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Genetic fingerprinting reveals natal origins of male leatherback turtles encountered in the Atlantic Ocean and Mediterranean Sea

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Abstract

Understanding population dynamics in broadly distributed marine species with cryptic life history stages is challenging. Information on the population dynamics of sea turtles tends to be biased toward females, due to their accessibility for study on nesting beaches. Males are encountered only at sea; there is little information about their migratory routes, residence areas, foraging zones, and population boundaries. In particular, male leatherbacks (Dermochelys coriacea) are quite elusive; little is known about adult and juvenile male distribution or behavior. The at-sea distribution of male turtles from different breeding populations is not known. Here, 122 captured or stranded male leatherback turtles from the USA, Turkey, France, and Canada (collected 1997–2012) were assigned to one of nine Atlantic basin populations using genetic analysis with microsatellite DNA markers. We found that all turtles originated from western Atlantic nesting beaches (Trinidad 55%, French Guiana 31%, and Costa Rica 14%). Although genetic data for other Atlantic nesting populations were represented in the assignment analysis (St. Croix, Brazil, Florida, and Africa (west and south), none of the male leatherbacks included in this study were shown to originate from these populations. This was an unexpected result based on estimated source population sizes. One stranded turtle from Turkey was assigned to French Guiana, while others that were stranded in France were from Trinidad or French Guiana breeding populations. For 12 male leatherbacks in our dataset, natal origins determined from the genetic assignment tests were compared to published satellite and flipper tag information to provide evidence of natal homing for male leatherbacks, which corroborated our genetic findings. Our focused study on male leatherback natal origins provides information not previously known for this cryptic, but essential component of the breeding population. This method should provide a guideline for future studies, with the ultimate goal of improving management and conservation strategies for threatened and endangered species by taking the male component of the breeding population into account.

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References

  • Åkesson S, Weimerskirch H (2014) Evidence for sex-segregated ocean distributions of first-winter wandering albatrosses at Crozet islands. PLoS One 9:e86779. doi:10.1371/journal.pone.0086779

    Article  Google Scholar 

  • Bailey H, Benson SR, Shillinger GL et al (2012) Leatherback turtle movement patterns. Bull Ecol Soc Am 93:165–169

    Article  Google Scholar 

  • Baker JD, Antonelis GA, Fowler CW, York AE (1995) Natal site fidelity in northern fur seals, Callorhinus ursinus. Anim Behav 50(1):237–247

    Article  Google Scholar 

  • Bannister N, Holland J, Farrelly T (2016) Nest site fidelity of flatback Turtles (‘Natator depressus’) on Bare Sand Island, Northern Territory, Australia. North Territ Nat 27:47–53

    Google Scholar 

  • Billes A, Fretey J, Verhage B et al (2006) First evidence of leatherback movement from Africa to South America. Mar Turt Newsl 111:13–14

    Google Scholar 

  • Block BA, Jonsen ID, Jorgensen SJ et al (2011) Tracking apex marine predator movements in a dynamic ocean. Nature 475:86–90. doi:10.1038/nature10082

    Article  CAS  Google Scholar 

  • Bolker B, Okayama T, Bjorndal KA, Bolten AB (2007) Incorporating multiple mixed stocks in mixed stock analysis: “many-to-many” analyses. Mol Ecol 16:685–695. doi:10.1111/j.1365-294X.2006.03161.x

    Article  CAS  Google Scholar 

  • Bowen BW, Karl SA (2007) Population genetics and phylogeography of sea turtles. Mol Ecol 16:4886–4907. doi:10.1111/j.1365-294X.2007.03542.x

    Article  CAS  Google Scholar 

  • Bowen BW, Bass AL, Soares LS, Toonen RJ (2005) Conservation implications of complex population structure: lessons from the loggerhead turtle (Caretta caretta). Mol Ecol 14:2389–2402

    Article  CAS  Google Scholar 

  • Casale P, Freggi D, Cinà A, Rocco M (2012) Spatio-temporal distribution and migration of adult male loggerhead sea turtles (Caretta caretta) in the Mediterranean Sea: further evidence of the importance of neritic habitats off North Africa. Mar Biol 160:703–718. doi:10.1007/s00227-012-2125-0

    Article  Google Scholar 

  • Chacón-Chaverri D, Eckert KL (2007) Leatherback sea turtle nesting at Gandoca Beach in Caribbean Costa Rica: management recommendations from fifteen years of conservation. Chelonian Conserv Biol 6:101–110. doi:10.2744/1071-8443(2007)6[101:LSTNAG]2.0.CO;2

