Conserv. Biol. 16, 815–825. Fushimi, H., 2001. Production of juvenile marine finfish for stock enhancement in Japan. Aquaculture 200, 33–53. Gaston, K.J., Blackburn, T.M., Lawton, J.H., 1997. Inter-specific abundance–range size relationships: an appraisal of mechanisms. J. Anim. Ecol. 66, 579–601. Hattori, T., Narimatsu, Y., Ito, M., Ueda, Y., Fujiwara, K., Kitagawa, D., 2007. Growth changes in bighand thornyhead Sebastolobus macrochir off the Pacific coast of northern Honshu, Japan. Fish. Sci. 73, 341–347.
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