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Effects of environmental change on helminth infections in amphibians: exploring the emergence of Ribeiroia and Echinostoma infections in North America.

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The Biology of Echinostomes

Abstract

Amphibians have long served as model organisms for studying animal physiology, vertebrate anatomy, and host–parasite interactions. Recently, however, the occurrence of precipitous declines in many amphibian populations and of severe limb malformations in others has catalyzed renewed efforts to understand the effects of parasites on amphibians. In this brief review, we examine the importance of two groups of trematodes that utilize amphibians as intermediate hosts: species in the genus Ribeiroia and the broader “echinostome” group which collectively includes the genera Echinostoma and Echinoparyphium. For each, we specifically explore the pathology resulting from infection, whether the parasite has recently increased in abundance or geographic range, and the biotic and abiotic factors likely to influence infection. Both groups of parasites can induce significant pathology in amphibian hosts. Exposure to Ribeiroia cercariae causes substantial increases in mortality and limb malformations in larval amphibians. These malformations, which include missing, malformed and extra limbs, may further reduce survival in amphibians; malformations are extremely rare in adult frogs, even following years in which they are abundant (>50%) among juvenile frogs. Similarly, the echinostomes, which colonize the kidneys of amphibians, can reduce the survival and increase the incidence of edema and renal failure, particularly in laboratory experiments. Recent surveys of National Wildlife Refuges across the USA suggest that both groups of parasites are widespread and sometimes extremely abundant (~1,000 metacercariae per frog). Infections appear to be most common along major rivers and bird flyways in the northern half of the country. While limited evidence suggests a recent increase in amphibian malformations and Ribeiroia infection, the paucity of available historical data precludes a definitive assessment of whether either parasite group has recently emerged. We discuss future approaches to this question and explore contemporary ecological changes known or hypothesized to influence patterns of infection, including changes in land use, increases in nutrient and pesticide runoff, decreases in community diversity and shifts in climate. Considering the documented pathologies of each parasite group, their widespread and often abundant infection patterns, and the ongoing declines observed in amphibian populations, we emphasize the urgent need for further study of Ribeiroia and echinostome infections in amphibians.

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References

  • Alden, K. J. 1995. Helminths of the opossum, Didelphis virginiana., in southern Illinois, with a compilation of all helminths reported from this host in North America. Journal of the Helminthological Society of Washington 62: 197–208.

    Google Scholar 

  • Andrews, K. D., Lampley, R. L., Gillman, M. A., Corey, D. T., Ballard, S. R., Blasczyk, M. J., and Dyer, W. G. 1992. Helminths of Rana catesbeiana. in southern Illinois with a checklist of helminths in bullfrogs of North America. Transactions of the Illinois State Academy of Science 85: 147–172.

    Google Scholar 

  • Beasley, V. R., Faeh, S. A., Wikoff, B., Staehle, C., Eisold, J., Nichols, D., Cole, R., Schotthoefer, A. M., Greenwell, M., and Brown, L. E. 2005. Risk factors and the decline of the cricket frog, Acris crepitans: evidence for involvement of herbicides, parasitism, and habitat modificationsLannoo, M. J., Amphibian Declines: The Conservation Status of United States Species, University of Chicago Press.Chicago: 75–87

    Google Scholar 

  • Beaver, P. C. 1937. Experimental studies on Echinostoma revolutum. (Froelich) a fluke from birds and mammals. Illinois Biological Monographs 15: 1–96.

    Google Scholar 

  • Beaver, P. C. 1939. The morphology and life history of Psilostomum ondatrae, Price 1931 (Trematoda: Psilostomidae), Journal of Parasitology 25: 383–393.

    Article  Google Scholar 

  • Benoy, G. A., Nudds, T. D., and Dunlop, E. 2002. Patterns of habitat and invertebrate diet overlap between tiger salamanders and ducks in prairie potholes. Hydrobiologia 481: 47–59.

    Article  Google Scholar 

  • Blaustein, A. R., and Johnson, P. T. J. 2003. The complexity of deformed amphibians. Frontiers in Ecology and the Environment 1: 87–94.

    Google Scholar 

  • Bowerman, J., and Johnson, P. T. J. 2003. Timing of trematode-related malformations in Oregon spotted frogs and Pacific treefrogs. Northwestern Naturalist 84: 142–145.

    Article  Google Scholar 

  • Bradley, C. A., and Altizer, S. 2007. Urbanization and the ecology of wildlife diseases. Trends in Ecology and Evolution 22: 95–102.