  • Davenport J (1997) Temperature and the life-history strategies of sea turtles. J Therm Biol 22:479–488. doi:10.1016/S0306-4565(97)00066-1

  • Dizon AE, Balazs GH (1982) Radio telemetry of Hawaiin green turtles at their breeding colony. Mar Fish 44:13–20

    Google Scholar 

  • Dodge KL, Logan JM, Lutcavage ME (2011) Foraging ecology of leatherback sea turtles in the Western North Atlantic determined through multi-tissue stable isotope analyses. Mar Biol 158:2813–2824. doi:10.1007/s00227-011-1780-x

    Article  Google Scholar 

  • Dodge KL, Galuardi B, Miller TJ, Lutcavage ME (2014) Leatherback turtle movements, dive behavior, and habitat characteristics in ecoregions of the Northwest Atlantic ocean. PLoS One 9(3):e91726. doi:10.1371/journal.pone.0091726

    Article  Google Scholar 

  • Doyle TK, Houghton JD, O’Súilleabháin PF, Hobson VJ, Marnell F, Davenport J, Hays GC (2008) Leatherback turtles satellite-tagged in European waters. Endanger Species Res 4:23–31. doi:10.3354/esr00076

    Article  Google Scholar 

  • Dutton PH (1995) Molecular evolution of sea turtles with special reference to the leatherback, Dermochelys coriacea. Dissertation, Texas A&M University, College Station

  • Dutton PH, Frey A (2009) Characterization of polymorphic microsatellite markers for the green turtle (Chelonia mydas). Mol Ecol Resour 9:354–356. doi:10.1111/j.1755-0998.2008.02443.x

    Article  CAS  Google Scholar 

  • Dutton PH, Roden SE, Stewart KR et al (2013) Population stock structure of leatherback turtles (Dermochelys coriacea) in the Atlantic revealed using mtDNA and microsatellite markers. Conserv Genet 14:625–636. doi:10.1007/s10592-013-0456-0

    Article  Google Scholar 

  • FitzSimmons NN, Limpus CJ, Norman JA et al (1997) Philopatry of male marine turtles inferred from mitochondrial DNA markers. Proc Natl Acad Sci 94:8912–8917

    Article  CAS  Google Scholar 

  • Fossette S, Witt MJ, Miller P et al (2014) Pan-Atlantic analysis of the overlap of a highly migratory species, the leatherback turtle, with pelagic longline fisheries. Proc R Soc London B Biol Sci. doi:10.1098/rspb.2013.3065

    Google Scholar 

  • Fuentes MMPB, Hamann M, Limpus CJ (2010) Past, current and future thermal profiles of green turtle nesting grounds: implications from climate change. J Exp Mar Biol Ecol 383:56–64

    Article  Google Scholar 

  • Geldiay R, Koray T, Balik S (1995) Status of sea turtle populations (Caretta caretta and Chelonia mydas) in the Northern Mediterranean Sea, Turkey. In: Bjorndal KA (ed) Biology and conservation of sea turtles, Revised edn. Smithsonian Institution Press, Washington D.C., pp 425–434

    Google Scholar 

  • Groombridge B (1990) Marine turtles in the Mediterranean: distribution, population status, conservation. A report to the Council of Europe, Environment Conservation and Management Division

  • Hamann M, Godfrey M, Seminoff J et al (2010) Global research priorities for sea turtles: informing management and conservation in the 21st century. Endanger Species Res 11:245–269. doi:10.3354/esr00279

    Article  Google Scholar 

  • Hart KM, Mooreside P, Crowder LB (2006) Interpreting the spatio-temporal patterns of sea turtle strandings: going with the flow. Biol Conserv 129:283–290

    Article  Google Scholar 

  • Hays GC, Ferreira LC, Sequeira AMM et al (2016) Key questions in marine megafauna movement ecology. Trends Ecol Evol. doi:10.1016/j.tree.2016.02.015

    Google Scholar 

  • Hoffman JI, Forcada J (2012) Extreme natal philopatry in female Antarctic fur seals (Arctocephalus gazella). Mamm Biol Zeitschrift für Säugetierkd 77:71–73. doi:10.1016/j.mambio.2011.09.002

