Advertisement

Biological Invasions

, Volume 14, Issue 11, pp 2255–2270 | Cite as

Ongoing invasions of the African clawed frog, Xenopus laevis: a global review

  • G. J. Measey
  • D. Rödder
  • S. L. Green
  • R. Kobayashi
  • F. Lillo
  • G. Lobos
  • R. Rebelo
  • J.-M. Thirion
Original Paper

Abstract

We conducted a literature review on the current status of all known extralimital populations of the African clawed frog, Xenopus laevis, to identify commonality in invasion pathways, lag between discovery and introduction, and whether old populations are in decline. Further, we investigated which locations are vulnerable to future establishment using geospatial data (1,075 native and 124 invasive records) in a Maxent model developed with data from the Worldclim database. We found introductions of X. laevis to be continuous over the last 50 years and invasions to be ongoing on four continents: Asia, Europe, North and South America. Invasion pathways were related to scientific use and the pet trade, with high rates of deliberate release followed by a lag of 2–25 years to first reports. No populations were found to be declining although some have been extirpated. Optimal uninvaded bioclimatic space was identified in central Mexico and southern Australia, while larger suitable areas were found in southern South America and southwestern Europe. Xenopus laevis is a cryptic invasive species that is likely to increase its invasive distribution, through new introductions and by the spread of ongoing invasions. Many more invasive populations are likely to exist than are currently recognised and reducing invasive potential will largely rely on education of those involved with their captive care.

Keywords

Xenopus laevis Detection lag Amphibians Invasion pathways Species distribution model Chytridiomycosis 

Notes

Acknowledgments

We would like to thank all those colleagues who were able to share and clarify information on reports of extralimital populations of X. laevis. Two anonymous reviewers and Fred Kraus provided constructive feedback which improved the quality of the manuscript. GJM would like to thank the Royal Society (UK), the European Union (HPMF-CT-2001-01407) and NERC (UK) who supplied funding for field-work in Chile, USA, France and UK. We would also like to thank all contributors to the South African Frog Atlas Project for data on X. laevis occurrence in South Africa.

Supplementary material

10530_2012_227_MOESM1_ESM.pdf (2.7 mb)
Supplementary material 1 (PDF 2770 kb)