    Article  PubMed  Google Scholar 

  • Centers for Disease Control and Prevention 1994. Addressing emerging infectious disease threats: a prevention strategy for the United States. Atlanta: US Department of Health and Human Services, Public Health Service.

    Google Scholar 

  • Chase, J. M. 2003. Strong and weak trophic cascades along a productivity gradient. Oikos 101: 187–195.

    Article  Google Scholar 

  • Chernin, E. 1968. Interference with the capacity of Schistosoma mansoni. miracidia to infect the molluscan host. Journal of Parasitology 54: 509–516.

    Article  CAS  PubMed  Google Scholar 

  • Esch, G. W. 1971. Impact of ecological succession on parasite fauna in centrarchids from oligotrophic and eutrophic ecosystems. American Midland Naturalist 86: 160–168.

    Article  Google Scholar 

  • Forrester, D. J., and Spalding, M. G. 2003. Parasites and Diseases of Wild Birds in Florida. University Press of Florida.Gainesville:

    Google Scholar 

  • Forrester, D. J., Kinsella, J. M., Mertins, J. W., Price, R. D., and Turnbull, R. E. 1994. Parasitic helminths and arthropods of fulvous whistling-ducks (Dendrocygna bicolor.) in southern Florida. Journal of the Helminthological Society of Washington 61: 84–88.

    Google Scholar 

  • Fried, B., and Graczyk, T. K. 2004. Recent advances in the biology of Echinostoma. species in the “revolutum” group. Advances in Parasitology 58: 139–195.

    Article  PubMed  Google Scholar 

  • Fried, B., Scheuermann, S., and Moore, J. 1987. Infectivity of Echinostoma revolutum. miracidia for laboratory-raised pulmonate snails. Journal of Parasitology 73: 1047–1048.

    Article  CAS  PubMed  Google Scholar 

  • Fried, B., Pane, P. L., and Reddy, A. 1997. Experimental infection of Rana pipiens. tadpoles with Echinostoma trivolvis cercariae. Parasitology Research 83: 666–669.

    Article  CAS  PubMed  Google Scholar 

  • Fried, B., Frazer, B. A., and Kanev, I. 1998. Comparative observations on cercariae and metacercariae of Echinostoma trivolvis. and Echinoparyphium sp. Journal of Parasitology 84: 623–626.

    Article  CAS  PubMed  Google Scholar 

  • Friend, M., McLean, R. G., and Dein, F. J. 2001. Disease emergence in birds: challenges for the twenty-first century. The Auk 118: 290–303.

    Article  Google Scholar 

  • Gosner, K. L. 1960. A simplified table for staging anuran embryos and larvae with notes of identification. Herpetologica 16: 183–190.

    Google Scholar 

  • Gray, R. H. 2000. Historical occurrence of malformations in the cricket frog, Acris crepitans., in Illinois. Transactions of the Illinois State Academy of Sciences 93: 279–284.

    Google Scholar 

  • Hechinger, R. F., Lafferty, K. D., Huspeni, T. C., Brooks, A. J., and Kuris, A. M. 2007. Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and fishes. Oecologia 151: 82–92.

    Article  PubMed  Google Scholar 

  • Holland, M. P., Skelly, D. K., Kashgarian, M., Bolden, S. R., Harrison, L. M., and Cappello, M. 2007. Echinostome infection in green frogs (Rana clamitans.) is stage and age dependent. Journal of Zoology 271: 455–462.

    Article  Google Scholar 

  • Hoppe, D. M. 2000. History of Minnesota frog abnormalities: do recent findings represent a new phenomenon? In: Kaiser, H., Casper, G. S., and Bernstein, N., eds., Investigating Amphibian Declines. Journal of the Iowa Academy of Science 107: 86–89.

    Google Scholar 

  • Hoppe, D. M. 2005. Malformed frogs in Minnesota: history and interspecific differences. Lannoo, M. J., Amphibian Declines: The Conservation Status of United States Species, University of California PressCalifornia: 75–87.

    Google Scholar 

  • Houlahan, J. E., Findlay, C. S., Schmidt, B. R., Meyer, A. H., and Kuzmin, S. L. 2000. Quantitative evidence for global amphibian population declines. Nature 404: 752–755.

    Article  CAS  PubMed  Google Scholar 

  • Hudson, P. J., Dobson, A. P., and Lafferty, K. D. 2006. Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 21: 381–385.

