Repeated reduction in parasite diversity in invasive populations of Xenopus laevis: a global experiment in enemy release

Abstract

The introduction of species to multiple continents creates natural experiments suited to the evaluation of ecological hypotheses. For the Enemy Release Hypothesis (ERH), which postulates that the success of invasive populations hinges upon release from the effects of their natural enemies, assessments of parasite loss during invasion across independent geographical replicates are scarce. This study is the first to test the ERH for a globally invasive amphibian, Xenopus laevis, a successful invader on four continents with a well-described parasite fauna. In this study, the metazoan parasite communities of X. laevis from 20 invasive and 27 native sites in five countries and three continents were compared. An overall pattern of reduced parasite diversity in invasive X. laevis was not yet countered by acquisition of novel parasites. Invasive X. laevis harboured impoverished parasite communities that were distinct from those of native X. laevis from undisturbed habitats. Conversely, parasite communities from native X. laevis from disturbed habitats were similar to those from the invasive range. Accompanying parasites were common in the native range and included both generalists with indirect and specialists with direct life cycles. Our findings emphasise that parasite loss is characteristic of the invasion process of X. laevis and possibly contributes to its success as a global invader. The ERH is supported in terms of metazoan parasites as natural enemies, irrespective of the geographical origin, climatic conditions and invasion history of the host populations. This study also draws attention to parasites that co-invade with their hosts as invaders in their own right.

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References

  1. Amundsen PA, Lafferty KD, Knudsen R, Primicerio R, Kristoffersen R, Klemetsen A, Kuris AM (2013) New parasites and predators follow the introduction of two fish species to a subarctic lake: implications for food-web structure and functioning. Oecologia 171:993–1002. https://doi.org/10.1007/s00442-012-2461-2

    Article  PubMed  Google Scholar 

  2. Avery RA (1971) A preliminary list of parasites collected from reptiles and amphibians in northern Nigeria British. J Herpetol 4:217–219

    Google Scholar 

  3. Bar-On YM, Phillips R, Milo R (2018) The biomass distribution on Earth. In: Proceedings of the National Academy of Sciences of the United States of America. https://doi.org/10.1073/pnas.1711842115

  4. Beverley-Burton M (1963) Some digenetic trematodes from amphibians and reptiles in Southern Rhodesia including two new species and a new genus: Sarumitrema hystatorchis n.gen., n.sp. (Plagiorchiidae) and Halipegus rhodiensis n.sp. (Halipegidae). Proc Helminthol Soc Wash 30:49–59

    Google Scholar 

  5. Blackburn TM, Ewen JG (2017) Parasites as drivers and passengers of human-mediated biological invasions. EcoHealth 14:61–73. https://doi.org/10.1007/s10393-015-1092-6

    Article  PubMed  Google Scholar 

  6. Bush AO, Lafferty KD, Lotz JM, Shostak AW et al (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583. https://doi.org/10.2307/3284227

    CAS  Article  Google Scholar 

  7. Castillo C, Lobos G, González-Acuña D, Moreno L, González CE, Landaeta-Aqueveque C (2017) First parasitological study of the African clawed frog (Xenopus laevis, Amphibia) in Chile. Revista Brasileira de Parasitologia Veterinária 26:243–247. https://doi.org/10.1590/s1984-29612017029

    Article  PubMed  Google Scholar 

  8. Ceballos G, Ehrlich PR, Dirzo R (2017) Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. Proc Natl Acad Sci USA 114:E6089–E6096. https://doi.org/10.1073/pnas.1704949114

    CAS  Article  PubMed  Google Scholar 

  9. Clarke KR, Somerfield PJ, Chapman MG (2006) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages. J Exp Mar Biol Ecol 330:55–80. https://doi.org/10.1016/j.jembe.2005.12.017

    Article  Google Scholar 

  10. Cohn L (1906) Zur Anatomie zweier Cestoden. Zentralbl Bakteriol Parasit 40:362–367

    Google Scholar 

  11. Cosgrove GE, Jared DW Diseases and parasites of Xenopus, the Clawed Toad. In: Amborski RL, Hood MA, Miller RR (eds) Gulf coast regional symposium on diseases of aquatic animals, Louisiana State University, Baton Rouge, 1974. Centre for Wetland Resources, pp 225–242