References

  1. Alexander SS, Bellerby CW (1938) Experimental studies on the sexual cycle of the South African clawed toad (Xenopus laevis). I. J Exp Biol 15:74–81Google Scholar
  2. Arao K, Kitano T (2006) Xenopus laevis from Hamamatsu City, Shizuoka Prefecture, Japan. Bull Herpetol Soc Jpn 2006:17–19Google Scholar
  3. Avila VL, Frye PG (1978) Feeding behaviour of the African clawed frog (Xenopus laevis Daudin) (Amphibia, Anura, Pipidae); effect of prey type. J Herpetol 12:391–396CrossRefGoogle Scholar
  4. Balinsky JB (1981) Adaptation of nitrogen-metabolism to hyperosmotic environment in Amphibia. J Exp Zool 215:335–350CrossRefGoogle Scholar
  5. Balinsky JB, Cragg MM, Baldwin E (1961) Adaptation of amphibian waste nitrogen excretion to dehydration. Comp Biochem Physiol 3:236–244PubMedCrossRefGoogle Scholar
  6. Balinsky JB, Choritz EL, Coe CGL, Van der Schans GS (1967) Amino acid metabolism and urea synthesis in naturally aestivating Xenopus laevis. Comp Biochem Physiol 22:59–68PubMedCrossRefGoogle Scholar
  7. Beaumont LJ, Hughes L, Poulsen M (2005) Predicting species distributions: use of climatic parameters in BIOCLIM and its impact on predictions of species’ current and future distributions. Ecol Model 186:250–269CrossRefGoogle Scholar
  8. Beaumont LJ, Gallagher RV, Thuiller W, Downey PO, Leishman MR, Hughes L (2009) Different climatic envelopes among invasive populations may lead to underestimations of current and future biological invasions. Divers Distrib 15:409–420CrossRefGoogle Scholar
  9. Beebee TJC, Griffiths RA (2005) The amphibian decline crisis: a watershed for conservation biology? Biol Conserv 125:271–285CrossRefGoogle Scholar
  10. Bentley PJ (1973) Role of skin in amphibian sodium metabolism. Science 181:686–687PubMedCrossRefGoogle Scholar
  11. Broennimann O, Guisan A (2008) Predicting current and future biological invasions: both native and invaded ranges matter. Biol Lett 4:585–589PubMedCrossRefGoogle Scholar
  12. Busby JR (1991) BIOCLIM—a bioclimatic analysis and prediction system. In: Margules CR, Austin MP (eds) Nature conservation: cost effective biological surveys and data analysis. CSIRO, Melbourne, pp 64–68Google Scholar
  13. Carreno CA, Nishikawa KC (2010) Aquatic feeding in pipid frogs: the use of suction for prey capture. J Exp Biol 213:2001–2008PubMedCrossRefGoogle Scholar
  14. Cheng TL, Rovito SM, Wake DB, Vredenburg VT (2011) Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Science, USAGoogle Scholar
  15. Christy MT, Savidge JA, Rodda GH (2007) Multiple pathways for invasion of anurans on a Pacific island. Divers Distrib 13:598–607CrossRefGoogle Scholar
  16. Crayon JJ (2005) Species account: Xenopus laevis. In: Lannoo MJ (ed) Amphibidan declines: the conservation status of United States species. University of California Press, Berkeley, pp 522–525Google Scholar
  17. Cunningham AA, Garner TWJ, Aguilar-Sanchez V, Banks B, Foster J, Sainsbury AW, Perkins M, Walker SF, Hyatt AD, Fisher MC (2005) Emergence of amphibian chytridiomycosis in Britain. Vet Rec 157:386–387PubMedGoogle Scholar
  18. Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Divers Distrib 9:141–150CrossRefGoogle Scholar
  19. Du Preez LH, Kunene N, Hanner R, Giesy JP, Solomon KR, Hosmer A, Van der Kraak GJ (2009) Population-specific incidence of testicular ovarian follicles in Xenopus laevis from South Africa: a potential issue in endocrine testing. Aquat Toxicol 95:10–16PubMedCrossRefGoogle Scholar
  20. Duffey E (1964) The terrestrial ecology of Ascension Island. J Appl Ecol 1:219–251CrossRefGoogle Scholar
  21. Duffus ALJ, Cunningham AA (2010) Major disease threats to European amphibians. Herpetol J 20:117–127Google Scholar
