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Discrimination of nursery locations of juvenile Japanese flounder Paralichthys olivaceus on the Pacific coast of northern Japan based on carbon and nitrogen stable isotope ratios

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Abstract

To test whether stable isotope ratios of carbon (δ13C) and nitrogen (δ15N) can be used to understand the ecological connectivity of Japanese flounder Paralichthys olivaceus, we evaluated the isotopic signatures of juvenile P. olivaceus from the Pacific coast of northern Japan (i.e., from Aomori to Ibaraki Prefectures). We measured δ13C and δ15N in muscle and collagen extracted from vertebrae and found that isotope ratios were strongly correlated in both. The discrimination models we developed for muscle and collagen proved useful in distinguishing among juvenile P. olivaceus collected from the five prefectures (Aomori, Iwate, Miyagi, Fukushima, and Ibaraki). Juveniles collected in Aomori in particular showed significantly lower values of δ13C and δ15N than those from the other prefectures, which likely reflects the greater influence of the Tsugaru Warm Current in that region. Because collagen in the vertebral centrum can be used to reconstruct annual isotopic records, our results may also assist in developing migration tracking procedures for adult P. olivaceus along the Pacific coast of northern Japan.

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References

  • Bowen GJ (2010) Isoscapes: spatial pattern in isotopic biogeochemistry. Annu Rev Earth Planet Sci 38:161–187

    Article  CAS  Google Scholar 

  • Bradbury IR, DiBacco C, Thorrold SR, Snelgrove PVR, Campana SE (2011) Resolving natal tags using otolith geochemistry in an estuarine fish, rainbow smelt Osmerus mordax. Mar Ecol Prog Ser 433:195–204

    Article  Google Scholar 

  • Cook BD, Bunn SE, Hughes JM (2007) Molecular genetic and stable isotope signatures reveal complementary patterns of population connectivity in the regionally vulnerable southern pygmy perch (Nannoperca australis). Biol Conserv 138:60–72

    Article  Google Scholar 

  • Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527

    Article  CAS  PubMed  Google Scholar 

  • Cowen RK, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annu Rev Mar Sci 1:443–466

    Article  Google Scholar 

  • Estrada JA, Rice AN, Natanson LJ, Skomal GB (2016) Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87:829–834

    Article  Google Scholar 

  • Fisheries Agency and Fisheries Research and Education Agency of Japan (2019) Marine fisheries stock assessment and evaluation for Japanese waters (fiscal year 2018/2019). Tokyo

  • Fontugne MR, Duplessy JC (1981) Organic carbon isotopic fractionation by marine plankton in the temperature range − 1 to 31 °C. Oceanol Acta 4:85–90

    CAS  Google Scholar 

  • Fraile I, Arrizabalaga H, Santiago J, Goñi N, Arregi I, Madinabeitia S, David Wells RJ, Rooker JR (2016) Otolith chemistry as an indicator of movements of albacore (Thunnus alalunga) in the North Atlantic Ocean. Mar Freshwater Res 67:1002–1013

    Article  CAS  Google Scholar 

  • Furuta S, Watanabe T, Yamada H, Miyanaga T (1997a) Changes in feeding condition of released hatchery-reared Japanese flounder, Paralichthys olivaceus, and prey mysid density in the coastal area of Tottori Prefecture. Nippon Suisan Gakkaishi 63:886–891 (in Japanese with English abstract)

    Article  Google Scholar 

  • Furuta S, Watanabe T, Yamada H, Nishida T, Miyanaga T (1997b) Changes in distribution, growth and abundance of hatchery-reared Japanese flounder Paralichthys olivaceus released in the coastal area of Tottori Prefecture. Nippon Suisan Gakkaishi 63:877–885 (in Japanese with English abstract)

    Article  Google Scholar 

  • Furuta S, Watanabe T, Yamada H (1998) Predation by fishes on hatchery-reared Japanese flounder Paralichthys olivaceus juveniles released in the coastal area of Tottori Prefecture. Nippon Suisan Gakkaishi 64:1–7 (in Japanese with English abstract)

    Article  Google Scholar 

  • Gao Y, Bean D (2008) Stable isotope analyses of otoliths in identification of hatchery origin of Atlantic salmon (Salmo salar) in Maine. Environ Biol Fishes 83:429–437

