Skip to main content

Advertisement

Log in

The role of trematode parasites in larval anuran communities: an aquatic ecologist’s guide to the major players

  • Community Ecology - Original paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Conservation strategies depend on our understanding of the ecosystem and community dynamics. To date, such understanding has focused mostly on predator–prey and competitor interactions. It is increasingly clear, however, that parasite–host interactions may represent a large, and important, component of natural communities. The need to consider multiple factors and their synergistic interactions if we are to elucidate the contribution of anthropogenic factors to loss in biodiversity is exemplified by research into present-day amphibian declines. Only recently has the role of factors such as trematode parasite infections been incorporated into studies of the population and community dynamics of aquatic systems. We argue that this is due, at least in part, to difficulties faced by aquatic ecologists in sifting through the complex systematics that pervade the parasite literature. We note that two trematode species are of dominant importance with regard to North American larval anuran communities, and provide in this review a clear explanation of how to distinguish between the infective stages of these two parasites. We describe the general biology and life history of these parasites, as well as what is known about their effect on larval anurans, and the interactive effects of environmental stressors (typically anthropogenic in nature) and parasites on larval anurans. We hope that this review will convince the reader of the potential importance of these parasites to aquatic communities in general, and to amphibian communities specifically, and will also provide the information necessary for aquatic ecologists to more frequently consider the role of these parasites in their studies of aquatic ecology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alford RA, Richards SJ (1999) Global amphibian declines: a problem in applied ecology. Annu Rev Ecol Syst 30:133–165

    Article  Google Scholar 

  • Anderson JW, Fried B (1987) Experimental infection of Physa heterostropha, Helisoma trivolvis, and Biomaphalareia glabrata (Gastropoda) with Echinostoma reolutum (Trematoda) cercariae. J Parasitol 73:49–54

    Article  PubMed  CAS  Google Scholar 

  • Ankley GT, Degitz SJ, Diamond SA, Tietge JE (2004) Assessment of environmental stressors potentially responsible for malformations in North American anuran amphibians. Ecotoxicol Environ Saf 58:7–16

    Article  PubMed  CAS  Google Scholar 

  • Arkoosh MR, Casillas E, Huffman P, Clemons E, Evered J, Stein JE, Varanasi U (1998) Increased susceptibility of juvenile chinook salmon from a contaminated estuary to Vibrio anguillarum. Trans Am Fish Soc 127:360–374

    Article  Google Scholar 

  • Bancroft BA, Baker NJ, Blaustein AR (2008) A meta-analysis of the effects of ultraviolet-B radiation and its synergistic interactions with pH, contaminants, and disease on amphibian survival. Conserv Biol 22:987–996

    Article  PubMed  Google Scholar 

  • Basch PF, Sturrock RF (1969) Life history of Ribeiroia marini (Faust and Hoffman, 1934) Comb N (Trematoda: Cathaemasiidae). J Parasitol 55:1180

    Article  Google Scholar 

  • Beasley VR, Faeh SA, Wikoff B, Stahle C, Eisold J, Douglas N, Cole R, Schotthoefer AM, Greenwell M, Brown LE (2005) Risk factors and the decline of the Northern cricket frog (Acris crepitans). In: Lannoo MJ (ed) Amphibian declines: the conservation status of United States species. University of Chicago Press, Chicago, pp 75–87

    Google Scholar 

  • Beaver PC (1937) Experimental studies on Echinostoma revolutum (Froelich) a fluke from birds and mammals. Ill Biol Monogr 15:1–96

    Google Scholar 

  • Beaver PC (1939) The morphology and life history of Psilostomum ondatrae Price 1931 (Trematoda: Psilostomidae). J Parasitol 25:383–393

    Article  Google Scholar 

  • Belden LK (2006) Impact of eutrophication on wood frog, Rana sylvatica, tadpoles infected with Echinostoma trivolvis cercariae. Can J Zool 84:1315–1321

    Article  Google Scholar 

  • Blaustein AR, Johnson PT (2003) The complexity of deformed amphibians. Front Ecol Environ 1:87–94

