Conservation Genetics

, Volume 16, Issue 5, pp 1069–1083 | Cite as

Population structure enhances perspectives on regional management of the western Indian Ocean green turtle

  • Jérôme Bourjea
  • Jeanne A. Mortimer
  • Julie Garnier
  • Gladys Okemwa
  • Brendan J. Godley
  • George Hughes
  • Mayeul Dalleau
  • Claire Jean
  • Stéphane Ciccione
  • Delphine Muths
Research Article


To refine our understanding of the spatial structure of the green turtle (Chelonia mydas) populations in the South West Indian Ocean (SWIO), we analysed patterns of mitochondrial DNA (396 base pairs control region fragment) variation among 171 samples collected at five distinct locations (Kenya, Northern Mozambique, and three locations in the Republic of Seychelles: the Granitic, Amirantes, and Farquhar groups) and compared them to genetic data (n = 288), previously collected from 10 southern locations in the SWIO. We also analysed post-nesting satellite tracks (n = 4) from green turtles nesting in the Amirantes group. Pairwise comparisons of haplotype frequencies showed significant genetic differentiation amongst rookeries and suggest that the SWIO hosts two main genetic stocks of nesting green turtles that could themselves be divided in two sub-stocks that still need to be confirmed: A. the Southern Mozambique Channel, that could be composed of two sub-stocks (a1) Europa and (a2) Juan de Nova, and B. the Northern SWIO (N-SWIO) comprising two sub-stocks (b1) the Seychelles archipelago stock—SEY; and (b2) the remaining Northern SWIO rookeries. The newly revealed differentiation of the Seychelles population is supported by restricted migration of females tracked from the Amirantes group suggesting relatively limited links with other regional stocks. We hypothesize that this differentiation could be due to local and regional current patterns and to the role of the Indo-Pacific Barrier as a genetic break, enhanced during periods of sea level decrease associated with a rare but continuous flow of hatchlings and young juveniles from Western Australia.


Indian Ocean mtDNA Satellite tracking Phylogeography Management unit Chelonia mydas 



The authors are most grateful for the financial support of this study provided by European Union (FSE and FEDER), Regional Council of La Réunion, FAO within the framework of the FAO project GCP/INT/919/JPN “Interactions between Sea Turtles and Fisheries within an Ecosystem Approach to Fisheries Management”, the EU 7th Funding Program - Capacities, Research Potential (project RUNSeaSciences) and the SWIOFP project funded by the GEF and World Bank. In Seychelles, for assistance with genetic sample collection, JAM is grateful to: R. Bresson (Bird); L. Vanherck, U. Bristol (Ile du Nord); P. Hitchins (Cousine); A. Burt, N. Dunn (Curieuse); T. Reposa, G. Canning (Fregate); C. Arnold (Aride); E. Talma (Mahé); N. Boniface, D. Bristol, W. Labrosse, C. Boyes, R. von Brandis (D’Arros & St. Joseph); T. Jupiter (Desroches); A. Duhec, R. Jeanne, P-A. Adam, S. Balderson (Alphonse); and G. Esparon (Farquhar). In Chagos, for assistance with sample collection, JAM is grateful to: N. Esteban, N. Guzman, G. Hays, the 1996 and 2006 Chagos Expeditions, Fauna & Flora International, the BIOT Scientific Advisory Group (SAG), and Darwin Initiative Challenge Fund grant (EIDCF008). Field assistance to attach the satellite tags at St. Joseph was provided by R. von Brandis, N. Boniface, W. Labrosse, and D. Bristol. Organizational support in Seychelles came from D’Arros Research Centre (DRC), Island Conservation Society (ICS), Islands Development Company (IDC), Save Our Seas Foundation (SOSF), Seychelles Islands Foundation (SIF), Seychelles Department of Environment; while project funding came from the GEF EMPS-J1: Turtle and Tortoise Conservation Project, and Turtle Component of the GEF-SEYMEMP Project. The turtle project in northern Mozambique was funded by the Maluane/Cabo Delgado Biodiversity and Tourism Project, the Zoological Society of London, Tusk Trust, the European Association of Zoo and Aquaria. BJG was supported by the Darwin Initiative. Samples for Kenya collected through KESCOM, by Watamu Turtle Watch. Finally, we would like to thank Laurence Maurel for the IDW approach used in his study.

