Conservation Genetics

, Volume 14, Issue 3, pp 649–659 | Cite as

Are captive tortoises a reservoir for conservation? An assessment of genealogical affiliation of captive Gopherus agassizii to local, wild populations

Research Article


The conservation of tortoises poses a unique situation because several threatened species are commonly kept as pets within their native ranges. Thus, there is potential for captive populations to be a reservoir for repatriation efforts. We assess the utility of captive populations of the threatened Agassiz’s desert tortoise (Gopherus agassizii) for recovery efforts based on genetic affinity to local areas. We collected samples from 130 captive desert tortoises from three desert communities: two in California (Ridgecrest and Joshua Tree) and the Desert Tortoise Conservation Center (Las Vegas) in Nevada. We tested all samples for 25 short tandem repeats and sequenced 1,109 bp of the mitochondrial genome. We compared captive genotypes to a database of 1,258 Gopherus samples, including 657 wild caught G. agassizii spanning the full range of the species. We conducted population assignment tests to determine the genetic origins of the captive individuals. For our total sample set, only 44 % of captive individuals were assigned to local populations based on genetic units derived from the reference database. One individual from Joshua Tree, California, was identified as being a Morafka’s desert tortoise, G. morafkai, a cryptic species which is not native to the Mojave Desert. Our data suggest that captive desert tortoises kept within the native range of G. agassizii cannot be presumed to have a genealogical affiliation to wild tortoises in their geographic proximity. Precautions should be taken before considering the release of captive tortoises into the wild as a management tool for recovery.


Captivity Conservation Genetics Gopherus Repatriation Testudinidae Translocation 



We thank J. Novak and T. Thorson for supporting the health clinics through their hospitals and appreciate the assistance of T. Bailey, K. Anderson, and J. Mack in sampling captive tortoises. M. McDermott at the DTCC made arrangements for sampling. Z. Brown assisted with sample processing and K. Ross and Z. Wolfenburger contributed to the data preparation. B. Sigafus helped with manuscript preparation, and S. Jones, A. Vandergast, and two anonymous reviewers provided constructive reviews. R. Murphy and A. McLuckie contributed significantly to the reference database of Mojave tortoise samples. M. Forstner and A. Fujii at Texas State University provided the reference database of Texas tortoise samples. We obtained Mexican samples through a multinational, collaborative effort including C. Meléndez and M. Villa of Comisión de Ecología y Desarrollo Sustentable del Estado de Sonora (CEDES) and F. R. Méndez de la Cruz, Instituto de Biologìa, Universidad Nacional Autónoma de México (UNAM). Special thanks go to the dedicated field crew that volunteered to make this possible, as well as M. Vaughn, R. Murphy, A. Karl, M. Brown, L. Wendland, C. Schwalbe, and P. Rosen. Permits for Mexican samples were facilitated by Secretaría de Medio Ambiente y Recursos Naturales (SEMARNAT). Funding and support for sample collection was provided by Tucson Herpetological Society, Desert Tortoise Council, Royal Ontario Museum, Canada, Arizona Game and Fish Department, University of Florida, University of Arizona, Department of Defense (Army, Marine Corps), and the U.S. Geological Survey. Tortoise handling protocols were approved by the University of Arizona (IACUC 09-138). Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.


