Abstract
We examined the patterns of distribution, vectors of introduction, and potential ecological impacts of freshwater exotic species in Texas over the last 45 years. Currently, five species of exotic gastropods are established: channeled-type applesnail (Pomacea insularum), red-rim melania (Melanoides tuberculatus), quilted melania (Tarebia granifera), giant rams-horn snail (Marisa cornuarietis), and Chinese mysterysnail (Cipangopaludina chinensis). In contrast to the northern part of the US, where shipping appears to be the most important vector for the introduction of aquatic invasive species, aquarium and ornamental trade dominated among unintentional vectors of introduction of all freshwater exotics in Texas, resulting in different patterns of distribution, spread, and ecological impacts. The rate of spread of exotic gastropods in Texas varied from 39 waterbodies colonized over 18 years for P. insularum to only three waterbodies during last 45 years for C. chinensis. Four of five exotic gastropods were found in highly vulnerable aquifer-fed springs and rivers, which contain numerous endemic and endangered species. The fifth species, Pomacea insularum, is an agricultural pest. Potential negative ecological effects of exotic gastropods include impacts on wetlands and wetland restoration, competitive exclusion of native snails, and the introduction of exotic parasites, trematodes, which could infect fish and waterfowl, including federally protected species. Aquifer springs with stable temperature regimes are refuges for both cold and warm intolerant species.
Similar content being viewed by others
References
Abbot, R. T., 1952. A study of an intermediate snail host (Thiara granifera) of the oriental lung fluke (Paragonimus). Proceedings of the United States National Museum 102: 71–116.
Abbot, R. T., 1973. Spread of Melanoides tuberculata. The Nautilus 87: 29.
Burlakova, L. E., A. Y. Karatayev, D. K. Padilla, L. D. Cartwright & D. N. Hollas, 2008. Wetland restoration and invasive species: applesnail (Pomacea insularum) feeding on native and invasive aquatic plants. Restoration Ecology (in press). doi:10.1111/j.1526-100X.2008.00429.x
Benson, A., 2007. Bellamya (Cipangopaludina) chinensis. USGS Nonindigenous Aquatic Species Database, Gainesville, FL. http://nas.er.usgs.gov/queries/FactSheet.asp?speciesID=1044 Revision Date: 4/24/2006.
Biserova, L. I., 1990. Occurrence and distribution of Lithoglyphus naticoides (Gastropoda, Lithoglyphidae) in the Volga Delta. Gydrobiologicheskiy zhurnal 26(2): 98–100. (in Russian).
Biserova, L. I., 2005. The trematodes Apophallus muehlingi and Rossicotrema donicum—parasites of fishes of the River Volga Delta (peculiarities of ecology and induced diseases). PhD thesis. Institute of parasitology of the Russian Academy of Sciences, Moscow (in Russian).
Butler, J. M., F. F. Ferguson, J. R. Palmer & W. R. Jobin, 1980. Displacement of a colony of Biomphalaria glabrata by an invading population of Tarebia granifera in a small stream of Puerto Rico. Caribbean Journal of Science 16: 73–79.
Chaniotis, B. N., J. M. Butler Jr., F. F. Ferguson & W. R. Jobin, 1980. Thermal limits, desiccation tolerance, and humidity reactions of Thiara (Tarebia) granifera Mauiensis (Gastropoda: Thiaridae) host of the Asiatic lung fluke disease. Caribbean Journal of Science 16(1–4): 91–93.
Chernin, E., E. H. Michelson & D. L. Augustine, 1956. Studies on the biological control of schistosome-bearing snails. American Journal of Tropical Medicine and Hygiene 5: 297–307.
Clench, W. J. & S. L. H. Fuller, 1965. The genus Viviparus (Viviparidae) in North America. Occasional Papers on Mollusks 2(32): 385–412.
Cowie, R. H., 2001. Can snails ever be effective and safe biocontrol agents? International Journal of Pest Management 47: 23–40.
Cowie, R. H. & S. C. Thiengo, 2003. The apple snails of the Americas (Mollusca: Gastropoda: Ampullariidae: Asolene, Felipponea, Marisa, Pomacea, Pomella): a nomenclatural and type catalog. Malacologia 45: 41–100.
Drake, J. M. & D. M. Lodge, 2007. Rate of species introductions in the Great Lakes via ships’ ballast water and sediments. Canadian Journal of Fisheries and Aquatic Sciences 64(3): 530–538.
Duggan, I. C., 2002. First record of a wild population of the tropical snail Melanoides tuberculata in New Zealand natural waters. New Zealand Journal of Marine and Freshwater Research 36: 825–829.
Dundee, D. S., 1974. Catalogue of introduced mollusks of eastern North America (north of Mexico). Sterkiana 55: 1–37.