Supplementary material

10592_2015_723_MOESM1_ESM.doc (89 kb)
Supplementary material 1 (DOC 89 kb)


  1. Abdul-Muneer PM (2014) Application of microsatellite markers in conservation genetics and fisheries management: recent advances in population structure analysis and conservation strategies. Genet Res Int. doi: 10.1155/2014/691759 PubMedCentralPubMedGoogle Scholar
  2. Abreu-Grobois FA, Horrocks JA, Formia A, Dutton PH, LeRoux R, Velez-Zuazo X et al. (2006) New mtDNA D-loop primers which work for a variety of marine turtle species may increase the resolution of mixed stock analysis. pp. 179 in M. Frick, A. Panagopoulous, A. F. Rees, K. Williams, eds. Proceedings of the 26th annual symposium on sea turtle biology, Book of Abstracts. ISTS, Island of Crete, GreeceGoogle Scholar
  3. Adnyana IBW (2003) Preliminary assessment of Berau green turtle population. Report to WWF Indonesia Turtle ProgramGoogle Scholar
  4. Al-Mohanna SY, Al-Zaidan AY, George P (2014) Green turtles (Chelonia mydas) of the north-western Arabian Gulf, Kuwait: the need of conservation. Aquat Conserv 24:166–178CrossRefGoogle Scholar
  5. Alvarado Bremer JR, Stequert B, Robertson NW, Ely B (1998) Genetic evidence for inter-oceanic subdivision of bigeye tuna (Thunnus obesus) populations. Mar Biol 132:547–557CrossRefGoogle Scholar
  6. Avise JC (1998) Conservation genetics in the marine realm. J Hered 89:377–382CrossRefGoogle Scholar
  7. Blumenthal JM, Abreu-Grobois FA, Austin TJ, Broderick AC, Bruford MW, Coyne MS, Ebanks-Petrie G, Formia F, Meylan PA, Meylan AB, Godley B (2009) Turtle groups or turtle soup: dispersal patterns of hawksbill turtles in the Caribbean. Mol Ecol 18:4841–4853CrossRefPubMedGoogle Scholar
  8. Bourjea J, Frappier J, Quillard M, Ciccione S, Roos D, Hughes G, Grizel H (2007a) Mayotte Island: another important green turtle nesting site in the south west Indian Ocean. Endang Species Res 3:273–282CrossRefGoogle Scholar
  9. Bourjea J, Lapegue S, Gagnevin L, Broderick D, Mortimer JA, Roos D, Taquet C, Grizel H (2007b) Phylogeography of the green turtle, Chelonia mydas, in the southwest Indian Ocean. Mol Ecol 16:175–186CrossRefPubMedGoogle Scholar
  10. Bourjea J, Nel R, Jiddawi NS, Koonjul MS, Bianchi G (2009) Sea turtle bycatch in the West Indian Ocean: review, recommendations and research priorities. West Ind Ocean J Mar Sci 7(2):137–150Google Scholar
  11. Bourjea J, Ciccione S, Dalleau M (2013). Dynamique migratoire des tortues marines nidifiant dans les îles françaises de l’océan Indien. Rapport Scientifique et Technique Ifremer, RST-DOI/2013-02.