  22. Eggert C, Fouquet A (2006) A preliminary biotelemetric study of a feral invasive Xenopus laevis population in France. Alytes 23:144–149Google Scholar
  23. Elepfandt A, Eistetter I, Fleig A, Gunther E, Hainich M, Hepperle S, Traub B (2000) Hearing threshold and frequency discrimination in the purely aquatic frog Xenopus laevis (Pipidae): measurement by means of conditioning. J Exp Biol 203:3621–3629PubMedGoogle Scholar
  24. Elith J, Kearney M, Phillips S (2010) The art of modelling range-shifting species. Methods Ecol Evol 1:330–342CrossRefGoogle Scholar
  25. Evans BJ, Morales JC, Picker MD, Melnick DJ, Kelley DB (1998) Absence of extensive introgression between Xenopus gilli and Xenopus laevis laevis (Anura : Pipidae) in southwestern Cape Province, South Africa. Copeia 1998:504–509CrossRefGoogle Scholar
  26. Evans BJ, Kelley DB, Tinsley RC, Melnick DJ, Cannatella DC (2004) A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution. Mol Phylogenet Evol 33:197–213PubMedCrossRefGoogle Scholar
  27. Evans BJ, Greenbaum E, Kusamba C, Carter TF, Tobias ML, Mendel SA, Kelley DB (2011) Description of a new octoploid frog species (Anura: Pipidae: Xenopus) from the Democratic Republic of the Congo, with a discussion of the biogeography of African clawed frogs in the Albertine Rift. J Zool 283:276–290CrossRefGoogle Scholar
  28. Faraone FP, Lillo F, Giacalone G, Lo Valvo M (2008) The large invasive population of Xenopus laevis in Sicily (Italy). Amphib-Reptil 29:405–412CrossRefGoogle Scholar
  29. Fitzpatrick MC, Hargrove WW (2009) The projection of species distribution models and the problem of non-analogous climate. Biodivers Conserv 18:2255–2261CrossRefGoogle Scholar
  30. Flower SS (1936) Further notes on the duration of life in animals—II amphibians. Proc Zool Soc Lond 1936:369–394Google Scholar
  31. Fouquet A (2001) Des clandestins aquatiques. Zamenis 6:10–11Google Scholar
  32. Fouquet A, Measey GJ (2006) Plotting the course of an African clawed frog invasion in Western France. Anim Biol 56:95–102CrossRefGoogle Scholar
  33. Frost DR (2011) Amphibian species of the world: an online reference. Version 5.5 (31 January, 2011). Electronic Database accessible at http://research.amnh.org/vz/herpetology/amphibia/ Accessed on 25 June 2011
  34. Garner TWJ, Perkins MW, Govindarajulu P, Seglie D, Walker S, Cunningham AA, Fisher MC (2006) The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biol Lett 2:455–459PubMedCrossRefGoogle Scholar
  35. Garner TWJ, Stephen I, Wombwell E, Fisher MC (2009) The amphibian trade: bans or best practice? EcoHealth 6:148–151PubMedCrossRefGoogle Scholar
  36. Glade AA (1988) Libro Rojo de los Vertebrados Terrestres de Chile. Corporación Nacional Forestal, SantiagoGoogle Scholar
  37. Green SL (2010) Husbandry. In: Green SL (ed) The laboratory Xenopus sp., CRC Press, Taylor and Francis Group, Boca Raton, p 16–61Google Scholar
  38. Green SL, Felt S and Wilson S (2010) South African clawed frogs (Xenopus laevis) in Golden Gate Park, San Francisco. In: Proceedings 17th international conference on aquatic invasive species, San Diego, CA, USAGoogle Scholar
  39. Guo QF, Ricklefs RE (2011) Domestic exotics and the perception of invasibility. Divers Distrib 16:1034–1039CrossRefGoogle Scholar
  40. Gurdon J (1996) Introductory comments: Xenopus as a laboratory animal. In: Tinsley RC, Kobel HR (eds) The biology of Xenopus. Oxford University Press, Oxford, pp 3–6Google Scholar
  41. Gurdon JB, Hopwood N (2000) The introduction of Xenopus laevis into developmental biology: of empire, pregnancy testing and ribosomal genes. Int J Dev Biol 44:43–50PubMedGoogle Scholar
