Turtle groups or turtle soup: Dispersal patterns of hawksbill turtles in the Caribbean

Molecular Ecology

Volumn 18, Issue 23, 2009, Pages 4841-4853

  Blumenthal, J M ^a,b   Abreu Grobois, F A ^c   Austin, T J ^a   Broderick, A C ^b   Bruford, M W ^d   Coyne, M S ^b,e   Ebanks Petrie, G ^a   Formia, A ^d   Meylan, P A ^f   Meylan, A B ^g   Godley, B J ^b  

^a Box 486 ^*  (Cayman Islands)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^d CARDIFF UNIVERSITY   (United Kingdom)

^e SEATURTLEORG   (United States)

^f ECKERD COLLEGE   (United States)

^g FISH AND WILDLIFE RESEARCH INSTITUTE   (United States)

Author keywords

Conservation genetics; Hawksbill; Marine turtle; Migratory species; Mixed stock; Ocean currents

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CENTRAL AMERICA; DNA SEQUENCE; ENVIRONMENTAL PROTECTION; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; HAPLOTYPE; POPULATION GENETICS; TURTLE; WATER FLOW;

ANIMALS; CARIBBEAN REGION; CONSERVATION OF NATURAL RESOURCES; DNA, MITOCHONDRIAL; GENETIC VARIATION; GENETICS, POPULATION; GEOGRAPHY; HAPLOTYPES; MODELS, BIOLOGICAL; SEQUENCE ANALYSIS, DNA; TURTLES; WATER MOVEMENTS;

CHELONIIDAE; ERETMOCHELYS IMBRICATA; TESTUDINES;

EID: 70449719225     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2009.04403.x     Document Type: Article

References (90)