  1. Arévalo E, Davis SK, Sites JW Jr (1994) Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of the Sceloporus grammicus complex (Phrynosomatidae) in central Mexico. Syst Biol 43:387–418Google Scholar
  2. Ashton KG, Burke RL (2007) Long-term retention of a relocated population of gopher tortoises. J Wildlife Manage 71:783–787CrossRefGoogle Scholar
  3. Banks MA, Eichert W (2000) WHICHRUN (version 3.2): a computer program for population assignment of individuals based on multilocus genotype data. J Hered 91:87–89PubMedCrossRefGoogle Scholar
  4. Benavides E, Russello M, Boyer D, Wiese RJ, Kajdacsi B, Marquez L, Garrick R, Caccone A (2012) Lineage identification and genealogical relationships among captive Galápagos tortoises. Zoo Biol 120:107–120CrossRefGoogle Scholar
  5. Berry KH (1986) Desert tortoise (Gopherus agassizii) relocation: implications of social behavior and movements. Herpetologica 42:113–125Google Scholar
  6. Berry KH, Morafka DJ, Murphy RW (2002) Defining the desert tortoise(s): our first priority for a coherent conservation strategy. Chelonian Conserv Biol 4:249–262Google Scholar
  7. Bertolero A, Oro D, Besnard A (2007) Assessing the efficacy of reintroduction programmes by modeling adult survival: the example of Hermann’s tortoise. Anim Conserv 10:360–368CrossRefGoogle Scholar
  8. Britten HB, Riddle BR, Brussard PF, Marlow R, Lee TE Jr (1997) Genetic delineation of management units for the desert tortoise, Gopherus agassizii, in northeastern Mojave Desert. Copeia 1997:523–530CrossRefGoogle Scholar
  9. Bury RB, Germano DJ, Van Devender TR, Martin BE (2002) The desert tortoise in Mexico: distribution, ecology, and conservation. In: Van Devender TR (ed) The sonoran desert tortoise. Natural history, biology, and conservation. The University of Arizona Press and Arizona-Sonora Desert Museum, TucsonGoogle Scholar
  10. Buskirk JR (1993) Distribution, status and biology of the tortoise, Geochelone chilensis, in Río Negro Province, Argentina. Stud Neotrop Fauna Environ 28:233–249CrossRefGoogle Scholar
  11. Christie MR, Marine ML, French RA, Blouin MS (2012) Genetic adaptation to captivity can occur in a single generation. Proc Natl Acad Sci USA 109:238–242PubMedCrossRefGoogle Scholar
  12. Christopher MM, Berry KH, Henen BT, Nagy KA (2003) Clinical disease and laboratory abnormalities in free-ranging desert tortoises (Gopherus agassizii) in California (1990–1995). J Wildlife Dis 39:35–56Google Scholar
  13. Clostio RW, Martinez AM, LeBlanc KE, Anthony NM (2012) Population genetic structure of a threatened tortoise across the south-eastern United States: implications for conservation management. Anim Conserv. doi: 10.1111/j.1469-1795.2012.00557.x Google Scholar
  14. Cunningham AA (1996) Disease risks of wildlife translocations. Conserv Biol 10:349–353CrossRefGoogle Scholar
  15. Curl DA, Scoones IC, Guy MK (1985) The Madagascar tortoise Geochelone yniphora: current status and distribution. Biol Conserv 34:35–54CrossRefGoogle Scholar
  16. Davy CM, Edwards T, Lathrop A, Bratton M, Hagan M, Henen B, Nagy KA, Stone J, Hillard LS, Murphy RW (2011) Polyandry and multiple paternities in the threatened desert tortoise, Gopherus agassizii. Conserv Genet 12:1313–1322CrossRefGoogle Scholar
  17. Dodd CK Jr, Seigel RA (1991) Relocation, repatriation, and translocation of amphibians and reptiles: are they conservation strategies that work? Herpetologica 47:336–350Google Scholar
  18. Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475PubMedCrossRefGoogle Scholar