    Article  Google Scholar 

  • Innis C, Merigo C, Dodge KL et al (2010) Health evaluation of leatherback turtles (Dermochelys coriacea) in the Northwestern Atlantic during direct capture and fisheries gear disentanglement. Chelonian Conserv Biol 9:205–222. doi:10.2744/CCB-0838.1

    Article  Google Scholar 

  • Innis CJ, Merigo C, Cavin JM, Hunt K, Dodge KL, Lutcavage M (2014) Serial assessment of the physiological status of leatherback turtles (Dermochelys coriacea) during direct capture events in the northwestern Atlantic Ocean: comparison of post-capture and pre-release data. Conserv Physiol. doi:10.1093/conphys/cou048

    Google Scholar 

  • James MC, Eckert SA, Myers RA (2005) Migratory and reproductive movements of male leatherback turtles (Dermochelys coriacea). Mar Biol 147:845–853. doi:10.1007/s00227-005-1581-1

    Article  Google Scholar 

  • James M, Sherrill-Mix S, Myers R (2007) Population characteristics and seasonal migrations of leatherback sea turtles at high latitudes. Mar Ecol Prog Ser 337:245–254. doi:10.3354/meps337245

    Article  Google Scholar 

  • Jensen MP, FitzSimmons NN, Dutton PH, Michael P (2013) Molecular genetics of sea turtles. In: Wyneken J, Lohmann KJ, Musick JA (eds) Biology of sea turtles, vol 3. CRC Press. Boca Raton, FL, pp 135–154

    Chapter  Google Scholar 

  • Kalinowski ST, Manlove KR, Taper ML (2007) ONCOR: a computer program for genetic stock identification. Montana State University, Bozeman, Montana. www.montana.edu/kalinowski/Software/ONCOR.htm. Accessed 26 Sept 2014

  • Komoroske LM, Jensen MP, Stewart KR, Shamblin BM, Dutton PH (2017) Advances in the application of genetics in marine turtle biology and conservation. Front Mar Sci 4:156. doi:10.3389/fmars.2017.00156

    Article  Google Scholar 

  • Laloë J-O, Cozens J, Renom B et al (2014) Effects of rising temperature on the viability of an important sea turtle rookery. Nat Clim Chang 4:513–518. doi:10.1038/NCLIMATE2236

    Article  Google Scholar 

  • Levy Y, King R, Aizenberg I (2005) Holding a live leatherback turtle in Israel: lessons learned. Mar Turt Newsl 107:7–8

    Google Scholar 

  • Limpus CJ (1993) The green turtle, Chelonia mydas, in Queensland: breeding males in the southern Great Barrier Reef. Wildl Res 20:513. doi:10.1071/WR9930513

    Article  Google Scholar 

  • López-Mendilaharsu M, Rocha CFD, Miller P, Domingo A, Prosdocimi L (2009) Insights on leatherback turtle movements and high use areas in the Southwest Atlantic Ocean. J Exp Mar Biol Ecol 378:31–39

    Article  Google Scholar 

  • Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions with appropriate techniques. Trends Ecol Evol 20:136–142. doi:10.1016/j.tree.2004.12.004

    Article  Google Scholar 

  • Maniatis T, Fritsch E, Sambrook J (1982) Molecular cloning laboratory manual. Cold Spring Harbor Press, Cold Spring

    Google Scholar 

  • Mrosovsky N, Dutton PH, Whitmore CP (1984) Sex ratios of two species of sea turtle nesting in Suriname. Can J Zool 62:2227–2239. doi:10.1139/z84-324

    Article  Google Scholar 

  • Murphy TM, Murphy SR, Griffin DB, Hope CP (2006) Recent occurrence, spatial distribution, and temporal variability of leatherback turtles (Dermochelys coriacea) in nearshore waters of South Carolina, USA. Chelonian Conserv Biol 5:216–224. doi:10.2744/1071-8443(2006)5[216:ROSDAT]2.0.CO;2

  • Ordoñez C, Troëng S, Meylan A, Meylan P, Ruiz A (2007) Chiriqui Beach, Panama, the most important leatherback nesting beach in Central America. Chelonian Conserv Biol 6:122–126. doi:10.2744/1071-8443(2007)6[122:CBPTMI]2.0.CO;2

  • Prosdocimi L, Dutton PH, Albareda D, Remis MI (2014) Origin and genetic diversity of leatherbacks (Dermochelys coriacea) at Argentine foraging grounds. J Exp Mar Bio Ecol 458:13–19. doi:10.1016/j.jembe.2014.04.025

