Population origin and historical demography in hawksbill (Eretmochelys imbricata) feeding and nesting aggregates from Brazil

Journal of Experimental Marine Biology and Ecology

Volumn 446, Issue , 2013, Pages 334-344

  Vilaca S T ^a   Lara Ruiz, P ^a   Marcovaldi, M A ^b   Soares, L S ^b   Santos, F R ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b Universidade Do Estado Do Rio de Janeiro (UERJ)   (Brazil)

Author keywords

Hawksbill populations; Hybrids; Mixed stock analysis; MtDNA; Nuclear markers; Population genetic structure

Indexed keywords

COLONY; DEMOGRAPHY; FEEDING BEHAVIOR; FEEDING GROUND; GENETIC MARKER; GENETIC STRUCTURE; HYBRID; MIGRATORY BEHAVIOR; MITOCHONDRIAL DNA; NESTING; PHYLOGEOGRAPHY; STOCK ASSESSMENT; TURTLE;

ATLANTIC OCEAN; ATLANTIC OCEAN (EAST); BAHIA; BRAZIL; FERNANDO DE NORONHA; PERNAMBUCO; RIO GRANDE DO NORTE; ROCAS ATOLL;

EID: 84880105525     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2013.06.004     Document Type: Article

References (75)

1. Abreu-Grobois F.A., Horrocks J., Formia A., LeRoux R., Velez-Zuazo X., Dutton P., Soares L., Meylan P., Browne D. New mtDNA Dloop primers which work for a variety of marine turtle species may increase the resolution capacity of mixed stock analysis. 26th Annual Symposium on Sea Turtle Biology and Conservation, Crete, Greece 2006, 179. M. Frick, A. Panagopoulou, A.F. Rees, K. Williams (Eds.).
2. Avise J.C., Bowen B.W., Lamb T., Meylan A.B., Bermingham E. Mitochondrial-DNA evolution at a turtles pace - evidence for low genetic-variability and reduced microevolutionary rate in the testudines. Mol. Biol. Evol. 1992, 9:457-473.
3. Bandelt H.J., Forster P., Rohl A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 1999, 16:37-48.
4. Bass A.L., Witzell W.N. Demographic composition of immature green turtles (Chelonia mydas) from the east central Florida coast: evidence from mtDNA markers. Herpetologica 2000, 3:357-367.
5. Bass A.L., Epperly S.P., Braun-McNeill J. Green turtle (Chelonia mydas) foraging and nesting aggregations in the Caribbean and Atlantic: impact of currents and behavior on dispersal. J. Hered. 2006, 97:346-354.
6. Bass A.L., Good D.A., Bjorndal K.A., Richardson J.I., Hillis Z.M., Horrocks J.A., Bowen B.W. Testing models of female reproductive migratory behaviour and population structure in the Caribbean hawksbill turtle, Eretmochelys imbricata, with mtDNA sequences. Mol. Ecol. 1996, 5:321-328.
7. Bellini C., Sanches T.M., Formia A. Hawksbill tagged in Brazil captured in Gabon, Africa. Mar. Turt. Newsl. 2000, 87:11-12.
8. Bickham J.W. 200,000,000-year-old chromosomes - deceleration of the rate of karyotypic evolution in turtles. Science 1981, 212:1291-1293.
9. Blumenthal J.M., Abreu-Grobois F.A., Austin T.J., Broderick A.C., Bruford M.W., Coyne M.S., Ebanks-Petrie G., Formia A., Meylan P.A., Meylan A.B., Godley B.J. Turtle groups or turtle soup: dispersal patterns of hawksbill turtles in the Caribbean. Mol. Ecol. 2009, 18:4841-4853.
10. Bolker B.M. mixstock: mixed stock analysis in R. R Package Version 0.9.2 2008.
11. Bolker B.M., Okuyama T., Bjorndal K.A., Bolten A.B. Incorporating multiple mixed stocks in mixed stock analysis: 'many-to-many' analyses. Mol. Ecol. 2007, 16:685-695.
12. Bolten A.B., Bjorndal K.A., Martins H.R., Dellinger T., Biscoito M.J., Encalada S.E., Bowen B.W. Transatlantic developmental migrations of loggerhead sea turtles demonstrated by mtDNA sequence analysis. Ecol. Appl. 1998, 8:1-7.
13. Bowen B.W., Karl S.A. Population genetics and phylogeography of sea turtles. Mol. Ecol. 2007, 16:4886-4907.
14. Bowen B.W., Grant W.S., Hillis-Starr Z., Shaver D.J., Bjorndal A., Bolten A.B., Bass A.L. Mixed-stock analysis reveals the migrations of juvenile hawksbill turtles (Eretmochelys imbricata) in the Caribbean Sea. Mol. Ecol. 2007, 16:49-60.