  12. Courant J, Secondi J, Bereiziat V, Herrel A (2017) Resources allocated to reproduction decrease at the range edge of an expanding population of an invasive amphibian. Biol J Lin Soc 122:157–165. https://doi.org/10.1093/biolinnean/blx048

    Article  Google Scholar 

  13. Crayon JJ (2005) Species account: Xenopus laevis. In: Lannoo MJ (ed) Amphibian declines: the conservation status of United States species. University of California Press, Berkeley, pp 522–525

    Google Scholar 

  14. Crous HP, du Preez LH (1997) Morphology of Gyrdicotylus gallieni Vercammen-Grandjean, 1960 (Monogenea: Gyrodactylidae) from Xenopus laevis (Daudin, 1803). In: Proceedings of the Microscopy Society of Southern Africa 27, p 117

  15. de Busschere C, Courant J, Herrel A, Rebelo R, Rödder D, Measey GJ, Backeljau T (2016) Unequal contribution of native South African phylogeographic lineages to the invasion of the African clawed frog, Xenopus laevis, in Europe. PeerJ 4:e1659. https://doi.org/10.7717/peerj.1659

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. de Villiers FA, Measey GJ (2017) Overland movement in African clawed frogs (Xenopus laevis): empirical dispersal data from within their native range. PeerJ 5:e4039. https://doi.org/10.7717/peerj.4039

    Article  PubMed  PubMed Central  Google Scholar 

  17. Dick RI (1959) Preliminary notes on the relationships existing between the leech, Marsupiobdella africana, the river-crab, Potamon perlatus, and the platanna, Xenopus laevis, as observed in specimens taken from the Kromboom River in the Cape Province of the Union of South Africa. J Sci Soc Cape Town 2:47–49

    Google Scholar 

  18. Dollfus RP (1968) Presence insolité chez un urodele et en Afrique du nord d’un Cephalochlamys (Cestoda: Pseudophyllidea). Bull du Muséum National d’Histoire Naturelle 39:1192–1201

    Google Scholar 

  19. du Preez LH, Crous HP, Kok DJ (1996) Morphology of an unknown cyclophyllidean cysticercoid found in the Clawed Frog, Xenopus laevis. Proc Microsc Soc South Afr 26:111

    Google Scholar 

  20. Dunn AM et al (2012) Indirect effects of parasites in invasions. Funct Ecol 26:1262–1274. https://doi.org/10.1111/j.1365-2435.2012.02041.x

    Article  Google Scholar 

  21. Elkan E, Murray RW (1952) A larval trematode infection of the lateral line system of the Toad Xenopus laevis (Daudin). Proc Zool Soc Lond 122:121–126. https://doi.org/10.1111/j.1469-7998.1952.tb06314.x

    Article  Google Scholar 

  22. Elton C (1958) The ecology of invasions by animals and plants. Methuen, London

    Google Scholar 

  23. Engemann K et al (2015) Limited sampling hampers “big data” estimation of species richness in a tropical biodiversity hotspot. Ecol Evol 5:807–820. https://doi.org/10.1002/ece3.1405

    Article  PubMed  PubMed Central  Google Scholar 

  24. Ferguson RR, Appleton CC (1988a) Some aspects of the morphology, population structure and larval biology of Cephalochlamys namaquensis (Cestoda: Diphyllidea), a parasite of the Clawed Toad, Xenopus laevis. South Afr J Zool 23:117–123. https://doi.org/10.1080/02541858.1988.11448087

    Article  Google Scholar 

  25. Ferguson RR, Appleton CC (1988b) The tapeworm Cephalochlamys namaquensis (Pseudophyllidea) in a population of Clawed Toad, Xenopus laevis, in Natal. S Afr J Sci 84:140

    Google Scholar 

  26. Fischthal JH, Thomas JD (1968) Digenetic trematodes of amphibians and reptiles from Ghana. Proc Helminthol Soc Wash 35:1–15

