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Ecoregional-Level Assessment of the Potential Distribution of the Invasive Apple Snail Pomacea maculata Perry, 1810 (Gastropoda: Ampullariidae): Setting Geographically Explicit Priorities for the Management of the Invasion

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Abstract

Pomacea species, also known as apple snails, are highly invasive freshwater organisms now occurring in Central and North America, Asia and Europe. Species misidentification within the genus has hampered efforts to manage their spread and impact, and thus Pomacea maculata have received much less attention that P. canaliculata. Species Distribution Models are well suited for a global screening for suitable regions for the establishment of apple snails. Here, a global distribution model for the distribution of P. maculata based on an extensive database allowed us to identify current and future potential receptor freshwater ecoregions (FEOws) and to set priorities for the development of early warning strategies under climate change scenarios. Model performance was adequate, predicting accurately most invaded FEOWs across the world. Performing a global balance for climate change scenarios, and considering only FEOWs with medium and high ecoregional susceptibility (ES), the potential native distribution of P. maculata is reduced in ca. 945,701 km2, while the exotic potential distribution area increases in 1,118,111 km2. To minimize risks of future invasions, uninvaded FEOWs with both high values of ES and a predicted increase in environmental quality for the establishment of P. maculata were identified across the globe. The development of early warning schemes aiming to detect the initial phase of invasions may provide a unique opportunity for control of this highly invasive species before a much damage to the socio-ecological system is inflicted.

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REFERENCES

  1. Abell, R., Thieme, M., Revenga, C., Bryer, M., Kottelat, M., Bogutskaya, N., Coad, B., Mandrak, N., Balderas, S., Bussing, W., Stiassny, M., Skelton, P., Allen, G., Unmack, P., Naseka, A., et al., Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation, BioScience, 2008, vol. 58, pp. 403–414.

    Google Scholar 

  2. Adhikari, D., Barik, S.K., and Upadhaya, K., Habitat distribution modelling for reintroduction of Ilex khasiana Purk., a critically endangered tree species of northeastern India, Ecol. Eng., 2012, vol. 40, pp. 37–43.

    Google Scholar 

  3. Arfan, A.G., Muhamad, R., Omar, D., Nor Azwady, A.A., and Manjeri, G., Population fluctuation and dispersion patterns of apple snails, Pomacea spp. (Gastropoda: Ampullariidae) in a rice ecosystem, Pertanika J. Trop. Agric. Sci., 2016, vol. 39, no. 3, pp. 343–357.

    Google Scholar 

  4. Bernatis, J.L., McGaw, I.J., and Cross, C.L., Abiotic tolerances in different life stages of apple snails Pomacea canaliculata and Pomacea maculata and the implications for distribution, 2016, J. Shellfish Res., 2016, vol. 35, pp. 1013–1025.

    Google Scholar 

  5. Burks, R., Hensley, S., and Kyle, C.H., Quite the appetite: juvenile island apple snails (Pomacea insularum) survive consuming only exotic invasive plants, J. Molluscan Stud., 2011, vol. 77, pp. 423–428.

    Google Scholar 

  6. Burlakova, L., Padilla, D., Karatayev, A., Hollas, D., Cartwright, L., and Nichol, K., Differences in population dynamics and potential impacts of a freshwater invader driven by temporal habitat stability, Biol. Invasions, 2010, vol. 12, pp. 927–941.

    Google Scholar 

  7. Burrows, M.T., Schoeman, D.S., Richardson, A.J., Molinos, J.G., Hoffmann, A., Buckley, L.B., Moore, P.J., Brown, C.J., Bruno, J.F., Duarte, C.M., Halpern, B.S., Hoegh-Guldberg, O., Kappel, C.V., Kiessling, W., O’Connor, M.I., et al., Geographical limits to species-range shifts are suggested by climate velocity, Nature, 2014, vol. 507, pp. 492–495.

    Google Scholar 

  8. Byers, J.E., McDowell, W.G., Dodd, S.R., Haynie, R.S., Pintor, L.M., and Wilde, S.B., Climate and pH predict the potential range of the invasive apple snail (Pomacea insularum) in the southeastern United States, PLoS One, 2013, vol. 8, no. 2: e586812.

