Skip to main content

Advertisement

SpringerLink
Log in

Land Use and Wetland Spatial Position Jointly Determine Amphibian Parasite Communities

  • Original Contribution
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

Land use change is one of the most commonly cited contributing factors to infectious disease emergence, yet the mechanisms responsible for such changes and the spatial scales at which they operate are rarely identified. The distributions of parasites with complex life cycles depend on interactions between multiple host species, suggesting the net effects of land use on infection patterns may be difficult to predict a priori. Here, we used an information-theoretic approach to evaluate the importance of land use and spatial scale (local, watershed, and regional) in determining the presence and abundance of multi-host trematodes of amphibians. Among 40 wetlands and 160 hosts sampled, trematode abundance, species richness, and the presence and abundance of pathogenic species were strongly influenced by variables at the watershed and regional scales. Based on model averaging results, overall parasite richness and abundance were higher in forested wetlands than in agricultural areas; however, this pattern was influenced by a wetland’s proximity to the Mississippi Flyway at the regional scale. These patterns likely reflect the activity of trematode definitive hosts, such as mammals and especially birds, such that infections decreased with increasing distance from the Mississippi River. Interestingly, despite lower mean infections, agricultural wetlands had higher variances and maximum infections. At the wetland scale, phosphorus concentrations and the abundances of intermediate hosts, such as snails and larval amphibians, positively affected parasite distributions. Taken together, these results contribute to our understanding of how altered landscapes affect parasite communities and inform further research on the environmental drivers of amphibian parasite infections.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  • Bellrose, FC (1968) Waterfowl migration corridors east of the Rocky Mountains of the United States. Illinois Natural History Survey Biological Notes No. 61. pp. 1–24.

  • Best LB, Freemark KE, Dinsmore JJ, Camp M (1995) A review and synthesis of habitat use by breeding birds in agricultural landscapes of Iowa. American Midland Naturalist 134:1–29.

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd ed., New York, NY: Springer.

    Google Scholar 

  • Bustnes JO, Galaktionov K (1999) Anthropogenic influences on the infestation of intertidal gastropods by seabird trematode larvae on the southern Barents Sea coast. Marine Biology 133:449–453.

    Article  Google Scholar 

  • Byers JE, Blakeslee AMH, Linder E, Cooper AB, Maguire TJ (2008) Controls of spatial variation in the prevalence of trematode parasites infecting a marine snail. Ecology 89:439–451.

    Article  PubMed  Google Scholar 

  • Christin M-S, Gendron AD, Brousseau P, Ménard L, Marcogliese DJ, Cyr D, Ruby S, Fournier M (2003) Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environmental Toxicology and Chemistry 22:1127–1133.

    PubMed  CAS  Google Scholar 

  • Chu, GWT (1958) Pacific area distribution of fresh-water and marine cercarial dermatitis. Pacific Science 12:299-312.

    Google Scholar 

  • Cole RA (2002) What are parasitologists doing in the United States Geological Survey? Comparative Parasitology 69:132-134.

    Article  Google Scholar 

  • Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London Series B 345:101-118.

    Article  PubMed  CAS  Google Scholar 

  • Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85:2717-2727.

    Article  Google Scholar 

  • Craig HL, Craig PS (2005) Helminth parasites of wolves (Canis lupus): a species list and analysis of published prevalence studies in Nearctic and Palearctic populations. Journal of Helminthologia 79:95-103.

    Article  CAS  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious disease in wildlife. Acta Tropica 78:103–116.

    Article  PubMed  CAS  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Diversity and Distributions 9:141–150.

    Article  Google Scholar 

  • Dillon RT (2000) Parasitism. In: The Ecology of Freshwater Molluscs, Cambridge: Cambridge University Press, pp 227–272.

  • Dove ADM, Cribb TH (2006) Species accumulation curves and their applications in parasite ecology. Trends in Parasitology 22: 568-574.

    Article  PubMed  Google Scholar 

  • Fredensborg BL, Mouritsen KN, Poulin R (2006) Relating bird host distribution and spatial heterogeneity in trematode infections in an intertidal snail-from small to large scale. Marine Biology 149:275-283.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Friend M, Mclean RG, Dein FJ (2001) Disease emergence in birds: challenges for the twenty-first century. The Auk 118:290-303.

    Article  Google Scholar 

  • Gendron AD, Marcogliese DJ, Barbeau S, Christin M-S, Brousseau P, Ruby S, Cyr D, Fourinier 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 

  • Grettenberger J (1991) Habitat fragmentation and forested wetlands on the Upper Mississippi River: potential impacts on forest interior birds. Passenger Pigeon 53:227-241.

    Google Scholar 

  • Hechinger RF, Lafferty KD (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society of London Series B 272:1059-1066.

    Article  PubMed  Google Scholar 

  • Heyer WR, Donnelly MA, McDiarmid RW, Hayek LAC, Foster MS (1994) Measuring and monitoring biological diversity: standard methods for amphibians, Washington, DC: Smithsonian Institution Press.