1. Abreu-Grobois FA, Horrocks JA, Formia A et al. (2006) New mtDNA dloop primers which work for a variety of marine turtle species may increase the resolution capacity of mixed stock analyses. Poster presented at the 26th Annual Symposium on Sea Turtle Biology and Conservation, Crete, Greece, 2-8 April 2006. Available from http://www.iucnmtsg.org/genetics/meth/primers/abreu- grobois-etal-new-dloop-primers.pdf. Accessed 1 March 2008.
2. Aiken JJ, Godley BJ, Broderick AC, Austin T, Ebanks-Petrie G, Hays GC (2001) Two hundred years after a commercial marine turtle fishery: the current status of marine turtles nesting in the Cayman Islands. Oryx, 35, 145 151.
3. Allard MW, Miyamoto MM, Bjorndal KA, Bolten AB, Bowen BW (1994) Support for natal homing in green turtles from mitochondrial DNA sequences. Copeia, 1994, 34 41.
4. Allen M, Engstrom AS, Meyers S et al. (1998) Mitochondrial DNA sequencing of shed hairs and saliva on robbery caps: sensitivity and matching probabilities. Journal of Forensic Science, 43, 453 464.
5. Andersen LW, Ruzzante DE, Walton M et al. (2001) Conservation genetics of harbour porpoises, Phocoena phocoena, in eastern and central North Atlantic. Conservation Genetics, 2, 309 324.
6. Baillie JEM, Hilton-Taylor C, Stuart SN (2004) IUCN red List of Threatened Species. A Global Species Assessment. IUCN, Gland Switzerland.
7. Baker CS, Patenaude NJ, Bannister JL, Robins J, Kato H (1999) Distribution and diversity of mtDNA lineages among southern right whales (Eubalaena australis) from Australia and New Zealand. Marine Biology, 134, 1 7.
8. Bass AL (1999) Genetic analysis to elucidate the natural history and behavior of hawksbill turtles (Eretmochelys imbricata) in the Wider Caribbean: a review and reanalysis. Chelonian Conservation and Biology, 3, 195 199.
9. Bass AL, Witzell WN (2000) Demographic composition of immature green turtles (Chelonia mydas) from the east central Florida coast: evidence from mtDNA markers. Herpetologica, 56, 357 367.
10. Bass AL, Good DA, Bjorndal KA et al. (1996) Testing models of female reproductive migratory behavior and population structure in the Caribbean hawksbill turtle, Eretmochelys imbricata, with mtDNA sequences. Molecular Ecology, 5, 321 328.
11. 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. Journal of Heredity, 97, 346 354.
12. Beggs JA, Horrocks JA, Krueger BH (2007) Increase in hawksbill sea turtle Eretmochelys imbricata nesting in Barbados, West Indies. Endangered Species Research, 3, 159 168.
13. Bell CD, Solomon JL, Blumenthal JM et al. (2007) Monitoring and conservation of critically-reduced marine turtle nesting populations: lessons from the Cayman Islands. Animal Conservation, 10, 39 47.
14. Bjorndal KA, Bolten AB (2008) Annual variation in source contributions to a mixed stock: implications for quantifying connectivity. Molecular Ecology, 17, 2185 2193.
15. Blumenthal JM, Austin TJ, Bell CD et al. (2009a) Ecology of hawksbill turtles Eretmochelys imbricata on a western Caribbean foraging area. Chelonian Conservation and Biology, 8, 1 10.
16. Blumenthal JM, Austin TJ, Bothwell JB et al. (2009b) Diving behaviour and movements of juvenile hawksbill turtles Eretmochelys imbricata on a Caribbean coral reef. Coral Reefs, 28, 55 65.
17. Bolker BM, Okuyama T, Bjorndal KA, Bolten AB (2007) Incorporating multiple mixed stocks in mixed stock analysis: 'many-to-many' analyses. Molecular Ecology, 16, 685 695.
18. Bolten AB (2003) Variation in sea turtle life-history patterns: neritic vs. oceanic developmental stages. In : The Biology of Sea Turtles, Volume I (eds Lutz PL, Musick JA, Wyneken J). pp. 243 257, CRC Press, Boca Raton.
19. Bolten AB, Bjorndal KA, Martins HR et al. (1998) Trans-Atlantic developmental migrations of loggerhead sea turtles demonstrated by mtDNA sequence analyses. Ecological Applications, 8, 1 7.
20. Botsford LW, White JW, Coffroth M-A et al. (2009) Connectivity and resilience of coral reef metapopulations in marine protected areas: matching empirical efforts to predictive needs. Coral Reefs, 28, 303 305.
21. Bowen BW, Bass AL (1997) Movement of hawksbill turtles: what scale is relevant to conservation and what scale is resolvable with mtDNA data? Chelonian Conservation and Biology, 3, 440 442.
