Abstract
In order to develop effective conservation strategies for endangered migratory species, the link between feeding and breeding grounds needs to be clarified. In this study, the genetic compositions of consecutive Japanese feeding aggregations of green turtles (Chelonia mydas) along the Kuroshio Current were examined by mixed-stock analyses of mitochondrial DNA control-region sequences. The results indicated that the southern feeding aggregation around Yaeyama (24.3°N, 124.0°E) was sourced from various Pacific rookeries in the Yaeyama, Ogasawara, Western Pacific, and Indian Oceans and Southeast Asia. Among northern feeding aggregations, the Ginoza (26.5°N, 128.0°E) aggregation was also sourced from the Western Pacific Ocean, but the Nomaike (31.4°N, 130.1°E), Muroto (33.2°N, 134.2°E), and Kanto (35.6°N, 140.5°E) aggregations were contributed mostly by the closer Ogasawara rookeries. The reduced contribution from tropical Pacific rookeries to northern feeding aggregations and the significant correlation between genetic differentiation and geographical distance matrices of feeding aggregations indicated that most hatchlings from these regions transported by the Kuroshio Current settle in upstream feeding grounds along the Japanese archipelago, implying that current flow influences the composition of feeding aggregations. Differences in the composition of relatively close neritic feeding aggregations have important conservation implications, for which both regional and multinational conservation strategies are needed.
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References
Abe O, Minami H (2008) Mitigation measures to reduce incidental catch of sea turtles: status of sea turtle populations and holistic management. Nippon Suisan Gakkaishi 74:230–233 (in Japanese, with English abstract)
Amorocho DF, Abreu-Grobois FA, Dutton PH, Reina RD (2012) Multiple distant origins for green sea turtles aggregating off Gorgona Island in the Colombian eastern Pacific. PLoS ONE 7:e31486
Bass AL, Epperly SP, Braun-McNeill J (2006) Green turtle (Chelonia mydas) foraging and nesting aggregations in the Caribbean and Atlantic: impact of currents and behavior on dispersal. J Hered 97:346–354
Bjorndal KA, Bolten AB (2008) Annual variation in source contributions to a mixed stock: implications for quantifying connectivity. Mol Ecol 17:2185–2193
Blumenthal JM, Abreu-Brobois FA, Austin TJ, Broderick AC, Bruford MW, Coyne MS, Ebanks-Petrie G, Formia A, Meylan PA, Meylan AB, Godley BJ (2009) Turtle groups or turtle soup: dispersal patterns of hawksbill turtles in the Caribbean. Mol Ecol 18:4841–4853
Bolker B, Okuyama T, Bjorndal K, Bolten A (2003) Sea turtle stock estimation using genetic markers: accounting for sampling error of rare genotypes. Ecol Appl 13:763–775
Bolker B, Okuyama T, Bjorndal K, Bolten A (2007) Incorporating multiple mixed stocks in mixed stock analysis: ‘many-to-many’ analysis. Mol Ecol 16:685–695
Bowen BW, Meylan AB, Ross JP, Limpus CJ, Balazs GH, Avise JC (1992) Global population structure and natural history of the green turtle (Chelonia mydas) in terms of matriarchal phylogeny. Evolution 46:865–881
Bowen BW, Bass AL, Chow S-M, Bostrom M, Bjorndal KA, Bolten AB, Okuyama T, Bolker BM, Epperly S, Lacashella E, Shaver D, Dodd M, Hopkins-Murphy SR, Musick JA, Swingle M, Rankin-Baransky K, Teas W, Witzell WN, Dutton PH (2004) Natal homing in juvenile loggerhead turtles (Caretta caretta). Mol Ecol 13:3797–3808
Bowen BW, Grant WS, Hillis-Starr Z, Shaver DJ, Bjorndal KA, Bolten AB, Bass AL (2007) Mixed-stock analysis reveals the migrations of juvenile hawksbill turtles (Eretmochelys imbricata) in the Caribbean Sea. Mol Ecol 16:49–60
Boyle MC, FitzSimmons NN, Limpus CJ, Kelez S, Velez-Zuazo X, Waycott M (2009) Evidence for transoceanic migrations by loggerhead sea turtles in the southern Pacific Ocean. Proc R Soc B 276:1993–1999