    Google Scholar 

  • Hoff CC (1941) A case of correlation between infection of snail hosts with Cryptocotyle lingua and the habits of gulls. Journal of Parasitology 27:539.

    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. Journal of Zoology 271:455–462.

    Article  Google Scholar 

  • Holmes JC (1996) Parasites as threats to biodiversity in shrinking ecosystems. Biodiversity and Conservation 5:975-983.

    Article  Google Scholar 

  • Jarcho S., Van Burkhalow A. (1952) A geographical study of “swimmer’s itch” in the United States and Canada. Geographical Review 42:212-226.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Johnson PTJ, McKenzie VJ (2008) Effects of environmental change on helminth infections in amphibians: exploring the emergence of Ribeiroia and Echinostoma infections in North America. In: The Biology of Echinostomes, from the Molecule to the Community, Fried B, Toledo R (editors), New York: Springer, pp 249-280.

    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 (2001) Ribeiroia ondatrae (Trematoda: Digenea) infection induces severe limb malformations in western toads (Bufo boreas). Canadian Journal of Zoology 79:370–379.

    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. Proceedings of the National Academy of Sciences of the United States of America 104:15781–15786.

    Article  PubMed  CAS  Google Scholar 

  • Joly DO, Samuel MD, Langenberg JA, Blanchong JA, Batha CA, Rolley RE, Keane DP, Ribic CA (2006). Spatial epidemiology of chronic wasting disease in Wisconsin white-tailed deer. Journal of Wildlife Diseases 42:578-588.

    PubMed  Google Scholar 

  • Jourdain E, Gauthier-Clerc M, Bicout DJ, Sabatier P (2007) Bird migration routes and risk for pathogen dispersion into western Mediterranean wetlands. Emerging Infectious Diseases 13:365-372.

    Article  PubMed  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. Systematic Parasitology 32:61–70.

    Article  Google Scholar 

  • Kiesecker JM (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  PubMed  CAS  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, McLaughlin JD, Boily M, Marcogliese DJ (2010) Effects of agricultural landscape and pesticides on parasitism in native bullfrogs. Biological Conservation 143:302-310.

    Article  Google Scholar 

  • Knutson MG, Hoover JP, Klaas EE (1996) The importance of floodplain forests in the conservation and management of Neotropical migratory birds in the Midwest. In: Management of Midwestern Landscapes for the Conservation of Neotropical Migratory Birds, US Forest Service General Technical Report, Thompson FR (editor), NC-187, St Paul, MN, pp 168–188.

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

    Article  PubMed  Google Scholar 

  • Lafferty KD (1997) Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitology Today 13:251-255.

    Article  PubMed  CAS  Google Scholar 

  • Latham ADM, Poulin R (2003) Spatiotemporal heterogeneity in recruitment of larval parasites to shore crab intermediate hosts: the influence of shorebird definitive hosts. Canadian Journal of Zoology 81:1282-1291.

    Article  Google Scholar 

  • Lemly AD, Kingsford RT, Thompson JR (2000) Irrigated agriculture and wildlife conservation: conflict on a global scale. Environmental Management 25:485-512.

    Article  PubMed  Google Scholar 

  • Lewis DB, Magnuson JJ (2000) Landscape spatial patterns in freshwater snail assemblages across Northern Highland catchments. Freshwater Biology 43:409-420.

    Article  Google Scholar 

  • Lincoln, Frederick C, Steven R. Peterson, John L. Zimmerman (1998) Migration of birds. U.S. Department of the Interior, U.S. Fish and Wildlife Service, Washington, D.C. Circular 16. Jamestown, ND: Northern Prairie Wildlife Research Center Online. http://www.npwrc.usgs.gov/resource/birds/migratio/index.htm (Version 02APR2002). Accessed November 2010.

  • Linzey DW, Burroughs J, Hudson L, Marini M, Robertson J, Bacon JP, Nagarkatti M, Nagarkatti PS (2003) Role of environmental pollutants on immune functions, parasitic infections and limb malformations in marine toads and whistling frogs from Bermuda. International Journal of Environmental Health Research 13:125–148.

    Article  PubMed  CAS  Google Scholar 

  • Lomolino MV, Perault DR (2000) Assembly and disassembly of mammal communities in a fragmented temperate rain forest. Ecology 81:1517-1532.

    Google Scholar 

  • Marchetti MP, Light T, Moyle PB, Viers JH (2004) Fish invasions in California watersheds: testing hypotheses using landscape patterns. Ecological Applications 14:1507-1525.

    Article  Google Scholar 

  • Omernik JM, Chapman SS, Lillie RA, Dumke RT (2000) Ecoregions of Wisconsin. Transactions of the Wisconsin Academy of Sciences, Arts and Letters. 88:77-104.