    Google Scholar 

  27. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299

    CAS  Google Scholar 

  28. Fouquet A, Measey GJ (2006) Plotting the course of an African clawed frog invasion in Western France. Anim Biol 56:95–102. https://doi.org/10.1163/157075606775904722

    Article  Google Scholar 

  29. Furman BL, Bewick AJ, Harrison TL, Greenbaum E, Gvozdik V, Kusamba C, Evans BJ (2015) Pan-African phylogeography of a model organism, the African clawed frog ‘Xenopus laevis’. Mol Ecol 24:909–925. https://doi.org/10.1111/mec.13076

    CAS  Article  PubMed  Google Scholar 

  30. Galazzo DE, Dayanandan S, Marcogliese DJ, McLaughlin JD (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA sequence data and comparisons with European congeners. Can J Zool 80:2207–2217. https://doi.org/10.1139/Z02-198

    CAS  Article  Google Scholar 

  31. Gurdon JB, Hopwood N (2000) The introduction of Xenopus laevis into developmental biology: of empire, pregnancy testing and ribosomal genes. Int J Dev Biol 44:43–50

    CAS  PubMed  Google Scholar 

  32. Harris PD, Tinsley RC (1987) The biology of Gyrdicotylus gallieni (Gyrodactylidea), an unusual vivparous monogenean from the African Clawed Toad, Xenopus laevis. Proc Zool Soc Lond 212:325–346. https://doi.org/10.1111/j.1469-7998.1987.tb05993.x

    Article  Google Scholar 

  33. Heger T, Jeschke JM (2014) The enemy release hypothesis as a hierarchy of hypotheses. Oikos 123:741–750. https://doi.org/10.1111/j.1600-0706.2013.01263.x

    Article  Google Scholar 

  34. Héritier L, Badets M, du Preez LH, Aisien MS, Lixian F, Combes C, Verneau O (2015) Evolutionary processes involved in the diversification of chelonian and mammal polystomatid parasites (Platyhelminthes, Monogenea, Polystomatidae) revealed by palaeoecology of their hosts. Mol Phylogen Evol 92:1–10. https://doi.org/10.1016/j.ympev.2015.05.026

    Article  Google Scholar 

  35. Hope RM (2013) Rmisc: Ryan Miscellaneous. R Package version 1.5. https://CRAN.R-project.org/package=Rmisc

  36. Ihlow F et al (2016) Impacts of climate change on the global invasion potential of the African clawed frog Xenopus laevis. PLoS ONE 11:e0154869. https://doi.org/10.1371/journal.pone.0154869

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Jackson JA, Tinsley RC (1988) Environmental influences on egg production by the monogenean Protopolystoma xenopodis. Parasitology 97:115–128. https://doi.org/10.1017/S0031182000066798

    Article  Google Scholar 

  38. Jackson JA, Tinsley RC (1995a) Evolutionary relationships, host range and geographical distribution of Camallanus Railliet & Henry, 1915 species (Nematoda: Camallaninae) from clawed toads of the genus Xenopus (Anura: Pipidae). Syst Parasitol 32:1–21. https://doi.org/10.1007/BF00009463

    Article  Google Scholar 

  39. Jackson JA, Tinsley RC (1995b) Representatives of Batrachocamallanus n. g. (Nematoda: Procamallaninae) from Xenopus spp. (Anura: Pipidae): geographical distribution, host range and evolutionary relationships. Syst Parasitol 31:159–188. https://doi.org/10.1007/BF00009115

    Article  Google Scholar 

  40. Jackson JA, Tinsley RC (1998) Paramphistome digeneans from Xenopus species (Pipidae) in Africa: taxonomy, host-specificity and biogeography. Syst Parasitol 40:143–160. https://doi.org/10.1023/A:1005936429562

    Article  Google Scholar 

  41. Jackson JA, Tinsley RC (2001) Host-specificity and distribution of cephalochlamydid cestodes: correlation with allopolyploid evolution of pipid anuran hosts. J Zool 254:405–419. https://doi.org/10.1017/S0952836901000905