Dundee, D. S. & A. Paine, 1977. Ecology of the snail Melanoides tuberculata (Müller), intermediate host of the human liver fluke (Opisthorchis sinensis) in New Orleans, Louisiana. The Nautilus 91: 17–20.
Ferguson, F. F. & J. R. Palmer, 1958. Biological notes on Marisa cornuarietis, a predator of Australorbis glabratus, the snail intermediate host of schistosomiasis in Puerto Rico. American Journal of Tropical Medicine and Hygiene 7(6): 640–642.
Fofonoff, P. W., G. M. Ruiz, B. Stewens & J. T. Carlton, 2003. In ships or on ships? Mechanisms of transfer and invasion for nonnative species to the coast of North America. In Ruiz, G. M. & J. T. Carlton (eds), Invasive Species: Vectors and Management Strategies. Island Press, Washington: 152–182.
Fullington, R. W., 1978. The recent and fossil freshwater gastropod fauna of Texas. Ph.D. Dissertation, North Texas State University, Denton.
Havel, J. E. & P. D. N. Hebert, 1993. Daphnia lumholtzi in North America: another exotic zooplankter. Limnology and Oceanography 38: 1837–1841.
Horne, F. R., T. L. Arsuffi & R. W. Neck, 1992. Recent introduction and potential impact of the giant rams-horn snail, Marisa cornuarietis (Pilidae), in the Comal Springs ecosystem of Central Texas. Southwestern Naturalist 37(2): 194–214.
Howells, R. G., 2001a. Introduced non-native fishes and shellfishes in Texas waters: an updated list and discussion. Management data series. Parks and Wildlife Department (Texas). Austin TX 188.
Howells, R. G., 2001b. History and status of applesnail (Pomacea spp.) introductions in Texas. Management data series. Parks and Wildlife Department (Texas). Austin TX 183.
Howells, R. G., 2001c. The channeled applesnail (Pomacea canaliculata) invasion: a threat to aquatic ecosystems and the price of rice crispies. American Conchologist 29(4): 8–10.
Howells, R. G. & J. W. Smith, 2002. Status of the applesnail Pomacea canaliculata in the United States. In Wada, T., Y. Yusa & R. C. Joshi (eds), Proceedings of the Special Working Group on the Golden Apple Snail (Pomacea spp.). The Seventh International Congress on Medical and Applied Malacology (7th ICMAM). Los Banos, Laguna, Philippines, SEAMEO Regional Center for Graduate Study and Research in Agriculture (SEARCA): 86–96
Howells, R. G., L. E. Burlakova, A. Y. Karatayev, R. K. Marfurt & R. L. Burks, 2006. Native and introduced Ampullaridae in North America: history, status, and ecology. In Joshi, R. C. & L. S. Sebastian (eds), Global Advances in Ecology and Management of Golden Apple Snails. Philippines, Philippine Rice Research Institute (PhilRice): 73–112.
Hunt, B. P., 1958. Introduction of Marisa into Florida. The Nautilus 72: 53–55.
Ismail, N. S. & A. M. S. Arif, 1993. Population dynamics of Melanoides tuberculata (Thiaridae) snails in a desert spring, United Arab Emirates and interaction with larval trematodes. Hydrobiologia 257: 57–64.
Jacobson, M. K., 1975. The freshwater prosobranch, Tarebia granifera, in oriente, Cuba. The Nautilus 89: 106.
Jobin, W. R., 1970. Population dynamics of aquatic snails in three farm ponds of Puerto Rico. American Journal of Tropical Medicine and Hygiene 19: 1038–1048.
Jokinen, E. H., 1982. Cipangopaludina chinensis (Gastropoda: Viviparidae) in North America, review and update. The Nautilus 96(3): 89–95.
Jokinen, E. H., 1992. The freshwater snails (Mollusca: Gastropoda) of New York state. New York State Museum Bulletin 482.
Karatayev, A. Y., R. G. Howells, L. E. Burlakova & B. D. Sewell, 2005. History of spread and current distribution of Corbicula fluminea (Müller) in Texas. Journal of Shellfish Research 24: 553–559.
Karatayev, A. Y., L. E. Burlakova, S. E. Mastitsky & S. Olenin, 2008. Past, current, and future of the Central European Corridor for aquatic invasions in Belarus. Biological Invasions 10: 215–232.
Karatayev, A. Y., L. E. Burlakova, D. K. Padilla, S. E. Mastitsky & S. Olenin (Accepted). Invaders are not a random selection of species. Biological Invasions.