    Google Scholar 

  9. Capon, S.J., Lynch, A.J.J., Bond, N., Chessman, B.C., Davis, J., Davidson, N., Finlayson, M., Gell, P.A., Hohnberg, D., Humphrey, C., Kingsford, R.T., Nielsen, D., Thomson, J.R., Ward, K., and Nally, R.M., Regime shifts, thresholds and multiple stable states in freshwater ecosystems; a critical appraisal of the evidence, Sci. Total Environ., 2015, vol. 534, pp. 122–130.

    Google Scholar 

  10. Carlsson, N.O.L., Brönmark, C., and Hansson, L.A., Invading herbivory: the golden apple snail alters ecosystem functioning in Asian wetlands, Ecology, 2004, vol. 85, pp. 1575–1580.

    Google Scholar 

  11. Database, Global Invasive Species Database, 2019. http://www.iucngisd.org/gisd/search.php on 06-03-2019.

  12. Elith, J.Ç., Graham, C.H., Anderson, R.P., Dudík, M., Ferrier, S., Guisan, A., Hijmans, R.J., Huettmann, F., Leathwick, J.R., Lehmann, A., Li, J., Lohmann, L.G., Loiselle, Manion, G., Moritz, C., et al., Novel methods improve prediction of species’ distributions from occurrence data, Ecography, 2006, vol. 29, pp. 129–151.

    Google Scholar 

  13. Estebenet, A. and Martin, P., Pomacea canaliculata (Gastropoda: Ampullariidae): life-history traits and their plasticity, Biocell, 2002, vol. 26, pp. 83–89.

    Google Scholar 

  14. Glasheen, P.M., Calvo, C., Meerhoff, M., Hayes, K.A., and Burks, R.L., Survival, recovery, and reproduction of apple snails (Pomacea spp.) following exposure to drought conditions, Freshwater Sci., 2017, vol. 36, pp. 316–324.

    Google Scholar 

  15. Hayes, K.A., Joshi, R.C., Thiengo, S.C., and Cowie, R.H., Out of South America: multiple origins of non-native apple snails in Asia, Divers. Distrib., 2008, vol. 14, pp. 701–712.

    Google Scholar 

  16. Hayes, K.A., Cowie, R.H., Thiengo, S.C., and Strong, E.E., Comparing apples with apples: clarifying the identities of two highly invasive Neotropical Ampullariidae (Caenogastropoda), Zool. J. Linn. Soc., 2012, vol. 166, pp. 723–753.

    Google Scholar 

  17. Heino, J., Virkkala, R., and Toivonen, H., Climate change and freshwater biodiversity: detected patterns, future trends and adaptations in northern regions, Biol. Rev., 2009, vol. 84, pp. 39–54.

    PubMed  Google Scholar 

  18. Hellman, J., Byers, J., Bierwagen, B., and Dukes, J., Five potential consequences of climate change for invasive species, Conserv. Biol., 2008, vol. 22, pp. 534–543.

    Google Scholar 

  19. Hesselschwerdt, J. and Wantzen, K.M., Global warming may lower thermal barriers against invasive species in freshwater ecosystems—a study from Lake Constance, Sci. Total Environ., 2018, vol. 645, pp. 44–50.

    PubMed  Google Scholar 

  20. Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., and Jarvisc, A., Very high resolution interpolated climate surfaces for global land areas, Int. J. Climatol., 2005, vol. 25, pp. 1965–1978.

    Google Scholar 

  21. Horgan, F.G., The ecophysiology of apple snails in rice: implications for crop management and policy, Ann. Appl. Biol., 2018, vol. 172, pp. 245–267.

    Google Scholar 

  22. Hutchinson, G.E., Concluding remarks, Cold Spring Harb. Symp. Quant. Biol., 1957, vol. 22, pp. 415–427.

    Google Scholar 

  23. Jenks, G.F., The data model concept in statistical mapping, International Yearbook Cartography, 1967, vol. 7, pp. 186–190.