    Google Scholar 

  • Blaustein AR, Kiesecker JM (2002) Complexity in conservation: lessons from the global decline of amphibian populations. Ecol Lett 5:597–608

    Article  Google Scholar 

  • Carey C (1993) Hypothesis concerning the cause of the disappearance of boreal toads from the mountains of Colorado. Conserv Biol 7:355–362

    Article  Google Scholar 

  • Carey C, Cohen N, Rollins-Smith L (1999) Amphibian declines: an immunological perspective. Dev Comp Immunol 23:459–472

    Article  PubMed  CAS  Google Scholar 

  • Chase JM (2003) Strong and weak trophic cascades along a productivity gradient. Oikos 101:187–195

    Article  Google Scholar 

  • Christin MS, Menard L, Gendron AD, Ruby S, Cyr D, Marcogliese DJ, Rollins-Smith L, Fournier M (2004) Effects of agricultural pesticides on the immune system of Xenopus laevis and Rana pipiens. Aquat Toxicol 67:33–43

    Article  PubMed  CAS  Google Scholar 

  • Clarke AH (1981) The freshwater molluscs of Canada. National Museum of Natural Sciences, Ottawa

    Google Scholar 

  • Crump D, Berrill M, Coulson D, Lean D, McGillivray L, Smith A (1999) Sensitivity of amphibian embryos, tadpoles, and larvae to enhanced UV-B radiation in natural pond conditions. Can J Zool 77:1956–1966

    Article  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2000) Wildlife ecology—emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449

    Article  PubMed  CAS  Google Scholar 

  • Degitz SJ, Durhan EJ, Tietge JE, Kosian PA, Holcombe GW, Ankley GT (2003) Developmental toxicity of methoprene and several degradation products in Xenopus laevis. Aquat Toxicol 64:97–105

    Article  PubMed  CAS  Google Scholar 

  • Drost CA, Fellers GM (1996) Collapse of a regional frog fauna in the Yosemite area of the California Sierra Nevada, USA. Conserv Biol 10:414–425

    Article  Google Scholar 

  • Eaton BR, Eaves S, Stevens C, Puchniak A, Paszkowski CA (2004) Deformity levels in wild populations of the wood frog (Rana sylvatica) in three ecoregions of Western Canada. J Herpetol 38:283–287

    Article  Google Scholar 

  • Fox H (1963) The amphibian pronephros. Q Rev Biol 38:1–25

    Article  PubMed  CAS  Google Scholar 

  • Fried B, Toledo R (2004) Criteria for species determination in the ‘revolutum’ group of Echinostoma. J Parasitol 90:917

    Article  PubMed  Google Scholar 

  • Fried B, Pane PL, Reddy A (1997) Experimental infection of Rana pipiens tadpoles with Echinostoma trivolvis cercariae. Parasitol Res 83:666–669

    Article  PubMed  CAS  Google Scholar 

  • Gealekman O, Warburg MR (2000) Changes in numbers and dimensions of glomeruli during metamorphosis of Pelobates syriacus (Anura: Pelodatidae). Eur J Morphol 38:80–87

    Article  PubMed  CAS  Google Scholar 

  • Gendron AD, Bishop CA, Fortin R, Hontela A (1997) In vivo testing of the functional integrity of the corticosterone-producing axis in mudpuppy (Amphibia) exposed to chlorinated hydrocarbons in the wild. Environ Toxicol Chem 16:1694–1706

    Article  CAS  Google Scholar 

  • Gendron AD, Marcogliese DJ, Barbeau S, Christin MS, Brousseau P, Ruby S, Cyr D, Fournier M (2003) Exposure of leopard frogs to a pesticide mixture affects life history characteristics of the lungworm Rhabdias ranae. Oecologia 135:469–476

    PubMed  CAS  Google Scholar 

  • Gosner LK (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Graham AL (2003) Effects of snail size and age on the prevalence and intensity of avian schistosome infection: relating laboratory to field studies. J Parasitol 89:458–463

    Article  PubMed  Google Scholar 

  • Harmon MA, Boehm MF, Heyman RA, Mangelsdorf DJ (1995) Activation of mammalian retinoid-X receptors by the insect growth regulator methoprene. Proc Natl Acad Sci USA 92:6157–6160

