Abstract
Carbon and nitrogen stable isotope ratios of Japanese anchovy (Engraulis japonicus) and their stomach contents were examined and compared among various regions around Japan. Geographical variations in the isotope ratios were found between inshore and Pacific offshore regions. While most of the anchovy samples had isotope ratios around −17.6‰ for δ13C and 10.0‰ for δ15N as median values, higher (more enriched) isotope values were found in the anchovy sampled from inshore regions. On the contrary, lower (more depleted) values were found mostly in the anchovy from the Pacific offshore region including the Kuroshio Extension and Kuroshio-Oyashio transition zones. Higher carbon isotope ratios in the inshore regions may reflect a carbon source from benthic primary producers in addition to phytoplankton possibly through the consumption of the larvae of benthic organisms such as bivalves or decapods, which were found in the stomach contents of the inshore anchovy. Variations in the nitrogen isotope ratio may reflect not only differences in the trophic level of prey species, but also variations in the baseline level of food webs. Stable isotope ratios are potentially a useful tool for understanding the stock/population structure and migration of anchovy. The present findings indicate the potential importance of the “inshore–offshore” variations in the biology of Japanese anchovy populations in the northwestern Pacific waters.
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References
Altabet MA, Francois R, Murray DW, Prell WL (1995) Climate-related variations in denitrification in the Arabian Sea from sediment 15N/14N ratios. Nature 373:506–509
Aoki I, Miyashita K (2000) Dispersal of larvae and juveniles of Japanese anchovy Engraulis japonicus in the Kuroshio Extension and Kuroshio-Oyashio transition regions, western North Pacific Ocean. Fish Res 49:155–164
Cabana G, Rasmussen JB (1996) Comparison of aquatic food chains using nitrogen isotopes. Proc Natl Acad Sci USA 93:10844–10847
Chihara M, Murano M (1997) An illustrated guide to marine plankton in Japan. Tokai University Press, Tokyo
DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506
DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351
France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307–312
Fry B, Sherr EB (1984) δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib Mar Sci 27:13–47
Funakoshi S (1992) Relationship between stock levels and the population structure of the Japanese anchovy. Mar Behav Physiol 21:1–84
Funamoto T, Aoki I (2002) Reproductive ecology of Japanese anchovy off the Pacific coast of eastern Honshu, Japan. J Fish Biol 60:154–169
Funamoto T, Aoki I, Wada Y (2004) Reproductive characteristics of Japanese anchovy, Engraulis japonicus, in two bays of Japan. Fish Res 70:71–81
Hatase H, Takai N, Matsuzawa Y, Sakamoto W, Omuta K, Goto K, Arai N, Fujiwara T (2002) Size-related differences in feeding habitat use of adult female loggerhead turtles Caretta caretta around Japan determined by stable isotope analyses and satellite telemetry. Mar Ecol Prog Ser 233:273–281
Hatase H, Sato K, Yamaguchi M, Takahashi K, Tsukamoto K (2006) Individual variation in feeding habitat use by adult female green sea turtles (Chelonia mydas): are they obligately neritic herbivores? Oecologia 149:52–64
Hayashi S, Kondo K (1957) Growth of the Japanese anchovy—IV. Age determination with the use of scales. Tokai Reg Fish Res Lab 17:31–64
Hirakawa K, Ogawa Y (1996) Characteristics of the copepod assemblage in the southwestern Japan Sea and its implications for anchovy population dynamics. Bull Jpn Sea Natl Fish Res Inst 46:45–64