    Google Scholar 

  24. Joshi, R., Problems with the management of the golden apple snail Pomacea canaliculata: an important exotic pest of rice in Asia, in Area-Wide Control of Insect Pests, Vreysen, M., Robinson, A., and Hendrichs, J., Eds., Vienna, Austria, 2007, pp. 257–264.

    Google Scholar 

  25. Keawjam, R. and Upatham, E., Shell morphology, reproductive anatomy and genetic patterns of three species of apple snails of the genus Pomacea in Thailand, J. Med. Appl. Malacol., 1990, vol. 2, pp. 45–57.

    Google Scholar 

  26. Kwong, K.L., Chan, R.K.Y., and Qiu, J.W., The potential of the invasive snail Pomacea canaliculata as a predator of various life-stages of five species of freshwater snails, Malacologia, 2009, vol. 51, no. 2, pp. 343–356.

    Google Scholar 

  27. Kyle, C.H., Plantz, A.L., Shelton, T., and Burks, R.L., Count your eggs before they invade: identifying and quantifying egg clutches of two invasive apple snail species (Pomacea), PLoS One, 2013, vol. 9, no. 5: e99149.

    Google Scholar 

  28. Lempert, R., Nakicenovic, N., Sarewitz, D., and Schlesinger, M., Characterizing climate-change uncertainties for decision-makers. An editorial essay, Climatic Change, 2004, vol. 65, pp. 1–9.

    Google Scholar 

  29. Lobo, J.M., Jimenez-Valverde, A., and Real, R., AUC: a misleading measure of the performance of predictive distribution models, Global Ecol. Biogeogr., 2008, vol. 17, pp. 145–151.

    Google Scholar 

  30. Lopez, M., Altaba, C., Andree, K., and Lopez, V., First invasion of the apple snail Pomacea insularum in Europe, Tentacle, 2010, vol. 18, pp. 27–29.

    Google Scholar 

  31. Low, L. and Anderson, C.J., The threat of a nonnative, invasive apple snail to oligohaline marshes along the Northern Gulf of Mexico, J. Coast. Res., 2017, vol. 33, pp. 1376–1382.

    Google Scholar 

  32. Manyangadze, T., Chimbari, M.J., Gebreslasie, M., Ceccato, P., and Mukaratirwa, S., Modelling the spatial and seasonal distribution of suitable habitats of schistosomiasis intermediate host snails using Maxent in Ndumo area, KwaZulu-Natal Province, South Africa, Parasites Vectors, 2016, vol. 9, no. 1, p. 572.

    PubMed  PubMed Central  Google Scholar 

  33. Matsukura, K., Okuda, M., Cazzaniga, N.J., and Wada, T., Genetic exchange between two freshwater apple snails, Pomacea canaliculata and Pomacea maculata invading East and Southeast Asia, Biol. Invasions, 2013, vol. 15, pp. 2039–2048.

    Google Scholar 

  34. Matsukura, K., Tsumuki, H., Izumi, Y., and Wada, T., Physiological response to low temperature in the freshwater apple snail, Pomacea canaliculata (Gastropoda: Ampullariidae), J. Exp. Biol., 2009, vol. 212, pp. 2558–2563.

    Google Scholar 

  35. Moss, R.H., Edmonds, J.A., Hibbard, K.A., Manning, M.R., Rose, S.K., van Vuuren, D.P., Carter, T.R., Emori, S., Kainuma, M., Kram, T., Meehl, G.A., Mitchell, J.F.B., Nakicenovic, N., Riahi, K., Smith, S.J., et al., The next generation of scenarios for climate change research and assessment, Nature, 2010, vol. 463, pp. 747–756.

    Google Scholar 

  36. Olson, D.H., Anderson, P.D., Frissell, C.A., Welsh, H.H., Jr., and Bradford, D.F., Biodiversity management approaches for stream-riparian areas: perspectives for Pacific Northwest headwater forests, microclimates, and amphibians. Forest Ecol. Manag., 2007, vol. 246, pp. 81–107.

    Google Scholar 

  37. Padalia, H., Srivastava, V., and Kushwaha, S.P.S., Modeling potential invasion range of alien invasive species, Hyptis suaveolens (L.) Poit. in India: comparison of MaxEnt and GARP, Ecol. Inform., 2014, vol. 22, pp. 36–43.