  12. Bourjea J, Dalleau M. Derville S, Beudard F, Marmoex C, M’soili A, Roos D, Ciccione S, Frazier J submitted. Seasonality and increasing nesting of green turtles at Itsamia, Mohéli, Comoros. Endang Species ResGoogle Scholar
  13. Bowen BW, Karl SA (2007) Population genetics and phylogeography of sea turtles. Mol Ecol 16:4886–4907CrossRefPubMedGoogle Scholar
  14. Bowen BW, Grant WS, Hillis-Starr Z, Shaver DJ, Bjorndal KA, Bolten AB, Bass AL (2007) Mixed-stock analysis reveals the migration of juvenile hawksbill turtles (Eretmochelys imbricata) in the Caribbean Sea. Mol Ecol 16:49–60CrossRefPubMedGoogle Scholar
  15. Carlsson J, McDowell JR, Diaz-Jaimes P, Carlsson EL, Boles SB, Gold JR, Graves JE (2004) Microsatellite and mitochondrial DNA analyses of Atlantic bluefin tuna (Thynnus thynnus) population structure in the Mediterranean Sea. Mol Ecol 13:3345–3356CrossRefPubMedGoogle Scholar
  16. Carr AF (1967) So excellent a fishe: a natural history of sea turtles. Natural History Press, Garden City 248Google Scholar
  17. Carreras C, Pont S, Maffuci F, Pascual M, Barcelo A, Bentivegna F, Cardona L, Alegre F, SanFélix M, Fernandez G, Aguilar A (2006) Genetic structuring of immature loggerhead turtles (Caretta caretta) in the Mediterranean Sea reflects water circulation patterns. Mar Biol 149:1269–1279CrossRefGoogle Scholar
  18. CLS (2014) Argos User’s Manual V.1.6.3—Worldwide tracking and environmental monitoring by satellite. CLS—Argos. 66 ppGoogle Scholar
  19. Dalleau M (2013) Ecologie spatiale des tortues marines dans le Sud-ouest de l’océan Indien. Apport de la géomatique et de la modélisation pour la conservation. Thèse de doctorat. Université de La Réunion. 330 ppGoogle Scholar
  20. Dalleau M, Ciccione S, Mortimer JA, Garnier J, Benhamou S, Bourjea J (2012) Nesting phenology of marine turtles: insights from a regional comparative analysis on green turtle (Chelonia mydas). PLoS ONE 7:e46920Google Scholar
  21. DeSalle R, Amato G (2004) The expansion of conservation genetics. Nat Rev Genet 5:702–712CrossRefPubMedGoogle Scholar
  22. Dethmers K, Broderick D, Moritz C, Limpus C, FitzSimmons NN (2006) The genetic structure of Australasian green turtles (Chelonia mydas): geographic scale of genetic exchange. Mol Ecol 15:3931–3946CrossRefPubMedGoogle Scholar
  23. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11(12):2571–2581CrossRefPubMedGoogle Scholar
  24. Durand J, Collet A, Chow S, Guinand B, Borsa P (2005) Nuclear and mitochondrial DNA markers indicate unidirectional gene flow of Indo-Pacific to Atlantic bigeye tuna (Thunnus obesus) populations, and their admixture off southern Africa. Mar Biol 147:313–322CrossRefGoogle Scholar
  25. Dutton PH (1996) Methods for collection and preservation of samples for sea turtle genetic studies. In: Bowen BW, Witzell WN (ed) Proceedings of the International Symposium on Sea Turtle Conservation Genetics. NOAA Technical Memorandum, NMFS-SEFSC-396 Miami, pp. 17–24Google Scholar
  26. 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 5:37–44CrossRefGoogle Scholar
  27. Dutton PH, Roden SE, Stewart KR, Lacasella E, Tiwari M, Formia A, Thomé JC, Livingstone SR, Eckert S, Chacon-Chaverri D, Rivalan P, Allman P (2013) Population stock structure of leatherback turtles (Dermochelys coriacea) in the Atlantic revealed using mtDNA and microsatellite markers. Conserv Genet 14:625–636CrossRefGoogle Scholar
