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Non-native populations and global invasion potential of the Indian bullfrog Hoplobatrachus tigerinus: a synthesis for risk-analysis

Abstract

Invasive amphibians have considerable ecological and socio-economic impact. However, strong taxonomic biases in the existing literature necessitate synthesizing knowledge on emerging invaders. The Indian bullfrog, Hoplobatrachus tigerinus, a large dicroglossid frog (snout to vent length: up to 160 mm), is native to the Indian sub-continent. Despite the high likelihood of invasion success for H. tigerinus, based on the species’ natural history traits and human use, the status of its non-native populations and global invasion potential has not yet been assessed. In this paper, we provide a profile of H. tigerinus as an invasive species to aid in risk analyses and management of existing populations. We review the available knowledge on non-native populations of H. tigerinus and model its potential distribution in the non-native range and globally; finally, we evaluate its ecological and socio-economic impact using standard impact classification schemes. We confirm successful invasions on the Andaman archipelago and Madagascar. The ensemble species distribution model, with ‘good’ predictive ability and transferability, predicts tropical regions of the world to be climatically suitable for the species. Considering potential for propagule pressure, we predict the climatically suitable Mascarene Islands, Malaysia and Indonesia, and East Africa to likely be recipients of bridgehead invasions. We assign the species two impact scores: both socio-economic and environmental scores were ‘moderate’ with ‘medium’ confidence levels in our assessment. Finally, this synthesis outlines the invasion process of the genus Hoplobatrachus, which is an emerging group of amphibian invaders.

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References

  1. Abdulali H (1985) On the export of frog legs from India. J Bombay Nat Hist Soc 82(2):347–375

    Google Scholar 

  2. Allen WL, Street SE, Capellini I (2017) Fast life history traits promote invasion success in amphibians and reptiles. Ecol Lett 20(2):222–230

    PubMed  PubMed Central  Google Scholar 

  3. Allouche O, Tsoar A, Kadmon R (2006) Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J Appl Ecol 43:1223–1232. https://doi.org/10.1111/j.1365-2664.2006.01214.x

    Article  Google Scholar 

  4. Andreone F, Glaw F, Nussbaum RA, Raxworthy CJ, Vences M, Randrianirina JE (2003) The amphibians and reptiles of Nosy Be (NW Madagascar) and nearby islands: a case study of diversity and conservation of an insular fauna. J Nat Hist 37:2119–2149

    Google Scholar 

  5. Araújo MB, New M (2007) Ensemble forecasting of species distributions. Trends Ecol Evol 22(1):42–47

    PubMed  Google Scholar 

  6. Bacher S, Blackburn TM, Essl F et al (2018) Socio-economic impact classification of alien taxa (SEICAT). Methods Ecol Evol 9(1):159–168

    Google Scholar 

  7. Barbet-Massin M, Jiguet F, Albert CH, Thuiller W (2012) Selecting pseudo-absences for species distribution models: How, where and how many? Methods Ecol Evol 3(2):327–338

    Google Scholar 

  8. Barve N, Barve V, Jiménez-Valverde A et al (2011) The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecol Model 222:1810–1819. https://doi.org/10.1016/j.ecolmodel.2011.02.011

    Article  Google Scholar 

  9. Blackburn TM, Pyšek P, Bacher S et al (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26(7):333–339

    PubMed  Google Scholar 

  10. Blackburn TM, Essl F, Evans T et al (2014) A unified classification of alien species based on the magnitude of their environmental impacts. PLoS Biol. https://doi.org/10.1371/journal.pbio.1001850

    Article  PubMed  PubMed Central  Google Scholar 

  11. Borroto-Páez R, Bosch RA, Fabres BA, García OA (2016) Introduced amphibians and reptiles in the Cuban archipelago. Herpetol Conserv Biol 10:985–1012

    Google Scholar 

  12. Both C, Grant T (2012) Biological invasions and the acoustic niche: the effect of bullfrog calls on the acoustic signals of white-banded tree frogs. Biol Lett 8:714–716. https://doi.org/10.1098/rsbl.2012.0412

    Article  PubMed  PubMed Central  Google Scholar 

  13. Capinha C, Seebens H, Cassey P et al (2017) Diversity, biogeography and the global flows of alien amphibians and reptiles. Divers Distrib 23:1313–1322. https://doi.org/10.1111/ddi.12617

