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Summer migration to temperate foraging habitats and active winter diving of juvenile loggerhead turtles Caretta caretta in the western North Pacific

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Abstract

Endangered loggerhead turtles (Caretta caretta) are highly migratory marine reptiles that spend extended maturation periods at sea. Although an understanding of the biology and ecology of juveniles is essential for effective conservation of this species, such information is still limited, especially for the North Pacific population. The first quantitative bycatch survey in northern Japan revealed that the Sanriku coastal area served as an important summer foraging habitat for large juvenile loggerhead turtles in the western North Pacific. To examine their year-round distribution and diving behaviour, we deployed satellite-relayed data loggers on six turtles (mean SCLn–t ± SD = 69.2 ± 9.2 cm, range = 58.3–82.5 cm). While turtles predominantly utilize the Sanriku coastal area and surrounding oceanic waters during summer, all turtles spent most of their time travelling in oceanic waters (>200 m) several kilometres east of Japan and sometimes in association with the Kuroshio Extension Current during winter. Although water temperature experienced by turtles significantly decreased during winter, they predominantly stayed in water >15 °C. There was no strong seasonal pattern in diving behaviour, and daily average dive duration was 20.9 ± 11.6 min regardless of summer or winter. In addition, turtles sporadically performed deep dives, including the deepest dive (>340 m) ever recorded for this species, during winter. These results suggest that juveniles remained active and possibly foraging in oceanic habitats throughout the winter rather than adopting the quiescent overwintering strategy (i.e. undertaking prolonged dives lasting >300 min) previously reported in adult females.

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References

  • Alerstam T, Hedenström A, Åkesson S (2003) Long-distance migration: evolution and determinants. OIKOS 103:247–260

    Article  Google Scholar 

  • Angel MV, Pugh PR (2000) Quantification of diel vertical migration by micronektonic taxa in the northeast Atlantic. Hydrobiologia 440:161–179

    Article  Google Scholar 

  • Baba N, Nitto H, Nitta A (2000) Satellite tracking of young Steller sea lion off the coast of northern Hokkaido. Fish Sci 66:180–181

    Article  CAS  Google Scholar 

  • Balazs GH, Chaloupka M (2004) Spatial and temporal variability in somatic growth of green sea turtles (Chelonia mydas) resident in the Hawaiian Archipelago. Mar Biol 145:1043–1059

    Article  Google Scholar 

  • Bolten AB (1999) Techniques for measuring sea turtles. In: Eckert KL, Bjorndal KA, Abreu-Grobois FA, Donelly M (eds) Research and management techniques for the conservation of sea turtles, IUCN/SSC Marie Turtle Specialist Group 4, pp 110-14

  • Bowen BW, Abreu-Grobois FA, Balazs GH, Kamezaki N, Limpus CJ, Feri RJ (1995) Trans-pacific migrations of the loggerhead turtles (Caretta caretta) demonstrated with mitochondrial DNA markers. PNAS 92:3731–3734

    Article  CAS  Google Scholar 

  • Broderick AC, Coyne MS, Fuller WJ, Glen F, Godley BJ (2007) Fidelity and over-wintering of sea turtles. Proc R Soc B 274:1533–1538

    Article  Google Scholar 

  • Carr A, Ogren L, McVea C (1980–1981) Apparent hibernation by the Atlantic loggerhead turtle Caretta caretta off Cape Canaveral, Florida. Biol Conserv 19:7–14

  • Casale P, Abbate G, Freggi D, Conte N, Oliverio M, Argano R (2008) Foraging ecology of loggerhead sea turtles Caretta caretta in the central Mediterranean Sea: evidence for a relaxed life history model. Mar Ecol Prog Ser 372:265–276

    Article  Google Scholar 

  • Casale P, Broderick AC, Freggi D, Mencacci R, Fuller WJ, Godley BJ, Luschi P (2012) Long-term residence of juvenile loggerhead turtles to foraging grounds: a potential conservation hotspot in the Mediterranean. Aquatic Conserv Mar Freshw Ecosyst 22:144–154

    Article  Google Scholar 

  • Coles WC, Musick JA (2000) Satellite sea surface temperature analysis and correlation with turtle distribution off North Carolina. Copeia 2000:551–554