Hirakawa K, Goto T, Hirai M (1997) Diet composition and prey size of larval anchovy, Engraulis japonicus, in Toyama Bay, southern Japan Sea. Bull Jpn Sea Natl Fish Res Inst 47:67–78
Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326
Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 63:786–798
Hyslop EJ (1980) Stomach contents analysis – a review of methods and their application. J Fish Biol 17:411–429
Jennings S, Warr KJ (2003) Environmental correlates of large-scale spatial variation in the δ15N of marine animals. Mar Biol 142:1131–1140
Kasuya E (2001) Mann–Whitney U test when variances are unequal. Anim Behav 61:1247–1249
Kasai A, Horie H, Sakamoto W (2004) Selection of food sources by Ruditapes philippinarum and Mactra veneriformis (Bivalvia: Mollusca) determined from stable isotope analysis. Fish Sci 70:11–20
Kleppel GS (1993) On the diets of calanoid copepods. Mar Ecol Prog Ser 99:183–195
Koike H, Saito T, Kosugi M, Kakino J (1992) Shell growth and diet of Tapes philippinarum from the tidal flats of the Obitsu River, Tokyo Bay (in Japanese with English abstract). Fish Eng 29:105–112
Li XY, Kawasaki T, Honda H (1992) The niches of the far eastern sardine and Japanese anchovy. Asian Fish Sci 5:315–326
Lindsay DJ, Minagawa M, Mitani I, Kawaguchi K (1998) Trophic shift in the Japanese anchovy Engraulis japonicus in its early life history stages as detected by stable isotope ratios in Sagami Bay, central Japan. Fish Sci 64:403–410
Liu KK, Su MJ, Hsueh CR, Gong GC (1996) The nitrogen isotopic composition of nitrate in the Kuroshio water northeast of Taiwan: evidence for nitrogen fixation as a source of isotopically light nitrate. Mar Chem 54:273–292
Maruyama A, Yamada Y, Yuma M, Rusuwa B (2001) Stable nitrogen and carbon isotope ratios as migration tracers of a landlocked goby, Rhinogobius sp. (the orange form), in the Lake Biwa water system. Ecol Res 16:697–703
McClelland JW, Valiela I, Michener RH (1997) Nitrogen-stable isotope signatures in estuarine food webs: a record of increasing urbanization in coastal watersheds. Limnol Oceanogr 42:930–937
Mihara Y (1994) Distribution of eggs and larvae of the Japanese anchovy, Engraulis japonica, off southeastern Hokkaido (in Japanese with English abstract). Sci Rep Hokkaido Fish Exp Stn 44:1–8
Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: Further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140
Mishima Y, Hoshika A (2002) Carbon and nitrogen stable isotope ratios of fish collected in Iyo-Nada and Osaka Bay, the Seto Inland Sea (in Japanese with English abstract). Bull Coast Oceanogr 39:145–150
Mitani I (1988) Food habits of Japanese anchovy in the Shirasu fishing ground within Sagami Bay (in Japanese with English abstract). Nippon Suisan Gakkaishi 54:1859–1865
Mitani Y, Bando T, Takai N, Sakamoto W (2006) Patterns of stable carbon and nitrogen isotopes in the baleen of common minke whale Balaenoptera acutorostrata from the western North Pacific. Fish Sci 72:69–76
Nakagawa Y, Endo Y, Taki K (2001) Diet of Euphausia pacifica Hansen in Sanriku waters off northeastern Japan. Plankton Biol Ecol 48:68–77
Ogawa N, Ogura N (1997) Dynamics of particulate organic matter in the Tamagawa Estuary and inner Tokyo Bay. Estuar Coast Shelf Sci 44:263–273
Owens NJP (1987) Natural variations in 15N in the marine environment. Adv Mar Biol 24:389–451
Pinnegar JK, Polunin NVC (1999) Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Funct Ecol 13:225–231
Preston NP, Burford MA, Coman FE, Rothlisberg PC (1992) Natural diet of larval Penaeus merguiensis (Decapoda: Penaeidae) and its effect on survival. Mar Biol 113:181–191
Rubenstein DR, Hobson KA (2004) From birds to butterflies: animal movement patterns and stable isotopes. Trends Ecol Evol 19:256–263