    Article  Google Scholar 

  14. Carpenter AI, Andreone F, Moore RD, Griffiths RA (2014) A review of the international trade in amphibians: the types, levels and dynamics of trade in CITES-listed species. Oryx 48:565–574. https://doi.org/10.1017/S0030605312001627

    Article  Google Scholar 

  15. Dufresnes C, Dubey S, Ghali K, Canestrelli D, Perrin N (2015) Introgressive hybridization of threatened European tree frogs (Hyla arborea) by introduced H. intermedia in Western Switzerland. Conserv Genet 16(6):1507–1513

    Google Scholar 

  16. Dutta SK (1997) Amphibians of India and Sri Lanka: checklist and bibliography. Odyssey Publishing House, San Diego

    Google Scholar 

  17. Elith J, Kearney M, Phillips S (2010) The art of modelling range-shifting species. Methods Ecol Evol 1(4):330–342

    Google Scholar 

  18. Environmental Systems Research Institute (ESRI) (2012) Arc-GIS Release 10.3.1. Redlands, CA

  19. Ficetola GF, Coïc C, Detaint M et al (2007a) Pattern of distribution of the American bullfrog Rana catesbeiana in Europe. Biol Invasions 9:767–772. https://doi.org/10.1007/s10530-006-9080-y

    Article  Google Scholar 

  20. Ficetola GF, Thuiller W, Miaud C (2007b) Prediction and validation of the potential global distribution of a problematic alien invasive species: the American bullfrog. Divers Distrib 13:476–485. https://doi.org/10.1111/j.1472-4642.2007.00377.x

    Article  Google Scholar 

  21. Ficetola GF, Maiorano L, Falcucci A et al (2010) Knowing the past to predict the future: land-use change and the distribution of invasive bullfrogs. Glob Chang Biol 16:528–537. https://doi.org/10.1111/j.1365-2486.2009.01957.x

    Article  Google Scholar 

  22. Fonseca É, Both C, Cechin SZ (2019) Introduction pathways and socio-economic variables drive the distribution of alien amphibians and reptiles in a megadiverse country. Divers Distrib 25:1130–1141. https://doi.org/10.1111/ddi.12920

    Article  Google Scholar 

  23. Gallardo B, Zieritz A, Aldridge DC (2015) The importance of the human footprint in shaping the global distribution of terrestrial, freshwater and marine invaders. PLoS ONE 10:1–17. https://doi.org/10.1371/journal.pone.0125801

    CAS  Article  Google Scholar 

  24. Gallien L, Münkemüller T, Albert CH, Boulangeat I, Thuiller W (2010) Predicting potential distributions of invasive species: Where to go from here? Divers Distrib 16(3):331–342

    Google Scholar 

  25. Garcia RA, Burgess ND, Cabeza M, Rahbek C, Araújo MB (2012) Exploring consensus in 21st century projections of climatically suitable areas for African vertebrates. Global Change Biol 18(4):1253–1269

    Google Scholar 

  26. Gardner C, Jasper L (2009) The urban herpetofauna of Toliara, Southwest Madagascar. Herpetol Notes 2:239–242

    Google Scholar 

  27. Glaw F, Vences M (2007) A field guide to the amphibians and reptiles of Madagascar. ISBN-13: 9783929449037

  28. Grosjean S, Vences M, Dubois A (2004) Evolutionary significance of oral morphology in the carnivorous tadpoles of tiger frogs, genus Hoplobatrachus (Ranidae). Biol J Linn Soc 81:171–181. https://doi.org/10.1111/j.1095-8312.2003.00272.x

    Article  Google Scholar 

  29. Guibé J (1953) Au sujet de l’introduction de Rana tigrine tigerina Daudin à Madagascar. Nat Malgache 5:241–242

    Google Scholar 

  30. Harikrishnan S, Vasudevan K (2013) Recent introduction and spread of Indian bullfrog Hoplobatrachus tigerinus (Daudin, 1802) into the Andaman Islands. Aliens 33:42–43

    Google Scholar 

  31. Harikrishnan S, Vasudevan K (2018) Amphibians of the Andaman & Nicobar Islands: distribution, natural history, and notes on taxonomy. Alytes 36:238–265