    Google Scholar 

  • Ostfeld RS, Glass GE, Keesing F (2005) Spatial epidemiology: an emerging (or re-emerging) discipline. Trends in Ecology and Evolution 20:328-336.

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Poulin R (2007) Are there general laws in parasite ecology? Parasitology 134: 763–776.

    Article  PubMed  CAS  Google Scholar 

  • Reed KD, Meece JK, Henkel JS, Shukla SK (2003) Birds, migration and emerging zoonoses: West Nile virus, Lyme disease, Influenza A and enteropathogens. Clinical Medicine and Research 1:5-12.

    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 (2008) Agrochemicals increase trematode infections in a declining amphibian species. Nature 455:1235-1240.

    Article  PubMed  CAS  Google Scholar 

  • Russell GJ (2006) Species Richness v2.1. Eco-Tools. http://www.eco-tools.net. Accessed July 19, 2010.

  • Schell SC (1985) Trematodes of North America north of Mexico. San Francisco, California: University Press of Idaho.

    Google Scholar 

  • Schotthoefer AM, Cole R, Beasley VR (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 

  • Skelly DK, Bolden SR, Holland MP, Freidenburg LK, Friedenfelds NA, Malcolm TR (2006) Urbanization and disease in amphibians. In: Disease Ecology: Community Structure and Pathogen Dynamics, Collinge SK, Ray C (editors), Cary, NC: Oxford University Press, pp. 153–167.

    Google Scholar 

  • Skirnisson K, Galaktionov KV, Kozminsky EV (2004) Factors influencing the distribution of digenetic trematode infections in a mudsnail (Hydrobia ventrosa) population inhabiting salt marsh ponds in Iceland. Journal of Parasitology 90:50-59.

    Article  PubMed  Google Scholar 

  • Smith NF (2001) Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts. Oecologia 127:115-122.

    Article  Google Scholar 

  • Smith NF (2007) Associations between shorebird abundance and parasites in the sand crab, Emerita analoga, along the California coast. Journal of Parasitology 93:265-273.

    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: Amphibian Declines: the Conservation Status of United States Species, Lannoo MJ (editor), Berkeley, CA: University of California Press, pp. 109–123.

    Google Scholar 

  • Swaddle JP, Calos SE (2008) Increased avian diversity is associated with lower incidence of human West Nile infection: observation of the dilution effect. PLoS ONE 3:e2488.

    Article  PubMed  Google Scholar 

  • Thieltges DW, Reise K (2007) Spatial heterogeneity in parasite infections at different spatial scales in an intertidal bivalve. Oecologia 150:569-581.

    Article  PubMed  Google Scholar 

  • Walter BA, Moore JL (2005) The concepts of bias, precision and accuracy, and their use in testing the performance of species richness estimators, with a literature review of estimator performance. Ecography 28: 815-829.

    Article  Google Scholar 

  • Walther BA, Morand S (1998) Comparative performance of species richness estimation methods. Parasitology 116: 395-405.

    Article  PubMed  Google Scholar 

  • Yamaguti S (1975) A Synoptical Review of Life Histories of Digenetic Trematodes of Vertebrates with Special Reference to the Morphology of their Larval Forms. Tokyo, Japan: Keigaku Publishing Co.

    Google Scholar 

  • Zelmer DA, Esch GW (1999) Robust estimation of parasite component community richness. Journal of Parasitology 85: 592-594.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank T. Kratz, P. Montz, and the Trout Lake Research Station for logistical support of field and laboratory activities, and J. Orlofske, D. Preston, and B. Goodman for early reviews of the manuscript. We would also like to thank J. Thoyre, M. Lochner, E. Stanley and the Center for Limnology for providing support to analyze nutrient samples. Finally, we thank the late D. Sutherland for his guidance, training, and inspiration in this research. R. Hartson was supported through a generous research fellowship from the Juday Family Foundation. S. Orlofske was supported through a Graduate Research Fellowship from NSF. P. Johnson gratefully acknowledges support from the David and Lucile Packard Foundation and NSF (DEB-0841758).

Author information

Authors and Affiliations

  1. Department of Water Resources, University of Idaho, Moscow, ID, 83843, USA

    Richard B. Hartson

  2. Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA

    Sarah A. Orlofske & Pieter T. J. Johnson

  3. Department of Biology, University of Wisconsin, La Crosse, WI, 54601, USA

    Vanessa E. Melin

  4. Department of Biology, College of Charleston, Charleston, SC, 29424, USA

    Robert T. Dillon Jr.

Authors
  1. Richard B. Hartson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarah A. Orlofske
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vanessa E. Melin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert T. Dillon Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pieter T. J. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pieter T. J. Johnson.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 58 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hartson, R.B., Orlofske, S.A., Melin, V.E. et al. Land Use and Wetland Spatial Position Jointly Determine Amphibian Parasite Communities. EcoHealth 8, 485–500 (2011). https://doi.org/10.1007/s10393-011-0715-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-011-0715-9

Keywords

Search

Navigation