    Google Scholar 

  38. Parmesan, C., Gaines, S., Gonzalez, L., Kaufman, D.M., Kingsolver, J., Peterson, A.T., and Sagarin, R., Empirical perspectives on species borders: from traditional biogeography to global change, Oikos, 2005, vol. 108, pp. 58–75.

    Google Scholar 

  39. Phillips, S.J., Anderson, R.P., and Schapire, R.E., Maximum entropy modeling of species geographic distributions, Ecol. Model., 2006, vol. 190, pp. 231–259.

    Google Scholar 

  40. Rahel, F.J., Biogeographic barriers, connectivity and homogenization of freshwater faunas: it’s a small world after all, Freshw. Biol., 2007, vol. 52, pp. 696–710.

    Google Scholar 

  41. Rahel, F.J. and Olden, J.D., Assessing the effects of climate change on aquatic invasive species, Conserv. Biol., 2008, vol. 22, pp. 521–533.

    Google Scholar 

  42. Ramakrishnan, V., Salinity, pH, temperature, desiccation and hypoxia tolerance in the invasive freshwater applesnail Pomacea insularum, PhD. Thesis, Arlington: Texas Univ., 2007.

  43. Rawlings, T., Hayes, K., Cowie, R., and Collins, T., The identity, distribution, and impacts of non-native apple snails in the continental United States, BMC Evol. Biol., 2007, vol. 7: 97.

    PubMed  PubMed Central  Google Scholar 

  44. Ricciardi, A. and Macisaac, H.J., Impacts of biological invasions on freshwater ecosystems, in Fifty Years of Invasion Ecology: The Legacy of Charles Elton, 2010, pp. 211–224.

  45. Roll, U., Dayan, T., Simberloff, D., and Mienis, H.K., Non-indigenous land and freshwater gastropods in Israel, Biol. Invasions, 2009, vol. 11, pp. 1963–1972.

    Google Scholar 

  46. Sala, O.E., Chapin, F.S., III, Armesto, J.J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L.F., Jackson, R.B., Kinzig, A., Leemans, R., Lodge, D.M., Mooney, H.A., Oesterheld, M., Poff, N.L., et al., Global biodiversity scenarios for the year 2100, Science, 2000, vol. 287, pp. 1770–1774.

    Google Scholar 

  47. Seuffert, M. and Martín, P. Influence of temperature, size and sex on aerial respiration of Pomacea canaliculata (Gastropoda: Ampullariidae) from southern Pampas, Argentina, Malacologia, 2009, vol. 51, pp. 191–200.

    Google Scholar 

  48. Shan, L., Zhang, Y., Steinmann, P., Yang, G.J., Yang, K., Zhou, X.N., and Utzinger, J., The emergence of angiostrongyliasis in the People’s Republic of China: the interplay between invasive snails, climate change and transmission dynamics, Freshw. Biol., 2011, vol. 56, pp. 717–734.

    Google Scholar 

  49. Smith, C., Boughton, E.H., and Pierre, S., Pomacea maculata (Island Apple Snail) invasion in seasonal wetlands on Florida Ranchland: association with plant-community structure and aquatic-predator abundance, Southeast. Nat., 2015, vol. 14, pp. 561–576.

    Google Scholar 

  50. Strayer, D.L., Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future, Freshw. Biol., 2010, vol. 55, pp. 152–174.

    Google Scholar 

  51. Technical Summary, in Climate Change 2007: Impacts, Adaptation and Vulnerability, Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Parry, M.L., Canziani, O.F., Palutikof, J.P., Linden, P.J.V.D., and Hanson, C.E., Eds., Cambridge: Cambridge University, 2007, pp. 23–78.

  52. Van Vuuren, D.P., Meinshausen, M., Plattner, G.K., Joos, F., Strassmann, K.M., Smith, S.J., Wigley, T.M.L., Raper, S.C.B., Riahi, K., De La, Chesnaye, F. Den Elzen, M.G.J., Fujino, J., Jiang, K., Nakicenovic, N., Paltsev, S., and Reilly, J.M., Temperature increase of 21st century mitigation scenarios, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 15 15258–15262.