    Article  Google Scholar 

  • Gaston TF, Suthers IM (2004) Spatial variation in δ13C and δ15N of liver, muscle and bone in a rocky reef planktivorous fish: the relative contribution of sewage. J Exp Mar Biol Ecol 304:17–33

    Article  CAS  Google Scholar 

  • Goericke R, Fry B (1994) Variations of marine plankton δ13C with latitude, temperature, and dissolved CO2 in the world ocean. Glob Biogeochem Cycles 8:85–90

    Article  CAS  Google Scholar 

  • Goto T, Sasaki R (2015) Migration pattern of Japanese flounder, Paralichthys olivaceus, from the north region of Iwate Prefecture, Pacific coast of northeastern Japan, based on tagging and recapture data. Bull Iwate Pref Fish Technol Cent 8:5–11 (in Japanese with English abstract)

    Google Scholar 

  • Green BC, Smith DJ, Grey J, Underwood GJC (2012) High site fidelity and low site connectivity in temperate salt marsh fish populations: a stable isotope approach. Oecologia 168:245–255

    Article  PubMed  Google Scholar 

  • Hanawa K, Mitsudera H (1986) Variation of water system distribution in the Sanriku Coastal Area. J Oceanogr Soc Jpn 42:435–446

    Article  Google Scholar 

  • Harrison HB, Williamson DH, Evans RD et al (2012) Larval export from marine reserves and the recruitment benefit for fish and fisheries. Curr Biol 22:1023–1028

    Article  CAS  PubMed  Google Scholar 

  • Ishido Y (1990) Distribution and migration of the young Japanese flounder (Paralichthys olivaceus) along the northeastern coast of Japan. Bull Tohoku Natl Fish Res Inst 52:33–43 (in Japanese with English abstract)

    Google Scholar 

  • Japan Sea-Farming Association (1987) Fisheries and seedling release for Japanese flounder on the Pacific coast of northern Japan. Tokyo (in Japanese)

  • Kerr LA, Andrews AH, Cailliet GM, Brown TA, Coale KH (2006) Investigations of Δ14C, δ13C, and δ15N in vertebrae of white shark (Carcharodon carcharias) from the eastern North Pacific Ocean. Environ Biol Fishes 77:337–353

    Article  Google Scholar 

  • Kidokoro H, Togashi H, Narimatsu Y, Shibata Y (2019) Stock assessment and evaluation for the Japanese flounder stock in the Pacific coast of northern Japan in fiscal year 2018. In: Japan Fisheries Research and Education Agency (ed) Marine fisheries stock assessment and evaluation for Japanese waters (fiscal year 2018). Japan Fisheries Research and Education Agency, Tokyo, pp 1760–1891 (in Japanese)

  • Kimoto K, Fujita K, Noguchi M, Koshiishi Y (2001) Development of the two-meter beam trawl (NRIFE ll type) and estimate of the catch efficiency for juvenile Japanese Flounder. Bull Natl Res Inst Fish Eng 22:67–90 (in Japanese with English abstract)

    Google Scholar 

  • Kurita Y, Okazaki Y, Yamashita Y (2018) Ontogenetic habitat shift of age-0 Japanese flounder Paralichthys olivaceus on the Pacific coast of northeastern Japan: differences in timing of the shift among areas and potential effects on recruitment success. Fish Sci 84:173–187

    Article  CAS  Google Scholar 

  • Kurle CM, McWhorter JK (2017) Spatial and temporal variability within marine isoscapes: implications for interpreting stable isotope data from marine systems. Mar Ecol Prog Ser 568:31–45

    Article  CAS  Google Scholar 

  • Longin R (1971) New method of collagen extraction for radiocarbon dating. Nature 230:241–242

    Article  CAS  PubMed  Google Scholar 

  • Lorrain A, Graham BS, Popp BN, Allain V, Olson RJ, Hunt BPV, Potier M, Fry B, Galván-Magaña F, Menkes CER, Kaehler S, Ménard F (2015) Nitrogen isotopic baselines and implications for estimating foraging habitat and trophic position of yellowfin tuna in the Indian and Pacific Oceans. Deep Sea Res Part II Top Stud Oceanogr 113:188–198

    Article  CAS  Google Scholar 

  • Magozzi S, Yool A, Vander Zanden HB, Wunder MB, Trueman CN (2017) Using ocean models to predict spatial and temporal variation in marine carbon isotopes. Ecosphere 8:e01763