    Article  Google Scholar 

  42. Jeschke JM (2014) General hypotheses in invasion ecology. Divers Distrib 20:1229–1234. https://doi.org/10.1111/ddi.12258

    Article  Google Scholar 

  43. Jovani R, Tella JL (2006) Parasite prevalence and sample size: misconceptions and solutions. Trends Parasitol 22:214–218. https://doi.org/10.1016/j.pt.2006.02.011

    Article  PubMed  Google Scholar 

  44. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. https://doi.org/10.1016/S0169-5347(02)02499-0

    Article  Google Scholar 

  45. King PH, van As JG (1992) Scanning electron microscopy of Diplostomum (Tylodelphys) xenopodis (Southwell & Kirshner, 1937) (Trematoda: Diplostomatidae). Electron Microsc Soc South Afr 22:127–128

    Google Scholar 

  46. King PH, van As JG (1997) Description of the adult and larval stages of Tylodelphys xenopi (Trematoda: Diplostomidae) from Southern Africa. J Parasitol 83:287–295. https://doi.org/10.2307/3284458

    CAS  Article  PubMed  Google Scholar 

  47. King PH, van As JG (2000) Morphology and life history of Petasiger variospinosus (Trematoda: Echinostomatidae) in the Free State. South Afr J Parasitol 86:312–318. https://doi.org/10.1645/0022-3395(2000)086%5b0312:MALHOP%5d2.0.CO;2

    CAS  Article  Google Scholar 

  48. Kołodziej-Sobocińska M, Brzeziński M, Niemczynowicz A, Zalewski A (2018) High parasite infection level in non-native invasive species: it is just a matter of time. Ecography 41:1283–1294. https://doi.org/10.1111/ecog.03362

    Article  Google Scholar 

  49. Kruger N, du Preez L (2015) Reproductive strategies of the kangaroo leech, Marsupiobdella africana (Glossiphoniidae). Int J Parasitol Parasites Wildl 4:142–147. https://doi.org/10.1016/j.ijppaw.2015.01.005

    Article  PubMed  PubMed Central  Google Scholar 

  50. Kuperman BI, Matey VE, Fisher RN, Ervin EL, Warburton ML, Bakhireva L, Lehman CA (2004) Parasites of the African Clawed Frog, Xenopus laevis, in Southern California, U.S.A. Comp Parasitol 71:229–232. https://doi.org/10.1654/4112

    Article  Google Scholar 

  51. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280. https://doi.org/10.1007/s004420100716

    Article  Google Scholar 

  52. Lester PJ et al (2015) No evidence of enemy release in pathogen and microbial communities of common wasps (Vespula vulgaris) in their native and introduced range. PLoS ONE 10:e0121358. https://doi.org/10.1371/journal.pone.0121358

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. Littlewood DTJ, Rohdes K, Clough KA (1997) Parasite speciation within or between host species? Phylogenetic evidence from site-specific polystome monogeneans. Int J Parasitol 27:1289–1297. https://doi.org/10.1016/S0020-7519(97)00086-6

    CAS  Article  PubMed  Google Scholar 

  54. Lobos G, Cattan P, Estades C, Jaksic FM (2013) Invasive African clawed frog Xenopus laevis in southern South America: key factors and predictions. Stud Neotrop Fauna Environ 48:1–12. https://doi.org/10.1080/01650521.2012.746050

    Article  Google Scholar 

  55. Locke SA, Levy MS, Marcogliese DJ, Ackerman S, McLaughlin JD (2012) The decay of parasite community similarity in ring-billed gulls Larus delawarensis and other hosts. Ecography 35:530–538. https://doi.org/10.1111/j.1600-0587.2011.07244.x

    Article  Google Scholar 

  56. Louppe V, Courant J, Herrel A (2017) Differences in mobility at the range edge of an expanding invasive population of Xenopus laevis in the west of France. J Exp Biol 220:278–283. https://doi.org/10.1242/jeb.146589