    Google Scholar 

  32. Hattab T, Garzón-López CX, Ewald M et al (2017) A unified framework to model the potential and realized distributions of invasive species within the invaded range. Divers Distrib 23(7):806–819

    Google Scholar 

  33. Hawkins CL, Bacher S, Essl F et al (2015) Framework and guidelines for implementing the proposed IUCN Environmental Impact Classification for Alien Taxa (EICAT). Divers Distrib 21:1360–1363. https://doi.org/10.1111/ddi.12379

    Article  Google Scholar 

  34. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Google Scholar 

  35. Hirschfeld M, Rödel MO (2011) The diet of the African Tiger Frog, Hoplobatrachus occipitalis, in northern Benin. Salamandra 47:125–132

    Google Scholar 

  36. Hirzel AH, Le Lay G, Helfer V et al (2006) Evaluating the ability of habitat suitability models to predict species presences. Ecol Model 199:142–152. https://doi.org/10.1016/j.ecolmodel.2006.05.017

    Article  Google Scholar 

  37. Hoplobatrachus tigerinus (Daudin, 1802) in GBIF Secretariat (2018) GBIF Backbone Taxonomy. Checklist dataset. https://doi.org/10.15468/39omei. Accessed via GBIF.org on 2018-09-10

  38. Jarnevich CS, Stohlgren TJ, Kumar S, Morisette JT, Holcombe TR (2015) Caveats for correlative species distribution modeling. Ecol Inform 29:6–15

    Google Scholar 

  39. Jenkins RKB, Andrianasolonjatovo MN, Freeman K, Rabearivelo A, Rampilimanana RL, Randrianavelona R (2008) The exploitation of amphibians for food in Madagascar. In: Andreone F (ed) A conservation strategy for the amphibians of madagascar—monografie XLV. Museo Regionale di Scienze Naturali, Torino, pp 343–356

    Google Scholar 

  40. Jiménez-Valverde A, Peterson AT, Soberón J et al (2011) Use of niche models in invasive species risk assessments. Biol Invasions 13:2785–2797. https://doi.org/10.1007/s10530-011-9963-4

    Article  Google Scholar 

  41. Khan M (1996) The oropharyngeal morphology and feeding habits of tadpole of Tiger Frog Rana tigerina Daudin. Russ J Herpetol 3:163–171

    Google Scholar 

  42. Kosuch J, Vences M, Dubois A et al (2001) Out of Asia: mitochondrial DNA evidence for an oriental origin of tiger frogs, genus Hoplobatrachus. Mol Phylogenet Evol 21:398–407. https://doi.org/10.1006/mpev.2001.1034

    CAS  Article  PubMed  Google Scholar 

  43. Kraus F (2009) Alien reptiles and amphibians: a scientific compendium and analysis, vol 4. Springer, Berlin

    Google Scholar 

  44. Kumschick S, Wilson JR, Foxcroft LC Framework and guidelines for conducting risk analyses for Alien Species. https://doi.org/10.20944/preprints201811.0551.v1

  45. Kumschick S, Vimercati G, de Villiers FA et al (2017) Impact assessment with different scoring tools: How well do alien amphibian assessments match? NeoBiota 33:53–66. https://doi.org/10.3897/neobiota.33.10376

    Article  Google Scholar 

  46. Liu X, Li X, Liu Z et al (2014) Congener diversity, topographic heterogeneity and human-assisted dispersal predict spread rates of alien herpetofauna at a global scale. Ecol Lett 17:821–829. https://doi.org/10.1111/ele.12286

    Article  PubMed  Google Scholar 

  47. Measey GJ, Rödder D, Green SL 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 

  48. Measey GJ, Vimercati G, de Villiers FA et al (2016) A global assessment of alien amphibian impacts in a formal framework. Divers Distrib 22:970–981. https://doi.org/10.1111/ddi.12462

    Article  Google Scholar 

  49. Mellert KH, Fensterer V, Küchenhoff H et al (2011) Hypothesis-driven species distribution models for tree species in the Bavarian Alps. J Veg Sci 22:635–646. https://doi.org/10.1111/j.1654-1103.2011.01274.x

    Article  Google Scholar 

  50. Merow C, Smith MJ, Silander JA (2013) A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36:1058–1069. https://doi.org/10.1111/j.1600-0587.2013.07872.x