    Article  Google Scholar 

  • Crouse DT, Crowder LB, Caswell H (1987) A stage-based population model for loggerhead sea turtles and implications for conservation. Ecology 68:1412–1423

    Article  Google Scholar 

  • Crowder LB, Crouse T, Heppell SS, Martin TH (1994) Predicting the impact of turtle excluder devices on loggerhead sea turtle populations. Ecol Appl 4:437–445

    Article  Google Scholar 

  • Dodd CK Jr (1988) Synopsis of the biological data on the loggerhead sea turtle Caretta caretta (Linnaeus 1758). US Fish Wildl Serv Biol Rep 88:1–110

    Google Scholar 

  • Doyle TK, Houghton JDR, McDevitt R, Davenport J, Hays GC (2007) The energy density of jellyfish: estimates from bomb-calorimetry and proximate-composition. J Exp Mar Biol Ecol 343:239–252

    Article  Google Scholar 

  • Doyle TK, Georges JY, Houghton JDR (2013) A leatherback turtle’s guide to jellyfish in the North East Atlantic. Munibe Monographs. Nat Series 1:15–21

    Google Scholar 

  • Fedak M, Lovell P, McConnell B, Hunter C (2002) Overcoming the constraints of long range radio telemetry from animals: getting more useful data from smaller packages. Integr Comp Biol 42:3–10

    Article  Google Scholar 

  • Graham WM, Pages F, Hamner WM (2001) A physical context for gelatinous zooplankton aggregations: a review. Hydrobiologia 451:199–212

    Article  Google Scholar 

  • Hamann M, Godfrey MH, Seminoff JA, Arthur K et al (2010) Global research priorities for sea turtles: informing management and conservation in the 21st century. Endanger Species Res 11:245–269

    Article  Google Scholar 

  • Hanawa K, Mitsudera H (1987) Variation of water system distribution in Sanriku coastal area. J Oceanogr Soc Jpn 42:435–446

    Article  Google Scholar 

  • Hatase H, Goto K, Sato K, Bando T, Matsuzawa Y, Sakamoto W (2002a) Using annual body size fluctuations to explore potential causes for the decline in a nesting population of the loggerhead turtle Caretta caretta at Senri Beach, Japan. Mar Ecol Prog Ser 245:299–304

    Article  Google Scholar 

  • Hatase H, Takai N, Matsuzawa Y, Sakamoto W, Omuta K, Goto K, Arai N, Fujiwara T (2002b) 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

    Article  Google Scholar 

  • Hatase H, Kunoshita M, Bando T, Kamezaki N, Sato K, Matsuzawa Y, Goto K, Omuta K, Nakashima Y, Takeshita H, Sakamoto W (2002c) Population structure of loggerhead turtles, Caretta caretta, nesting in Japan: bottlenecks on the Pacific population. Mar Biol 141:299–305

    Article  Google Scholar 

  • Hatase H, Omuta K, Tsukamoto K (2007) Bottom or midwater: alternative foraging behaviours in adult female loggerhead sea turtles. J Zool 273:46–55

    Article  Google Scholar 

  • Hawkes LA, Broderick AC, Coyne MS, Godfrey MH, Lopez-Jurado LF, Lopez-Suarez P, Merino SE, Varo-Cruz N, Godley BJ (2006) Phenotypically linked dichotomy in sea turtle foraging requires multiple conservation approaches. Curr Biol 16:990–995

    Article  CAS  Google Scholar 

  • Hawkes LA, Broderick AC, Coyne MS, Godfrey MH, Godley BJ (2007) Only some like it hot—quantifying the environmental niche of the loggerhead sea turtle. Divers Distrib 13:447–457

    Article  Google Scholar 

  • Hawkes LA, Witt MJ, Broderick AC, Coker JW, Coyne MS, Dodd M, Frick MG, Godfrey MH, Griffin DB, Murphy SR, Murphy TM, Williams KL, Godley BJ (2011) Home on the range: spatial ecology of loggerhead turtles in Atlantic waters of USA. Divers Distrib 17:624–640

    Article  Google Scholar 

  • Hochscheid S, Bentivegna F, Speakman JR (2004) Long-term cold acclimation leads to high Q10 effects on oxgen consumption of loggerhead sea turtle Caretta caretta. Physiol Biochem Zool 77:209–222