  28. Dutton PH, Jensen MP, Frey A, LaCasella E, Balazs GH, Zarate P, Chassin-Noria O, Sarti-Martinez AL, Velez E (2014a) Population structure and phylogeography reveal pathways of colonization by a migratory marine reptile (Chelonia mydas) in the central and eastern Pacific. Ecol Evol 4(22):4317–4331PubMedCentralPubMedGoogle Scholar
  29. Dutton PH, Jensen MP, Frutchey K, Frey A, LaCasella E, Balazs GH, Cruce J, Tagarino A, Farman R, Tatarata M (2014b) Genetic stock structure of green turtle (Chelonia mydas) nesting populations across the Pacific Islands. Pac Sci 68(4):451–464CrossRefGoogle Scholar
  30. Ely B, Vinas J, Alvarado Bremer JR, Black D, Lucas L, Covello K, Labrie AV, Thelen E (2005) Consequences of the historical demography on the global population structure of two highly migratory cosmopolitan marine fishes: the yellowfin tuna (Thunnus albacares) and the skipjack tuna (Katsuwonus pelamis). Evol Biol 5:1–19Google Scholar
  31. Encalada SE, Lahanas PN, Bjorndal KA, Bolten AB, Miyamoto MM, Bowen BW (1996) Phylogeography and population structure of the green turtle (Chelonia mydas) in the Atlantic Ocean and Mediterranean Sea: a mitochondrial DNA control region sequence assessment. Mol Ecol 5:473–484CrossRefPubMedGoogle Scholar
  32. Excoffier L, Lischer HEL (2010) Arlequin ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefPubMedGoogle Scholar
  33. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes—application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedCentralPubMedGoogle Scholar
  34. Formia A, Godley BJ, Dontaine J-F, Bruford MW (2006) Mitochondrial DNA diversity and phylogeography of endangered green turtle (Chelonia mydas) populations in Africa. Conserv Genet 7:353–369CrossRefGoogle Scholar
  35. Formia A, Broderick AC, Glen F, Godley BJ, Hays GC, Bruford MW (2007) Genetic composition of the Ascension Island green turtle rookery based on mitochondrial DNA: implications for sampling and diversity. Endang Species Res 3:145–158CrossRefGoogle Scholar
  36. Frazier J (1975) Marine turtles of the western Indian Ocean. Oryx 13:164–175. doi: 10.1017/S0030605300013387
  37. Frazier J (1984) Marine turtles in the Seychelles and adjacent territories. In: Stoddardt DR (ed) Biogeography and ecology of the Seychelles Islands. Dr W. Junk Publishers, The Netherlands, pp 417–468Google Scholar
  38. Garnier J, Hill N, Guissamulo A, Silva I, Debney A, Godley B (2012) Status and community-based conservation of marine turtles in the northern Querimbas Islands (Mozambique). Oryx 46(3):359–367CrossRefGoogle Scholar
  39. Gaspar P, Benson SR, Dutton PH, Reveillere A, Jacob G, Meetoo C, Dehecq A, Fossette S (2012) Oceanic dispersal of juvenile leatherback turtles: going beyond passive drift modeling. Mar Ecol Prog Ser 457:265–284CrossRefGoogle Scholar
  40. 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 47:769–778CrossRefGoogle Scholar
  41. Hamabata T, Kamezaki N, Hikida T (2014) Genetic structure of green turtle (Chelonia mydas) peripheral populations nesting in the northwestern Pacific rookeries: evidence for northern refugia and postglacial colonization. Mar Biol 161:495–507CrossRefGoogle Scholar
  42. Hawkes LA, Tomás J, Revuelta O, León YM, Blumenthal JM, Broderick AC, Fish M, Raga JA, Witt MJ, Godley BJ (2012) Migratory patterns in hawksbill turtles described by satellite tracking. Mar Ecol Prog Ser 461:223–232CrossRefGoogle Scholar
