Mating system in a gopher tortoise population established through multiple translocations: Apparent advantage of prior residence

Biological Conservation

Volumn 144, Issue 1, 2011, Pages 175-183

  Tuberville, Tracey D ^a   Norton, Terry M ^b,c   Waffa, Bradley J ^d,e   Hagen, Cris ^a   Glenn, Travis C ^a,f  

^a UNIVERSITY OF GEORGIA   (United States)

^b St Catherines Island Wildlife Survival Center   (United States)

^c Georgia Sea Turtle Center   (United States)

^d UNIVERSITY OF THE SOUTH   (United States)

^e NORTH CAROLINA STATE UNIVERSITY   (United States)

^f UNIVERSITY OF GEORGIA   (United States)

Author keywords

Augmentation; Gopherus polyphemus; Mating system; Microsatellite; Reproductive success; Translocation

Indexed keywords

CLUTCH SIZE; DISPERSAL; FREQUENCY ANALYSIS; FUNCTIONAL MORPHOLOGY; GENETIC MARKER; GENOTYPE; MANAGEMENT PRACTICE; POLYMORPHISM; POPULATION DECLINE; POPULATION STRUCTURE; RARE SPECIES; REPRODUCTION; REPRODUCTIVE STRATEGY; REPRODUCTIVE SUCCESS; SPECIES CONSERVATION; SURVIVORSHIP; TRANSLOCATION; TURTLE;

GOPHERUS; GOPHERUS POLYPHEMUS; TESTUDINIDAE;

EID: 78751572845     PISSN: 00063207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocon.2010.08.012     Document Type: Article

References (73)