    Article  PubMed  CAS  Google Scholar 

  • Hatcher MJ, Dick JTA, Dunn AM (2006) How parasites affect interactions between competitors and predators. Ecol Lett 9:1253–1271

    Article  PubMed  Google Scholar 

  • Hechinger RF, Lafferty KD, Kuris AM (2008) Trematodes indicate animal biodiversity in the Chilean intertidal and Lake Tanganyika. J Parasitol 94:966–968

    Article  PubMed  Google Scholar 

  • Holland MP, Skelly DK, Kashgarian M, Bolden SR, Harrison LM, Cappello M (2007) Echinostome infection in green frogs (Rana clamitans) is stage and age dependent. J Zool 271:455–462

    Article  Google Scholar 

  • Huffman JE, Fried B (1990) Echinostoma and Echinostomiasis. Adv Parasitol 29:215–269

    Article  PubMed  CAS  Google Scholar 

  • Johnson PTJ, Chase JM (2004) Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecol Lett 7:521–526

    Article  Google Scholar 

  • Johnson PTJ, Hartson RB (2009) All hosts are not equal: explaining differential patterns of malformations in an amphibian community. J Anim Ecol 78:191–201

    Article  PubMed  Google Scholar 

  • Johnson PTJ, Sutherland DR (2003) Amphibian deformities and Ribeiroia infection: an emerging helminthiasis. Trends Parasitol 19:332–335

    Article  PubMed  Google Scholar 

  • Johnson PTJ, Lunde KB, Ritchie EG, Launer AE (1999) The effect of trematode infection on amphibian limb development and survivorship. Science 284:802–804

    Article  PubMed  CAS  Google Scholar 

  • Johnson PTJ, Lunde KB, Haight RW, Bowerman J, Blaustein AR (2001a) Ribeiroia ondatrae (Trematoda: Digenea) infection induces severe limb malformations in western toads (Bufo boreas). Can J Zool 79:370–379

    Article  Google Scholar 

  • Johnson PTJ, Lunde KB, Ritchie EG, Reaser JK, Launer AE (2001b) Morphological abnormality patterns in a California amphibian community. Herpetologica 57:336–352

    Google Scholar 

  • Johnson PTJ, Lunde KB, Thurman EM, Ritchie EG, Wray SN, Sutherland DR, Kapfer JM, Frest TJ, Bowerman J, Blaustein AR (2002) Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States. Ecol Monogr 72:151–168

    Article  Google Scholar 

  • Johnson PTJ, Sutherland DR, Kinsella JM, Lunde KB (2004) Review of the trematode genus Ribeiroia (Psilostomidae): ecology, life history and pathogenesis with special emphasis on the amphibian malformation problem. Adv Parasitol 57:191–253

    Article  PubMed  Google Scholar 

  • Johnson PTJ, Chase JM, Dosch KL, Hartson RB, Gross JA, Larson DJ, Sutherland DR, Carpenter SR (2007) Aquatic eutrophication promotes pathogenic infection in amphibians. Proc Natl Acad Sci USA 104:15781–15786

    Article  PubMed  CAS  Google Scholar 

  • Johnson PTJ, Hartson RB, Larson DJ, Sutherland DR (2008) Diversity and disease: community structure drives parasite transmission and host fitness. Ecol Lett 11:1017–1026

    Article  PubMed  Google Scholar 

  • Kanev I (1994) Life-cycle, delimitation and redescription of Echinostoma revolutum (Froelich, 1802) (Trematoda, Echinostomatidae). Syst Parasitol 28:125–144

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Kiesecker JM (2002) Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proc Natl Acad Sci USA 99:9900–9904

    Article  PubMed  CAS  Google Scholar 

  • Kiesecker JM, Skelly DK (2001) Effects of disease and pond drying on gray tree frog growth, development, and survival. Ecology 82:1956–1963

    Google Scholar 

  • King KC, McLaughlin JD, Gendron AD, Pauli BD, Giroux I, Rondeau B, Boily M, Juneau P, Marcogliese DJ (2007) Impacts of agriculture on the parasite communities of northern leopard frogs (Rana pipiens) in southern Quebec, Canada. Parasitology 134:2063–2080

