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Marine Biology

, Volume 158, Issue 3, pp 571–587 | Cite as

Genetic structure of the southeastern United States loggerhead turtle nesting aggregation: evidence of additional structure within the peninsular Florida recovery unit

  • Brian M. Shamblin
  • Mark G. Dodd
  • Dean A. Bagley
  • Llewellyn M. Ehrhart
  • Anton D. Tucker
  • Chris Johnson
  • Raymond R. Carthy
  • Russell A. Scarpino
  • Erin McMichael
  • David S. Addison
  • Kristina L. Williams
  • Michael G. Frick
  • Stefanie Ouellette
  • Anne B. Meylan
  • Matthew H. Godfrey
  • Sally R. Murphy
  • Campbell J. NairnEmail author
Original Paper

Abstract

The southeastern United States supports one of two large loggerhead turtle (Caretta caretta) nesting aggregations worldwide and is therefore critical to global conservation and recovery efforts for the species. Previous studies have established the presence of four demographically distinct nesting populations (management units) corresponding to beaches from (1) North Carolina through northeastern Florida, (2) peninsular Florida, (3) the Dry Tortugas, and (4) northwest Florida. Temporal and geographic genetic structure of the nesting aggregation was examined utilizing partial mitochondrial control region haplotype frequencies from 834 samples collected over the 2002 through 2008 nesting seasons from 19 beaches as well as previously published haplotype data. Most rookeries did not exhibit interannual genetic variation. However, the interannual variation detected did significantly impact the interpretation of spatial genetic structure in northeastern Florida. Based on pairwise F ST comparisons, exact tests of population differentiation, and analysis of molecular variance, the present study upholds the distinctiveness of the four currently recognized management units and further supports recognition of discrete central eastern, southern (southeastern and southwestern), and central western Florida management units. Further subdivision may be warranted, but more intensive genetic sampling is required. In addition, tools such as telemetry and mark-recapture are needed to complement genetic data and overcome limitations of genetic markers in resolving loggerhead turtle rookery connectivity in the southeastern USA.

Keywords

Haplotype Frequency Management Unit Green Turtle Nest Density Nest Season 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

In additional to the many students, interns, technicians, and volunteers associated with authors’ institutions, we thank individuals representing the following organizations for providing samples: Bald Head Island Conservancy, Amelia Island Sea Turtle Watch, Ponte Vedra Turtle Patrol, Vilano Marine Turtle Patrol, Guana Tolomato Matanzas National Estuarine Research Reserve, Flagler-Volusia Turtle Patrol, Ecological Associates, Inc., John U. Lloyd State Park, National Marine Fisheries Service Southeast Fisheries Science Center, Bill Baggs Cape Florida State Park, St. George Island Volunteer Turtlers, and T. H. Stone Memorial St. Joseph Peninsula State Park. We thank D. Browning and S. Dawsey of Cape Romain National Wildlife Refuge, J. Stiner and C. Carter of Canaveral National Seashore, and P. Tritaik of Archie Carr National Wildlife Refuge for permitting beach access and logistical assistance. D. Griffin from South Carolina Department of Natural Resources and A. McKee of the University of Georgia assisted with sample collection on Cape Island. Thanks to M. Koperski and R. Trindell for assistance with Florida permitting, and G. Clark of the University of Florida sequencing core facility for haplotype assignments of the CSB samples. The Florida Fish and Wildlife Conservation Commission’s nest survey program is supported by the US Fish and Wildlife Service and the Florida Sea Turtle License Plate. We gratefully acknowledge funding provided by the National Oceanic and Atmospheric Administration’s Protected Species Cooperative Conservation Grant Program, the Georgia Department of Natural Resources, The Environmental Resource Network, and the University of Georgia Warnell School of Forestry and Natural Resources. This research was funded in part by a grant awarded from the Sea Turtle Grants Program. The Sea Turtle Grants Program is funded from proceeds from the sale of the Florida Sea Turtle License Plate. Learn more at www.helpingseaturtles.org. We would also like to thank two anonymous reviewers for substantially increasing the quality of the manuscript.