1. Aresco M.J., Guyer C. Efficacy of using scute annuli to determine growth histories and age of Gopherus polyphemus in southern Alabama. Copeia 1998, 1998:1094-1100.
2. Aresco M.J., Guyer C. Growth of the tortoise Gopherus polyphemus in slash pine plantations of southcentral Alabama. Herpetologica 1999, 55:499-506.
3. Armstrong D.P., Seddon P.J. Directions in reintroduction biology. Trends in Ecology and Evolution 2008, 23:20-25.
4. Ashton K.G., Burke R.L., Layne J.N. Geographic variation in body and clutch size of gopher tortoises. Copeia 2007, 2007:355-363.
5. Berry K.H. Desert tortoise (Gopherus agassizii) relocation: implications of social behavior and movements. Herpetologica 1986, 42:113-125.
6. Bertolero A., Oro D. Conservation diagnosis of reintroducing Mediterranean pond turtles: what is wrong?. Animal Conservation 2009, 12:581-591.
7. Bertolero A., Oro D., Besnard A. Assessing the efficacy of reintroduction programmes by modelling adult survival: the example of Hermann's tortoise. Animal Conservation 2007, 10:360-368.
8. Boglioli M.D., Guyer C., Michener W.K. Mating opportunities of female gopher tortoises, Gopherus polyphemus, in relation to spatial isolation of females and their burrows. Copeia 2003, 2003:846-850.
9. Brownstein M.J., Carpten J.D., Smith J.R. Modulation of non-templated nucleotide addition by Taq DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 1996, 20:1004.
10. Burke R.L., Ewert M.A., McLemore J.B., Jackson D.R. Temperature-dependent sex determination and hatching success in the gopher tortoise (Gopherus polyphemus). Chelonian Conservation and Biology 1996, 2:86-88.
11. Carter M.J., Milton I.D. An inexpensive and simple method for DNA purifications on silica particles. Nucleic Acids Research 1993, 21:1044.
12. Cohen J.E. Natural primate troops and a stochastic population model. American Naturalist 1969, 103:455-477.
13. Cook R.P. Dispersal, home range establishment, survival, and reproduction of translocated eastern box turtles, Terrapene c. carolina. Applied Herpetology 2004, 1:197-228.
14. Courchamp F., Clutton-Brock T., Grenfell B. Inverse density dependence and the Allee effect. Trends in Ecology and Evolution 1999, 14:405-410.
15. Cristol D.A., Nolan V., Ketterson E.D. Effect of prior residence status of dark-eyed juncos, Junco hyemalis. Animal Behaviour 1990, 40:580-586.
16. Demuth J.P. The Effects of constant and fluctuating incubation temperature on sex determination, growth, and performance in the gopher tortoise Gopherus polyphemus. Canadian Journal of Zoology 2001, 79:1609-1620.
17. Dickens M.J., Delehanty D.J., Romero L.M. Stress: an inevitable component of animal translocation. Biological Conservation 2010, 143:1329-1341.
18. Diemer, J.E., Moore, C.T., 1994. Reproduction of gopher tortoises in north-central Florida. In: Bury, R.B., Germano, D.J. (Eds.), Biology of North American Tortoises. Fish and Wildlife Research, vol. 13, pp. 129-137.
19. DeWoody A.J., Schupp J., Kenefic L., Busch J., Murfitt L., Keim P. Universal method for producing ROX-labeled size standards suitable for automated genotyping. BioTechniques 2004, 37:348-350.
20. Don R.H., Cox P.T., Wainwright B.J., Baker K., Mattick J.S. 'Touchdown' PCR to circumvent spurious priming during gene amplification. Nucleic Acids Research 1991, 19:4008.
21. Douglass, J., 1976. The mating system of the gopher tortoise, Gopherus polyphemus, in southern Florida. MS Thesis, University of South Florida, Tampa, FL.
22. Eden S.F. Dispersal and competitive ability in the magpie: an experimental study. Animal Behaviour 1987, 35:764-772.
23. Eubanks J.O., Michener W.K., Guyer C. Patterns of movement and burrow use in a population of gopher tortoises (Gopherus polyphemus). Herpetologica 2003, 59:311-321.
24. Ewert M.A., Legler J.M. Hormonal induction of oviposition in turtles. Herpetologica 1978, 34:314-318.
25. FitzSimmons N.N., Moritz C., Moore S.S. Conservation and dynamics of microsatellite loci over 300 million years of marine turtle evolution. Molecular Biology and Evolution 1995, 12:432-440.
26. Galbraith, D.A., 1991. Studies of mating systems in wood turtles (Clemmys insculpta) and snapping turtles (Chelydra serpentina) using DNA fingerprinting. PhD Dissertation, Queen's University, Kingston, Ontario.