15. Bowen B.W., Bass A.L., GarciaRodriguez A., Diez C.E., vanDam R., Bolten A., Bjorndal K.A., Miyamoto M.M., Ferl R.J. Origin of hawksbill turtles in a Caribbean feeding area as indicated by genetic markers. Ecol. Appl. 1996, 6:566-572.
16. Broderick D., Moritz C., Miller J.D., Guinea M., Prince R.J., Limpus C.J. Genetic studies of the hawksbill turtle: evidence for multiple stocks and mixed feeding grounds in Australian waters. Pacific Conserv. Biol. 1994, 1.
17. Browne D.C., Horrocks J.A., Abreu-Grobois F.A. Population subdivision in hawksbill turtles nesting on Barbados, West Indies, determined from mitochondrial DNA control region sequences. Conserv. Genet. 2010, 11:1541-1546.
18. Carr A., Meylan A.B. Evidence of passive migration of green turtle hatchlings in Sargassum. Copeia 1980, 366-368.
19. Carr A., Hirth H., Ogren L. The ecology and migrations of sea turtles, 6. The hawksbill turtle in the Caribbean Sea. Am. Mus. Novit. 1966, 2248:1-29.
20. Carr A.F. New perspectives on the pelagic stage of sea turtle development. Conserv. Biol. 1987, 1:103-121.
21. Diaz-Fernandez R., Okayama T., Uchiyama T., Carrillo E., Espinosa G., Márquez R., Diez C.E., Koike H. Genetic sourcing for the hawksbill turtle, Eretmochelys imbricata, in the northern Caribbean region. Chelonian Conserv. Biol. 1999, 3:296-300.
22. Drummond A.J., Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007, 7:214.
23. Eckert K.L., Bjorndal K.A., Abreu-Gobrois F.A., Donnelly M. Research and management techniques for the conservation of sea turtles. IUCN/SSC Marine Turtle Specialist Group Publication No. 4 1999.
24. Engstrom T.N., Meylan P.A., Meylan A.B. Origin of juvenile loggerhead turtles (Caretta caretta) in a tropical developmental habitat in Caribbean Panama. Anim. Conserv. 2002, 5:125-133.
25. Ewing B., Green P. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 1998, 8:186-194.
26. Ewing B., Hillier L., Wendl M.C., Green P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 1998, 8:175-185.
27. Excoffier L., Lischer H.E.L. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 2010, 10:564-567.
28. FitzSimmons N.N., Limpus C.J., Norman J.A., Goldizen A.R., Miller J.D., Moritz C. Philopatry of male marine turtles inferred from mitochondrial DNA markers. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:8912-8917.
29. Gaspar P., Benson S.R., Dutton P.H., Reveillere A., Jacob G., Meetoo C., Dehecq A., Fossette S. Oceanic dispersal of juvenile leatherback turtles: going beyond passive drift modeling. Mar. Ecol. Prog. Ser. 2012, 457:265-284.
30. Gelman A., Rubin D.B. Inference from iterative simulation using multiple sequences. Stat. Sci. 1992, 7:457-511.
31. Gordon D., Abajian C., Green P. Consed: a graphical tool for sequence finishing. Genome Res. 1998, 8:195-202.
32. Grossman A., Bellini C., Fallabrino A., Formia A., Mba J.M., Mba J.N., Obama C. Second TAMAR-tagged hawksbill recaptured in Corisco Bay, West Africa. Mar. Turt. Newsl. 2007, 116:26.
33. Hays G.C., Fossette S., Katselidis K.A., Mariani P., Schofield G. Ontogenetic development of migration: Lagrangian drift trajectories suggest a new paradigm for sea turtles. J. R. Soc. Interface 2010, 7:1319-1327.
34. Heled J., Drummond A.J. Bayesian inference of population size history from multiple loci. BMC Evol. Biol. 2008, 8:289.
35. Ho S.Y.W., Shapiro B. Skyline-plot methods for estimating demographic history from nucleotide sequences. Mol. Ecol. Resour. 2011, 11:423-434.
36. Horrocks J.A., Vermeer L.A., Kreuger B., Coyne M., Schroeder B., Balazs G. Migration routes and destination characteristics of post-nesting hawksbill turtles satellite-tracked from Barbados, West Indies. Chelonian Conserv. Biol. 2001, 4:107-114.
37. IUCN IUCN Red List of Threatened Species 2012.
38. IUCN/SSC Marine Turtle Specialist Group Hawksbill Turtles in the Caribbean Region: Basic Biological Characteristics and Population Status http://www.cites.org/common/prog/hbt/consolidated_paper.pdf.