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References

  1. Allendorf FW, Waples RS (1995) Conservation and genetics of salmonid fishes. In: Avise JC, Hamrick JL (eds) Conservation genetics. Chapman and Hall, New York, pp 238–280Google Scholar
  2. Avise JC (1992) Molecular population structure and the biogeographic history of a regional fauna: a case history with lessons for conservation biology. Oikos 63:62–76CrossRefGoogle Scholar
  3. Avise JC (1995) Mitochondrial DNA polymorphism and a connection between genetics and demography of relevance to conservation. Conserv Biol 9:686–690CrossRefGoogle Scholar
  4. Avise JC, Bowen BW, Lamb T, Meylan AB, Bermingham E (1992) Mitochondrial DNA evolution at a turtle’s pace: evidence for low genetic variability and reduced microevolutionary rate in the testudines. Mol Biol Evol 9:457–473Google Scholar
  5. Baldwin R, Hughes GR, Price RIT (2003) Loggerhead turtles in the Indian Ocean. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Institution Press, Washington, DC, pp 218–232Google Scholar
  6. Bell R, Richardson JI (1978) An analysis of tag recoveries from loggerhead sea turtles (Caretta caretta) nesting on Little Cumberland Island, Georgia. Fla Mar Res Publ 33:1–66Google Scholar
  7. Bjorndal K, Bolten A (2008) Annual variation in source contributions to a mixed stock: implications for quantifying connectivity. Mol Ecol 17:2185–2193CrossRefGoogle Scholar
  8. Bjorndal K, Bolten A, Troeng S (2005) Population structure and genetic diversity in green turtles nesting at Tortuguero, Costa Rica, based on mitochondrial DNA control region sequences. Mar Biol 147:1449–1457CrossRefGoogle Scholar
  9. Bolten AB (2003) The loggerhead sea turtle- so excellent a fishe. In: Bolten AB, Witherington BE (eds) Loggerhead sea turtles. Smithsonian Institution Press, Washington, pp 1–3Google Scholar
  10. Bolten AB, Bjorndal KA, Martins HR, Dellinger T, Biscoito MJ, Encalada SE, Bowen BW (1998) Transatlantic developmental migrations of loggerhead sea turtles demonstrated by mtDNA sequence analysis. Ecol Appl 8:1–7CrossRefGoogle Scholar
  11. Bowen BW, Karl SA (2007) Population genetics and phylogeography of sea turtles. Mol Ecol 16:4886–4907CrossRefGoogle Scholar
  12. Bowen B, Avise JC, Richardson JI, Meylan AB, Margaritoulis D, Hopkins-Murphy SR (1993) Population structure of loggerhead turtles (Caretta caretta) in the northwestern Atlantic Ocean and Mediterranean Sea. Conserv Biol 7:834–844CrossRefGoogle Scholar
  13. Bowen BW, Kamezaki N, Limpus CJ, Hughes GR, Meylan AB, Avise JC (1994) Global phylogeography of the loggerhead turte (Caretta caretta) as indicated by mitochondrial DNA haplotypes. Evolution 48:1820–1828CrossRefGoogle Scholar
  14. Bowen BW, Bass AL, Chow S-M, Bostrom M, Bjorndal KA, Bolten AB, Okuyama T, Bolker BM, Epperly S, La Casella E, Shaver D, Dodd M, Hopkins-Murphy SR, Musick JA, Swingle M, Rankin-Baransky K, Teas W, Witzell WN, Dutton PH (2004) Natal homing in juvenile loggerhead turtles (Caretta caretta). Mol Ecol 13:3797–3808CrossRefGoogle Scholar
  15. Bowen BW, Bass AL, Soares L, Toonen RJ (2005) Conservation implications of complex population structure: lessons from the loggerhead turtle (Caretta caretta). Mol Ecol 14:2389–2402CrossRefGoogle Scholar
  16. Carr A, Carr MH (1970) Modulated reproductive periodicity in Chelonia. Ecology 51:335–337CrossRefGoogle Scholar