    Article  Google Scholar 

  • Hochscheid S, Bentivegna F, Hays GC (2005) First records of dive durations for a hibernating sea turtle. Biol Lett 1:82–86

    Article  Google Scholar 

  • Hochscheid S, Bentivegna F, Bradai MN, Hays GC (2007) Overwintering behaviour in sea turtles: dormancy is optional. Mar Ecol Prog Ser 340:287–298

    Article  Google Scholar 

  • Houghton JDR, Doyle TK, Davenport J, Wilson RP, Hays GC (2008) The role of infrequent and extraordinary deep dives in leatherback turtles (Dermochelys coriacea). J Exp Biol 211:2566–2575

    Article  Google Scholar 

  • Ishihara T, Kamezaki N (2011) Size at maturity and tail elongation of loggerhead turtles (Caretta caretta) in the North Pacific. Chelon Conserv Biol 10:281–287

    Article  Google Scholar 

  • Ishihara T, Kamezaki N, Matsuzawa Y, Iwamoto F, Oshika T, Miyanaga Y, Ebisui C, Yamashita S (2011) Reentry of juvenile and subadult loggerhead turtles into natal waters of Japan. Curr Herpetol 30:63–68

    Article  Google Scholar 

  • Kamezaki N, Miyawaki I, Suganuma H, Omuta K, Nakajima Y, Goto K, Sato K, Matsuzawa Y, Samejima M, Ishii M, Iwamoto T (1997) Post-nesting migration of Japanese loggerhead turtle, Caretta caretta. Wildl Conserv Jpn 3:29–39 (In Japanese)

    Google Scholar 

  • Kamezaki N, Matsuzawa Y, Abe O et al (2003) Loggerhead turtles nesting in Japan. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Institution, Washington, pp 210–217

    Google Scholar 

  • Kimura S, Nakata H, Okazaki Y (2000) Biological production in meso-scale eddies caused by frontal disturbances of the Kuroshio Extension. ICES J Mar Sci 57:133–142

    Article  Google Scholar 

  • Lewison RL, Freeman SA, Crowder LB (2004) Quantifying the effects of fisheries on threatened species: the impact of pelagic longlines on loggerhead and leatherback sea turtles. Ecol Lett 7:221–231

    Article  Google Scholar 

  • Lohrenz SE, Castro BM (2006) Western ocean boundaries. In: Robinson AR, Brink KH (eds) The sea, Volume14A: the global coastal ocean. Harvard University Press, Harvard, pp 3–20

    Google Scholar 

  • Lutcavage M, Musick JA (1985) Aspects of the biology of sea turtles in Virginia. Copeia 1985:449–456

    Article  Google Scholar 

  • Lutz PL, Bergey A, Bergey M (1989) Effects of temperature on gas exchange and aid-base balance in the sea turtle Caretta caretta at rest and during routine activity. J Exp Biol 144:155–169

    Google Scholar 

  • Mansfield KL, Saba VS, Keinath JA, Musick JA (2009) Satellite tracking reveals a dichotomy in migration strategies among juvenile loggerhead turtles in the Northwest Atlantic. Mar Biol 156:2555–2570

    Article  Google Scholar 

  • McClellan CM, Read AJ (2007) Complexity and variation in loggerhead sea turtle life history. Biol Lett 3:592–594

    Article  Google Scholar 

  • Mendoca MT, Ehrhart LM (1982) Activity, population size and structure of immature Chelonia mydas and Caretta caretta in mosquito Lagoon, Florida. Copeia 1982:161–167

    Article  Google Scholar 

  • Milton SL, Lutz PL (2003) Physiological and genetic responses to environmental stress. In: Lutz PL, Musick JA, Wyneken J (eds) The biology of sea turtles, vol II. CRC Press, Florida, pp 163–197

    Google Scholar 

  • Minamikawa S, Naito Y, Sato K, Matsuzawa Y, Bando T, Sakamoto W (2000) Maintenance of neutral buoyancy by depth selection in the loggerhead turtle Caretta caretta. J Exp Biol 203:2967–2975

    CAS  Google Scholar 

  • Morreale SJ, Meylan AB, Sadove SS, Standora EA (1992) Annual occurrence and winter mortality of marine turtles in New York waters. J Herpetol 26:301–308