39. Jombart T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 2008, 24:1403-1405.
40. Jombart T., Devillard S., Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 2010, 11:94.
41. Kumar S., Nei M., Dudley J., Tamura K. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief. Bioinform. 2008, 9:299-306.
42. Lahanas P.N., Bjorndal K.A., Bolten A.B., Encalada S.E., Miyamoto M.M., Valverde R.A., Bowen B.W. Genetic composition of a green turtle (Chelonia mydas) feeding ground population: evidence for multiple origins. Mar. Biol. 1998, 130:345-352.
43. Lara-Ruiz P., Lopez G.G., Santos F.R., Soares L.S. Extensive hybridization in hawksbill turtles (Eretmochelys imbricata) nesting in Brazil revealed by mtDNA analyses. Conserv. Genet. 2006, 7:773-781.
44. Leroux R.A., Dutton P.H., Abreu-Grobois F.A., Lagueux C.J., Campbell C.L., Delcroix E., Chevalier J., Horrocks J.A., Hillis-Starr Z., Troëng S., Harrison E., Stapleton S. Re-examination of population structure and phylogeography of hawksbill turtles in the wider Caribbean using longer mtDNA sequences. J. Hered. 2012, 103:806-820.
45. Luke K., Horrocks J., LeRoux R., Dutton P. Origins of green turtle (Chelonia mydas) feeding aggregations around Barbados, West Indies. Mar. Biol. 2004, 144:799-805.
46. Marcovaldi M.A., Filippini A. Trans-Atlantic movement by a juvenile hawksbill turtle. Mar. Turt. Newsl. 1991, 52:3.
47. Marcovaldi M.A., Laurent A. A six season study of marine turtle nesting at Praia do Forte, Bahia, Brazil, with implications for conservation and management. Chelonian Conserv. Biol. 1996, 55-59.
48. Marcovaldi M.A., Vieitas C.F., Godfrey M.H. Nesting and conservation of hawksbill turtles (Eretmochelys imbricata) in northern Bahia, Brazil. Chelonian Conserv. Biol. 1999, 3:301-307.
49. Marcovaldi M.A., Lopez G.G., Soares L.S., Lopez-Mendilaharsu M. Satellite tracking of hawksbill turtles Eretmochelys imbricata nesting in northern Bahia, Brazil: turtle movements and foraging destinations. Endanger. Species Res. 2012, 17:123-132.
50. Marcovaldi M.A., Lopez G.G., Soares L.S., Santos A.J.B., Bellini C., Barata P.C.R. Fifteen years of hawksbill sea turtle (Eretmochelys imbricata) nesting in northern Brazil. Chelonian Conserv. Biol. 2007, 6:223-228.
51. Marcovaldi M.Â., Lopez G.G., Soares L.S., Belini C., Santos A.S.D., Lopez M. Avaliação do estado de conservação da tartaruga marinha Eretmochelys imbricata (Linnaeus, 1766) no Brasil. Rev. Biodivers. Bras. 2011, 1:20-27.
52. Matsuda Y., Nishida-Umehara C., Tarui H., Kuroiwa A., Yamada K., Isobe T., Ando J., Fujiwara A., Hirao Y., Nishimura O., Ishijima J., Hayashi A., Saito T., Murakami T., Murakami Y., Kuratani S., Agata K. Highly conserved linkage homology between birds and turtles: bird and turtle chromosomes are precise counterparts of each other. Chromosome Res. 2005, 13:601-615.
53. Meylan A. Spongivory in hawksbill turtles - a diet of glass. Science 1988, 239:393-395.
54. Meylan A.B. International movements of immature and adult hawksbill turtles (Eretmochelys imbricata) in the Caribbean region. Chelonian Conserv. Biol. 1999, 3:189-194.
55. Meylan A.B., Donnelly M. Status justification for listing the hawksbill turtle (Eretmochelys imbricata) as critically endangered on the 1996 IUCN red list of threatened animals. Chelonian Conserv. Biol. 1999, 3:200-224.
56. Miller J.D., Dobbs K.A., Limpus C.J., Mattocks N., Landry A.M. Long-distance migrations by the hawksbill turtle, Eretmochelys imbricata, from north-eastern Australia. Wildlife Res. 1998, 25:89-95.
57. Monzón-Argüello C., Rico C., Marco A., Lopez P., Lopez-Jurado L.F. Genetic characterization of eastern Atlantic hawksbill turtles at a foraging group indicates major undiscovered nesting populations in the region. J. Exp. Mar. Biol. Ecol. 2010, 387:9-14.