  42. Heikkinen RK, Luoto M, Araújo MB, Virkkala R, Thuiller W, Sykes MT (2006) Methods and uncertainties in bioclimatic envelope modeling under climate change. Prog Phys Geogr 30:751–777CrossRefGoogle Scholar
  43. Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J, Kapitonov V, Ovcharenko I, Putnam NH, Shu SQ, Taher L, Blitz IL, Blumberg B, Dichmann DS, Dubchak I, Amaya E, Detter JC, Fletcher R, Gerhard DS, Goodstein D, Graves T, Grigoriev IV, Grimwood J, Kawashima T, Lindquist E, Lucas SM, Mead PE, Mitros T, Ogino H, Ohta Y, Poliakov AV, Pollet N, Robert J, Salamov A, Sater AK, Schmutz J, Terry A, Vize PD, Warren WC, Wells D, Wills A, Wilson RK, Zimmerman LB, Zorn AM, Grainger R, Grammer T, Khokha MK, Richardson PM, Rokhsar DS (2010) The genome of the Western clawed frog Xenopus tropicalis. Science 328:633–636PubMedCrossRefGoogle Scholar
  44. Hewitt J, Power JH (1913) A list of South African Lacertilia, Ophidia and Batrachia in the McGregor Museum, Kimberly; with field-notes on various species. Transact Royal Soc S Afr 3:147–176CrossRefGoogle Scholar
  45. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  46. Hillman SS, Withers PC, Drewes RC, Hillyard SD (2009) Ecological and environmental physiology of amphibians. Oxford University Press Inc., New York 469 pGoogle Scholar
  47. Iskandar DT (1998) The amphibians of Java and Bali. Research and Development Centre for Biology—LIPI, Bogor, Indonesia, p 117Google Scholar
  48. Jaksic FM (1998) Vertebrate invaders and their ecological impacts in Chile. Biodivers Conserv 7:1427–1445CrossRefGoogle Scholar
  49. Jokumsen A, Weber RE (1980) Hemoglobin-oxygen binding-properties in the blood of Xenopus laevis, with special reference to the influences of estivation and of temperature and salinity acclimation. J Exp Biol 86:19–37Google Scholar
  50. Kats LB, Ferrer RP (2003) Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Divers Distrib 9:99–110CrossRefGoogle Scholar
  51. King W, Krakauer T (1996) The exotic herpetofauna of Southeast Florida. Q J Fla Acad Sci 29:144–154Google Scholar
  52. Kobayashi R, Hasegawa M (2005) Can the African clawed frog Xenopus laevis become established in Japan?-An inference from recent distribution records in the Kanto plain. Bull Herpetol Soc Jpn 2005:169–173Google Scholar
  53. Kobel HR, Loumont C, Tinsley RC (1996) The extant species. In: Tinsley RC, Kobel HR (eds) The biology of Xenopus. Oxford University Press, Oxford, pp 9–34Google Scholar
  54. Kokuryo Y (2009) A survey of feral populations of African clawed toad in Shizuoka Prefecture. Bull Herpetol Soc Jpn 2009:103–106Google Scholar
  55. Kraus F (2009) Alien reptiles and amphibians: a scientific compendium and analysis—Springer Series in Invasion Ecology 4. Springer Science & Business Media B.V., NetherlandsGoogle Scholar
  56. Krysko KL, Burgess JP, Rochford MR, Gillette CR, Cueva D, Enge KM, Somma LA, Stabile JL, Smith DC, Wasilewski JA, Kieckhefer GN, Granatosky MC, Nielsen SV (2011) Verified non-indigenous amphibians and reptiles in Florida from 1863 through 2010: outlining the invasion process and identifying invasion pathways and stages. Zootaxa 3028:1–64Google Scholar
  57. Lafferty KD, Page CJ (1997) Predation on the endangered tidewater goby, Eucyclogobius newberryi, by the introduced African clawed frog, Xenopus laevis, with notes on the frog’s parasites. Copeia 1997:589–592CrossRefGoogle Scholar
  58. Lever C (2003) Naturalized reptiles and amphibians of the world. Oxford University Press, New YorkGoogle Scholar
