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
Abdulali H (1985) On the export of frog legs from India. J Bombay Nat Hist Soc 82(2):347–375
Allen WL, Street SE, Capellini I (2017) Fast life history traits promote invasion success in amphibians and reptiles. Ecol Lett 20(2):222–230
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
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
Araújo MB, New M (2007) Ensemble forecasting of species distributions. Trends Ecol Evol 22(1):42–47
Bacher S, Blackburn TM, Essl F et al (2018) Socio-economic impact classification of alien taxa (SEICAT). Methods Ecol Evol 9(1):159–168
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
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
Blackburn TM, Pyšek P, Bacher S et al (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26(7):333–339
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
Borroto-Páez R, Bosch RA, Fabres BA, García OA (2016) Introduced amphibians and reptiles in the Cuban archipelago. Herpetol Conserv Biol 10:985–1012
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
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
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
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
Dutta SK (1997) Amphibians of India and Sri Lanka: checklist and bibliography. Odyssey Publishing House, San Diego
Elith J, Kearney M, Phillips S (2010) The art of modelling range-shifting species. Methods Ecol Evol 1(4):330–342
Environmental Systems Research Institute (ESRI) (2012) Arc-GIS Release 10.3.1. Redlands, CA
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
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
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
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
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
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
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
Gardner C, Jasper L (2009) The urban herpetofauna of Toliara, Southwest Madagascar. Herpetol Notes 2:239–242
Glaw F, Vences M (2007) A field guide to the amphibians and reptiles of Madagascar. ISBN-13: 9783929449037
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
Guibé J (1953) Au sujet de l’introduction de Rana tigrine tigerina Daudin à Madagascar. Nat Malgache 5:241–242
Harikrishnan S, Vasudevan K (2013) Recent introduction and spread of Indian bullfrog Hoplobatrachus tigerinus (Daudin, 1802) into the Andaman Islands. Aliens 33:42–43
Harikrishnan S, Vasudevan K (2018) Amphibians of the Andaman & Nicobar Islands: distribution, natural history, and notes on taxonomy. Alytes 36:238–265
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
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
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
Hirschfeld M, Rödel MO (2011) The diet of the African Tiger Frog, Hoplobatrachus occipitalis, in northern Benin. Salamandra 47:125–132
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
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
Jarnevich CS, Stohlgren TJ, Kumar S, Morisette JT, Holcombe TR (2015) Caveats for correlative species distribution modeling. Ecol Inform 29:6–15
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
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
Khan M (1996) The oropharyngeal morphology and feeding habits of tadpole of Tiger Frog Rana tigerina Daudin. Russ J Herpetol 3:163–171
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
Kraus F (2009) Alien reptiles and amphibians: a scientific compendium and analysis, vol 4. Springer, Berlin
Kumschick S, Wilson JR, Foxcroft LC Framework and guidelines for conducting risk analyses for Alien Species. https://doi.org/10.20944/preprints201811.0551.v1
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
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
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
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
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
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
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
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
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
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
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
Mohneke M, Onadeko AB, Rödel MO (2009) Exploitation of frogs—a review with a focus on West Africa. Salamandra 45:193–202
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
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
Oza GM (1990) Ecological effects of the frog’s legs trade. Environmentalist 10:39–42. https://doi.org/10.1007/BF02239556
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
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
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
R Core Team (2019) R: a language and environment for statistical computing. R Core Team, Vienna
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
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
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
Sinha B (1994) Geo-economic survey of Lakshadweep. Concept Publishing Company, Delhi
Thuiller W, Georges D, Engler R, Breiner F (2016) biomod2: Ensemble platform for species distribution modeling. R package version 3.3-7
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
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
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
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
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
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
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
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
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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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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DOI: https://doi.org/10.1007/s10530-020-02356-9