Kipp, R. M. & A. Benson, 2008. Cipangopaludina (Bellamya) japonica. USGS Nonindigenous Aquatic Species Database, Gainesville, FL. http://nas.er.usgs.gov/queries/FactSheet.asp?speciesID=1046
Kotrla, M. B., 1975. New geographical locations for Philophthalmus sp. In:Thiarid Snails and Waterfowl in Texas. Bulletin of the American Malacological Union, Inc.: 41–42.
Lindholm, J. T. & D. G. Huffman, 1979. The gastropods of the San Marcos River and their trematode parasites. Southwest Texas State University Research Station Report 79.
Livshits, G. & L. Fishelson, 1983. Biology and reproduction of the freshwater snail Melanoides tuberculata (Gastropoda: Prosobranchia) in Israel. Israel Journal of Zoology 32: 21–35.
Martin, P. R., A. L. Estebenet & N. J. Cazzaniga, 2001. Factors affecting the distribution of Pomacea canaliculata (Gastropoda: Ampullariidae) along its southernmost natural limit. Malacologia 43: 13–23.
McDermott, K. S., 2000. Distribution and infection relationships of an undescribed digenetic trematode, its exotic intermediate host, and endangered fishes in springs of West Texas. M.D. Thesis, Southwest Texas State University, San Marcos.
Mills, E. L., J. H. Leach, J. T. Carlton & C. L. Secor, 1993. Exotic species in the Great-Lakes – a history of biotic crises and anthropogenic introductions. Journal of Great Lakes Research 19: 1–54.
Mills, E. L., D. L. Strayer, M. D. Scheuerell & J. T. Carlton, 1996. Exotic species in the Hudson River basin: a history of invasions and introductions. Estuaries 19: 814–823.
Mills, E. L., S. R. Hall & N. K. Pauliukonis, 1998. Exotic species in the Laurentian Great Lakes: from science to policy. Great Lakes Research Review 3: 1–7.
Mitchell, A. J. & T. M. Brandt, 2003. Thermal limits of red-rimmed melania Melanoides tuberculata, (Gastropoda: Prosobranchia: Thiaridae): implication for control and distribution of a snail that vectors a gill trematode causing serious infection in fish. Annual Eastern Fish Health Workshop: 52 pp.
Mitchell, A. J. & T. M. Brandt, 2005. Temperature tolerance of red-rimmed melania, an exotic aquatic snail established in the United States. Transactions of the American Fisheries Society 134: 126–131.
Mitchell, A. J., M. J. Salmon, D. G. Huffman, A. E. Goodwin & T. M. Brandt, 2000. Prevalence and pathogenicity of a heterophyid trematode infecting the gills of endangered fish, the fountain darter, in two Central Texas spring-fed rivers. Journal of Aquatic Animal Health 12: 283–289.
Mitchell, A. J., R. M. Overstreet, A. E. Goodwin & T. M. Brandt, 2005. Spread of exotic fish-gill trematode: a far-reaching and complex problem. Fisheries 30(8): 11–16.
Morrison, J. P. E., 1954. The relationships of Old and New World melanians. Proceedings of the United States National Museum 103(3325): 357–393.
Murray, H. D., 1964. Tarebia granifera and Melanoides tuberculata in Texas. American Malacological Union Annual Reports 1964: 15–16
Murray, H. D., 1971. The introduction and spread of thiarids in the United States. The Biologist 53(3): 133–135.
Murray, H. D., 1975. Melanoides tuberculata (Müller), Las Moras Creek, Bracketville, Texas. Bulletin of the American Malacological Union, Inc. 1975: 43.
Murray, H. D. & D. Haines, 1969. Philophthalmus sp. (Trematoda) in Tarebia granifera and Melanoides tuberculatus in South Texas. American Malacological Union Annual Reports 1969: 44–45.
Murray, H. D. & L. J. Wopschell, 1965. Ecology of Melanoides tuberculata (Müller) and Tarebia granifera (Lamarck) in South Texas (abstract). American Malacological Union Annual Reports 1965: 25–26.
Neck, R. W., 1984. Occurrence of the striped ram’s horn snail, Marisa cornuarietis, in Central Texas (Ampullariidae). The Nautilus 98(3): 119–120.
Neck, R. W., 1985. Melanoides tuberculata in extreme Southern Texas. Texas Conchologist 21(4): 150–152.
Neck, R. W., 1986. A second record of an introduced apple snail, Pomacea canaliculata, from the lower Rio Grande Valley of Texas. Texas Conchologist 22: 54–57.
Neck, R. W. & J. G. Schultz, 1992. First record of living channeled applesnail, Pomacea canaliculata (Pilidae) in Texas. Texas Journal of Science 44: 115–116.