  59. Lillo F, Marrone F, Sicilia A, Castelli G (2005) An invasive population of Xenopus laevis (Daudin, 1802) in Italy. Herpetozoa 18:63–64Google Scholar
  60. Lillo F, Faraone FP, Lo Valvo M (2011) Can the introduction of Xenopus laevis affect native amphibian populations? Reduction of reproductive occurrence in presence of the invasive species. Biol Invasions 13:1533–1541CrossRefGoogle Scholar
  61. Liu C, Pam M, Dawson TP, Pearson RG (2005) Selecting thresholds of occurrence in the prediction of species distributions. Ecography 28:385–393CrossRefGoogle Scholar
  62. Lobos G, Garín C (2002) Xenopus laevis (African clawed frog). Behav Herpetol Rev 33:132Google Scholar
  63. Lobos G, Jaksic FM (2005) The ongoing invasion of African clawed frogs (Xenopus laevis) in Chile: causes of concern. Biodivers Conserv 14:429–439CrossRefGoogle Scholar
  64. Lobos G, Measey GJ (2002) Invasive populations of Xenopus laevis (Daudin) in Chile. Herpetol J 12:163–168Google Scholar
  65. Lobos G, Cattan P, Lopez M (1999) Antecedentes de la ecología trófica del sapo africano Xenopus laevis en la zona central de Chile. Boletín del Museo Nacional de Historia Natural 48:7–18Google Scholar
  66. Loveridge A (1953) Zoological results of a fifth expedition to East Africa. IV. Amphibians from Nyasalandand Tete. Bull Mus Comp Zool 110:325–406Google Scholar
  67. Loveridge A (1959) Notes on the present herpetofauna of Ascension Island. Copeia 1959:69–70CrossRefGoogle Scholar
  68. Luja VH, Rodrıguez-Estrella R (2010) The invasive bullfrog Lithobates catesbeianus in oases of Baja California Sur, Mexico: potential effects in a fragile ecosystem. Biol Invasions 12:2979–2983CrossRefGoogle Scholar
  69. Mahrdt C, Knefler FT (1972) Pet or pest? The African clawed frog. Environ Southwest 446:2–5Google Scholar
  70. Matz E, Bouley DM and Green SL (2005) A field survey of wild Xenopus laevis at Golden Gate Park, San Francisco. In: Proceedings 55th wildlife disease association annual international meeting, Cairns, AustraliaGoogle Scholar
  71. McCoid MJ, Fritts TH (1980) Notes on the diet of a feral population of Xenopus laevis (Pipidae) in California. Southwestern Nat 25:272–275CrossRefGoogle Scholar
  72. McCoid MJ, Fritts TH (1995) Female reproductive potential and winter growth of African clawed frogs (Pipidae: Xenopus laevis) in California. Calif Fish Game 81:39–42Google Scholar
  73. Measey GJ (1997) The ecology of feral Xenopus laevis, Dissertation. University of Bristol, BristolGoogle Scholar
  74. Measey GJ (1998a) Diet of feral Xenopus laevis (Daudin) in South Wales, UK. J Zool 246:287–298CrossRefGoogle Scholar
  75. Measey GJ (1998b) Terrestrial prey capture in Xenopus laevis. Copeia 1998:787–791CrossRefGoogle Scholar
  76. Measey GJ (2001) Growth and ageing of feral Xenopus laevis (Daudin) in South Wales, UK. J Zool 254:547–555CrossRefGoogle Scholar
  77. Measey GJ (2004a) Species account: Xenopus laevis (Daudin 1802). In: Minter LR, Burger M, Harrison JA, Braack H, Bishop PJ, Kloepfer D (eds) Atlas and red data book of the frogs of South Africa, Lesotho and Swaziland. Smithsonian Institution Press, Washington DCGoogle Scholar
  78. Measey GJ (2004b) Xenopus laevis: una perspectiva sobre invasiones globales. In: Solis R, Lobos G, Irirarte A (eds) Antecedentes sobre la biologia de Xenopus laevis y su introduccion en Chile. Maval Ltda, Santiago, pp 3–8Google Scholar
  79. Measey GJ, Channing A (2003) Phylogeography of the genus Xenopus in southern Africa. Amphibia-Reptil 24:321–330CrossRefGoogle Scholar
  80. Measey GJ, Davies SJ (2011) Struggling against domestic exotics at the southern end of Africa. FrogLog 97:28–30Google Scholar
  81. Measey GJ, Tinsley RC (1998) Feral Xenopus laevis in South Wales. Herpetol J 8:23–27Google Scholar