    PubMed  CAS  Google Scholar 

  • King KC, Gendron AD, McLaughlin JD, Giroux I, Brousseau P, Cyr D, Ruby SM, Fournier M, Marcogliese DJ (2008) Short-term seasonal changes in parasite community structure in northern leopard froglets (Rana pipiens) inhabiting agricultural wetlands. J Parasitol 94:13–22

    Article  PubMed  Google Scholar 

  • Klockars J, Huffman J, Fried B (2007) Survey of seasonal trematode infections in Helisoma trivolvis (Gastropoda) from lentic ecosystems in New Jersey, USA. Comp Parasitol 74:75–80

    Article  Google Scholar 

  • Koprivnikar J, Forbes MR, Baker RL (2006a) Effects of atrazine on cercarial longevity, activity, and infectivity. J Parasitol 92:306–311

    Article  PubMed  CAS  Google Scholar 

  • Koprivnikar J, Baker RL, Forbes MR (2006b) Environmental factors influencing trematode prevalence in grey tree frog (Hyla versicolor) tadpoles in southern Ontario. J Parasitol 92:997–1001

    Article  PubMed  Google Scholar 

  • Koprivnikar J, Forbes MR, Baker RL (2006c) On the efficacy of anti-parasite behaviour: a case study of tadpole susceptibility to cercariae of Echinostoma trivolvis. Can J Zool 84:1623–1629

    Article  Google Scholar 

  • Koprivnikar J, Baker RL, Forbes MR (2007) Environmental factors influencing community composition of gastropods and their trematode parasites in southern Ontario. J Parasitol 93:992–998

    Article  PubMed  Google Scholar 

  • Kostadinova A, Gibson DI (2000) The systematics of the echinostomes. In: Fried B, Graczyk T (eds) Echinostomes as experimental models for biological research. Kluwer, Boston, pp 31–52

    Google Scholar 

  • Kostadinova A, Herniou EA, Barrett J, Littlewood DTJ (2003) Phylogenetic relationships of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA and morphological analyses. Syst Parasitol 54:159–176

    Article  PubMed  CAS  Google Scholar 

  • Kuris A (1990) Guild structure of larval trematodes in molluscan hosts: prevalence, dominance and significance of competition. In: Esch GW, Bush AO, Aho JM (eds) Parasite communities: patterns and processes. Chapman and Hall, New York, pp 69–100

    Google Scholar 

  • Kuris AM, Lafferty KD (1994) Community structure: larval trematodes in snail hosts. Annu Rev Ecol Syst 25:189–217

    Article  Google Scholar 

  • Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP, Dunham EJ, Fredensborg BL, Huspeni TC, Lorda J, Mababa L, Mancini FT, Mora AB, Pickering M, Talhouk NL, Torchin ME, Lafferty KD (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515–518

    Article  PubMed  CAS  Google Scholar 

  • La Clair JJ, Bantle JA, Dumont J (1998) Photoproducts and metabolites of a common insect growth regulator produce developmental deformities in Xenopus. Environ Sci Technol 32:1453–1461

    Article  Google Scholar 

  • Lafferty KD, Kuris AM (1999) How environmental stress affects the impacts of parasites. Limnol Oceanogr 44:925–931

    Google Scholar 

  • Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci USA 103:11211–11216

    Article  PubMed  CAS  Google Scholar 

  • Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546

    Article  PubMed  Google Scholar 

  • Lefevre T, Lebarbenchon C, Gauthier-Clerc M, Misse D, Poulin R, Thomas F (2009) The ecological significance of manipulative parasites. Trends Ecol Evol 24:41–48

    Article  PubMed  Google Scholar 

  • Loeffler IK, Stocum DL, Fallon JF, Meteyer CU (2001) Leaping lopsided: a review of the current hypotheses regarding etiologies of limb malformations in frogs. Anat Rec 265:228–245

    Article  PubMed  CAS  Google Scholar 

  • Martin TR, Conn DB (1990) The pathogenicity, localization, and cyst structure of Echinostomatid metacercariae (Trematoda) infecting the kidneys of the frogs Rana clamitans and Rana pipiens. J Parasitol 76:414–419