    Article  PubMed  Google Scholar 

  • Huffman, J. E., and Fried, B. 1990. Echinostoma. and Echinostomiasis. Advances in Parasitology 29: 215–269.

    Article  CAS  PubMed  Google Scholar 

  • Huspeni, T. C., and Lafferty, K. D. 2004. Using larval trematodes that parasitize snails to evaluate a saltmarsh restoration project. Ecological Applications 14: 795–804.

    Article  Google Scholar 

  • Inlges, L. 1933. The specificity of frog flukes. Science 78: 168.

    Google Scholar 

  • Johnson, P. T. J. 2006. Amphibian diversity: decimation by disease. Proceedings of the National Academy of Sciences of the United States of America 103: 3011–3012.

    Article  CAS  PubMed  Google Scholar 

  • Johnson, P. T. J., and Chase, J. M. 2004. Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecology Letters 7: 521–526.

    Article  Google Scholar 

  • Johnson , P. T. J., and Hartson, R. B. 2008. All hosts are not equal: explaining differential patterns of malformations in an amphibian community (submitted).

    Google Scholar 

  • Johnson, P. T. J., and Lunde, K. B. 2005. Parasite infection and limb malformations: a growing problem in amphibian conservation. In: Lannoo, M. J., Amphibian Declines: The Conservation Status of United States Species, University of California PressCalifornia: 124–138.

    Google Scholar 

  • Johnson, P. T. J., Lunde, K. B., Ritchie, E. G., and Launer, A. E. 1999. The effect of trematode infection on amphibian limb development and survivorship. Science 284: 802–804.

    Article  CAS  PubMed  Google Scholar 

  • Johnson, P. T. J., Lunde, K. B., Haight, R. W., Bowerman, J., and Blaustein, A. R. 2001a. Ribeiroia ondatrae. (Trematoda: Digenea) infection induces severe limb malformations in western toads (Bufo boreas). Canadian Journal of Zoology 79: 370–379.

    Article  Google Scholar 

  • Johnson, P. T. J., Lunde, K. B., Ritchie, E. G., Reaser, J. K., and Launer, A. E. 2001b. Morphological abnormality patterns in a California amphibian community. Herpetologica 57: 336–352.

    Google Scholar 

  • Johnson, P. T. J., Lunde, K. B., Thurman, E. M., Ritchie, E. G., Wray, S. N., Sutherland, D. R., Kapfer, J. M., Frest, T. J., Bowerman, J., and Blaustein, A. R. 2002. Parasite (Ribeiroia ondatrae.) infection linked to amphibian malformations in the western United States. Ecological Monographs 72: 151–168.

    Article  Google Scholar 

  • Johnson, P. T. J., Lunde, K. B., Zelmer, D. A., and Werner, J. K. 2003. Limb deformities as an emerging parasitic disease in amphibians: evidence from museum specimens and resurvey data. Conservation Biology 17: 1724–1737.

    Article  Google Scholar 

  • Johnson, P. T. J., Sutherland, D. R., Kinsella, J. M., and Lunde, K. B. 2004. Review of the trematode genus Ribeiroia. (Psilostomidae): Ecology, life history, and pathogenesis with special emphasis on the amphibian malformation problem. Advances in Parasitology 57: 191–253.

    Article  PubMed  Google Scholar 

  • Johnson, P. T. J., Chase, J. M., Dosch, K. L., Hartson, R. B., Gross, J. A., Larson, D. J., Sutherland, D. R., and Carpenter, S. R. 2007. Aquatic eutrophication promotes pathogenic infection in amphibians. Proceedings of the National Academy of Sciences of the United States of America 104: 15781–15786.

    Article  CAS  PubMed  Google Scholar 

  • Johnson , P. T. J., Hartson, R. B., Larson, D. J., and Sutherland, D. R. 2008. Linking biodiversity loss and disease emergence: amphibian community structure determines parasite transmission and pathology (in preparation).

    Google Scholar 

  • Kaiser, J. 1997. Ecology – deformed frogs leap into spotlight at health workshop. Science 278: 2051–2052.

    Article  CAS  PubMed  Google Scholar 

  • Kaiser, J. 1999. Frog declines – deformities – a trematode parasite causes some frog deformities. Science 284: 731.