27. Galbraith D.A. Review: multiple paternity and sperm storage in turtles. Herpetological Journal 1993, 3:117-123.
28. Galbraith D.A., White B.N., Brooks R.J., Boag P.T. The fine structure of home ranges of male Chelydra serpentina: are snapping turtles territorial?. Canadian Journal of Zoology 1987, 65:2623-2629.
29. Gibbons J.W., Greene J.L. X-ray photography: a technique to determine reproductive patterns of freshwater turtles. Herpetologica 1979, 35:86-89.
30. Gibbons J.W., Scott D.E., Ryan T.J., Buhlmann K.A., Tuberville T.D., Metts B.S., Greene J.L., Mills T., Leiden Y., Poppy S., Winne C.T. The global decline of reptiles, déjà vu amphibians. BioScience 2000, 50:653-666.
31. Gist D.H., Congdon J.D. Oviductal sperm storage as a reproductive tactic of turtles. The Journal of Experimental Zoology 1998, 282:526-534.
32. Glenn T.C., Schable N.A. Isolating microsatellite DNA loci. Methods in Enzymology 2005, 395:202-222.
33. Griffith B., Scott J.M., Carpenter J.W., Reed C. Translocation as a species conservation tool: status and strategy. Science 1989, 245:477-480.
34. Hernandez-Divers S.M., Hernandez-Divers S.J., Wyneken J. Angiographic, anatomic, and clinical technique descriptions of a subcarapacial venipuncture site for chelonians. Journal of Herpetological Medicine and Surgery 2002, 12:32-37.
35. Holberton R.L., Hanano R., Able K.P. Age-related dominance in male dark-eyed juncos: effects of plumage and prior residence. Animal Behaviour 1990, 40:573-579.
36. Iverson J.B. The reproductive biology of Gopherus polyphemus (Chelonia: Testudinidae). American Midland Naturalist 1980, 103:353-359.
37. Johnson A.M., Chappell G., Price A.C., Rodd F.H., Olendorf R., Hughes K. Inbreeding depression and inbreeding avoidance in a natural population of guppies (Poecilia reticulata). Ethology 2010, 116:448-457.
38. Johnson V.M., Guyer C., Boglioli M.D. Phenology of attempted matings in gopher tortoises. Copeia 2007, 2007:490-495.
39. Johnson V.M., Guyer C., Hermann S.M., Eubanks J., Michener W.K. Patterns of dispersion and burrow use support scramble competition polygyny in Gopherus polyphemus. Herpetologica 2009, 65:214-218.
40. Jones A.G. GERUD 2.0: a computer program for the reconstruction of parental genotypes from half-sib arrays with known or unknown parents. Molecular Ecology Notes 2005, 5:708-711.
41. Jones A.G., Ardren W.R. Methods of parentage analysis in natural populations. Molecular Ecology 2003, 12:2511-2523.
42. Kalinowski S.T., Taper M.L., Marshall T.C. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 2007, 16:1099-1106.
43. Kaufmann J.H. The social behavior of wood turtles, Clemmys insculpta, in central Pennsylvania. Herpetological Monographs 1992, 6:1-25.
44. Keogh J.S. Evolutionary, behavioural and molecular ecology must meet to achieve long-term conservation goals. Molecular Ecology 2009, 18:3761-3762.
45. Lance S.L., Tuberville T.D., Dueck L., Holz-Schietinger C., Trosclair P.L., Elsey R.M., Glenn T.C. Multiyear multiple paternity and mate fidelity in the American alligator, Alligator mississippiensis. Molecular Ecology 2009, 18:4508-4520.
46. Landers J.L., Garner J.A., McRae W.A. Reproduction of gopher tortoises (Gopherus polyphemus) in southwestern Georgia. Herpetologica 1980, 36:353-361.
47. Lihoreau M., Zimmer C., Rivault C. Mutual mate choice: when it pays both sexes to avoid inbreeding. PLoS ONE 2008, 3:e3365.
48. Limmer B., Becker P.H. Improvement of reproductive performance with age and breeding experience depends on recruitment age in a long-lived seabird. Oikos 2010, 119:500-507.
49. Massot M., Clobert J., Lecomte J., Barbault R. Incumbent advantage in common lizards and their colonizing ability. Journal of Animal Ecology 1994, 63:431-440.
50. Milinkovitch M.C., Monteyne D., Gibbs J.P., Fritts T.H., Tapia W., Snell H.L., Tiedemann R., Caccone A., Powell J.R. Genetic analysis of a successful repatriation programme: giant Galápagos tortoises. Proceedings of the Royal Society of London B 2004, 271:341-345.
