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The distribution of echinostome parasites in ponds and implications for larval anuran survival

Published online by Cambridge University Press:  11 January 2017

JOHN A. MARINO JR. ,
MANJA P. HOLLAND  and
EARL E. WERNER
JOHN A. MARINO JR.*
Affiliation:
Department of Ecology and Evolutionary Biology, 2019 Kraus Natural Sciences Building, 830 North University Ave., University of Michigan, Ann Arbor, MI 48109, USA
MANJA P. HOLLAND
Affiliation:
Department of Ecology and Evolutionary Biology, 2019 Kraus Natural Sciences Building, 830 North University Ave., University of Michigan, Ann Arbor, MI 48109, USA
EARL E. WERNER
Affiliation:
Department of Ecology and Evolutionary Biology, 2019 Kraus Natural Sciences Building, 830 North University Ave., University of Michigan, Ann Arbor, MI 48109, USA
*
*Corresponding author: Department of Biology, Bradley University, 06 Olin Hall, 1501 W. Bradley Ave., Peoria, IL 61625, USA. E-mail: jmarino@fsmail.bradley.edu
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Summary

Parasites can influence host population dynamics, community composition and evolution. Prediction of these effects, however, requires an understanding of the influence of ecological context on parasite distributions and the consequences of infection for host fitness. We address these issues with an amphibian – trematode (Digenea: Echinostomatidae) host–parasite system. We initially performed a field survey of trematode infection in first (snail) and second (larval green frog, Rana clamitans) intermediate hosts over 5 years across a landscape of 23 ponds in southeastern Michigan. We then combined this study with a tadpole enclosure experiment in eight ponds. We found echinostomes in all ponds during the survey, although infection levels in both snails and amphibians differed across ponds and years. Echinostome prevalence (proportion of hosts infected) in snails also changed seasonally depending on host species, and abundance (parasites per host) in tadpoles depended on host size and prevalence in snails. The enclosure experiment demonstrated that infection varied at sites within ponds, and tadpole survival was lower in enclosures with higher echinostome abundance. The observed effects enhance our ability to predict when and where host–parasite interactions will occur and the potential fitness consequences of infection, with implications for population and community dynamics, evolution and conservation.