  43. Hays GC, Mortimer JA, Ierodiaconou D, Esteban N (2014) Use of long-distance migration patterns of an endangered species to inform conservation planning for the world’s largest marine protected area. Conserv Biol. 145 pp. doi: 10.1111/cobi.12325
  44. Henley S (1981) Nonparametric geostatistics. Wiley, New YorkCrossRefGoogle Scholar
  45. Howell KM, Mbindo C (1996) The status of sea turtle conservation in Tanzania. In: Humphrey SL, Salm RV (ed), Status of Sea Turtle Conservation in the Western Indian Ocean. UNEP Regional Seas Reports and Studies. IUCN/UNEP, Nairobi, Kenya, pp. 73–80Google Scholar
  46. Hughes GR (1973) The sea turtles of south east Africa. Doctoral thesis. University of Natal, DurbanGoogle Scholar
  47. Hughes GR (1996) Nesting of leatherback turtle (Dermochelys coriacea) in Tongaland, KwaZulu- Natal, South Africa, 1963-1995. Chelonian Conserv Biol 2:153–158Google Scholar
  48. Jaquemet S, Lecorre M, Quartly GD (2007) Ocean control of the breeding regime of the sooty tern in the southwest Indian Ocean. Deep-Sea Res I 54:130–142CrossRefGoogle Scholar
  49. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMedGoogle Scholar
  50. Knittweis L, Kraemer WE, Timm J, Kochzius M (2009) Genetic structure of Heliofungia actiniformis (Scleractinia: Fungiidae) populations in the Indo-Malay Archipelago: implications for live coral trade management efforts. Conserv Genet 10:241–249CrossRefGoogle Scholar
  51. Kumar S, Tamura K, Jakobsen I, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245CrossRefPubMedGoogle Scholar
  52. Lauret-Stepler M, Bourjea J, Roos D, Pelletier D, Ryan PG, Ciccione S, Grizel H (2007) Reproductive seasonality and trend of Chelonia mydas in the SW Indian Ocean: a 20 yr study based on tracks counts. Endang Species Res 3:217–227CrossRefGoogle Scholar
  53. Lauret-Stepler M, Ciccione S, Bourjea J (2010) Monitoring of marine turtles reproductive activities in Juan de Nova, Eparses Islands, south western Indian Ocean, based on tracks counts and width. Indian Ocean Mar Turt Newsl 11:18–24Google Scholar
  54. Le Corre M (1999) Plumage polymorphism of red-footed boobies (Sula sula) in the western Indian Ocean: an indicator of biogeographic isolation. J Zool Soc London 249:411–415CrossRefGoogle Scholar
  55. Le Corre M (2000) Taxonomic affinities of Audubon’s shearwater from Europa Island. Condor 102:187–190CrossRefGoogle Scholar
  56. Le Gall JY (1988) Biologie et évaluation des populations de tortues vertes Chelonia mydas des atolls Tromelin et Europa (Océan Indien S.O.). Mésogée 48:33–42Google Scholar
  57. Le Gall JY, Bosc P, Château D, Taquet M (1986) Estimation du nombre de tortues vertes femelles adultes Chelonia mydas par saison de ponte a Tromelin et Europa (Océan Indien) (1973–1985). Océanographie Tropicale 21:3–22Google Scholar
  58. Lee PLM (2008) Molecular ecology of marine turtles: new approaches and future directions. J Exp Mar Biol Ecol 356:25–42CrossRefGoogle Scholar
  59. LeRoux RA, Dutton PH, Abreu-Grobois FA, Lagueux JC, Campbell CL, Delcrois E, Chevalier J, Horrocks JA, Hillis-Starr A, Troeng S, Harrison E, Stapleton S (2012) Re-examination of population structure and phylogeography of hawksbill turtles in the Wider Caribbean using longer mtDNA sequences. J Hered 103:806–820CrossRefPubMedGoogle Scholar
  60. Lutjeharms JRE (2005) The coastal oceans of south-eastern Africa. In: Robinson AR, Brink K (eds) The sea. Chicago University Press, Chicago, pp 781–832Google Scholar