51. Miller E.J., Eldridge M.D.B., Cooper D.W., Herbert C.A. Dominance, body size and internal relatedness influence male reproductive success in eastern grey kangaroos (Macropus giganteus). Reproduction, Fertility and Development 2010, 22:539-549.
52. Miller K.A., Nelson N.J., Smith H.G., Moore J.A. How do reproductive skew and founder group size affect genetic diversity in reintroduced populations?. Molecular Ecology 2009, 18:3792-3802.
53. Moon J.C., McCoy E.D., Mushinsky H.R., Karl S.A. Multiple paternity and breeding system in the gopher tortoise, Gopherus polyphemus. Journal of Heredity 2006, 97:150-157.
54. Ott J.A., Mendonca M.T., Guyer C., Michener W.K. Seasonal changes in sex and adrenal steroid hormones of gopher tortoises (Gopherus polyphemus). General and Comparative Endocrinology 2000, 117:229-312.
55. Pearse D.E., Avise J.C. Turtle mating systems: behavior, sperm storage, and genetic paternity. Journal of Heredity 2001, 92:206-211.
56. Pearse D.E., Janzen F.J., Avise J.C. Multiple paternity, sperm storage, and reproductive success of female and male painted turtles (Chrysemys picta) in nature. Behavioral Ecology and Sociobiology 2002, 51:14-171.
57. Pulliam H.R. Sources, sinks, and population regulation. The American Naturalist 1988, 132:652-661.
58. Raymond M., Rousset F. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 1995, 86:248-249.
59. Reinert H.K., Rupert R.R. Impacts of translocation on behavior and survival of timber rattlesnakes, Crotalus horridus. Journal of Herpetology 1999, 33:45-61.
60. Rostal D.C., Jones D.N. Population biology of the gopher tortoise (Gopherus polyphemus) in southeast Georgia. Chelonian Conservation and Biology 2002, 4:479-487.
61. Schable N.A., Fischer R.U., Glenn T.C. Tetranucleotide microsatellite DNA loci from the dollar sunfish (Lepomis marginatus). Molecular Ecology Notes 2002, 2:509-511.
62. Seddon P.J. Persistence without intervention: assessing success in wildlife reintroductions. Trends in Ecology and Evolution 1999, 14:503.
63. Seigel R.A., Dodd C.K. Manipulations of turtle populations for conservation: halfway technologies or viable options?. Turtle Conservation 2000, 218-238. Smithsonian Institution Press, Washington, DC. M.W. Klemens (Ed.).
64. Sigg D.P., Goldizen A.W., Pople A.R. The importance of mating system in translocation programs: reproductive success of released male bridled nailtail wallabies. Biological Conservation 2005, 123:289-300.
65. Stephens P.A., Sutherland W.J. Consequences of the Allee effect for behaviour, ecology and conservation. Trends in Ecology and Evolution 1999, 14:401-405.
66. Teixeira C.P., de Azevedo C.S., Mendl M., Cipreste C.F., Young R.J. Revisiting translocation and reintroduction programmes: the importance of considering stress. Animal Behaviour 2007, 73:1-13.
67. Todd B.D., Willson J.D., Gibbons J.W. The global status of reptiles and causes of their decline. Ecotoxicology of Amphibians and Reptiles 2010, 47-67. CRC Press, New York, (Chapter 3). second ed. D.W. Sparling, G. Linder, C.A. Bishop, S. Krest (Eds.).
68. Tuberville, T.D., 2008. Evaluating the utility of translocation for turtle conservation: a case study based on the behavioral and demographic responses of gopher tortoises (Gopherus polyphemus). Dissertation, University of Georgia, Athens, GA, 189 pp.
69. Tuberville T.D., Norton T.M., Todd B.D., Spratt J.S. Long-term apparent survival of translocated gopher tortoises: a comparison of newly released and previously established animals. Biological Conservation 2008, 141:2690-2697.
70. Tuberville T.D., Clark E.E., Buhlmann K.A., Gibbons J.W. Translocation as a conservation tool: site fidelity and movements of repatriated gopher tortoises (Gopherus polyphemus). Animal Conservation 2005, 8:349-358.
71. Turtle Conservation Fund, 2002. A Global Action Plan for Conservation of Tortoises and Freshwater Turtles. Strategy and Funding Prospectus 2002-2007. Conservation International and Chelonian Research Foundation, Washington, DC.
72. Wiley R.H. Prior-residence and coat-tail effects in dominance relationships of male dark-eyed juncos, Junco hyemalis. Animal Behaviour 1990, 40:587-596.
73. Wingfield J.C., Sapolsky R.M. Reproduction and resistance to stress: when and how. Journal of Neuroendocrinology 2003, 15:711-724.