22. Bowen BW, Abreu-Grobois FA, Balazs GH et al. (1995) Trans-Pacific migrations of the loggerhead sea turtle demonstrated with mitochondrial DNA markers. Proceedings of the National Academy of Sciences USA, 92, 3731 3734.
23. Bowen BW, Bass AL, Garcia A et al. (1996) The origin of hawksbill turtles in a Caribbean feeding area as indicated by genetic markers. Ecological Applications, 6, 566 572.
24. Bowen BW, Bass AL, Chow S et al. (2004) Natal homing in juvenile loggerhead turtles (Caretta caretta). Molecular Ecology, 13, 3797 3808.
25. Bowen BW, Bass AL, Soares L, Toonen RJ (2005) Conservation implications of complex population structure: lessons from the loggerhead turtle (Caretta caretta). Molecular Ecology, 14, 2389 2402.
26. Bowen BW, Grand WS, Hillis-Starr Z et al. (2007a) Mixed-stock analysis reveals the migrations of juvenile hawksbill turtles (Eretmochelys imbricata) in the Caribbean sea. Molecular Ecology, 16, 49 60.
27. Bowen BW, Grant WS, Hillis-Starr Z et al. (2007b) The advocate and the scientist: debating the commercial exploitation of endangered hawksbill turtles. Molecular Ecology, 16, 3514 3515.
28. Broderick D, Moritz C, Miller JD, Guinea ML, Prince JR, Limpus CJ (1994) Genetic studies of the hawksbill turtle (Eretmochelys imbricata): evidence for multiple stocks and mixed feeding grounds in Australian waters. Pacific Conservation Biology, 1, 123 131.
29. Browne DC, Horrocks JA, Abreu-Grobois FA (in press) Population subdivision in hawksbill turtles nesting on Barbados, West Indies, determined from mitochondrial DNA control region sequences. Conservation Genetics, DOI
30. Carr AF (1987) New perspectives on the pelagic stage of sea turtle development. Conservation Biology, 1, 103 121.
31. Carreras C, Pont S, Maffucci F et al. (2006) Genetic structuring of immature loggerhead sea turtles (Caretta caretta) in the Mediterranean Sea reflects water circulation patterns. Marine Biology, 149, 1269 1279.
32. Chacón D (2004) Caribbean Hawksbills - An Introduction to Their Biology and Conservation Status. WWF-Regional Program for Latin America and the Caribbean, San Jose, Costa Rica.
33. Chung FC, Pilcher NJ, Salmon M, Wyneken J (2009a) Offshore migratory activity of hawksbill turtle (Eretmochelys imbricata) hatchlings, I. Quantitative analysis of activity, with comparisons to green turtles (Chelonia mydas). Chelonian Conservation and Biology, 8, 28 34.
34. Chung FC, Pilcher NJ, Salmon M, Wyneken J (2009b) Offshore migratory activity of hawksbill turtle (Eretmochelys imbricata) hatchlings II. Swimming gaits, swimming speed, and morphological comparisons. Chelonian Conservation and Biology, 8, 35 42.
35. van Dam RP, Diez CE, Balazs GH et al. (2008) Sex-specific migration patterns of hawksbill turtles from Mona Island, Puerto Rico. Endangered Species Research, 4, 85 94.
36. Diaz-Fernandez R, Okayama T, Uchiyama T et al. (1999) Genetic sourcing for the hawksbill turtle, Eretmochelys imbricata, in the northern Caribbean region. Chelonian Conservation and Biology, 3, 296 300.
37. Dutton PH (1996) Methods for collection and preservation of samples for sea turtle genetic studies. In : Proceedings of the International Symposium on Sea Turtle Conservation Genetics (eds Bowen BW, Witzell WN pp. 17 24. National Technical Information Service, Springfield, VA, USA, NOAA Technical Memorandum NMFS-SEFSC-396.
38. Encalada SE, Bjorndal KA, Bolten AB et al. (1998) Population structure of loggerhead turtle (Caretta caretta) nesting colonies in the Atlantic and Mediterranean as inferred from mitochondrial DNA control region sequences. Marine Biology, 130, 567 575.
39. Engstrom TN, Meylan PA, Meylan AB (2002) Origin of juvenile loggerhead turtles (Caretta caretta) in a tropical developmental habitat in Caribbean Panama. Animal Conservation, 5, 125 133.
40. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47 50.
41. Fiksen O, Jorgensen C, Kristiansen T, Vikebo F, Huse G (2007) Linking behavioural ecology and oceanography: larval behaviour determines growth, mortality and dispersal. Marine Ecology Progress Series, 347, 195 205.
42. Formia A, Godley BJ, Dontaine J-F, Bruford MW (2006) Mitochondrial DNA diversity and phylogeography of endangered green turtle (Chelonia mydas) populations in Africa. Conservation Genetics, 7, 353 369.