    Article  PubMed  CAS  Google Scholar 

  • Meteyer CU (2000) Field guide to malformations of frogs and toads with radiographic interpretations. Biological Science Rep. USGS/BRD/BSR-2000-0005, U.S. Fish and Wildlife Service National Conservation Training Center, Sherperdstown, WV

  • Moore J (2002) Behavioral alterations and parasite transmission. In: May RM, Harvey PH (eds) Parasites and the behavior of animals. Oxford University Press, Oxford, pp 35–89

    Google Scholar 

  • Muths E, Corn PS, Pessier AP, Green DE (2003) Evidence for disease-related amphibian decline in Colorado. Biol Conserv 110:357–365

    Article  Google Scholar 

  • Olsen OW (1974) Animal parasites: their life cycles and ecology, 3rd edn. University Park Press, Baltimore

    Google Scholar 

  • Peterson NA (2007) Seasonal prevalence of Ribeiroia ondatrae in one population of Planorbella trivolvis (=Helisoma trivolvis), including notes on the larval trematode component community. Comp Parasitol 74:312–318

    Article  Google Scholar 

  • Pietrock M, Marcogliese DJ (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends Parasitol 19:293–299

    Article  PubMed  Google Scholar 

  • Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390

    Article  PubMed  Google Scholar 

  • Prudhoe S, Bray RA (1982) Platyhelminth parasites of the Amphibia. Oxford University Press, Oxford

    Google Scholar 

  • Riffkin M, Seow HF, Jackson D, Brown L, Wood P (1996) Defence against the immune barrage: helminth survival strategies. Immunol Cell Biol 74:564–574

    Article  PubMed  CAS  Google Scholar 

  • Rohr JR, Crumrine PW (2005) Effects of an herbicide and an insecticide on pond community structure and processes. Ecol Appl 15:1135–1147

    Article  Google Scholar 

  • Rohr JR, Raffel TR, Sessions SK, Hudson PJ (2008a) Understanding the net effects of pesticides on amphibian trematode infections. Ecol Appl 18:1743–1753

    Article  PubMed  Google Scholar 

  • Rohr JR, Schotthoefer AM, Raffel TR, Carrick HJ, Halstead N, Hoverman JT, Johnson CM, Johnson LB, Lieske C, Piwoni MD, Schoff PK, Beasley VR (2008b) Agrochemicals increase trematode infections in a declining amphibian species. Nature 455:U1235–U1250

    Article  CAS  Google Scholar 

  • Schell SC (1970) How to know the trematodes. Brown, IA

    Google Scholar 

  • Schmidt KA, Fried B (1997) Prevalence of larval trematodes in Helisoma trivolvis (Gastropoda) from a farm pond in Northhampton county, Pennsylvania with special emphasis on Echinostoma trivolvis. J Helminthol 64:157–159

    Google Scholar 

  • Schoff PK, Ankley GT (2004) Effects of methoprene, its metabolites, and breakdown products on retinoid-activated pathways in transfected cell lines. Environ Toxicol Chem 23:1305–1310

    Article  PubMed  CAS  Google Scholar 

  • Schotthoefer AM, Cole RA, Beasley VR (2003a) Relationship of tadpole stage to location of echinostome cercariae encystment and the consequences for tadpole survival. J Parasitol 89:475–482

    Article  PubMed  Google Scholar 

  • Schotthoefer AM, Koehler AV, Meteyer CU, Cole RA (2003b) Influence of Ribeiroia ondatrae (Trematoda: Digenea) infection on limb development and survival of northern leopard frogs (Rana pipiens): effects of host stage and parasite-exposure level. Can J Zool 81:1144–1153

    Article  Google Scholar 

  • Sessions SK, Ruth SB (1990) Explanation for naturally-occurring supernumerary limbs in amphibians. J Exp Zool 254:38–47

    Article  PubMed  CAS  Google Scholar 

  • Sessions SK, Franssen RA, Horner VL (1999) Morphological clues from multilegged frogs: are retinoids to blame? Science 284:800–802