    Article  Google Scholar 

  • Rees AF, Saad A, Jony M (2004) First record of a leatherback turtle in Syria. Mar Turt Newsl 106:13

    Google Scholar 

  • Roden SE, Dutton PH (2011) Isolation and characterization of 14 polymorphic microsatellite loci in the leatherback turtle (Dermochelys coriacea) and cross-species amplification. Conserv Genet Resour 3:49–52. doi:10.1007/s12686-010-9284-4

    Article  Google Scholar 

  • Roden SE, Morin PA, Frey A, Balazs GH, Zarate P, Cheng IJ, Dutton PH (2013) Green turtle population structure in the Pacific: new insights from single nucleotide polymorphisms and microsatellites. Endanger Species Res 20:227–234. doi:10.3354/esr00500

    Article  Google Scholar 

  • Schofield G, Hobson VJ, Fossette S, Lilley MKS, Katselidis KA, Hays GC (2010) Biodiversity research: fidelity to foraging sites, consistency of migration routes and habitat modulation of home range by sea turtles. Divers Distrib 16:840–853. doi:10.1111/j.1472-4642.2010.00694.x

    Article  Google Scholar 

  • Shamblin BM, Bolten AB, Abreu-Grobois FA, Bjorndal KA, Cardona L et al (2014) Geographic patterns of genetic variation in a broadly distributed marine vertebrate: new insights into loggerhead turtle stock structure from expanded mitochondrial DNA sequences. PLoS One 9(1):e85956. doi:10.1371/journal.pone.0085956

    Article  Google Scholar 

  • Sönmez B, Sammy D, Yalçın-Özdilek Ş, Gönenler Ö, Açıkbaş U, Ergün Y, Kaska Y (2008) A stranded leatherback sea turtle in the northeastern Mediterranean, Hatay, Turkey. Mar Turt Newsl 119:12–13

    Google Scholar 

  • Stewart KR, Dutton PH (2014) Breeding sex ratios in adult leatherback turtles (Dermochelys coriacea) may compensate for female-biased hatchling sex ratios. PLoS One 9:e88138. doi:10.1371/journal.pone.0088138

    Article  Google Scholar 

  • Stewart KR, Johnson C, Godfrey MH (2007) The minimum size of leatherbacks at reproductive maturity, with a review of sizes for nesting females from the Indian, Atlantic and Pacific Ocean basins. Herpetol J 17:123–128

    Google Scholar 

  • Stewart KR, James MC, Roden SE, Dutton PH (2013) Assignment tests, telemetry and tag-recapture data converge to identify natal origins of leatherback turtles foraging in Atlantic Canadian waters. J Anim Ecol. doi:10.1111/1365-2656.12056

    Google Scholar 

  • Stewart KR, LaCasella EL, Roden SE et al (2016) Nesting population origins of leatherback turtles caught as bycatch in the US pelagic longline fishery. Ecosphere 7:01272

    Article  Google Scholar 

  • Taskavak E, Boulon RH Jr, Atatur MK (1998) An unusual stranding of a leatherback turtle in Turkey. Mar Turt Newsl 80:13

    Google Scholar 

  • Tucker AD, MacDonald BD, Seminoff JA (2014) Foraging site fidelity and stable isotope values of loggerhead turtles tracked in the Gulf of Mexico and northwest Caribbean. Mar Ecol Prog Ser 502:267–279. doi:10.3354/meps10655

    Article  CAS  Google Scholar 

  • Velez-Zuazo X, Ramos WD, Van Dam RP, Diez CE, Abreu-Grobois A, Mcmillan WO (2008) Dispersal, recruitment and migratory behaviour in a hawksbill sea turtle aggregation. Mol Ecol 17:839–853. doi:10.1111/j.1365-294X.2007.03635.x

    Article  CAS  Google Scholar 

  • Wallace BP, DiMatteo AD, Hurley BJ et al (2010) Regional management units for marine turtles: a novel framework for prioritizing conservation and research across multiple scales. PLoS One 5:e15465. doi:10.1371/journal.pone.0015465

    Article  Google Scholar 

  • Witt MJ, Augowet Bonguno E, Broderick AC et al (2011) Tracking leatherback turtles from the world’s largest rookery: assessing threats across the South Atlantic. Proc Biol Sci 278:2338–2347. doi:10.1098/rspb.2010.2467