43. Formia A, Broderick AC, Glen F et al. (2007) Genetic composition of the Ascension Island green turtle rookery based on mitochondrial DNA: implications for sampling and diversity. Endangered Species Research, 3, 145 158.
44. Garduño-Andrade M (1999) Nesting of the hawksbill turtle, Eretmochelys imbricata, in Rio Lagartos, Yucatan, Mexico, 1990-1997. Chelonian Conservation and Biology, 3, 281 285.
45. Girard C, Tucker AD, Calmettes B (2009) Post-nesting migrations of loggerhead sea turtles in the Gulf of Mexico: dispersal in highly dynamic conditions. Marine Biology, 156, 1827 1839.
46. Godfrey MH, Webb GJW, Manolis SC, Mrosovsky N (2007) Hawksbill sea turtles: can phylogenetics inform harvesting? Molecular Ecology, 16, 3511 3513.
47. Hasbún CR (2002) Observations on first day dispersal of neonatal hawksbill turtles (Eretmochelys imbricata). Marine Turtle Newsletter, 96, 7 10.
48. Hays GC, Marsh R (1997) Estimating the age of juvenile loggerhead sea turtles in the North Atlantic. Canadian Journal of Zoology, 75, 40 46.
49. Hood GM (2009) PopTools version 3.1.1. Available on the internet. URL http://www.cse.csiro.au/poptools. Accessed 20 July 2008.
50. Horrocks JA, Vermeer LA, Krueger B et al. (2001) Migration routes and destination characteristics of post-nesting hawksbill turtles satellite-tracked from Barbados, West Indies. Chelonian Conservation and Biology, 4, 107 114.
51. IUCN (2007) Red List of Threatened Species. Available from http://www.iucnredlist.org. Accessed 1 April 2008.
52. Kocher TD, Thomas WK, Meyers A et al. (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences of the USA, 86, 6196 6200.
53. Lahanas PN, Bjorndal KA, Bolten AB et al. (1998) Genetic composition of a green turtle (Chelonia mydas) feeding ground population: evidence for multiple origins. Marine Biology, 130, 345 352.
54. Laurent L, Casale P, Bradai N et al. (1998) Molecular resolution of marine turtle stock composition in fishery bycatch: a case study in the Mediterannean. Molecular Ecology, 7, 1529 1542.
55. Lewis CB (1940) The Cayman Islands and marine turtle. In : Herpetology of the Cayman Island (ed. Grant C). pp. 56 65, Bulletin of the Institute of Jamaica Science Series, Kingston.
56. Lohmann KJ, Cain SD, Dodge SA, Lohmann CM (2001) Regional magnetic fields as navigational markers for sea turtles. Science, 294, 364 366.
57. Luke K, Horrocks JA, LeRoux RA, Dutton PH (2004) Origins of green turtle (Chelonia mydas) feeding aggregations around Barbados, West Indies. Marine Biology, 144, 799 805.
58. Maffucci F, Kooistra WHCF, Bentivegna F (2006) Natal origin of loggerhead turtles, Caretta caretta, in the neritic habitat off the Italian coasts, Central Mediterranean. Biological Conservation, 127, 183 189.
59. Meylan AB (1999) International movements of immature and adult hawksbill turtles (Eretmochelys imbricata) in the Caribbean region. Chelonian Conservation and Biology, 3, 189 194.
60. Meylan A, Redlow A (2006) Eretmochelys imbricata - Hawksbill turtle. In : Biology and Conservation of Florida Turtles (ed. Meylan PA). Chelonian Research Foundation, Lunenburg, MA, USA, 3, 105 127.
61. Meylan AB, Bowen BW, Avise JC (1990) A genetic test of the natal homing versus social facilitation models for green turtle migration. Science, 248, 724 727.
62. Meylan PA, Meylan AB, Gray J, Ward J (2003) The hawksbill turtle in Bermuda. In : Proceedings of the Twenty-Second Annual Symposium on Sea Turtle Biology and Conservation (compiler, Seminoff JA p. 26. National Technical Information Service, Springfield, VA, USA. NOAA Technical Memorandum NMFS-SEFSC-503.
63. Millar RB (1987) Maximum likelihood estimation of mixed stock fishery composition. Canadian Journal of Fisheries and Aquatic Science, 44, 583 590.
64. Milligan BG (1998) Total DNA isolation. In : Molecular Genetic Analysis of Populations, a Practical Approach (ed Hoelzel AR). pp. 29 64, IRL Press, Oxford.
65. Moncada F, Carillo E, Saenz A, Nodarse G (1999) Reproduction and nesting of the hawksbill turtle, Eretmochelys imbricata, in the Cuban archipelago. Chelonian Conservation and Biology, 3, 257 263.