Chassin-Noria O, Abreu-Grobois A, Dutton PH, Oyama K (2004) Conservation genetics of the east Pacific green turtle (Chelonia mydas) in Michacan, Mexico. Genetica 121:195–206
Cheng I-J, Dutton PH, Chen C-L, Chen H-C, Chen Y-H, Shea J-W (2008) Comparisons of the genetics and nesting ecology of two green turtle rookeries. J Zool 267:375–384
Clarke J, Kerry K, Fowler C, Lawless R, Eberhard S, Murohy R (2003) Post-fledging and winter migration of Adélie penguins Pygoscelis adeliae in the Mawson region of East Antarctica. Mar Ecol Prog Ser 248:267–278
Dethmers KEM, Broderick D, Moritz C, Fitzsimmons NN, Limpus CJ, Lavery S, Whiting S, Guinea M, Prince RIT, Kennett R (2006) The genetic structure of Australasian green turtles (Chelonia mydas): exploring the geographical scale of genetic exchange. Mol Ecol 15:3931–3946
Dutton PH, Balazs GH, LeRoux RA, Murakawa SKK, Zarate P, Martinez LS (2008) Composition of Hawaiian green turtle foraging aggregations: mtDNA evidence for a distinct regional population. Endang Species Res 5:37–44
Encalada SE, Lahanas PN, Bjorndal KA, Bolten AB, Miyamoto MM, Bowen BW (1996) Phylogeography and population structure of the Atlantic and Mediterranean green turtle Chelonia mydas: a mitochondrial DNA control region sequence assessment. Mol Ecol 5:473–483
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7:457–511
Godley BJ, Barbosa C, Bruford M, Broderick AC, Catry P, Coyne MS, Formia A, Hays GC, Witt MJ (2010) Unravelling migratory connectivity in marine turtles using multiple methods. J Appl Ecol 47:769–778
Hamabata T, Nishida S, Kamezaki N, Koike H (2009) Genetic structure of populations of the green turtle (Chelonia mydas) in Japan using mtDNA control region sequences. Bull Grad School Soc Cult Stud Kyushu Univ 15:35–50
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
IUCN (2010) IUCN red list of threatened species. Version 2010.4. Accessed on 14 Mar 2011. http://www.iucnredlist.org
Karl SA, Toonen RJ, Grant WS, Bowen BW (2012) Common misconceptions in molecular ecology: echoes of the modern synthesis. Mol Ecol 21:4171–4189
Kimura S, Tsukamoto K, Sugimoto T (1994) A model for the larval migration of the Japanese eel: roles of the trade winds and salinity front. Mar Biol 119:185–190
Lahanas PN, Bjorndal KA, Bolten AB, Encalada SE, Miyamoto MM, Valverde RA, Bowen BW (1998) Genetic composition of a green turtle (Chelonia mydas) feeding ground population: evidence for multiple origins. Mar Biol 130:345–352
Luke K, Horrocks JA, LeRoux RA, Dutton PH (2004) Origins of green turtle (Chelonia mydas) feeding aggregations around Barbados, West Indies. Mar Biol 144:799–805
McConnell B, Fedak M, Burton HR, Engerlhard GH, Reijnders PJH (2002) Movements and foraging areas of naïve, recently weaned southern elephant seal pups. J Anim Ecol 71:65–78
Monzón-Argüello C, López-Jurado LF, Rico C, Marco A, López P, Hays GC, Lee PLM (2010) Evidence from genetic and Lagrangian drifter data for transatlantic transport of small juvenile green turtles. J Biogeogr 37:1752–1766
Moritz C, Broderick D, Dethmers K, FitzSimmons N, Limpus C (2002) Population genetics of Southeast Asian and Western Pacific green turtles, Chelonia mydas. Final report to UNEP/CM0053
Musick JA, Limpus CJ (1997) Habitat utilization and migration in juvenile sea turtles. In: Lutz PL, Musick JA (eds) The biology of sea turtles. CRC Press, Boca Raton, pp 137–163
Naro-Maciel E, Becker JH, Lima EHSM, Marcovaldi MA, DeSalle R (2007) Testing dispersal hypotheses in foraging green sea turtles (Chelonia mydas) of Brazil. J Hered 98:29–39