    Article  Google Scholar 

  • 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 137–164

    Google Scholar 

  • Narazaki T (2009) Diving behaviour of loggerhead turtles, Caretta caretta, migrating to the northern Pacific coast of Japan. Dissertation, The University of Tokyo

  • Narazaki T, Sato K, Abernathy KJ, Marshall GJ, Miyazaki N (2013) Loggerhead turtles (Caretta caretta) use vision to forage on gelatinous prey in mid-water. PLoS ONE 8:e66043. doi:10.1371/journal.pone.0066043

    Article  CAS  Google Scholar 

  • Nishizawa H, Narazaki T, Fukuoka T, Sato K, Hamabata T, Kinoshita M, Arai N (2014) Genetic composition of loggerhead turtle feeding aggregations: migration patterns in the North Pacific. Endanger Species Res 24:85–93

    Article  Google Scholar 

  • Norse EA, Crowder LB (2005) Why marine conservation biology? In: Norse EA, Crowder LB (eds) Marine conservation biology: The science of maintaining the sea’s biodiversity. Island press, Washington, pp 1–18

    Google Scholar 

  • Parker DM, Cooke WJ, Balazs GH (2005) Diet of oceanic loggerhead sea turtles (Caretta caretta) in the central North Pacific. Fish Bull 103:142–152

    Google Scholar 

  • Parrish JK (2005) Behavioural approaches to marine conservation. In: Norse EA, Crowder LB (eds) Marine conservation biology: the science of maintaining the sea’s biodiversity. Island Press, Washington, pp 80–104

    Google Scholar 

  • Plotkin PT (2003) Adult migrations and habitat use. In: Lutz PL, Musick JA, Wyneken J (eds) The biology of sea turtles, vol II. CRC Press, Florida, pp 225–241

    Google Scholar 

  • Polovina J, Kobayashi DR, Parker DM, Seki MP, Balazs GH (2000) Turtles on the edge: movement of loggerhead turtles (Caretta caretta) along oceanic fronts, spanning longline fishing grounds in the central North Pacific 1997–1998. Fish Oceanogr 9:71–82

    Article  Google Scholar 

  • Polovina JJ, Balazs GH, Howell EA, Parker DM, Seki MP, Dutton PH (2004) Forage and migration habitat of loggerhead (Caretta caretta) and olive ridley (Lepidochelys olivacea) sea turtles in the central North Pacific Ocean. Fish Oceanogr 13:36–51

    Article  Google Scholar 

  • Polovina J, Uchida I, Balazs G, Howell EA, Parker D, Dutton P (2006) The Kuroshio extension bifurcation region: a pelagic hotspot for juvenile loggerhead sea turtles. Deep-Sea Res PT II 53:326–339

    Article  Google Scholar 

  • Qiu B (2002) The Kuroshio Extension system: its large-scale variability and role in the midlatitude ocean-atmosphere interaction. J Oceanogr 58:57–75

    Article  Google Scholar 

  • Roe JH, Morreale SJ, Paladino FV, Shillinger GL, Benson SR, Eckert SA, Bailey H, Tomillo PS, Bograd SJ, Eguchi T, Dutton PH, Seminoff JA, Block BA, Spotila JR (2014) Predicting bycatch hotspots for endangered leatherback turtles on longlines in the Pacific Ocean. Proc R Soc B. doi:10.1098/rspb.2013.2559

    Google Scholar 

  • Sakamoto W, Uchida I, Naito Y, Kureha K, Tujiura M, Sato K (1990) Deep diving behaviour of loggerhead turtle near the frontal zone. Nippon Suisan Gakkaishi 56:1435–1443

    Article  Google Scholar 

  • Sato K (2014) Body temperature stability achieved by the large body mass of sea turtles. J Exp Biol 217:3607–3614

    Article  Google Scholar 

  • Sato K, Sakamoto W, Matsuzawa Y, Tanaka H, Naito Y (1994) Correlation between stomach temperatures and ambient water temperatures in free-ranging loggerhead turtles, Caretta caretta. Mar Biol 118:343–351