  61. Malakoff D (1997) Extinction of the high seas. Science 277(5325):486–488CrossRefGoogle Scholar
  62. Meylan AB, Bowen BW, Avise JC (1990) A genetic test of the natal homing versus social facilitation models for green turtle migration. Science 248:724–727CrossRefPubMedGoogle Scholar
  63. Monzon-Argüello C, Lopez-Jurado LF, Rico C, Marco A, Lopez P, Hays GC, Lee PLM (2010) Evidence from genetic and Lagrangian drifter data for transatlantic transport of small juvenile green turtles. J Biogeogr 37:1752–1766CrossRefGoogle Scholar
  64. Moritz C (1994) Applications of mitochondrial DNA analysis in conservation: a critical review. Mol Ecol 3:401–411CrossRefGoogle Scholar
  65. Mortimer JA (1984) Marine Turtles in the Republic of Seychelles: Status and Management. IUCN Conservation Library, Gland. 80 ppGoogle Scholar
  66. Mortimer JA (1985) Recovery of green turtles on Aldabra. Oryx 19:146–150CrossRefGoogle Scholar
  67. Mortimer JA (1988) Green turtle nesting at Aldabra Atoll–population estimates and trends. Bull Biol Soc Wash 8:116–128Google Scholar
  68. Mortimer JA (2001) Turtle Talk: international migrations of sea turtles tagged at Aldabra. Seychelles Isl Found Newsl 7:1–3Google Scholar
  69. Mortimer JA, Broderick D (1999) Population genetic structure and developmental migrations of sea turtles in the Chagos Archipelago and adjacent regions inferred from mtDNA sequence variation. In: Sheppard CRC, Seaward MRD (eds) Ecology of the Chagos Archipelago. Linnean Society of London (Occasional Publication 2), Westbury Publishing, Otley, UK, pp 185–194Google Scholar
  70. Mortimer JA, Day M (1999) Sea turtle populations and habitats in the Chagos Archipelago. In: Sheppard CRC, Seaward MRD (eds) Ecology of the Chagos Archipelago. Linnean Society of London (Occasional Publication 2), Westbury Publishing, Otley, UK, pp. 159–172Google Scholar
  71. Mortimer JA, Camille J-C, Boniface N (2011a) Seasonality and status of nesting hawksbill (Eretmochelys imbricata) and green turtles (Chelonia mydas) at D’Arros Island, Amirantes Group. Seychelles. Chelonian Conserv Biol 10(1):26–33CrossRefGoogle Scholar
  72. Mortimer JA, von Brandis RG, Liljevik A, Chapman R, Collie J (2011b) Fall and rise of nesting green turtles (Chelonian mydas) at Aldabra Atoll, Seychelles: positive response to four decades of protection (1968–2008). Chelonian Conserv Biol 10(2):165–176CrossRefGoogle Scholar
  73. Muths D, Le Couls S, Evano H, Grewe P, Bourjea J (2013) Multi-genetic marker approach and spatio-temporal analysis suggest there is a single panmictic population of swordfish Xiphias gladius in the Indian Ocean. PLoS One 8(5):e63558. doi: 10.1371/journal.pone.0063558 CrossRefPubMedCentralPubMedGoogle Scholar
  74. Muths D, Tessier E, Bourjea J (2014) Genetic structure of the reef grouper Epinephelus merra in the west Indian Ocean appears congruent with biogeographic and oceanographic boundaries. Mar Ecol. doi: 10.1111/maec.12153,1-15 Google Scholar
  75. NMFS, USFWS (National Marine Fisheries Service and United States Fish and Wildlife Service) (2007) Green sea turtle (Chelonia mydas) 5-year review: summary and evaluation. National Marine Fisheries Service, Silver Spring, Maryland, and U.S. Fish and Wildlife Service, Jacksonville, Florida, 105 ppGoogle Scholar