    Google Scholar 

  53. Vidal-Abarca Gutiérrez, M.R. and Suárez Alonso, M.L., Which are, what is their status and what can we expect from ecosystem services provided by Spanish rivers and riparian areas? Biodiv. Conserv., 2013, vol. 22, pp. 2469–2503.

  54. Watanabe, T.T., Hattori, G.Y., and Sant’Anna, B.S., Activity, substrate selection, and effect of a simulated Amazon flood regime on the behaviour of the apple snail, Pomacea bridgesii,Mar. Freshwater Res., 2015, vol. 66, pp. 815–821.

    Google Scholar 

  55. West, A.M., Kumar, S., Brown, C.S., Stohlgren, T.J., and Bromberg, J., Field validation of an invasive species Maxent model, Ecol. Inform., 2016, vol. 36, pp. 126–134.

    Google Scholar 

  56. Woodward, G., Perkins, D.M., and Brown, L.E., Climate change and freshwater ecosystems: impacts across multiple levels of organization, Philos. T. R. Soc. B: Biol. Sci., 2010, vol. 365, pp. 2093–2106.

    Google Scholar 

  57. Xenopoulos, M.A., Lodge, D.M., Alcamo, J., Marker, M., Schulze, K., and van Vuuren, D.P., Scenarios of freshwater fish extinctions from climate change and water withdrawal, Glob. Change Biol., 2005, vol. 11, pp. 1557–1564.

    Google Scholar 

  58. Yang, Q.Q., Liu, S.W., He, C., and Yu, X.P., Distribution and the origin of invasive apple snails, Pomacea canaliculata and P. maculata (Gastropoda: Ampullariidae) in China, Sci. Rep., 2018, vol. 8: 1185.

    PubMed  PubMed Central  Google Scholar 

  59. Yoshida, K., Matsukura, K., Cazzaniga, N.J., and Wada, T., Tolerance to low temperature and desiccation in two invasive apple snails, Pomacea canaliculata and P. maculata (Caenogastropoda: Ampullariidae), collected in their original distribution area (northern and central Argentina), J. Molluscan Stud., 2014, vol. 80, pp. 62–66.

    Google Scholar 

  60. Yoshioka, A., Miyazaki, Y., Sekizaki, Y., Suda, S.I., Kadoya, T., and Washitani, I., A “lost biodiversity” approach to revealing major anthropogenic threats to regional freshwater ecosystems, Ecol. Indic., 2014, vol. 36, pp. 348–355 .

    Google Scholar 

  61. Yusa, Y., Sugiura, N., and Wada, T., Predatory potential of freshwater animals on an invasive agricultural pest, the apple snail Pomacea canaliculata (Gastropoda: Ampullariidae), in southern Japan, Biol. Invasions, 2006, vol. 8, pp. 137–147.

    Google Scholar 

  62. Zeng, Y., Low, B.W., and Yeo, D.C.J., Novel methods to select environmental variables in MaxEnt: a case study using invasive crayfish, Ecol. Model., 2016, vol. 341, pp. 5–13.

    Google Scholar 

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ACKNOWLEDGMENTS

This work was part of the Degree Thesis of DB. We are grateful to Kenetth Hayes and Matthew Cannister (Invasive Species Program of the United States Geological Survey) who kindly provided occurrence records from both the native and the exotic range of the species. M. Meheroff and F. Scarabino provide useful insights that helped to improve the ms. Romi Burks and Project “Ampullariidae Model using Phylogeography, Laboratory Integration with Field Investigations into Ecology and Diversity” (IRES AMPLIFIED, NSF) are acknowledged for encouragement and support during field work.

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Barbitta, D., Clavijo, C. & Carranza, A. Ecoregional-Level Assessment of the Potential Distribution of the Invasive Apple Snail Pomacea maculata Perry, 1810 (Gastropoda: Ampullariidae): Setting Geographically Explicit Priorities for the Management of the Invasion. Russ J Biol Invasions 11, 172–181 (2020). https://doi.org/10.1134/S2075111720020022

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