    Article  Google Scholar 

  • Matsubayashi J, Saitoh Y, Osada Y, Uehara Y, Habu J, Sasaki T, Tayasu I (2017) Incremental analysis of vertebral centra can reconstruct the stable isotope chronology of teleost fishes. Methods Ecol Evol 8:1755–1763

    Article  Google Scholar 

  • Matsubayashi J, Umezawa Y, Matsuyama M, Kawabe R, Mei W, Wan X, Shimomae A, Tayasu I (2019) Using segmental isotope analysis of teleost fish vertebrae to estimate trophic discrimination factors of bone collagen. Limnol Oceanogr Methods 17:87–96

    Article  CAS  Google Scholar 

  • Minami T (1997) Life history. In: Minami T, Tanaka M (eds) Biology and stock enhancement of Japanese flounder. Kouseisha Kouseikaku, Tokyo, pp 9–24 (in Japanese)

    Google Scholar 

  • Navarro J, Coll M, Somes CJ, Olson RJ (2013) Trophic niche of squids: insights from isotopic data in marine systems worldwide. Deep Res Part II Top Stud Oceanogr 95:93–102

    Article  CAS  Google Scholar 

  • Nihira A, Takase H, Betsui K, Ishikawa K (1988) Results of mark-recapture experiments of flounder Paralichthys olivaceus (Temminck and Shlegel) on the coastal region of Ibaraki Prefecture. Bull Fish Exp Stn Ibaraki Ken 26:137–159

    Google Scholar 

  • Noichi T (1997) Early life history. In: Minami T, Tanaka M (eds) Biology and stock enhancement of Japanese flounder. Kouseisha Kouseikaku, Tokyo, pp 25–40 (in Japanese)

    Google Scholar 

  • Ohshimo S, Madigan DJ, Kodama T, Tanaka H, Komoto K, Suyama S, Ono T, Yamakawa T (2019) Isoscapes reveal patterns of δ13C and δ15N of pelagic forage fish and squid in the Northwest Pacific Ocean. Prog Oceanogr 175:124–138

    Article  Google Scholar 

  • Olin JA, Hussey NE, Rush SA, Poulakis GR, Simpfendorfer CA, Heupel MR, Fisk AT (2013) Seasonal variability in stable isotopes of estuarine consumers under different freshwater flow regimes. Mar Ecol Prog Ser 487:55–69

    Article  CAS  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical. R Core Team, Vienna

  • Rau GH, Sweeney RE, Kaplan IR (1982) Plankton 13C:12C ratio changes with latitude differences between northern and southern oceans. Deep Sea Res 29:1035–1039

    Article  CAS  Google Scholar 

  • Rodgers KL, Wing SR (2008) Spatial structure and movement of blue cod Parapercis colias in Doubtful Sound, New Zealand, inferred from δ13C and δ15N. Mar Ecol Prog Ser 359:239–248

    Article  Google Scholar 

  • Schoeninger MJ, DeNiro MJ (1984) Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochim Cosmochim Acta 48:625–639

    Article  CAS  Google Scholar 

  • Secor DH (1999) Specifying divergent migrations in the concept of stock: the contingent hypothesis. Fish Res 43:13–34

    Article  Google Scholar 

  • Shimizu Y, Yasuda I, Ito SI (2001) Distribution and circulation of the coastal Oyashio intrusion. J Phys Oceanogr 31:1561–1578

    Article  Google Scholar 

  • Sholto-Douglas A, Field J (1991) the Southern Benguela Ecosystem: indicators of food web relationships among different size-classes of plankton and pelagic fish; differences between fish. Mar Ecol Prog Ser 78:23–31

    Article  Google Scholar 

  • Sogawa S, Sugisaki H, Tadokoro K, Ono T, Sato E, Shimode S, Kikuchi T (2017) Feeding habits of six species of euphausiids (Decapoda: Euphausiacea) in the northwestern Pacific Ocean determined by carbon and nitrogen stable isotope ratios. J Crustac Biol 37:29–36

    Article  Google Scholar 

  • Tayasu I, Hirasawa R, Ogawa NO, Ohkouchi N, Yamada K (2011) New organic reference materials for carbon- and nitrogen-stable isotope ratio measurements provided by Center for Ecological Research, Kyoto University, and Institute of Biogeosciences, Japan Agency for Marine-Earth Science and Technology. Limnology 12:261–266