  17. Carr A, Carr M (1972) Site fixity in the Caribbean green turtle. Ecology 53:425–429CrossRefGoogle Scholar
  18. Carr A, Carr M, Meylan A (1978) The ecology and migrations of sea turtles. No. 7. The West Caribbean green turtle colony. Bull Am Mus Nat Hist 162:1–46Google Scholar
  19. Carreras C, Pascual M, Cardona L, Aguilar A, Margaritoulis D, Rees AF, Turkozan O, Levy Y, Gasith A, Aureggi M, Khalil M (2007) The genetic structure of the loggerhead sea turtle (Caretta caretta) in the Mediterranean as revealed by nuclear and mitochondrial DNA and its conservation implications. Conserv Genet 8:1572–9737CrossRefGoogle Scholar
  20. Davis GE, Whiting MC (1977) Loggerhead sea turtle nesting in Everglades National Park, Florida, USA. Herpetologica 33:18–28Google Scholar
  21. Dethmers KEM, Broderick D, Moritz C, FitzSimmons N, Limpus C, Lavery S, Whiting S, Guinea M, Prince RIT, Kennet R (2006) The genetic structure of Australasian green turtles (Chelonia mydas): exploring the geographical scale of genetic exchange. Mol Ecol 15:3931–3946CrossRefGoogle Scholar
  22. Dodd C, Byles R (2003) Post-nesting movements and behavior of loggerhead sea turtles (Caretta caretta) departing from east-central Florida nesting beaches. Chelonian Conserv Biol 4:530–536Google Scholar
  23. Dodd CK Jr (1988) Synopsis of the biological data on the loggerhead sea turtle Caretta caretta (Linnaeus 1758), 88(14)Google Scholar
  24. Encalada SE, Bjorndal KA, Bolten AB, Zurita JC, Schroeder B, Possardt E, Sears CJ, Bowen BW (1998) Population structure of loggerhead turtle (Caretta caretta) nesting colonies in the Atlantic and Mediterranean as inferred from mitochondrial DNA control region sequences. Mar Biol 130:567–575CrossRefGoogle Scholar
  25. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  26. Foley A, Schroeder BA, MacPherson S (2008) Post-nesting migrations and resident areas of Florida loggerheads. In: Kalb H, Rohde A, Gayheart K, Shanker K (eds) Proceedings of the Twenty-fifth annual symposium on sea turtle biology and conservation. NOAA Technical Memorandum NMFS-SEFSC-582Google Scholar
  27. Francisco AM, Bass AL, Bowen BW (1999) Genetic characterization of loggerhead turtles (Caretta caretta) nesting in Volusia CountyGoogle Scholar
  28. Fraser D, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752Google Scholar
  29. Girard C, Tucker AD, Calmettes B (2009) Post-nesting migrations of loggerhead sea turtles in the Gulf of Mexico: dispersal in highly dynamic conditions. Mar Biol 156:1827–1839CrossRefGoogle Scholar
  30. Hastings A (1993) Complex interactions between dispersal and dynamics: lessons from coupled logistic equations. Ecology 74:1362–1372CrossRefGoogle Scholar
  31. Hatase H, Kinoshita M, Bando T, Kamezaki N, Sato K, Matsuzawa Y, Goto K, Omuta K, Nakashima Y, Takeshita H, Sakamoto W (2002) Population structure of loggerhead turtles, Caretta caretta, nesting in Japan: bottlenescks on the Pacific population. Mar Biol 141:299–305CrossRefGoogle Scholar
  32. Hoelzel AR (1998) Genetic structure of cetacean populations in sympatry, parapatry, and mixed assemblages: implications for conservation policy. J Hered 89:451–458CrossRefGoogle Scholar
  33. Laurent L, Casale P, Bradai MN, Godley BJ, Gerosa G, Broderick AC, Schroth W, Schierwater B, Levy AM, Freggi D, El-Mawla EMA, Hadoud DA, Gomati HE, Domingo M, Hadjichristophorou M, Kornaraky L, Demirayak F, Gautier CH (1998) Molecular resolution of marine turtle stock composition in fishery bycatch: a case study in the Mediterranean. Mol Ecol 7:1529–1542CrossRefGoogle Scholar