  82. Meyerson LA, Reaser JK (2002) Biosecurity: moving toward a comprehensive approach. Bioscience 52:593–600CrossRefGoogle Scholar
  83. Miller K (1982) Effect of temperature on sprint performance in the frog Xenopus laevis and the salamander Necturus maculosus. Copeia 1982:695–698CrossRefGoogle Scholar
  84. Mitsuoka K, Toda M, Takahashi H, Tanimura N, Ogano D, Kobayashi R (2011) Current status of introduced African clawed frogs in the downstream reaches of the Tone River. Bull Herpetol Soc Jpn 2011:50–51Google Scholar
  85. Pascual G, Llorente GA, Richter-Boix AMA (2007) Primera localización de Xenopus laevis en libertad en España. Boletín de la Asociación Herpetológica Española 18:42–43Google Scholar
  86. Peeler EJ, Oidtmann BC, Midtlyng PJ, Miossec L, Gozlan RE (2011) Non-native aquatic animals introductions have driven disease emergence in Europe. Biol Invasions 13:1291–1303CrossRefGoogle Scholar
  87. Phillips SJ, Dudík M (2008) Modeling of species distributions with Maxent: new extensions and comprehensive evaluation. Ecography 31:161–175CrossRefGoogle Scholar
  88. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259CrossRefGoogle Scholar
  89. Picker MD (1985) Hybridization and habitat selection in Xenopus gilli and Xenopus laevis in the southwestern cape province. Copeia 1985:574–580CrossRefGoogle Scholar
  90. Picker MD, De Villiers AL (1989) The distribution and conservation status of Xenopus gilli (Anura, Pipidae). Biol Conserv 49:169–183CrossRefGoogle Scholar
  91. Reaser JK, Meyerson LA, Von Holle B (2008) Saving camels from straws: how propagule pressure-based prevention policies can reduce the risk of biological invasion. Biol Invasions 10:1085–1098CrossRefGoogle Scholar
  92. Rebelo R, Amaral P, Bernardes M, Oliveira J, Pinheiro P, Leitao D (2010) Xenopus laevis (Daudin, 1802), a new exotic amphibian in Portugal. Biol Invasions 12:3383–3387CrossRefGoogle Scholar
  93. Robert J, Abramowitz L, Gantress J, Morales HD (2007) Xenopus laevis: a possible vector of Ranavirus infection? J Wildl Dis 43:645–652PubMedGoogle Scholar
  94. Rowlands BW (2001) St Helena and the dependencies of Ascension Island and Tristan da Cunha, including Gough Island. In: Fishpool LDC and Evans MI (eds) Important bird areas in Africa and associated islands: Priority sites for conservation, Pisces Publications and BirdLife International, Newbury and Cambridge, UKGoogle Scholar
  95. Schmeller DS, Loyau A, Dejean T, Miaud C (2011) Using amphibians in laboratory studies: precautions against the emerging infectious disease chytridiomycosis. Lab Anim 45:25–30PubMedCrossRefGoogle Scholar
  96. Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR, Phillott AD, Hines HB, Kenyon N (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125–134CrossRefGoogle Scholar
  97. Solis R, Lobos G, Walker SF, Fisher M, Bosch J (2011) Presence of Batrachochytrium dendrobatidis in feral populations of Xenopus laevis in Chile. Biol Invasions 12:1641–1646CrossRefGoogle Scholar
  98. Soto-Azat C, Clarke BT, Poynton JC, Cunningham AA (2010) Widespread historical presence of Batrachochytrium dendrobatidis in African pipid frogs. Divers Distrib 16:126–131CrossRefGoogle Scholar
  99. St. Amant JA, Hoover FG (1969) Addition of Misgurnus anguillicaudatus (Cantor) to the California fauna. Calif Fish Game 55:330–331Google Scholar
  100. St. Amant JA, Hoover FG, Stewart G (1973) African clawed frog, Xenopus laevis (Daudin), established in California. Calif Fish Game 59:151–153Google Scholar
  101. Stebbins RC (1985) A field guide to western reptiles and amphibians, 2nd edn. Houghton Mifflin Company, Boston, MAGoogle Scholar