Nollen, P. M. & H. D. Murray, 1978. Philophthalmus gralli: identification, growth characteristics, and treatment of an oriental eyefluke of birds introduced into the continental United States. The Journal of Parasitology 94: 178–180.
Pace, G. L., 1973. The freshwater snails of Taiwan (Formosa). Malacological Review. Supplement 1: 1–117.
Padilla, D. K. & S. L. Williams, 2004. Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Frontiers in the Ecology and Environment 2: 131–138.
Prentice, M. A., 1983. Displacement of Biomphalaria glabrata by the snail Thiara granifera in field habitats in Santa Lucia, West Indies. Annals of Tropical Medicine and Parasitology 77: 51–59.
Pointer, J. P., 1999. Invading freshwater gastropods: some conflicting aspects for public health. Malacologia 41: 403–411.
Pointer, J. P., R. N. Incani, C. Balzan, P. Chroschiechowski & S. Prypchan, 1994. Invasion of the rivers of the littoral central region of Venezuela by Thiara granifera and Melanoides tuberculata (Mollusca, Prosobranchia, Thiaridae) and the absence of Biomphalaria glabrata, snail host of Schistosoma mansoni. The Nautilus 107(4): 124–128.
Radke, M. G., L. S. Ritchie & F. F. Ferguson, 1961. Demonstrated control of Australorbis glabratus by Marisa cornuarietis under field conditions in Puerto Rico. American Journal of Tropical Medicine and Hygiene 10: 370–373.
Ramakrishnan, V., 2007. Salinity, pH, temperature, desiccation and hypoxia tolerance in the invasive freshwater apple snail, Pomacea insularum. Ph.D. Dissertation, University of Texas at Arlington, Arlington, Texas: 241 pp.
Rawlings, T. A., K. A. Hayes, R. H. Cowie & T. M. Collins, 2007. The identity, distribution, and impacts of non-native apple snails in the continental United States. BMC Evolution Biology 7: 97.
Rixon, C. A. M., I. C. Duggan, N. M. N. Bergerson, A. Ricciardi & H. J. Macisaac, 2005. Invasion risk posed by the aquarium trade and live fish markets on the Laurentian Great Lakes. Biodiversity and Conservation 14: 1365–1381.
Robins, C. H., 1971. Ecology of the introduced snail Marisa cornuarietis (Ampullariidae) in Dade County, Florida. Biologist 58(3): 136–152.
Ruiz, G. M., J. T. Carlton, E. D. Grosholz & A. H. Hines, 1997. Global invasions of marine and estuarine habitats by no-indigenous species; mechanisms, extent and consequences. American Zoologist 37: 621–632.
Tolley-Jordan, L. R. & J. M. Owen, 2007. Habitat influences snail community structure and trematode infection levels in a spring-fed river, Texas, USA. Hydrobiologia 600(1): 29–40.
Westman, K., 2002. Alien crayfish in Europe: negative and positive impacts and interactions with native crayfish. In Leppäkoski, E., S. Gollasch & S. Olenin (eds), Invasive Aquatic Species of Europe: Distribution, Impacts and Management. Kluwer Academic Publishers, Dordrecht, The Netherlands: 76–95.
Wood, W. M., 1892. Plaudina japonica Mart. for sale in the San Francisco Chinese markets. The Nautilus 5: 114–115.
Acknowledgments
This study was supported by the State Wildlife Grants Program (US Fish and Wildlife Service and TPWD, grant # 434351). The survey of P. insularum was funded by US Fish and Wildlife Service, Galveston Bay Estuary Program (Texas Commission on Environmental Quality), and US. Department of Agriculture (APHIS). The support during the manuscript preparation for LEB was provided by the Research Foundation of SUNY. We thank David N. Hollas and Leah D. Cartwright who conducted much of the field survey of P. insularum in 2005, and Kevin D. Nichol for the survey in 2006. We are grateful to Randy Gibson and Tom Brandt (The San Marcos National Fish Hatchery & Technology Center, US Fish and Wildlife Service) for the help with sampling and for providing data on the distribution of exotic gastropods. We thank Sergey E. Mastitsky (Great Lakes Center, Research Foundation of SUNY), Michael J. Cook (Stephen F. Austin State University) and Bobbi Cook for the help with sampling and literature search. We would like to express our gratitude to Gordon W. Linam and Marsha E. May (TPWD) for their assistance and support during this project.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling editor: D. Dudgeon
Rights and permissions
About this article
Cite this article
Karatayev, A.Y., Burlakova, L.E., Karatayev, V.A. et al. Introduction, distribution, spread, and impacts of exotic freshwater gastropods in Texas. Hydrobiologia 619, 181–194 (2009). https://doi.org/10.1007/s10750-008-9639-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-008-9639-y