  76. Norman JA, Moritz C, Limpus C (1994) Mitochondrial DNA control region polymorphisms: genetic markers for ecological studies of marine turtles. Mol Ecol 3:363–373CrossRefPubMedGoogle Scholar
  77. O’Connell M, Wright JM (1997) Microsatellite DNA in fishes. Rev Fish Biol Fish 7:331–363CrossRefGoogle Scholar
  78. Okemwa GM, Nzuki S, Mueni EM (2004) The status and conservation of sea turtles in Kenya. Mar Turt Newsl 105:1–6Google Scholar
  79. Palumbi SR (2003) Population genetics, demographic connectivity and the design of marine protected areas. Ecol Appl 13:146–158CrossRefGoogle Scholar
  80. Parsons JJ (1962) The green turtle and man. University of Florida Press, GainesvilleGoogle Scholar
  81. Piton B, Magnier Y (1976) Les conditions favorables de la présence des thons de surface dans les parages de Madagascar. ORSTOM 47:293–309Google Scholar
  82. Putman NF, Abreu-Grobois FA, Broderick AC, Ciofi C, Formia A, Godley BJ, Stroud S, Pelembe T, Verley P, Williams N (2014) Numerical dispersal simulations and genetics help explain the origin of hawksbill sea turtles in Ascension Island. J Exp Mar Biol Ecol 450:98–108CrossRefGoogle Scholar
  83. Raymond M, Rousset F (1994) An exact test for population differentiation. Evolution 49(6):1280–1283CrossRefGoogle Scholar
  84. Raymond M, Rousset F (1995) GENEPOP (version 1. 2): a population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  85. Read TC, Wantiez L, Werry JM, Farman R, Petro G et al (2014) Migrations of green turtles (Chelonia mydas) between nesting and foraging grounds across the Coral Sea. PLoS One 9(6):e100083. doi: 10.1371/journal.pone.0100083 CrossRefPubMedCentralPubMedGoogle Scholar
  86. Reece JS, Castoe TA, Parkinson CL (2005) Historical perspectives on population genetics and conservation of three marine turtle species. Conserv Genet 6:235–251CrossRefGoogle Scholar
  87. Roden SE, Morin PA, Frey A, Balazs GH, Zarate P, Cheng I-J et al (2013) Green turtle population structure in the Pacific: new insights from single nucleotide polymorphisms and microsatellites. Endanger Species Res 20:227–234CrossRefGoogle Scholar
  88. Ross JP, Barwani MA (1982) Review of sea turtles in the Arabian area. In: Bjorndal KA (ed) Biology and conservation of sea turtles. Smithsonian Institution Press, Washington, DC, pp 373–383Google Scholar
  89. Schott FA, Xie S-P, McCreary JP (2009) Indian Ocean circulation and climate variability. Rev Geophys 47:RG1002CrossRefGoogle Scholar
  90. Schouten MW, Ruijter WPM, Leeuwen PJV, Ridderinkhof H (2003) Eddies and variability in the Mozambique Channel. Deep-Sea Res II 50:1987–2003CrossRefGoogle Scholar
  91. Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33CrossRefPubMedGoogle Scholar
  92. Shamblin BM, Bjorndal KA, Bolten AB, Hillis-Starr ZM, Lundgren A, Naro-Maciel E, Nairn CJ (2012) Mitogenomic sequences better resolve stock structure of southern Greater Caribbean green turtle rookeries. Mol Ecol 21:2330–2340CrossRefPubMedGoogle Scholar
  93. Sheppard CRC, Ateweberhan M, Bowen BW, Carr P, Chen CA et al (2012) Reefs and islands of the Chagos Archipelago, Indian Ocean: why it is the world’s largest no-take marine protected area. Aquat Conserv 22:232–261CrossRefPubMedCentralPubMedGoogle Scholar
  94. Taylor BL, Dizon AE (1999) First policy then science: why a management unit based solely on genetic criteria cannot work. Mol Ecol 8:S11–S16CrossRefPubMedGoogle Scholar