  19. Edmands S, Timmerman CC (2003) Modeling factors affecting the severity of outbreeding depression. Conserv Biol 17:883–892CrossRefGoogle Scholar
  20. Edwards T (2003) Desert tortoise conservation genetics. Unpublished M.S. Thesis, University of Arizona, TucsonGoogle Scholar
  21. Edwards T, Goldberg CS, Kaplan ME, Schwalbe CR, Swann DE (2003) PCR primers for microsatellite loci in the desert tortoise (Gopherus agassizii, Testudinidae). Mol Ecol Notes 3:589–591CrossRefGoogle Scholar
  22. Edwards T, Schwalbe CR, Swann DE, Goldberg CS (2004) Implications of anthropogenic landscape change on inter-population movements of the desert tortoise (Gopherus agassizii). Conserv Genet 5:485–499CrossRefGoogle Scholar
  23. Edwards T, Jarchow CJ, Bonine KE, Jones CA (2010) Tracing genetic lineages of captive desert tortoises in Arizona. J Wildlife Manage 7:801–807Google Scholar
  24. Edwards T, Lathrop A, Choffe K, Ngo A, Murphy RW (2011) STR/microsatellite primers for the desert tortoise, Gopherus agassizii, and its congeners. Conserv Genet Resour 3:365–368CrossRefGoogle 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. FitzSimmons NN, Moritz C, Moore SS (1995) Conservation and dynamics of microsatellite loci over 300 million years of marine turtle evolution. Mol Biol Evol 12:432–440PubMedGoogle Scholar
  27. Frankham R (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17:325–333PubMedCrossRefGoogle Scholar
  28. Frankham R, Ballou JD, Eldridge MDB, Lacy RC, Ralls K, Dudash MR, Fenster CB (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475PubMedCrossRefGoogle Scholar
  29. Fujii A, Forstner MRJ (2010) Genetic variation and population structure of the Texas tortoise, Gopherus berlandieri (Testudinidae), with implications for conservation. Chelonian Conserv Biol 9:61–69CrossRefGoogle Scholar
  30. Glenn JL, Straight RC, Sites JW Jr (1990) A plasma protein marker for population genetic studies of the desert tortoise (Xerobates agassizii). Great Basin Nat 50:1–8Google Scholar
  31. Hagerty BE, Tracy RC (2010) Defining population structure for the Mojave desert tortoise. Conserv Genet 11:1795–1807CrossRefGoogle Scholar
  32. Hagerty BE, Nussear KE, Esque TC, Tracy CR (2011) Making molehills out of mountain landscape genetics of the Mojave desert tortoise. Landscape Ecol 2:267–280CrossRefGoogle Scholar
  33. Hauswaldt JS, Glenn TC (2003) Microsatellite DNA loci from the diamondback terrapin (Malaclemys terrapin). Mol Ecol Notes 3:174–176CrossRefGoogle Scholar
  34. Hedrick P (1995) Gene flow and genetic restoration: the Florida panther as a case study. Conserv Biol 9:996–1007CrossRefGoogle Scholar
  35. International Union for the Conservation of Nature (2002) IUCN guidelines for the placement of confiscated animals. IUCN, Abu DhabiGoogle Scholar
  36. International Union for the Conservation of Nature (2011) IUCN red list of threatened species. Version 2011.2. Accessed 16 June 2012
  37. Jacobson ER (1993) Implications of infectious diseases for captive propagation and introduction programs of threatened/endangered reptiles. J Zoo Wildlife Med 24:245–255Google Scholar
  38. Jacobson ER, Berry KH (2012) Mycoplasma testudineum in free-ranging desert tortoises, Gopherus agassizii. J Wildlife Dis 48:1063–1068CrossRefGoogle Scholar
  39. Jacobson ER, Brown MB, Schumacher IM, Collins BR, Harris RK, Klein PA (1995) Mycoplasmosis and the desert tortoise, Gopherus agassizii, in Las Vegas Valley, Nevada. Chelonian Conserv Biol 1:279–284Google Scholar