  34. Lohmann K, Lohmann C, Putman N (2007) Magnetic maps in animals: nature’s GPS. J Exp Biol 211:3697–3705CrossRefGoogle Scholar
  35. Lohmann K, Luschi P, Hays G (2008a) Goal navigation and island-finding in sea turtles. J Exp Mar Biol Ecol 356:83–95CrossRefGoogle Scholar
  36. Lohmann K, Putman N, Lohmann C (2008b) Geomagnetic imprinting: a unifying hypothesis for long-distance natal homing in salmon and sea turtles. Proc Natl Acad Sci USA 105:19096–19101CrossRefGoogle Scholar
  37. Meylan AB, Bjorndal KA, Turner BJ (1983) Sea turtles nesting at Melbourne Beach, Florida, II. Post-nesting movements of Caretta caretta. Biol Conserv 26:79–90CrossRefGoogle Scholar
  38. Moore MK, Ball RM Jr (2002) Multiple paternity in loggerhead sea turtles (Caretta caretta) nests on Melbourne Beach, Florida: a microsatellite analysis. Mol Ecol 11:281–288CrossRefGoogle Scholar
  39. Moritz C (1994) Defining evolutionary significant units for conservation. Trends Ecol Evol 9:373–374CrossRefGoogle Scholar
  40. Mortimer JA (1982) Factors influencing beach selection by nesting sea turtles. In: Bjorndal KA (ed) Biology and conservation of sea turtles. Smithsonian Institution Press, Washington, pp 45–52Google Scholar
  41. National Marine Fisheries Service and US Fish and Wildlife Service (2008) Recovery plan for the Northwest atlantic population of the loggerhead sea turtle (Caretta caretta), Second Revision. National Marine Fisheries Service, Silver Spring, MDGoogle Scholar
  42. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  43. Norman JA, Moritz C, Limpus CJ (1994) Mitochondrial DNA control region polymorphisms: genetic markers for ecological studies of marine turtles. Mol Ecol 3:363–373CrossRefGoogle Scholar
  44. Pearce AF (2001) Contrasting population structure of the loggerhead turtle (Caretta caretta) using mitochondrial and nuclear DNA markers. Masters Thesis. University of Florida. Gainesville, FLGoogle Scholar
  45. Plotkin PT, Spotila JR (2002) Post-nesting migrations of loggerhead turtles Caretta caretta from Georgia, USA: conservation implications for a genetically distinct subpopulation. Oryx 36:396–399CrossRefGoogle Scholar
  46. Provancha JA, Ehrhart LM (1987) Sea turtle nesting trends at Kennedy space center and Cape Canaveral air force stattion, Florida, and relationships with factors influencing nest site selection. In: Witzell WN (ed) Ecology of East Florida sea turtles. NOAA Technical Report NMFS 53, Miami, FLGoogle Scholar
  47. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283CrossRefGoogle Scholar
  48. Reich K, Bjorndal K, Frick M, Witherington B, Johnson C, Bolten A (2010) Polymodal foraging in adult female loggerheads (Caretta caretta) Marine Biology 157:113–121Google Scholar
  49. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  50. Ruiz-Urquiola A, Vega-Polanco M, Riverón-Gíro F, Abreu-Grobois FA, Solano-Abadía J, Pérez-Bermúdez E, Frías-Soler R, Azanza-Ricardo J, Díaz-Fernández R, Ibarra-Martín M, Espinosa-López G (2010) Genetic structure of loggerhead populations in the greater Caribbean and Atlantic western shore based on mitochondrial DNA sequences, with an emphasis on the rookeries from southwestern Cuba. In: Dean K, López-Castro M (compilers) Proceedings of the Twenty-eighth Annual Symposium on Sea Turtle Biology and Conservation. NOAA Technical Memorandum NOAA NMFS-SEFSC-602Google Scholar