    Article  PubMed  Google Scholar 

  57. Lui H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545. https://doi.org/10.1007/s10530-005-5845-y

    Article  Google Scholar 

  58. Luque JL, Poulin R (2007) Metazoan parasite species richness in Neotropical fishes: hotspots and the geography of biodiversity. Parasitology 134:865–878. https://doi.org/10.1017/S0031182007002272

    CAS  Article  PubMed  Google Scholar 

  59. Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL (2014) Co-invaders: the effects of alien parasites on native hosts. Int J Parasitol Parasit Wildl 3:171–177. https://doi.org/10.1016/j.ijppaw.2014.04.002

    Article  Google Scholar 

  60. Macnae W, Rock L, Makowski M (1973) Platyhelminths from the South African Clawed Toad, or Platanna (Xenopus laevis). J Helminthol 47:199–235. https://doi.org/10.1017/S0022149X00023890

    Article  Google Scholar 

  61. Manter HW, Pritchard MH (1964) Mission de zoologie médicale au Maniema (Congo, Leopoldville). Annales du Musée Royal de l’Afrique Centrale 132:75–101

    Google Scholar 

  62. Marr SR, Mautz WJ, Hara AH (2008) Parasite loss and introduced species: a comparison of the parasites of the Puerto Rican tree frog, (Eleutherodactylus coqui), in its native and introduced ranges. Biol Invasions 10:1289–1298. https://doi.org/10.1007/s10530-007-9203-0

    Article  Google Scholar 

  63. Marra G, Wood SN (2011) Practical variable selection for generalized additive models. Comput Stat Data Anal 55:2372–2387. https://doi.org/10.1016/j.csda.2011.02.004

    Article  Google Scholar 

  64. Marzal A et al (2011) Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS ONE 6:e21905. https://doi.org/10.1371/journal.pone.0021905

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  65. Measey GJ (2004) Xenopus laevis. In: Minter LR, Burger M, Harrison JA, Braack H, Bishop PJ, Knoepfer D (eds) Atlas and red date book of the frogs of South Africa, Lesotho and Swaziland. SI/MAB Series, vol 9. Smithsonian Institution Press, Washington, DC

    Google Scholar 

  66. Measey GJ (2016) Overland movement in African clawed frogs (Xenopus laevis): a systematic review. PeerJ 4:e2474. https://doi.org/10.7717/peerj.2474

    Article  PubMed  Google Scholar 

  67. Measey GJ, Channing A (2003) Phylogeography of the genus Xenopus in southern Africa. Amphib Reptil 24:321–330. https://doi.org/10.1163/156853803322440781

    Article  Google Scholar 

  68. Measey GJ, Davies SJ (2011) Struggling against domestic exotics at the southern end of Africa. Froglog 97:28–30

    Google Scholar 

  69. Measey GJ et al (2012) Ongoing invasions of the African clawed frog, Xenopus laevis: a global review. Biol Invasions 14:2255–2270. https://doi.org/10.1007/s10530-012-0227-8

    Article  Google Scholar 

  70. Measey GJ, Davies SJ, Vimercati G, Rebelo A, Schmidt W, Turner A (2017) Invasive amphibians in southern Africa: a review of invasion pathways. Bothalia 47:a2117. https://doi.org/10.4102/abc.v47i2.2117

    Article  Google Scholar 

  71. Mettrick DF (1963) Some cestodes of reptiles and amphibians from the Rhodesias. Proc Zool Soc Lond 141:239–250. https://doi.org/10.1111/j.1469-7998.1963.tb01610.x

    Article  Google Scholar 

  72. Morand S et al (2015) Global parasite and Rattus rodent invasions: the consequences for rodent-borne diseases Integrative. Zoology 10:409–423. https://doi.org/10.1111/1749-4877.12143

    Article  Google Scholar 

  73. Moravec F, Cosgrove GE (1982) Pseudocapillaroides xenopi gen. et sp. nov. from the skin of the South African Clawed Frog Xenopus laevis Daud (Nematoda: Capillariidae). Revue de Zoologie Africaine 96:129–137