66. Monzón-Argüello C, Rico C, Carreras C, Calbuig P, Marco A, López-Jurado LF (2009) Variation in spatial distribution of juvenile loggerhead turtles in the eastern Atlantic and western Mediterranean sea. Journal of Experimental Marine Biology and Ecology, 373, 79 86.
67. Mora C, Sale PF (2002) Are populations of coral reef fish open or closed? Trends in Ecology and Evolution, 17, 422 428.
68. Mortimer JA, Donnelly M (2007) Marine Turtle Specialist Group 2007 IUCN Red List Status Assessment Hawksbill Turtle (Eretmochelys imbricata). Available from http://www.iucn-mtsg.org/red-list/ei/index.shtml. Accessed 1 March 2008.
69. Mortimer JA, Donnelly M, Meylan AB, Meylan PA (2007a) Critically endangered hawksbill turtles: molecular genetics and the broad view of recovery. Molecular Ecology, 16, 3516 3517.
70. Mortimer JA, Meylan PA, Donnelly M (2007b) Whose turtles are they, anyway? Molecular Ecology, 16, 17 18.
71. Mrosovsky N (1997) Movement of hawksbill turtles - a different perspective on the DNA data. Chelonian Conservation and Biology, 3, 438 439.
72. Musick JA, Limpus CJ (1997) Habitat utilization and migration in juvenile sea turtles. In : The Biology of Sea Turtle (eds Lutz PL, Musick JA). pp. 137 163, CRC Press, Boca Raton.
73. Naro-Maciel E, Becker HJ, Lima EHSM, Marcovaldi MA, DeSalle R (2007) Testing dispersal hypotheses in foraging green sea turtles (Chelonia mydas) of Brazil. Journal of Heredity, 98, 29 39.
74. Norman JA, Moritz C, Limpus CJ (1994) Mitochondrial DNA control region polymorphisms: genetic markers for ecological studies of marine turtles. Molecular Ecology, 3, 363 373.
75. Okuyama T, Bolker BM (2005) Combining genetic and ecological data to estimate sea turtle origins. Ecological Applications, 15, 315 325.
76. Owens DW, Ruiz GW (1980) New methods of obtaining blood and cerebrospinal fluid from marine turtles. Herpetologica, 36, 17 20.
77. Paris CB, Cherubin LM, Cowen RK (2007) Surfing, spinning, or diving from reef to reef: effects on population connectivity. Marine Ecology Progress Series, 347, 285 300.
78. Parker LG (1995) Encounter with a juvenile hawksbill turtle offshore Sapelo Island, Georgia. Marine Turtle Newsletter, 71, 19 22.
79. Pella J, Masuda M (2001) Bayesian methods for analysis of stock mixtures from genetic characters. Fishery Bulletin, 99, 151 167.
80. Pella J, Milner GB (1987) Use of genetic marks in stock composition analyses. In : Population Genetics and Fishery Managemen (eds Ryman N, Utter F). pp. 247 276, University of Washington Press, Seattle.
81. Reece JS, Ehrhart LM, Parkinson CL (2006) Mixed stock analysis of juvenile loggerheads (Caretta caretta) in Indian River lagoon, Florida: implications for conservation planning. Conservation Genetics, 7, 345 352.
82. Richardson JI, Hall DB, Mason PA et al. (2006) Eighteen years of saturation tagging data reveal a significant increase in nesting hawksbill sea turtles (Eretmochelys imbricata) on Long Island, Antigua. Animal Conservation, 9, 302 307.
83. Roberts H (1994) Reefs and lagoons of Grand Cayman. In : The Cayman Islands: Natural History and Biogeograph (eds Brunt MA, Davies JE). pp. 75 104, Kluwer Academic Publishers, Netherlands.
84. Spalding MD, Fox HE, Allen GR et al. (2007) Marine ecoregions of the world: a bioregionalization of coast and shelf areas. BioScience, 57, 573 583.
85. Troëng S, Dutton PH, Evans D (2005) Migration of hawksbill turtles Eretmochelys imbricata from Tortuguero, Costa Rica. Ecography, 28, 394 402. (Pubitemid 40809907)
86. Velez-Zuazo X, Ramos WD, van Dam RP et al. (2008) Dispersal, recruitment and migratory behaviour in a hawksbill sea turtle aggregation. Molecular Ecology, 17, 839 853.
87. Wessel P, Smith HF (1991) Free software helps map and display data. Eos, Transactions of the American Geophysical Union, 72, 441.
88. Whiting SD, Koch AU (2006) Oceanic movement of a benthic foraging juvenile hawksbill turtle from the Cocos (Keeling) Islands. Marine Turtle Newsletter, 112, 15 16.
89. Witherington BE (2002) Ecology of neonate loggerhead turtles inhabiting lines of downwelling near a Gulf Stream front. Marine Biology, 140, 843 853.
90. Witteveen BH, Straley JM, von Ziegesar O, Steel D, Baker CS (2004) Abundance and mtDNA differentiation of humpback whales (Megaptera novaeangliae) in the Shumagin Islands, Alaska. Canadian Journal of Zoology, 82, 1352 1359.