  95. Tisen OB, Bali J (2002) Current status of marine turtle conservation programmes in Sarawak, Malaysia. In: Witzell WN (ed) Proceeding of the Twentieth Annual Symposium on Sea Turtle Biology and Conservation. Orlando, Florida, USA, pp 12–14Google Scholar
  96. Vargas SM, Jensen MP, Mobaraki A, Santos FR, Broderick D, Mortimer JA, Limpus C, Whiting S, FitzSimmons N (2013) Phylogeography of the hawksbill turtle (Eretmochelys imbricata) from the Indo-Pacific Region. In: Proceedings of the 30th Annual Symposium on Sea Turtle Biology and Conservation. Blumenthal, J., Panagopouou, A., Rees, A.F. (compilers). NOAA Technical Memorandum NMFS-SEFSC-640: 177, p. 155Google Scholar
  97. Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167CrossRefGoogle Scholar
  98. Wallace BP, DiMatteo AD, Hurley BJ, Finkbeiner ME, Bolten AB et al (2010) Regional management units for marine turtles: a novel framework for prioritizing conservation and research across multiple scales. PLoS One 5(12):e15465. doi: 10.1371/journal.pone.0015465 CrossRefPubMedCentralPubMedGoogle Scholar
  99. Wallace BP, DiMatteo AD, Bolten AB, Chaloupka MY, Hutchinson BJ et al (2011) Global Conservation Priorities for Marine Turtles. PLoS One 6(9):e24510. doi: 10.1371/journal.pone.0024510 CrossRefPubMedCentralPubMedGoogle Scholar
  100. Ward RD (2000) Genetics in fisheries management. Hydrobiologia 420:191–201CrossRefGoogle Scholar
  101. Watson DF, Philip GM (1985) A refinement of inverse distance weighted interpolation. Geoprocessing 2:315–327Google Scholar
  102. Weir BS, Cockerham CC (1984) Estimating F statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  103. Whiting SD, Murray W, Macrae I, Thorn R, Chongkin M, Koch AU (2008) Non-migratory breeding by isolated green sea turtles (Chelonia mydas) in the Indian Ocean: biological and conservation implications. Naturwissenschaften 95:355–360CrossRefPubMedGoogle Scholar
  104. Wright S (1951) The genetical structure of population. Ann Eugen 15:323–354CrossRefPubMedGoogle Scholar
  105. Zbinden JA, Bearhop S, Bradshaw P, Gill B, Margaritoulis B, Newton J, Godley BJ (2011) Migratory dichotomy and associated phenotypic variation in marine turtles revealed by satellite tracking and stable isotope analysis. Mar Ecol Prog Ser 421:0291–0302CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Jérôme Bourjea
    • 1
    • 8
  • Jeanne A. Mortimer
    • 2
    • 10
    • 11
    • 12
  • Julie Garnier
    • 3
  • Gladys Okemwa
    • 4
    • 9
  • Brendan J. Godley
    • 5
  • George Hughes
    • 6
  • Mayeul Dalleau
    • 7
  • Claire Jean
    • 7
  • Stéphane Ciccione
    • 7
  • Delphine Muths
    • 1
  1. 1.Institut Français de Recherche pour l’Exploitation de la Mer, IfremerDélégation de La Réunion, Rue Jean BerthoLe Port CedexFrance
  2. 2.Department of BiologyUniversity of FloridaGainesvilleUSA
  3. 3.The Zoological Society of LondonLondonUK
  4. 4.Kenya Sea Turtle Conservation Committee (KESCOM)MombasaKenya
  5. 5.Marine Turtle Research Group, Centre for Ecology and ConservationUniversity of ExeterPenrynUK
  6. 6.HowickSouth Africa
  7. 7.KELONIA, l’observatoire des tortues marines de La RéunionSaint LeuFrance
  8. 8.University of Reunion Island, FRE3560 INEE-CNRSSaint DenisFrance
  9. 9.Kenya Marine and Fisheries Research InstituteMombasaKenya
  10. 10.VictoriaSeychelles
  11. 11.Save Our Seas Foundation D’Arros Research CentreD’Arros IslandSeychelles
  12. 12.Island Conservation SocietyVictoriaSeychelles

Personalised recommendations