58. Monzón-Argüello C., Loureiro N.S., Delgado C., Marco A., Lopes J.M., Gomes M.G., Abreu-Grobois F.A. Príncipe island hawksbills: genetic isolation of an eastern Atlantic stock. J. Exp. Mar. Biol. Ecol. 2011, 407:345-354.
59. Mortimer J.A., Donnelly M., (IUCN SSC Marine Turtle Specialist Group) Eretmochelys imbricata. IUCN Red List of Threatened Species. Version 2012.2 2008, www.ucnredlist.org.
60. Mortimer J.A., Donnelly M., Meylan A.B., Meylan P.A. Critically endangered hawksbill turtles: molecular genetics and the broad view of recovery. Mol. Ecol. 2007, 16:3516-3517.
61. Musick J.A., Limpus C.J. Habitat utilization and migration in juvenile sea turtles. The Biology of Sea Turtles 1997, CRC Press, Boca Raton. P.L. Lutz, J.A. Musick (Eds.).
62. Paradis E., Claude J., Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 2004, 20:289-290.
63. R: a language and environment for statistical computing. In: computing, R.F.f.S. (Ed.), Vienna, Austria.
64. Rankin-Baransky K., Williams C.J., Bass A.L., Bowen B.W., Spotila J.R. Origin of loggerhead turtle (Caretta caretta) strandings in the northwest Atlantic as determined by mtDNA analysis. J. Herpetol. 2001, 35:638-646.
65. Reis E.C., Soares L.S., Vargas S.M., Santos F.R., Young R.J., Bjorndal K.A., Bolten A.B., Lobo-Hajdu G. Genetic composition, population structure and phylogeography of the loggerhead sea turtle: colonization hypothesis for the Brazilian rookeries. Conserv. Genet. 2010, 11:1467-1477.
66. Richardson P.B., Bruford M.W., Calosso M.C., Campbell L.M., Clerveaux W., Formia A., Godley B.J., Henderson A.C., McClellan K., Newman S., Parsons K., Pepper M., Ranger S., Silver J.J., Slade L., Broderick A.C. Marine turtles in the Turks and Caicos Islands: remnant rookeries, regionally significant foraging stocks, and a major turtle fishery. Chelonian Conserv. Biol. 2009, 8:192-207.
67. Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, New York. 3rd ed.
68. Spotila J. Sea Turtles: A Complete Guide to Their Biology, Behavior, and Conservation 2004, Johns Hopkins University Press, Baltimore, MD.
69. Tabib M., Zolgharnein H., Mohammadi M., Salari-Aliabadi M., Qasemi A., Roshani S., Rajabi-Maham H., Frootan F. mtDNA variation of the critically endangered hawksbill turtle (Eretmochelys imbricata) nesting on Iranian islands of the Persian Gulf. Genet. Mol. Res. 2011, 10.
70. Troeng S., Dutton P.H., Evans D. Migration of hawksbill turtles Eretmochelys imbricata from Tortuguero, Costa Rica. Ecography 2005, 28:394-402.
71. Velez-Zuazo X., Ramos W.D., van Dam R.P., Diez C.E., Abreu-Grobois A., Mcmillan W.O. Dispersal, recruitment and migratory behaviour in a hawksbill sea turtle aggregation. Mol. Ecol. 2008, 17:839-853.
72. Vilaça S.T., Vargas S.M., Lara-Ruiz P., Molfetti É., Reis E.C., Lobo-Hajdu G., Soares L.S., Santos F.R. Nuclear markers reveal a complex introgression pattern among marine turtle species on the Brazilian coast. Mol. Ecol. 2012, 21:4300-4312.
73. Wallace B.P., DiMatteo A.D., Hurley B.J., Finkbeiner E.M., Bolten A.B., Chaloupka M.Y., Hutchinson B.J., Abreu-Grobois F.A., Amorocho D., Bjorndal K.A., Bourjea J., Bowen B.W., Duenas R.B., Casale P., Choudhury B.C., Costa A., Dutton P.H., Fallabrino A., Girard A., Girondot M., Godfrey M.H., Hamann M., Lopez-Mendilaharsu M., Marcovaldi M.A., Mortimer J.A., Musick J.A., Nel R., Pilcher N.J., Seminoff J.A., Troeng S., Witherington B., Mast R.B. Regional management units for marine turtles: a novel framework for prioritizing conservation and research across multiple scales. PLoS One 2010, 5.
74. Witham R. The "lost years" question in young sea turtles. Am. Zool. 1980, 20:525-530.
75. Wright L.I., Fuller W.J., Godley B.J., McGowan A., Tregenza T.O.M., Broderick A.C. Reconstruction of paternal genotypes over multiple breeding seasons reveals male green turtles do not breed annually. Mol. Ecol. 2012, 21:3625-3635.