    Article  Google Scholar 

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Acknowledgements

Samples were collected under ESA Section 10(a)(1)(A) permits issued by NMFS to the Southeast Fisheries Science Center (#1260, #1324, #1429 and #1552) and the University of New Hampshire (#1557 and #15672). These samples were imported from the high seas under the authority of the USFWS CITES Permit #US045532/9. Sample collection in Nova Scotia, Canada, was supported by funding from Canadian Wildlife Federation, Environment Canada, Fisheries and Oceans Canada, George Cedric Metcalf Foundation, Habitat Stewardship Program for Species at Risk, National Fish and Wildlife Foundation (USA), National Marine Fisheries Service (USA), Natural Sciences and Engineering Research Council of Canada, and World Wildlife Fund Canada. Funding for US samples was provided by National Oceanic and Atmospheric Administration, Massachusetts Division of Marine Fisheries, National Fish and Wildlife Foundation, and Cape Cod Commercial Fisherman’s Alliance. Funding support for this analysis and for Kelly R. Stewart was provided by a Lenfest Ocean Program Grant. The views expressed are those of the authors and do not necessarily reflect the views of the Lenfest Ocean Program or The Pew Charitable Trusts. We thank the Aquarium La Rochelle SAS Network and the Centre d’Etudes et de Soins pour les Tortues Marines for coordinating collection of samples from the Atlantic French Network: Réseau Tortues Marines Atlantique Est. For help with sample collection at sea in Canada, we thank S. Craig, B. Fricker, H. Fricker, J. Fricker, W. George, B. Mitchell, and M. Nicholson. We also thank D. Archibald, L. Bennett, C. Harvey-Clark, and K. Martin for stranding response and sample preparation in Canada. We are grateful to M. Lutcavage, A. Myers, C. Merigo, C. Innis, T. Norton, M. Dodge, G. Purmont, M. Leach, B. Sharp, S. Landry, T. Sheehan, V. Saba, M. Murphy, G. Tomasian, N. Fragoso, K. Sampson, R. Smolowitz, K. Hirokawa, J. Casey, S. Leach, J. Wilson, and E. Eldredge for associated field assistance in the USA. We thank the following individuals and organizations: in the USA, Lisa Belskis, Wendy Teas, Kate Sardi Sampson, Donna Shaver, Bob Prescott, Anthony Amos, and Sara McNulty, New England Aquarium and Center for Coastal Studies, and in Turkey, Ertan Taskavak. For laboratory, technical, and logistical assistance at the Southwest Fisheries Science Center, we thank Gabriela Serra-Valente, Amy Lanci, Amy Frey, Robin LeRoux, Amanda Bowman, and Victoria Pease. Thoughtful review and ideas that contributed to the original draft were provided by Michael Jensen and Amy Frey, while Erin LaCasella contributed maps made using Maptool at seaturtle.org. We sincerely thank the reviewers of this paper as well as the handling editor.

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Authors and Affiliations

  1. Marine Mammal and Turtle Division, Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 8901 La Jolla Shores Dr., La Jolla, CA, 92037, USA

    Suzanne E. Roden & Peter H. Dutton

  2. The Ocean Foundation, The Sunderland Building, 1320 19th Street, NW, 5th Floor, Washington, DC, 20036, USA

    Kelly R. Stewart

  3. Population Ecology Division, Fisheries and Oceans Canada, Bedford Institute of Oceanography, Dartmouth, NS, B2Y 4A2, Canada

    Michael C. James

  4. Biology Department, Woods Hole Oceanographic Institution, 266 Woods Hole Road, Woods Hole, MA, 02543, USA

    Kara L. Dodge

  5. Aquarium La Rochelle, Centre d’Etudes et de Soins pour les Tortues Marines, 17000, La Rochelle, France

    Florence Dell’Amico

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  1. Suzanne E. Roden
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  2. Kelly R. Stewart
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  3. Michael C. James
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  4. Kara L. Dodge
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  6. Peter H. Dutton
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Correspondence to Suzanne E. Roden.

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Roden, S.E., Stewart, K.R., James, M.C. et al. Genetic fingerprinting reveals natal origins of male leatherback turtles encountered in the Atlantic Ocean and Mediterranean Sea. Mar Biol 164, 181 (2017). https://doi.org/10.1007/s00227-017-3211-0

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