    Google Scholar 

  74. Nigrelli RF, Maraventano LW (1944) Pericarditis in Xenopus laevis caused by Diplostomulum xenopi sp. nov., a larval strigeid. J Parasitol 30:184–190. https://doi.org/10.2307/3272796

    Article  Google Scholar 

  75. Oksanen J et al. (2018) vegan: Community Ecology Package. R package version 2.5-1. https://CRAN.R-project.org/package=vegan

  76. Ortega N, Price W, Campbell T, Rohr J (2015) Acquired and introduced macroparasites of the invasive Cuban treefrog, Osteopilus septentrionalis. Int J Parasitol Parasit Wildl 4:379–384. https://doi.org/10.1016/j.ijppaw.2015.10.002

    Article  Google Scholar 

  77. Prior KM, Hellmann JJ (2015) Does enemy release contribute to the success of invasive species? A review of the enemy release hypothesis. In: Keller R, Cadotte M, Sandiford G (eds) Invasive species in a globalized world. University of Chicago Press, Chicago

    Google Scholar 

  78. Prior KM, Powell THQ, Joseph AL, Hellmann JJ (2015) Insight from community ecology into the role of enemy release in causing invasion success: the importance of native enemy effects. Biol Invasions. https://doi.org/10.1007/s10530-014-0800-4

    Article  Google Scholar 

  79. Pritchard MH (1964) Notes on four helminths from the Clawed Toad, Xenopus laevis (Daudin), in South Africa. Proc Helminthol Soc Wash 31:121–128

    Google Scholar 

  80. Prudhoe S, Bray RA (1982) Platyhelminth parasites of the Amphibia. Oxford University Press, Oxford

    Google Scholar 

  81. R Core Team (2018) R: A language and environment for statistical computing R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  82. Richardson DM, Ricciardi A (2013) Misleading criticisms of invasion science: a field guide. Divers Distrib 19:1461–1467. https://doi.org/10.1111/ddi.12150

    Article  Google Scholar 

  83. Richardson DM et al (2011) Human-mediated introductions of Australian acacias—a global experiment in biogeography. Divers Distrib 17:771–787. https://doi.org/10.1111/j.1472-4642.2011.00824.x

    Article  Google Scholar 

  84. Ricklefs RE (2010) Host-pathogen coevolution, secondary sympatry and species diversification. Philos Trans R Soc Lond B 365:1139–1147. https://doi.org/10.1098/rstb.2009.0279

    Article  Google Scholar 

  85. Ricotta C, Podani J (2017) On some properties of the Bray–Curtis dissimilarity and their ecological meaning. Ecol Complex 31:201–205. https://doi.org/10.1016/j.ecocom.2017.07.003

    Article  Google Scholar 

  86. Rödder D et al (2017) Global realized niche divergence in the African clawed frog Xenopus laevis. Ecol Evol 7:4044–4058. https://doi.org/10.1002/ece3.3010

    Article  PubMed  PubMed Central  Google Scholar 

  87. Rodrigues RAE (2014) Macroparasites of invasive Xenopus laevis (Amphibia: Anura): characterization and assessment of possible exchanges with native Pelophylax perezi in Oeiras streams. University of Lisboa, Portugal

    Google Scholar 

  88. Roy HE, Lawson Handley L-J (2012) Networking: a community approach to invaders and their parasites. Funct Ecol 26:1238–1248. https://doi.org/10.1111/j.1365-2435.2012.02032.x

    Article  Google Scholar 

  89. Schultheis EH, Berardi AE, Lau JA (2015) No release for the wicked: enemy release is dynamic and not associated with invasiveness. Ecology 96:2446–2457. https://doi.org/10.1890/14-2158.1

    Article  PubMed  Google Scholar 

  90. Shapiro HA, Zwarenstein H (1934) A rapid test for pregnancy of Xenopus laevis. Nature 133:762

    Article  Google Scholar 

  91. Southwell T, Kirshner A (1937) On some parasitic worms found in Xenopus laevis, the South African Clawed Toad. Ann Trop Med Parasitol 31:245–265. https://doi.org/10.1080/00034983.1937.11684979