    Article  CAS  PubMed  Google Scholar 

  • Kanev, I., Fried, B., Dimitrov, V., and Radev, V. 1995. Redescription of Echinostoma trivolvis. (Cort, 1914) (Trematoda, Echinostomatidae) with a discussion on its identity. Systematic Parasitology 32: 61–70.

    Article  Google Scholar 

  • Kanev, I., Sorensen, R., Sterner, M., Cole, R., and Fried, B. 1998. The identification and characteristics of Echinoparyphium rubrum. (Cort, 1914) comb. new (Trematoda, Echinostomatidae) based on experimental evidence of the life cycle. Acta Parasitologica 43: 181–188.

    Google Scholar 

  • Keesing, F., Holt, R. D., and Ostfeld, R. S. 2006. Effects of species diversity on disease risk. Ecology Letters 9: 485–498.

    Article  CAS  PubMed  Google Scholar 

  • Kiesecker, J. M. 2002. Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proceedings of the National Academy of Sciences of the United States of America 99: 9900–9904.

    Article  CAS  PubMed  Google Scholar 

  • King, K. C., McLaughlin, J. D., Gendron, A. D., Pauli, B. D., Giroux, I., Rondeau, B., Boily, M., Juneau, P., and Marcogliese, D. J. 2007. Impacts of agriculture on the parasite communities of northern leopard frogs (Rana pipiens.) in southern Quebec, Canada. Parasitology 134: 2063–2080.

    CAS  PubMed  Google Scholar 

  • Knutson, M. G., Richardson, W. B., Reineke, D. M., Gray, B. R., Parmelee, J. R., and Weick, S. E. 2004. Agricultural ponds support amphibian populations. Ecological Applications 14: 669–684.

    Article  Google Scholar 

  • Kopp, K., and Jokela, J. 2007. Resistant invaders can convey benefits to native species. Oikos 116: 295–301.

    Article  Google Scholar 

  • Koprivnikar, J., Baker, R. L., and Forbes, M. R. 2006. Environmental factors influencing trematode prevalence in grey tree frog (Hyla versicolor.) tadpoles in southern Ontario. Journal of Parasitology 92: 997–1001.

    Article  PubMed  Google Scholar 

  • Koprivnikar, J., Baker, R. L., and Forbes, M. R. 2007a. Environmental factors influencing community composition of gastropods and their trematode parasites in southern Ontario. Journal of Parasitology 93: 992–998.

    Article  Google Scholar 

  • Koprivnikar, J., Forbes, M. R., and Baker, R. L. 2007b. Contaminant effects on host–parasite interactions: atrazine, frogs and trematodes. Environmental Toxicology and Chemistry 26: 2166–2170.

    Article  CAS  Google Scholar 

  • Kostadinova, A., Herniou, E. A., Barrett, J., and Littlewood, D. T. J. 2003. Phylogenetic relationships of Echinostoma. Rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA and morphological analyses. Systematic Parasitology 54: 159–176.

    Article  CAS  PubMed  Google Scholar 

  • Kutz, S. J., Hoberg, E. P., Polley, L., and Jenkins, E. J. 2005. Global warming is changing the dynamics of Arctic host–parasite systems. Proceedings of the Royal Society B-Biological Sciences 272: 2571–2576.

    Article  CAS  Google Scholar 

  • Lafferty, K. D., and Holt, R. D. 2003. How should environmental stress affect the population dynamics of disease? Ecology Letters 6: 654–664.

    Article  Google Scholar 

  • Lannoo, M. J., Sutherland, D. R., Jones, P., Rosenberry, D., Klaver, R. W., Hoppe, D. M., Johnson, P. T. J., Lunde, K. B., Facemire, C., and Kapfer, J. M. 2003. Multiple causes for the malformed frog phenomenon. In: ATSM STP 1443, Linder, G., Little, E., Krest, S., and Sparling, D.,Multiple Stressor Effects in Relation to Declining Amphibian Populations. ASTM InternationalWest Conshoshocken:

    Google Scholar 

  • Marcogliese, D. J. 2001. Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79: 1331–1352.

    Article  Google Scholar 

  • Martin, T. R., and Conn. D. B. 1990. The pathogenicity, localization and cyst structure of echinostomatid metacercariae (Trematoda) infecting the kidneys of the frogs Rana clamitans. and Rana pipiens. Journal of Parasitology 76: 414–419.

    Article  CAS  PubMed  Google Scholar 

  • McAlpine, D. F., and Burt, M. D. B. 1998. Helminths of bullfrogs, Rana catesbeiana., green frogs, R. clamitans, and leopard frogs, R. pipiens in New Brunswick. Canadian Field-Naturalist 112: 50–68.