Shaber K, Sulkin S (2007) Feeding on dinoflagellates by intermediate and late stage crab zoeae raised in the laboratory and collected from the field. J Exp Mar Biol Ecol 340:149–159
Suzuki KW, Kasai A, Nakayama K, Tanaka M (2005) Differential isotopic enrichment and half-life among tissues in Japanese temperate bass (Lateolabrax japonicus) juveniles: implications for analyzing migration. Can J Fish Aquat Sci 62:671–678
Sweeting CJ, Polunin NVC, Jennings S (2004) Tissue and fixative dependent shifts of δ13C and δ15N in preserved ecological material. Rapid Commun Mass Spectrom 18:2587–2592
Takai N, Onaka S, Ikeda Y, Yatsu A, Kidokoro H, Sakamoto W (2000) Geographical variations in carbon and nitrogen stable isotope ratios in squid. J Mar Biol Ass UK 80:675–684
Takai N, Mishima Y, Yorozu A, Hoshika A (2002) Carbon sources for demersal fish in the western Seto Inland Sea, Japan, examined by δ13C and δ15N analyses. Limnol Oceanogr 47:730–741
Takasuka A, Oozeki Y, Kubota H, Tsuruta Y, Funamoto T (2005) Temperature impacts on reproductive parameters for Japanese anchovy: Comparison between inshore and offshore waters. Fish Res 76:475–482
Tanaka H (2006) Comparative study of the feeding ecology of small pelagic fishes with a focus on Japanese anchovy Engraulis japonicus. PhD thesis, The University of Tokyo, Tokyo, 189pp
Tanaka H, Aoki I, Ohshimo S (2006) Feeding habits and gill raker morphology of three planktivorous pelagic fish species off the coast of northern and western Kyushu in summer. J Fish Biol 68:1041–1061
Uotani I, Izuha A, Asai K (1978) Food habits and selective feeding of anchovy larvae (Engraulis japonica) (in Japanese with English abstract). Bull Jpn Soc Sci Fish 44:427–434
Uotani I (1985) The relation between feeding mode and feeding habit of the anchovy larvae (in Japanese with English abstract). Bull Jpn Soc Sci Fish 51:1057–1065
Wada E, Minagawa M, Mizutani H, Tsuji T, Imaizumi R, Karasawa K (1987) Biogeochemical studies on the transport of organic matter along the Otsuchi River watershed. Estuar Coast Shelf Sci 25:321–336
Wu CH, Hwang JS, Yang JS (2004) Diets of three copepods (Poecilostomatoida) in the southern Taiwan Strait. Zool Stud 43:388–392
Yamada Y, Ueda T, Wada E (1996) Distribution of carbon and nitrogen isotope ratios in the Yodo River watershed. Jpn J Limnol 57:467–477
Yamashita H (1957) Relations of the foods of sardine, jack mackerel, mackerel, and so on, in the waters adjacent to Kyushu (in Japanese with English abstract). Bull Seikai Natl Fish Res Inst 11:45–53
Yukami R, Aoki I, Mitani I (2008) Daily age of adult Japanese anchovy Engraulis japonicus off eastern Honshu, Japan, by otolith daily increment. Fish Sci (in press)
Acknowledgments
We are grateful to I. Mitani, Y. Wada, O. Funaki, S. Katayama and H. Watanabe for their help with the field sampling. T. Yamakawa gave us useful comments on the preliminary study. The authors also appreciate the kind co-operation during the sampling by the captain and crew of R/V Hakuho-maru, Yoko-maru and Shunyo-maru. Cruise of Shunyo-maru was conducted as a part the Japanese Whale Research Program under Special Permit in the western North Pacific Phase II. All samplings and experiments conducted in this study complied with the current Japanese laws. Finally, the manuscript was improved with the comments of three anonymous reviewers.
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Tanaka, H., Takasuka, A., Aoki, I. et al. Geographical variations in the trophic ecology of Japanese anchovy, Engraulis japonicus, inferred from carbon and nitrogen stable isotope ratios. Mar Biol 154, 557–568 (2008). https://doi.org/10.1007/s00227-008-0949-4
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DOI: https://doi.org/10.1007/s00227-008-0949-4