  102. Swets K (1988) Measuring the accuracy of diagnostic systems. Science 240:1285–1293PubMedCrossRefGoogle Scholar
  103. Tinsley RC, McCoid MJ (1996) Feral populations of Xenopus outside Africa. In: Tinsley RC, Kobel HR (eds) The biology of Xenopus. Oxford University Press, Oxford, pp 81–94Google Scholar
  104. Tinsley RC, Loumont C, Kobel HR (1996) Geographical distribution and ecology. In: Tinsley RC, Kobel HR (eds) The biology of Xenopus. Oxford University Press, Oxford, pp 33–39Google Scholar
  105. Tinsley RC, Minter LR, Measey GJ, Howell K, Veloso A, Núñez H and Romano A (2008) Xenopus laevis. In: IUCN 2011. IUCN red list of threatened species. Version 2011.1. www.iucnredlist.org. Accessed 11 Oct 2011
  106. Tobias ML, Viswanathan SS, Kelley DB (1998) Rapping, a female receptive call, initiates male-female duets in the South African clawed frog. Proc Nat Acad Sci USA 95:1870–1875PubMedCrossRefGoogle Scholar
  107. United States Geological Survey (2011) Nonindigenous Aquatic Species Database, Gainesville, FL. http://nas.er.usgs.gov, date of query. Accessed 15 June 2011
  108. Van Wilgen NJ, Roura-Pascual N, Richardson DM (2009) A quantitative climate-match score for risk-assessment screening of reptile and amphibian introductions. Environ Manage 44:590–607PubMedCrossRefGoogle Scholar
  109. Van Wilgen NJ, Wilson JRU, Elith J, Wintle BA, Richardson DM (2010) Alien invaders and reptile traders: what drives the live animal trade in South Africa? Anim Conserv 13:24–32CrossRefGoogle Scholar
  110. VanDerWal J, Shoo LP, Graham CH, Williams SE (2009) Selecting pseudo-absence data for presence-only distribution modeling: how far should you stray from what you know? Ecol Model 220:589–594CrossRefGoogle Scholar
  111. Veloso A, Navarro J (1988) Systematic list and geographic distribution of amphibians and reptiles from Chile. Museo Regionale di Scienze Naturali Bollettino (Turin) 6:481–540Google Scholar
  112. Vogel G (2008) Proposed frog ban makes a splash. Science 319:1472PubMedCrossRefGoogle Scholar
  113. Walsh PT, Downie JR, Monaghan P (2008) Plasticity of the duration of metamorphosis in the African clawed toad. J Zool 274:143–149CrossRefGoogle Scholar
  114. Weldon C, Du Preez LH, Hyatt AD, Muller R, Speare R (2004) Origin of the amphibian chytrid fungus. Emerg Infect Dis 10:2100–2105PubMedCrossRefGoogle Scholar
  115. Weldon C, De Villiers AL, Du Preez LH (2007) Quantification of the trade in Xenopus laevis from South Africa, with implications for biodiversity conservation. Afr J Herpetol 56:77–83CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • G. J. Measey
    • 1
  • D. Rödder
    • 2
  • S. L. Green
    • 3
  • R. Kobayashi
    • 4
  • F. Lillo
    • 5
  • G. Lobos
    • 6
  • R. Rebelo
    • 7
  • J.-M. Thirion
    • 8
  1. 1.School of Environmental Sciences and DevelopmentNorth-West UniversityPotchefstroomSouth Africa
  2. 2.Section of HerpetologyZoologisches Forschungsmuseum Alexander Koenig (ZFMK)BonnGermany
  3. 3.Department of Comparative Medicine, School of MedicineStanford UniversityStanfordUSA
  4. 4.Center for Toki and Ecological Restoration (CTER)Niigata UniversitySado-CityJapan
  5. 5.Dipartimento di Biologia Ambientale e BiodiveristàUniversita’ di PalermoPalermoItaly
  6. 6.Centro de Vida Silvestre, Facultad de Ciencias Veterinarias y PecuariasUniversidad de ChileSantiagoChile
  7. 7.Departamento de Biologia Animal, Centro de Biologia AmbientalFaculdade de Ciencias da Universidade de LisboaLisbonPortugal
  8. 8.Association Objectifs BIOdiversitéS (OBIOS)Pont-l’abbé-d’ArnoultFrance

Personalised recommendations