    Article  PubMed  CAS  Google Scholar 

  • Skelly DK, Bolden SR, Freidenburg LK, Friedenfelds NA, Malcolm TR (2006) Urbanization and disease on amphibians. In: Collinge SK, Ray C (eds) Disease ecology: community structure and pathogen dynamics. Oxford University Press, Oxford, pp 153–167

    Google Scholar 

  • Sorensen RE, Kanev I, Fried B, Minchella DJ (1997) The occurrence and identification of Echinostoma revolutum from North American Lymnaea elodes snails. J Parasitol 83:169–170

    Article  PubMed  CAS  Google Scholar 

  • Sorensen RE, Curtis J, Minchella DJ (1998) Intraspecific variation in the rDNA its loci of 37-collar-spined echinostomes from North America: implications for sequence-based diagnoses and phylogenetics. J Parasitol 84:992–997

    Article  PubMed  CAS  Google Scholar 

  • Sousa WP (1990) Spatial scale and the processes structuring a guild of larval trematode parasites. In: Esch GW, Bush AO, Aho JM (eds) Parasite communities: patterns and processes. Chapman and Hall, New York, pp 41–67

    Google Scholar 

  • Sousa WP, Grosholz ED (1991) The influence of habitat structure on the transmission of parasites. In: Bell SS, McCoy ED, Mushinsky HR (eds) Habitat structure: the physical arrangement of objects in space. Chapman and Hall, New York, pp 300–324

    Google Scholar 

  • Spangler HG (1988) Moth hearing, defense, and communication. Annu Rev Entomol 33:59–81

    Article  Google Scholar 

  • Stopper GF, Hecker L, Franssen RA, Sessions SK (2002) How trematodes cause limb deformities in amphibians. J Exp Zool 294:252–263

    Article  PubMed  Google Scholar 

  • Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786

    Article  PubMed  CAS  Google Scholar 

  • Sutherland DR (2005) Parasites of North American Frogs. In: Lannoo MJ (ed) Amphibian declines: the conservation status of United States species. University of California Press, Berkeley, pp 109–123

    Google Scholar 

  • Taylor CN, Oseen KL, Wassersug RJ (2004) On the behavioural response of Rana and Bufo tadpoles to echinostomatoid cercariae: implications to synergistic factors influencing trematode infections in anurans. Can J Zool 82:701–706

    Article  Google Scholar 

  • Thiemann GW, Wassersug RJ (2000) Biased distribution of trematode metacercariae in the nephric system of Rana tadpoles. J Zool 252:534–538

    Article  Google Scholar 

  • Toledo R, Munoz-Antoli C, Esteban JG (1999) Production and chronobiology of emergence of the cercariae of Euparyphium albuferensis (Trematoda : Echinostomatidae). J Parasitol 85:263–267

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Treat AE (1975) Mites of moths and butterflies. Cornell University Press, Ithaca

    Google Scholar 

  • Vermeer BJ, Hurks M (1996) The clinical immunotoxicity of pesticides. J Toxicol Environ Health 24:149–154

    Google Scholar 

  • Zaga A, Little EE, Rabeni CE, Ellersieck MR (1998) Photoenhanced toxicity of a carbamate insecticide to early life stage anuran amphibians. Environ Toxicol Chem 17:2543–2553

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank P. Johnson, J. Koprivnikar, J. Vickruck, L. Pinault and V. Cadena for their valuable input on earlier drafts of this review. We would also like to thank Brandon Ballengée for providing us with an incredible re-drawing of the R. ondatrae life cycle. This research was funded by the Department of Biological Sciences, Brock University, the National Science and Engineering Council of Canada (DG# 261587-03 to J.M.L.R.), the Canadian Foundation for Innovation and the Ontario Innovation Trust (Project #9369 to J.M.L.R.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dorina Szuroczki.

Additional information

Communicated by Ross Alford.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Szuroczki, D., Richardson, J.M.L. The role of trematode parasites in larval anuran communities: an aquatic ecologist’s guide to the major players. Oecologia 161, 371–385 (2009). https://doi.org/10.1007/s00442-009-1388-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-009-1388-8

Keywords

Navigation