  40. Jacobson ER, Berry KH, Wellehan JFX Jr, Origgi F, Childress AL, Braun J, Schrenzel M, Yee J, Rideout B (2012) Serologic and molecular evidence for Testudinid herpesvirus 2 infection in wild Agassiz’s desert tortoises, Gopherus agassizii. J Wildlife Dis 48:747–757Google Scholar
  41. Johnson AJ, Morafka DJ, Jacobson ER (2006) Seroprevalence of Mycoplasma agassizii and tortoise herpesvirus in captive desert tortoises (Gopherus agassizii) from the Greater Barstow Area, Mojave Desert, California. J Arid Environ 67(supplement):192–201CrossRefGoogle Scholar
  42. Jones CA (2008) Mycoplasma agassizii in the Sonoran population of the desert tortoise in Arizona. Unpublished M.S. Thesis, University of Arizona, TucsonGoogle Scholar
  43. Kampher K, Love J (1998) Motivational aspects of desert tortoise caretaking. Anthrozoos 11:87–97CrossRefGoogle Scholar
  44. Kock RA, Woodford MH, Rossiter PB (2010) Disease risks associated with the translocation of wildlife. Rev Sci Tech OIE 29:329–350Google Scholar
  45. Lamb T, Avise JC, Gibbons JW (1989) Phylogeographic patterns in mitochondrial DNA of the desert tortoise (Xerobates agassizi), and evolutionary relationships among the North American gopher tortoises. Evolution 43:76–87CrossRefGoogle Scholar
  46. Martel A, Blahak S, Vissenaekens H, Pasmans F (2009) Reintroduction of clinically healthy tortoises: the herpesvirus Trojan horse. J Wildlife Dis 45:218–220Google Scholar
  47. McCoy ED, Berry KH (2008) Using an ecological ethics framework to make decisions about the relocation of wildlife. Sci Eng Ethics 14:505–521PubMedCrossRefGoogle Scholar
  48. McDougall PT, Réale D, Sol D, Reader SM (2006) Wildlife conservation and animal temperament: causes and consequences of evolutionary change for captive, reintroduced, and wild populations. Anim Conserv 9:39–48CrossRefGoogle Scholar
  49. McLuckie AM, Lamb T, Schwalbe CR, McCord RD (1999) Genetic and morphometric assessment of an unusual tortoise (Gopherus agassizii) population in the Black Mountains of Arizona. J Herpetol 33:36–44CrossRefGoogle Scholar
  50. Milinkovitch MC, Monteyne D, Gibbs JP, Fritts TH, Tapia W, Snell HL, Tiedemann R, Caccone A, Powell JR (2004) Genetic analysis of a successful repatriation programme: giant Galápagos tortoises. Proc Royal Soc Lond B Biol 271:341–345CrossRefGoogle Scholar
  51. Morafka DJ, Aguirre G, Murphy RW (1994) Allozyme differentiation among gopher tortoises (Gopherus): conservation genetics and phylogenetic and taxonomic implications. Can J Zoolog 72:1665–1671CrossRefGoogle Scholar
  52. Moritz C (1999) Conservation units and translocations: strategies for conserving evolutionary processes. Hereditas 130:217–228CrossRefGoogle Scholar
  53. Murphy RW, Berry KH, Edwards T, McLuckie AM (2007) A genetic assessment of the recovery units for the Mojave population of desert tortoises, Gopherus agassizii. Chelonian Conserv Biol 6:229–251CrossRefGoogle Scholar
  54. Murphy RW, Berry KH, Edwards T, Leviton A, Lathrop A, Riedle JD (2011) The dazed and confused identity of Agassiz’s land tortoise, Gopherus agassizii (Testudines: Testudinidae) with the description of a new species and its consequences for conservation. Zookeys 113:39–71PubMedCrossRefGoogle Scholar
  55. Perez I (2004) Non-commercial collection of spur-thighed tortoises (Testudo graeca graeca): a cultural problem in southeast Spain. Biol Conserv 118:175–181CrossRefGoogle Scholar
  56. Poulakakis N, Russello M, Geist D, Caccone A (2012) Unravelling the peculiarities of island life: vicariance, dispersal and the diversification of the extinct and extant giant Galápagos tortoises. Mol Ecol 21:160–173PubMedCrossRefGoogle Scholar