    Article  Google Scholar 

  51. Merow C, Smith MJ, Edwards TC et al (2014) What do we gain from simplicity versus complexity in species distribution models? Ecography 37:1267–1281. https://doi.org/10.1111/ecog.00845

    Article  Google Scholar 

  52. Mohanty NP, Measey J (2018) What’s for dinner? Diet and potential trophic impact of an invasive anuran Hoplobatrachus tigerinus on the Andaman archipelago. PeerJ 6:e5698. https://doi.org/10.7717/peerj.5698

    Article  PubMed  PubMed Central  Google Scholar 

  53. Mohanty NP, Measey J (2019a) Reconstructing biological invasions using public surveys: a new approach to retrospectively assess spatio-temporal changes in invasive spread. Biol Invasions 21:467–480. https://doi.org/10.1007/s10530-018-1839-4

    Article  Google Scholar 

  54. Mohanty NP, Measey J (2019b) No survival of native larval frogs in the presence of invasive Indian bullfrog Hoplobatrachus tigerinus tadpoles. Biol Invasions 21:2281–2286. https://doi.org/10.1007/s10530-019-01985-z

    Article  Google Scholar 

  55. Mohanty NP, Measey J (2019c) The global pet trade in amphibians: species traits, taxonomic bias, and future directions. Biodivers Conserv 28(14):3915–3923. https://doi.org/10.1007/s10531-019-01857-x

    Article  Google Scholar 

  56. Mohneke M, Onadeko AB, Rödel MO (2009) Exploitation of frogs—a review with a focus on West Africa. Salamandra 45:193–202

    Google Scholar 

  57. Mutnale MC, Anand S, Eluvathingal LM, Roy JK, Reddy GS, Vasudevan K (2018) Enzootic frog pathogen Batrachochytrium dendrobatidis in Asian tropics reveals high ITS haplotype diversity and low prevalence. Scientific Reports 8(1):10125

    PubMed  PubMed Central  Google Scholar 

  58. Novoa A, Richardson DM, Pyšek P et al (2020) Invasion syndromes: a systematic approach for predicting biological invasions and facilitating effective management. Biol Invasions 22:1801–1820. https://doi.org/10.1007/s10530-020-02220-w

    Article  Google Scholar 

  59. Oza GM (1990) Ecological effects of the frog’s legs trade. Environmentalist 10:39–42. https://doi.org/10.1007/BF02239556

    Article  Google Scholar 

  60. Padhye A, Manamendra-Arachchi K, deSilva A, Dutta S, Kumar Shrestha T, Bordoloi S, Papenfuss T, Anderson S, Kuzmin S, Khan MS, Nussbaum R (2008) Hoplobatrachus tigerinus: The IUCN Red List of Threatened Species. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T58301A11760496.en

  61. Pearson RG (2015) Asian common toads in Madagascar: an urgent effort to inform surveys and eradication efforts. Glob Chang Biol 21:9. https://doi.org/10.1111/gcb.12693

    Article  PubMed  Google Scholar 

  62. Pili AN, Sy EY, Diesmos MLL, Diesmos AC (2019) Island hopping in a biodiversity hotspot archipelago: reconstructed invasion history and updated status and distribution of Alien Frogs in the Philippines. Pac Sci 73:321–343. https://doi.org/10.2984/73.3.2

    Article  Google Scholar 

  63. R Core Team (2019) R: a language and environment for statistical computing. R Core Team, Vienna

    Google Scholar 

  64. Rangasamy V, Chandra K, Raghunathan C, Venkataraman K (2014) Amphibians and reptiles in Andaman and Nicobar Islands: diversity and distribution. In: Souvenir: Island Biodiversity, Uttar Pradesh State Biodiversity Board, pp 124–130

  65. Rödder D (2009) Human footprint, facilitated jump dispersal, and the potential distribution of the invasive Eleutherodactylus johnstonei Barbour 1914 (Anura Eleutherodactylidae). Trop Zool 22:205–217

    Google Scholar 

  66. Seebens H, Blackburn TM, Dyer EE et al (2017) No saturation in the accumulation of alien species worldwide. Nat Commun 8:1–9. https://doi.org/10.1038/ncomms14435