    Article  Google Scholar 

  92. Svitin R, Schoeman AL, du Preez LH (2018) New information on morphology and molecular data of camallanid nematodes parasitising Xenopus laevis (Anura: Pipidae) in South Africa. Folia Parasitol 65:003. https://doi.org/10.14411/fp.2018.003

    CAS  Article  Google Scholar 

  93. Theunissen M, Tiedt L, du Preez LH (2014) The morphology and attachment of Protopolystoma xenopodis (Monogenea: Polystomatidae) infecting the African clawed frog Xenopus laevis. Parasite 21:20. https://doi.org/10.1051/parasite/2014020

    Article  PubMed  PubMed Central  Google Scholar 

  94. Thurston JP (1967) The morphology and life-cycle of Cephalochlamys namaquensis (Cohn, 1906) (Cestoda: Pseudophyllidea) from Xenopus muelleri and X. laevis. Parasitology 57:187–200. https://doi.org/10.1017/S0031182000072000

    Article  Google Scholar 

  95. Thurston JP (1970) Studies on some Protozoa and helminth parasites of Xenopus, the African Clawed Toad. Revue de Zoologie et de Botanique Africaines 82:349–368

    Google Scholar 

  96. Tinsley RC (1996) Parasites of Xenopus. In: Tinsley RC, Kobel HR (eds) The biology of Xenopus, vol 1. Clarendon Press, Oxford, pp 233–261

    Google Scholar 

  97. Tinsley RC, Jackson JA (1995) The genus Oligolecithus Vercammen-Grandjean (Digenea: Telorchiidae) from Xenopus spp. (Anura: Pipidae), with a description of O. siluranae n. sp. from X. tropicalis (Gray) in Ghana. Syst Parasitol 32:131–140. https://doi.org/10.1007/BF00009512

    Article  Google Scholar 

  98. Tinsley RC, Jackson JA (1998) Speciation of Protopolystoma Bychowsky, 1957 (Monogenea: Polystomatidae) in hosts of the genus Xenopus (Anura: Pipidae). Syst Parasitol 40:93–141. https://doi.org/10.1023/B:SYPA.0000004047.41228.a6

    Article  Google Scholar 

  99. Tinsley RC (1972) The adaptation of attachment by the Polystomatidae (Monogenoidea). In: Comptes-Rendus Multicolloque Europeen de Parasitologie, Rennes, pp 65–68

  100. Tinsley RC, Sweeting RA (1974) Studies on the biology and taxonomy of Diplostomulum (Tylodelphylus) xenopodis from the African Clawed Toad, Xenopus laevis. J Helminthol 48:247–263. https://doi.org/10.1017/S0022149X00022938

    Article  Google Scholar 

  101. Tinsley RC, Wynne Owen R (1979) The morphology and biology of Xenopodistomum xenopodis from the gall bladder of the African Clawed Toad, Xenopus laevis. J Helmintol 53:307–316

    Article  Google Scholar 

  102. Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2:183–190. https://doi.org/10.1890/1540-9295(2004)002

    Article  Google Scholar 

  103. Torchin ME, Lafferty KD, Kuris AM (2001) Release from parasites as natural enemies: Increased performance of a globally introduced marine crab. Biol Invasions 3:333–345. https://doi.org/10.1023/A:1015855019360

    Article  Google Scholar 

  104. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630. https://doi.org/10.1038/nature01346

    CAS  Article  Google Scholar 

  105. van der Lande VM, Tinsley RC (1976) Studies on the anatomy, life history and behaviour of Marsupiobdella africana (Hirudinea: Glossiphoniidae). J Zool 180:537–563. https://doi.org/10.1111/j.1469-7998.1976.tb04703.x

    Article  Google Scholar 

  106. van Sittert L, Measey GJ (2016) Historical perspectives on global exports and research of African clawed frogs (Xenopus laevis). Trans R Soc South Afr 71:157–166. https://doi.org/10.1080/0035919x.2016.1158747

    Article  Google Scholar 

  107. Vercammen-Grandjean PH (1960) Les trématodes du Lac Kivu Sud (Vermes). Annales du Musée Royal de l’Afrique Centrale 5:1–176