    Article  CAS  Google Scholar 

  • Tomaszewicz CNT, Seminoff JA, Avens L, Kurle CM (2016) Methods for sampling sequential annual bone growth layers for stable isotope analysis. Methods Ecol Evol 7:556–564

    Article  Google Scholar 

  • Tomiyama T, Uehara S, Kurita Y (2013) Feeding relationships among fishes in shallow sandy areas in relation to stocking of Japanese flounder. Mar Ecol Prog Ser 479:163–175

    Article  Google Scholar 

  • Van Klinken GJ, Mook WG (1990) Preparative high-performance liquid chromatographic separation of individual amino acids derived from fossil bone collagen. Radiocarbon 32:155–164

    Article  Google Scholar 

  • Van Klinken GJ (1999) Bone collagen quality indicators for palaeodietary and radiocarbon measurements. J Archaeol Sci 26:687–695

    Article  Google Scholar 

  • Wada E, Ohki K, Yoshikawa S, Parker PL, Van BC, Matsumoto GI, Aita MN, Saino T (2012) Ecological aspects of carbon and nitrogen isotope ratios of cyanobacteria. Plankt Benthos Res 7:135–145

    Article  Google Scholar 

  • Wells RD, Kinney MJ, Kohin S, Dewar H, Rooker JR, Snodgrass OE (2015) Natural tracers reveal population structure of albacore (Thunnus alalunga) in the eastern North Pacific. ICES J Mar Sci 72:2118–2127

    Article  Google Scholar 

  • West JB, Sobek A, Ehleringer JR (2008) A simplified GIS approach to modeling global leaf water isoscapes. PLOS ONE 3:e2447

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamada H, Sato K, Nagahora S, Kumagai A, Yamashita Y (1998) Feeding habits of the Japanese flounder Paralichthys olivacens in Pacific coastal waters of Tohoku District, Northeastern Japan. Nippon Suisan Gakkaishi 64:249–258 (in Japanese with English abstract)

    Article  Google Scholar 

  • Yamamoto M, Tominaga O (2014) Prey availability and daily growth rate of juvenile Japanese flounder Paralichthys olivaceus at a sandy beach in the central Seto Inland Sea, Japan. Fish Sci 80:1285–1292

    Article  CAS  Google Scholar 

  • Yoneda M, Suzuki R, Shibata Y, Morita M, Sukegawa T, Shigehara N, Akazawa T (2004) Isotopic evidence of inland-water fishing by a Jomon population excavated from the Boji site, Nagano, Japan. J Archaeol Sci 31:97–107

    Article  Google Scholar 

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Acknowledgments

We are grateful to Yuka Wada, Airi Takanashi, Mitsuharu Suzuki, Atsushi Sanematsu, and Yukio Yamazaki for providing fish samples. We also thank Chikage Yoshimizu for her help with the stable isotope analysis. Comments from Takanori Nakano and two anonymous reviewers helped to improve the manuscript. This work was supported by the CREST program administered by the Japan Science and Technology Agency (grant no. JPMJCR13A3), the Stock Assessment Program of the Japan Fisheries Research and Education Agency and Fisheries Agency, and a Japan Society for the Promotion of Science KAKENHI grant (no. 16H02524).

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  1. Research Institute for Humanity and Nature, 457-4 Motoyama, Kamigamo, Kita-ku, Kyoto, 603-8047, Japan

    Yoshikazu Kato, Hiromitsu Kamauchi & Ichiro Tayasu

  2. Graduate School of Environmental Studies, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi, 464-8601, Japan

    Yoshikazu Kato & Hiromitsu Kamauchi

  3. Tohoku National Fisheries Research Institute, Japan Fisheries Research and Education Agency, 3-27-5, Shinhama-cho, Shiogama, Miyagi, 985-0001, Japan

    Hiroyuki Togashi & Yutaka Kurita

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  1. Yoshikazu Kato
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  2. Hiroyuki Togashi
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Kato, Y., Togashi, H., Kurita, Y. et al. Discrimination of nursery locations of juvenile Japanese flounder Paralichthys olivaceus on the Pacific coast of northern Japan based on carbon and nitrogen stable isotope ratios. Fish Sci 86, 615–623 (2020). https://doi.org/10.1007/s12562-020-01436-y

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