    Google Scholar 

  • McCallum, M. L., and Trauth, S. E. 2003. A forty-three year museum study of northern cricket frog (Acris crepitans.) abnormalities in Arkansas: upward trends and distributions. Journal of Wildlife Diseases 39: 522–528.

    PubMed  Google Scholar 

  • McKenzie, V. J. 2007. Human land use and patterns of parasitism in tropical amphibian hosts. Biological Conservation 137: 102–116.

    Article  Google Scholar 

  • McKenzie, V. J., and Townsend, A. R. 2007. Parasitic and infectious disease responses to changing global nutrient cycles. Ecohealth 4: 384–396.

    Article  Google Scholar 

  • Mone, H., and Combes, C. 1986. Experimental analysis of the decoy effect exerted by nontarget mollusks on the Biomphalaria glabrata. (Say, 1818) – Schistosoma mansoni Sambon, 1907 host–parasite system. Acta Oecologica-Oecologia Applicata 7: 281–286.

    Google Scholar 

  • Moore, J. 2002. Parasites and the Behavior of Animals. Oxford University Press.New York:

    Google Scholar 

  • Muzzall, P. M., Gillilland, M. G., Summer, C. S., and Mehne, C. J. 2001. Helminth communities of green frogs Rana clamitans. Latreille, from southwestern Michigan. Journal of Parasitology 87: 962–968.

    Article  CAS  PubMed  Google Scholar 

  • Najarian, H. H. 1952. The metacercariae of Echinoparyphium flexum. (Linton) Dietz 1909 in frog kidneys. Journal of Parasitology 38: S38.

    Google Scholar 

  • Najarian, H. H. 1954. Developmental stages in the life cycle of Echinoparyphium flexum. (Linton, 1892) Dietz, 1910 (Trematoda, Echinostomatidae). Journal of Morphology 94: 165–197.

    Article  Google Scholar 

  • Ostfeld, R. S., and LoGiudice, K. 2003. Community disassembly, biodiversity loss, and the erosion of an ecosystem service. Ecology 84: 1421–1427.

    Article  Google Scholar 

  • Ouellet, M. 2000. Amphibian deformities: current state of knowledge. Sparling, D. W., Linder, G., and Bishop, C. A.,Ecotoxicology of Amphibians and Reptiles, Society of Environmental Toxicology and ChemistryPensacola: 617–661.

    Google Scholar 

  • Poulin, R. 2006. Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132: 143–151.

    Article  CAS  PubMed  Google Scholar 

  • Prudhoe, S., and Bray, R. A. 1982. Platyhleminth parasites of the Amphibia. Oxford University Press.Oxford:

    Google Scholar 

  • Riggin, G. T. 1956. A note on Ribeiroia ondatrae. (Price, 1931) in Puerto Rico. Proceedings of the Helominthological Society 32: 28–29.

    Google Scholar 

  • Schotthoefer, A. M., Cole, R. A., and Beasley, V. R. 2003. Relationship of tadpole stage to location of echinostome cercariae encystment and the consequences for tadpole survival. Journal of Parasitology 89: 475–482.

    Article  PubMed  Google Scholar 

  • Schotthoefer, A. M., Labak, K. M., and Beasley, V. R. 2007. Ribeiroia ondatrae. cercariae are consumed by aquatic invertebrate predators. Journal of Parasitology 93: 1240–1243.

    Article  PubMed  Google Scholar 

  • Sessions, S. K., and Ruth, S. B. 1990. Explanation for naturally-occurring supernumerary limbs in Amphibians. Journal of Experimental Zoology 254: 38–47.

    Article  CAS  PubMed  Google Scholar 

  • Skelly, D. K., Bolden, S. R., Holland, M. P., Friedenburg, L. K., Friedenfelds, N. A., and Malcom, T. R. 2006. Urbanization and disease in amphibians. Collinge, S. K., and Ray, C.,Disease Ecology: Community Structure and Pathogen Dynamics, Oxford University Press.Cary, NC: 153–167.

    Google Scholar 

  • Skelly, D. K., Bolden, S. R., Freidenburg, L. K., Freidenfelds, N. A., Levey, R. 2007. Ribeiroia. infection is not responsible for Vermont amphibian deformities. Ecohealth 4: 156–163.