Nishizawa H, Okuyama J, Kobayashi M, Abe O, Arai N (2010) Comparative phylogeny and historical perspectives on population genetics of the Pacific hawksbill (Eretmochelys imbricata) and green turtles (Chelonia mydas), inferred from feeding populations in the Yaeyama Islands, Japan. Zool Sci 27:14–18
Nishizawa H, Abe O, Okuyama J, Kobayashi M, Arai N (2011) Population genetic structure and implications for natal philopatry of nesting green turtles (Chelonia mydas) in the Yaeyama Islands, Japan. Endang Species Res 14:141–148
Norman JA, Moritz C, Limpus CJ (1994) Mitochondrial DNA control region polymorphisms: genetic markers for ecological studies of marine turtles. Mol Ecol 3:363–373
Okuyama J, Kitagawa T, Zenimoto K, Kimura S, Arai N, Sasai Y, Sasaki H (2011) Trans-Pacific dispersal of loggerhead turtle hatchlings inferred from numerical simulation modeling. Mar Biol 158:2055–2063
Pella J, Masuda M (2001) Bayesian methods for analysis of stock mixtures from genetic characters. Fish Bull 99:151–167
Pritchard PCH (1999) Status of the black turtle. Conserv Biol 13:1000–1003
Reich KJ, Bjorndal KA, Bolten AB (2007) The ‘lost years’ of green turtles: using stable isotopes to study cryptic lifestages. Biol Lett 3:712–714
Roberts MA, Anderson CJ, Stender B, Segars A, Whittaker JD, Grady JM, Quattro JM (2005) Estimated contribution of Atlantic Coastal loggerhead turtle nesting populations to offshore feeding aggregations. Conserv Genet 6:133–139
Scott R, Marsh R, Hays GC (2012) A little movement oriented to the geomagnetic field makes a big difference in strong flows. Mar Biol 159:481–488
Tsukamoto K (1990) Recruitment mechanism of the eel, Anguilla japonica, to the Japanese coast. J Fish Biol 36:659–671
Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT (2002) Links between worlds: unraveling migratory connectivity. Trends Ecol Evol 17:76–83
Acknowledgments
We would like to acknowledge the followings for providing information about the stranded turtles on Ishigaki Island and field sampling assistance in Yaeyama Islands: the member of the Ishigaki Island Sea Turtle Research Group; K. Okuzawa and the staff of the Ishigaki Tropical Station and Yaeyama Station, Seikai National Fisheries Research Institute; D. Imakita (Faculty of Agriculture, Kinki University); and Y. Kawabata, T. Yasuda, K. Ichikawa, and H. Watanabe (Graduate School of Informatics, Kyoto University). The staff of the Ogasawara Marine Center and fisheries cooperative associations in Hahajima Island and Chichijima Island and M. Kaneko (Club Noah Hahajima) kindly helped with sampling in Ogasawara Islands. Sampling in Ginoza was supported by N. Kamezaki and the Sea Turtle Association of Japan. M. Kinoshita, H. Sawada (Graduate School of Agriculture, Kyoto University), R. Matsuoka, and T. Nishizawa (IREIIMS, Tokyo Women’s Medical University) provided assistance with the DNA extraction, amplification, and sequencing analyses. T. Hamabata and H. Koike (Graduate School of Social and Cultural Studies, Kyushu University) kindly provided data on the Muroto and Nomaike aggregations. We thank the two anonymous reviewers for valuable comments on this manuscript. This study was partly supported by a Grant-in-Aid for JSPS Fellows (J.O. 17-1976), for Research Activity Start-up (J.O. No. 19880017), for Young Scientists B (J.O. No. 22710236), and the Global COE Program, Informatics Education and Research for a Knowledge–Circulating Society.
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Communicated by M. I. Taylor.
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Nishizawa, H., Naito, Y., Suganuma, H. et al. Composition of green turtle feeding aggregations along the Japanese archipelago: implications for changes in composition with current flow. Mar Biol 160, 2671–2685 (2013). https://doi.org/10.1007/s00227-013-2261-1
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DOI: https://doi.org/10.1007/s00227-013-2261-1