    CAS  Article  Google Scholar 

  67. Sinha B (1994) Geo-economic survey of Lakshadweep. Concept Publishing Company, Delhi

    Google Scholar 

  68. Thuiller W, Georges D, Engler R, Breiner F (2016) biomod2: Ensemble platform for species distribution modeling. R package version 3.3-7

  69. Timsina TP (2013) Mass production of frog through induced breeding and growth in laboratory and field condition–the case of Indian bullfrog (Rana tigerina). J Indian Res 1(4):89–94

    Google Scholar 

  70. Tingley R, Romagosa CM, Kraus F et al (2010) The frog filter: amphibian introduction bias driven by taxonomy, body size and biogeography. Glob Ecol Biogeogr 19:496–503. https://doi.org/10.1111/j.1466-8238.2010.00530.x

    Article  Google Scholar 

  71. Tingley R, García-Díaz P, Arantes CRR, Cassey P (2018) Integrating transport pressure data and species distribution models to estimate invasion risk for alien stowaways. Ecography 41:635–646. https://doi.org/10.1111/ecog.02841

    Article  Google Scholar 

  72. Van Wilgen NJ, Gillespie MS, Richardson DM, Measey J (2018) A taxonomically and geographically constrained information base limits non-native reptile and amphibian risk assessment: a systematic review. PeerJ 2018:1–25. https://doi.org/10.7717/peerj.5850

    Article  Google Scholar 

  73. Vences M, Raselimanana AP, Glaw F (2003) Ranidae; Hoplobatrachus, Indian Tiger Frog. In: M. Goodman S, Benstead JP (eds) The natural history of Madagascar. The University of Chicago Press, Chicago and London, pp 926–927

  74. Vences M, Brown J, Lathrop A et al (2017) Tracing a toad invasion: lack of mitochondrial DNA variation, haplotype origins, and potential distribution of introduced Duttaphrynus melanostictus in Madagascar. Amphibia-Reptilia 38(2):197–207

    Google Scholar 

  75. Wildlife Conservation Society-WCS, and Center for International Earth Science Information Network-CIESIN-Columbia University (2005) Last of the Wild Project, Version 2, 2005 (LWP-2): Global Human Influence Index (HII) Dataset (Geographic). Palisades, NY: NASA Socioeconomic Data and Applications Center (SEDAC). https://doi.org/10.7927/H4BP00QC

  76. Woolbright LL, Hara AH, Jacobsen CM et al (2006) Population densities of the Coquí, Eleutherodactylus coqui (Anura: Leptodactylidae) in Newly Invaded Hawaii and in Native Puerto Rico. J Herpetol 40:122–126. https://doi.org/10.1670/79-05w.1

    Article  Google Scholar 

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Acknowledgements

This research was supported by the DSI-NRF Centre of Excellence for Invasion Biology (CIB). We would like to thank: the Department of Environment and Forests, Andaman and Nicobar Islands, for granting permits (#CWLW/WL/134/350); the Inlaks Shivdasani Foundation—Ravi Sankaran Fellowship Programme and the Rufford Small Grants (#20818-2) for funding. Portuguese National Funds through FCT (Fundação para a Ciência e a Tecnologia) supported the Investigador FCT grant to AC (IF/00209/2014). NPM would like to thank Alex Rebelo and Mohlamatsane Mokhlatla for valuable inputs on the species distribution models. We extend our thanks to Karen Freeman, Virgina Rodriguez Ponga, staff of Madagascar Fauna and Flora Group in Tamatave, Abhijit Das, Rohan Arthur, Achille Raselimanana for sharing information and providing valuable inputs. Constructive criticism from three anonymous reviewers and the handling editor (Craig Guyer) helped improve the manuscript.

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Correspondence to Nitya Prakash Mohanty.

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Mohanty, N.P., Crottini, A., Garcia, R.A. et al. Non-native populations and global invasion potential of the Indian bullfrog Hoplobatrachus tigerinus: a synthesis for risk-analysis. Biol Invasions 23, 69–81 (2021). https://doi.org/10.1007/s10530-020-02356-9

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Keywords

  • Amphibian
  • Madagascar
  • Andaman Nicobar
  • Island invasive
  • Risk-assessment
  • Impact scoring
  • Environmental impact classification for Alien Taxa
  • Socio-economic impact classification of Alien Taxa
  • Pet trade