  57. Sainsbury AW, Vaughan-Higgins RJ (2012) Analyzing disease risks associated with translocations. Conserv Biol 26:442–452PubMedCrossRefGoogle Scholar
  58. Salinas M, Altet L, Clavel C, Almela RM, Bayón A, Burguete I, Sánchez A (2011) Genetic assessment, illegal trafficking and management of the Mediterranean spur-thighed tortoise in Southern Spain and Northern Africa. Conserv Genet 12:1–13CrossRefGoogle Scholar
  59. Schwartz TS, Karl SA (2005) Population and conservation genetics of the gopher tortoise (Gopherus polyphemus). Conserv Genet 6:917–928CrossRefGoogle Scholar
  60. Schwartz TS, Karl SA (2008) Population genetic assignment of confiscated gopher tortoises. J Wildlife Manage 72:254–259CrossRefGoogle Scholar
  61. Schwartz TS, Osentoski M, Lamb T, Karl SA (2003) Microsatellite loci for the North American tortoises (genus Gopherus) and their applicability to other turtle species. Mol Ecol Notes 3:283–286CrossRefGoogle Scholar
  62. Snyder NFR, Derrickson SR, Beissinger SR, Wiley JW, Smith TB, Toone WD, Miller B (1996) Limitations of captive breeding in endangered species recovery. Conserv Biol 10:338–348CrossRefGoogle Scholar
  63. Soares JF, Chalker VJ, Erles K, Holt S, Waters M, McArthur S (2004) Prevalence of Mycoplasma agassizii and chelonian herpesvirus in captive tortoises (Testudo sp.) in the United Kingdom. J Zoo Wildlife Med 35:25–33CrossRefGoogle Scholar
  64. Tallman DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496CrossRefGoogle Scholar
  65. U.S. Census Bureau (2012) State-to-state migration flows. Accessed 02 July 2012
  66. U.S. Fish and Wildlife Service (1990) Endangered and threatened wildlife and plants: determination of threatened status for the Mojave population of the desert tortoise. Fed Reg 55:12178–12191Google Scholar
  67. U.S. Fish and Wildlife Service (2010) Mojave population of the desert tortoise (Gopherus agassizii). 5-Year review: summary and evaluation. Reno, Nevada, Desert Tortoise Recovery Office, U.S. Fish and Wildlife Service, September 30, 2010Google Scholar
  68. U.S. Fish and Wildlife Service (2011) Revised recovery plan for the Mojave population of the desert tortoise (Gopherus agassizii). U.S Fish and Wildlife Service, Pacific Southwest Region, SacramentoGoogle Scholar
  69. Viggers KL, Lindenmayer DB, Spratt DM (1993) The importance of disease in reintroduction programs. Wildlife Res 20:687–698CrossRefGoogle Scholar
  70. Weeks AR, Sgro CM, Young AG, Frankham R, Mitchell NJ, Miller KA, Byrne M, Coates DJ, Eldridge MDB, Sunnucks P, Breed MF, James EA, Hoffmann AA (2011) Assessing the benefits and risks of translocations in changing environments: a genetic perspective. Evol Appl 4:709–725PubMedCrossRefGoogle Scholar
  71. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  72. Williams DA, Osentoski MF (2007) Genetic considerations for the captive breeding of tortoises and freshwater turtles. Chelonian Conserv Biol 6:302–313CrossRefGoogle Scholar
  73. Wimberger K, Armstrong AJ, Downs CT (2009) Can rehabilitated leopard tortoises, Stigmochelys pardalis, be successfully released into the wild? Chelonian Conserv Biol 8:173–184CrossRefGoogle Scholar
  74. Wimberger K, Armstrong AJ, Penning M (2011) Health checks of rehabilitated leopard tortoise, Stigmochelys pardalis, before release into the wild. S Afr J Wildlife Res 41:229–235CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.University of Arizona Genetics CoreTucsonUSA
  2. 2.U.S. Geological Survey, Western Ecological Research CenterRiversideUSA

Personalised recommendations