    Google Scholar 

  108. Verneau O, du Preez LH, Laurent V, Raharivololoniaina L, Glaw F, Vences M (2009) The double odyssey of Madagascan polystome flatworms leads to new insights on the origins of their amphibian hosts. Proc R Soc Lond B Biol Sci 276:1575–1583. https://doi.org/10.1098/rspb.2008.1530

    CAS  Article  Google Scholar 

  109. Wade SE (1981) The parasites of Xenopus laevis Daudin (South African Clawed Frog) with special reference to the bionomics and pathogenicity of Capillaria xenopodis sp. n. (Trichoidea: Trichuridae). College of Veterinary Science, Cornell University

  110. Wade SE (1982) Capillaria xenopodis sp. n. (Nematoda: Trichuroidea) from the epidermis of the South African Clawed Frog (Xenopus laevis Daudin). Proc Helminthol Soc Wash 49:86–92

    Google Scholar 

  111. Waeschenbach A, Brabec J, Scholtz T, Littlewood DTJ, Kuchta R (2017) The catholic taste of broad tapeworms—multiple routes to human infection. Int J Parasitol 47:831–843. https://doi.org/10.1016/j.ijpara.2017.06.004

    CAS  Article  PubMed  Google Scholar 

  112. Warburton EM, Kohler SL, Vonhof MJ (2016) Patterns of parasite community dissimilarity: the significant role of land use and lack of distance-decay in a bat–helminth system. Oikos 125:374–385. https://doi.org/10.1111/oik.02313

    Article  Google Scholar 

  113. 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 56:77–83. https://doi.org/10.1080/21564574.2007.9635553

    Article  Google Scholar 

  114. Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York

    Google Scholar 

  115. Wickham H, Francois R, Henry L, Müller K (2017) dplyr: A grammar of data manipulation. R package version 0.7.4. https://CRAN.R-project.org/package=dplyr

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Acknowledgements

The authors would like to express their sincere thanks to a number of persons who assisted in the collection of the frogs. Guénolé le Peutrec helped with the collection in France. In South Africa, several farm owners graciously gave permission for collection to take place on their properties and provided lodging for the research team: Fanus and Olga Kritzinger, William and Christa van Zyl, Dave Schlebusch, Fanus and Carin Oberholzer, Danie and Annalise Marais, Johan Hamann, Tobie Bielt, Gert Bench, Stoffel Labuschagne, Jannie and Susan van Rensburg, Jan Meintjies, Marthinus Hartman, Douw and Louise de Jager, Ernest de Villiers, and Danie and René Botha. Lastly, Mathys Schoeman, Annemie de Klerk, Clarke Scholtz, Andrea Darvall, Willie Landman, Ferdi de Lange and Roxanne Viviers assisted with the collection of frogs at the remainder of the localities in South Africa. A.L.S. received funding from the DST-NRF Centre of Excellence for Invasion Biology (South Africa). The utilisation of the frogs and the research protocols were approved by the Animal Care, Health and Safety in Research Ethics (AnimCare) Committee of the Faculty of Health Sciences of the North-West University (ethics number: NWU-0380-16-A5-01). Animals from the native South African populations were sampled under the permits 0056-AAA007-00224 (CapeNature) and FAUNA 1343-2017 (Northern Cape) provided by the Department of Economic Development, Environmental Affairs and Tourism.

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All authors were involved in initial conception, study design and data collection, as well as in editing and revision of the manuscript. A.L.S. generated the molecular data, performed the statistical analyses, prepared the tables and figures and led the manuscript writing.

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Correspondence to Anneke Lincoln Schoeman.

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Schoeman, A.L., Kruger, N., Secondi, J. et al. Repeated reduction in parasite diversity in invasive populations of Xenopus laevis: a global experiment in enemy release. Biol Invasions 21, 1323–1338 (2019). https://doi.org/10.1007/s10530-018-1902-1

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Keywords

  • African clawed frog
  • Enemy Release Hypothesis
  • Globally invasive amphibians
  • Invasion ecology
  • Natural experiments
  • Parasite loss