  51. Schroth W, Streit B, Schierwater B (1996) Evolutionary handcap for turtles. Nature 384:521–522CrossRefGoogle Scholar
  52. Shamblin BM, Faircloth BC, Dodd M, Wood-Jones A, Castleberry SB, Carroll JP, Nairn CJ (2007) Tetranucleotide microsatellites from the loggerhead sea turtle (Caretta caretta). Mol Ecol Notes 7:784–787CrossRefGoogle Scholar
  53. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792CrossRefGoogle Scholar
  54. Slatkin M (1993) Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47:264–279CrossRefGoogle Scholar
  55. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526Google Scholar
  56. Taylor B, Dizon AE (1996) The need to estimate power to link genetics and demography for conservation. Conserv Biol 10:661–664CrossRefGoogle Scholar
  57. Tröeng S, Chaloupka M (2007) Variation in adult annual survival probability and remigration intervals of sea turtles. Mar Biol 151:1721–1730CrossRefGoogle Scholar
  58. Turtle Expert Working Group (2009) An assessment of the loggerhead turtle population in the western North Atlantic Ocean. NOAA Technical Memorandum NMFS-SEFSC-575Google Scholar
  59. Velez-Zuazo X, Ramos WD, van Dam RP, Diez CE, Abreu-Grobois A, McMillan O (2008) Diespersal, recruiment and migratory behaviour in a hawksbill sea turtle aggregation. Mol Ecol 17:839–853CrossRefGoogle Scholar
  60. Williams KL, Frick MG (2008) Tag returns from loggerhead turtles from Wassaw Island, Georgia. Southeast Nat 7:165–172CrossRefGoogle Scholar
  61. Wisby WJ, Hasler AD (1954) Effect of olfactory occlusion on migrating silver salmon (O. kisutch). J Fish Res Board Canada 11:472–478Google Scholar
  62. Witherington B, Kubilis P, Brost B, Meylan A (2009) Decreasing annual nest counts in a globally important loggerhead sea turtle population. Ecol Appl 19:30–54CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Brian M. Shamblin
    • 1
  • Mark G. Dodd
    • 2
  • Dean A. Bagley
    • 3
  • Llewellyn M. Ehrhart
    • 3
  • Anton D. Tucker
    • 4
  • Chris Johnson
    • 5
  • Raymond R. Carthy
    • 6
  • Russell A. Scarpino
    • 6
  • Erin McMichael
    • 6
  • David S. Addison
    • 7
  • Kristina L. Williams
    • 8
  • Michael G. Frick
    • 8
  • Stefanie Ouellette
    • 9
  • Anne B. Meylan
    • 10
  • Matthew H. Godfrey
    • 11
  • Sally R. Murphy
    • 12
  • Campbell J. Nairn
    • 1
    Email author
  1. 1.Daniel B. Warnell School of Forestry and Natural ResourcesUniversity of GeorgiaAthensUSA
  2. 2.Georgia Department of Natural ResourcesBrunswickUSA
  3. 3.Department of BiologyUniversity of Central FloridaOrlandoUSA
  4. 4.Mote Marine LaboratorySarasotaUSA
  5. 5.Loggerhead Marinelife CenterJuno BeachUSA
  6. 6.Florida Fish and Wildlife Cooperative Research UnitUniversity of FloridaGainesvilleUSA
  7. 7.Conservancy of Southwest FloridaNaplesUSA
  8. 8.Caretta Research ProjectSavannahUSA
  9. 9.Broward County Sea Turtle Conservation ProgramNova Southeastern University Oceanographic CenterDaniaUSA
  10. 10.Florida Fish and Wildlife Conservation CommissionFish and Wildlife Research InstituteSt. PetersburgUSA
  11. 11.North Carolina Wildlife Resources CommissionBeaufortUSA
  12. 12.South Carolina Department of Natural Resources (retired)SheldonUSA

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