    Article  Google Scholar 

  • Sato K, Otsuki M, Morita K, Kurosawa M, Takada J (2007) Result of hydrographic meteorologic observation in 2006. Annual report of International Coastal Research Center, the University of Tokyo 32: 37–47 (in Japanese)

  • Seo Y, Sugimoto S, Hanawa K (2014) Long-term variation of the Kuroshio Extension path in winter: meridional movement and path state change. J Clim 27:5929–5940

    Article  Google Scholar 

  • Suganuma H, Kamezaki N (1991) Measuring and tagging procedures standardized in Japan. Mar Turt Newsl 54:16–17

    Google Scholar 

  • Takasugi S (1992) Distribution of Tsugaru warm Current water in the Iwate coastal area and their influence to the sea surface temperature at coastal hydrographic station. Fish Oceanogr 56:434–448 (in Japanese)

    Google Scholar 

  • Ultsch GR (2006) The ecology of overwintering among turtles: where turtles overwinter and its consequences. Biol Rev 81:339–367

    Article  Google Scholar 

  • Watanabe Y, Baranov EA, Sato K, Naito Y, Miyazaki N (2006) Body density affects stroke patterns in Baikal seals. J Exp Biol 209:3269–3280

    Article  Google Scholar 

  • Witherington BE, Ehrhart LM (1989) Hypothermic stunning and mortality of marine turtles in the Indian river lagoon system, Florida. Copeia 1989:696–703

    Article  Google Scholar 

  • Zbinden JA, Aebischer A, Margaritoulis D, Arlettaz R (2008) Important areas at sea for adult loggerhead sea turtles in the Mediterranean Sea: satellite tracking corroborates findings from potentially biased sources. Mar Biol 153:899–906

    Article  Google Scholar 

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Acknowledgments

This study was conducted with permission from the Ethics Committee of the University of Tokyo. This study could not be achieved without great volunteers from Fisheries Cooperative Association of Funakoshi Bay, Hirota Bay, Kamaishi Bay, Kamaishi-Tobu, Miyako, Ofunato, Okirai, Omoe, Otsuchi, Ryori, Sanriku-Yamada, Sasaki, Toni and Yoshihama for providing us with wild-caught sea turtles. We are grateful to Y. Fujiwara, H. Murasaki, K. Onizuka and S. Takuma for their assistance in collecting, measuring and handling the turtles. We gratefully acknowledge M. Kurosawa, K. Morita, J. Takada, M. Hirano, A. Koshida, R. Koshida, Y. Watanabe, N. Katsumata, E. Sawai and I. Nakamura for their assistance in the field. We also acknowledge NPO Everlasting Nature of Asia for recovering satellite-relayed data logger from a stranded turtle. Special thanks go to K. Aoki, H. Shimadzu, S. Isojunno and Y. Papastamatiou for lots of useful advices. This work was supported by the program ‘Bio-logging Science’, The University of Tokyo (UTBLS), a JSPS research grant (24241001 to KS), a JSPS Research Fellowship for Young Scientists to TN (21-7432) and a Sasakawa Scientific Research Grant from The Japan Science Society to TN (19-526). We also acknowledge the use of the Maptool (http://www.seaturtle.org/) program for the maps of study site. The AVHRR Oceans Pathfinder SST data were obtained from Physical Oceanography Distributed Active Archive Center (http://podaac.jpl.asa.gov). We thank two anonymous reviewers for the constructive comments. Finally, we would like to dedicate our work to all the people in our study site who were severely suffered by tsunami in 11 March 2011.

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  1. Sea Mammal Research Unit, School of Biology, University of St Andrews, Fife, KY16 9TS, UK

    Tomoko Narazaki

  2. Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba, 277-8564, Japan

    Katsufumi Sato

  3. Japan Marine Science Foundation, 1-1-1 Ikenohata, Taito-ku, Tokyo, 110-0008, Japan

    Nobuyuki Miyazaki

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  1. Tomoko Narazaki
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  2. Katsufumi Sato
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Correspondence to Tomoko Narazaki.

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Communicated by J. Houghton.

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Narazaki, T., Sato, K. & Miyazaki, N. Summer migration to temperate foraging habitats and active winter diving of juvenile loggerhead turtles Caretta caretta in the western North Pacific. Mar Biol 162, 1251–1263 (2015). https://doi.org/10.1007/s00227-015-2666-0

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