    Article  Google Scholar 

  • Skerratt, L. F., Berger, L., Speare, R., Cashins, S., McDonald, K. R., Phillott, A. D., Hines, H. B., and Kenyon, N. 2007. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. Ecohealth 4: 125–134.

    Article  Google Scholar 

  • Smyth, J. D., and Smyth, M. M. 1980. Frogs as host–parasite systems I. An introduction to parasitology through the parasites of Rana temporaria, R. esculenta and R. pipiens. London: Macmillan.

    Google Scholar 

  • Sorensen, R. E., Kanev, I., Fried, B., and Minchella, D. J. 1997. The occurrence and identification of Echinostoma revolutum. from North American Lymnaea elodes snails. Journal of Parasitology 83: 169–170.

    Article  CAS  PubMed  Google Scholar 

  • Souder, W. 2000. A Plague of Frogs. Hyperion.New York:

    Google Scholar 

  • Stopper, G. F., Hecker, L., Franssen, R. A., and Sessions, S. K. 2002. How trematodes cause limb deformities in amphibians. Journal of Experimental Zoology 294: 252–263.

    Article  PubMed  Google Scholar 

  • Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodrigues, A. S. L., Fischman, D. L., and Waller, R. W. 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306: 1783–1786.

    Article  CAS  PubMed  Google Scholar 

  • Sutherland, D. R. 2005. Parasites of North American Frogs. Lannoo, M. J., Amphibian Declines: The Conservation Status of United States Species, University of California Press.California: 109–123.

    Google Scholar 

  • Taft, S. J., Suchow, K., and Vanhorn, M. 1993. Helminths from some Minnesota and Wisconsin raptors. Journal of the Helminthological Society of Washington 60: 260–263.

    Google Scholar 

  • Taylor, C. N., Oseen, K. L., and Wassersug, R. J. 2004. On the behavioural response of Rana. and Bufo tadpoles to echinostomatoid cercariae: implications to synergistic factors influencing trematode infections in anurans. Canadian Journal of Zoology 82: 701–706.

    Article  Google Scholar 

  • Thieltges, D. W., Jensen, K. T., and Poulin, R. 2008The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135: 407–426.

    CAS  PubMed  Google Scholar 

  • Thiemann, G. W., and Wassersug, R. J. 2000a. Biased distribution of trematode metacercariae in the nephric system of Rana. tadpoles. Journal of Zoology 252: 534–538.

    Article  Google Scholar 

  • Thiemann, G. W., and Wassersug, R. J. 2000b. Patterns and consequences of behavioural responses to predators and parasites in Rana. tadpoles. Biological Journal of the Linnean Society 71: 513–528.

    Article  Google Scholar 

  • Toledo, R., Muñoz-Antoli, C., and Fried, B. 2007. The use of echinostomes to study host–parasite relationships between larval trematodes and invertebrate and cold-blooded vertebrate hosts. Parasitology Research 100: 1177–1185.

    Article  PubMed  Google Scholar 

  • Ulmer, M. J. 1970. Studies on the helminth fauna of Iowa I: trematodes of amphibians. American Midland Naturalist 83: 38–64.

    Article  Google Scholar 

  • Wisniewiski, W. L. 1958. Characterization of the parasitofauna of a eutrophic lake. Acta Parasitologica Polonica 6: 1–64.

    Google Scholar 

  • Zander, C. D., Koçogluk, Ö, Skroblies, M., and Strohbach, U. 2002. Parasite populations and communities from the shallow littoral of the Orther Bight (Fehmarn, SW Baltic Sea). Parasitology Research 88: 734–744.

    Article  PubMed  Google Scholar 

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Acknowledgments

We wish to thank the editors of this volume, R. Toledo and B. Fried, for inviting us to contribute, J. Koprivnikar for helpful comments on an earlier draft of this chapter, and all the participants in the US Fish and Wildlife Service’s Amphibian Abnormality Survey which contributed greatly to the development of ideas presented here. Finally, we gratefully acknowledge contributions from the late Dr. Daniel Sutherland, whose pioneering work in the area of amphibian parasitology remains an inspiration to us all.

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Johnson*, P.T.J., McKenzie, V.J. (2009). Effects of environmental change on helminth infections in amphibians: exploring the emergence of Ribeiroia and Echinostoma infections in North America.. In: Toledo, R., Fried, B. (eds) The Biology of Echinostomes. Springer, New York, NY. https://doi.org/10.1007/978-0-387-09577-6_11

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