Keywords

Host–parasite interactionsmortalityseasonalityEchinostomatidaeRana clamitans
Type
Research Article
Information
Parasitology , Volume 144 , Issue 6 , May 2017 , pp. 801 - 811
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Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. and Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467–484.CrossRefGoogle ScholarPubMed
Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–247.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 declines in northern cricket frogs (Acris crepitans). In Amphibian Declines: The Conservation Status of United States Species (ed. Lannoo, M.), pp. 75–86. University California Press, Berkeley.Google Scholar
Brown, K. M., Leathers, B. K. and Minchella, D. J. (1988). Trematode prevalence and the population dynamics of freshwater pond snails. The American Midland Naturalist 120, 289–301.CrossRefGoogle Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al revisited. Journal of Parasitology 83, 575–583.Google Scholar
Cornell, S. (2008). Seasonality, cohort-dependence and the development of immunity in a natural host-nematode system. Proceedings of the Royal Society B: Biological Sciences 275, 511–518.Google Scholar
Detwiler, J. T., Bos, D. H. and Minchella, D. J. (2010). Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostome parasites in North America. Molecular Phylogenetics and Evolution 55, 611–620.CrossRefGoogle ScholarPubMed
DeWitt, R. M. (1955). The ecology and life history of the pond snail Physa gyrina . Ecology 36, 40–44.Google Scholar
Dobson, A. P. and Hudson, P. J. (1986). Parasites, disease and the structure of ecological communities. Trends in Ecology & Evolution 1, 11–15.Google Scholar
Duffy, M. A., Brassil, C. E., Hall, S. R., Tessier, A. J., Caceres, C. E. and Conner, J. K. (2008). Parasite-mediated disruptive selection in a natural Daphnia population. BMC Evolutionary Biology 8, 80.Google Scholar
Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183–190.Google Scholar
Gustafson, K. D., Newman, R. A., Pulis, E. E. and Cabarle, K. C. (2015). A skeletochronological assessment of age-parasitism relationships in wood frogs (Lithobates sylvaticus). Journal of Herpetology 49, 122–130.CrossRefGoogle Scholar
Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S. and Samuel, M. D. (2002). Ecology – Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162.Google Scholar
Holland, M. P. (2010). Echinostome-induced mortality varies across amphibian species in the field. Journal of Parasitology 96, 851–855.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.Google Scholar
Hoverman, J. T., Davis, C. J., Werner, E. E., Skelly, D. K., Relyea, R. A. and Yurewicz, K. L. (2011). Environmental gradients and the structure of freshwater snail communities. Ecography 34, 1049–1058.Google Scholar
Hoverman, J. T., Mihaljevic, J. R., Richgels, K. L. D., Kerby, J. L. and Johnson, P. (2012). Widespread co-occurrence of virulent pathogens within California amphibian communities. Ecohealth 9, 288–292.Google Scholar
Hudson, P., Dobson, A. P. and Newborn, D. (1998). Prevention of population cycles by parasite removal. Science 282, 2256–2258.Google Scholar
Johnson, P. T. J. and Hoverman, J. T. (2012). Parasite diversity and coinfection determine pathogen infection success and host fitness. Proceedings of the National Academy of Sciences of the United States of America 109, 9006–9011.CrossRefGoogle ScholarPubMed
Johnson, P. T. J., Preston, D. L., Hoverman, J. T. and Richgels, K. L. D. (2013). Biodiversity decreases disease through predictable changes in host community competence. Nature 494, 230–233.CrossRefGoogle ScholarPubMed
Kanev, V. R., Sterner, M. and Fried, B. (2000). An overview of the biology of echinostomes. In Echinostomes as Experimental Models for Biological Research (ed. Fried, B. and Graczyk, T. K.), pp. 1–29. Kluwer Academic Publishers, Boston, Massachusetts, USA.Google Scholar
Karraker, N. E., Gibbs, J. P. and Vonesh, J. R. (2008). Impacts of road deicing salt on the demography of vernal pool-breeding amphibians. Ecological Applications 18, 724–734.CrossRefGoogle ScholarPubMed
Kiesecker, J. M. and Skelly, D. K. (2000). Choice of oviposition site by gray treefrogs: the role of potential parasitic infection. Ecology 81, 2939–2943.Google Scholar
King, K. K. C., McLaughlin, J. J. D., Gendron, A. A. D., Pauli, B. B. D., Giroux, I. I., Rondeau, B. B., Boily, M. M., Juneau, P. P. and Marcogliese, D. D. J. (2007). Impacts of agriculture on the parasite communities of northern leopard frogs (Rana pipiens) in southern Quebec, Canada. Parasitology 134, 2063–80.Google Scholar
Koprivnikar, J., Forbes, M. R. and Baker, R. L. (2006). On the efficacy of anti-parasite behaviour: a case study of tadpole susceptibility to cercariae of Echinostoma trivolvis . Canadian Journal of Zoology 84, 1623–1629.Google Scholar
Koprivnikar, J., Forbes, M. R. and Baker, R. L. (2008). Larval amphibian growth and development under varying density: are parasitized individuals poor competitors? Oecologia 155, 641–649.Google Scholar
Koprivnikar, J., Redfern, J. C. and Mazier, H. L. (2014). Variation in anti-parasite behaviour and infection among larval amphibian species. Oecologia 174, 1179–1185.Google Scholar
Lemly, A. and Esch, G. (1984). Population biology of the trematode Uvulifer ambloplitis (Hughes, 1927). Journal of Parasitology 70, 461–465.CrossRefGoogle Scholar
Marino, J. A. and Werner, E. E. (2013). Synergistic effects of predators and trematode parasites on larval green frog (Rana clamitans) survival. Ecology 94, 2697–2708.Google Scholar
Marino, J. A., Holland, M. P. and Middlemis Maher, J. (2014). Predators and trematode parasites jointly affect larval anuran functional traits and corticosterone levels. Oikos 123, 451–460.Google Scholar
Marino, J. A., Holland, M. P. and Werner, E. E. (2016). Competition and host size mediate larval anuran interactions with trematode parasites. Freshwater Biology 61, 621–632.Google Scholar
May, R. M. and Anderson, R. M. (1978). Regulation and stability of host-parasite population interactions: II. Destabilizing processes. Journal of Animal Ecology 47, 249–267.Google Scholar
Middlemis Maher, J., Werner, E. E. and Denver, R. J. (2013). Stress hormones mediate predator-induced phenotypic plasticity in amphibian tadpoles. Proceedings of the Royal Society B: Biological Sciences 280, 20123075.Google Scholar
Minchella, D. J. and Scott, M. E. (1991). Parasitism: a cryptic determinant of animal community structure. Trends in Ecology & Evolution 6, 250–254.Google Scholar
Morris, J. and Boag, D. (1982). On the dispersion, population-structure, and life-history of a basommatophoran snail, Helisoma trivolvis, in central Alberta. Canadian Journal of Zoology-Revue Canadienne De Zoologie 60, 2931–2940.CrossRefGoogle Scholar
Nikolaev, K. E., Sukhotin, A. A. and Galaktionov, K. V. (2006). Infection patterns in white sea blue mussels Mytilus edulis of different age and size with metacercariae of Himasthla elongata (Echinostomatidae) and Cercaria parvicaudata (Renicolidae). Diseases of Aquatic Organisms 71, 51–58.Google Scholar
Paull, S. H., Song, S., McClure, K. M., Sackett, L. C., Kilpatrick, A. M. and Johnson, P. T. J. (2012). From superspreaders to disease hotspots: linking transmission across hosts and space. Frontiers in Ecology and the Environment 10, 75–82.Google Scholar
Peterson, N. A. (2007). Seasonal prevalence of Ribeiroia ondatrae in one population of Planorbella trivolvis (= Helisoma trivolvis), including notes on the larval trematode component community. Comparative Parasitology 74, 312.Google Scholar
Raberg, L., Graham, A. L. and Read, A. F. (2009). Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 37–49.Google Scholar
Raffel, T. R., Hoverman, J. T., Halstead, N. T., Michel, P. J. and Rohr, J. R. (2010). Parasitism in a community context: trait-mediated interactions with competition and predation. Ecology 91, 1900–1907.Google Scholar
Raffel, T. R., Lloyd-Smith, J. O., Sessions, S. K., Hudson, P. J. and Rohr, J. R. (2011). Does the early frog catch the worm? Disentangling potential drivers of a parasite age-intensity relationship in tadpoles. Oecologia 165, 1031–1042.Google Scholar
Richgels, K. L. D., Hoverman, J. T. and Johnson, P. T. J. (2013). Evaluating the role of regional and local processes in structuring a larval trematode metacommunity of Helisoma trivolvis . Ecography 36, 854–863.Google Scholar
Rifkin, J. L., Nunn, C. L. and Garamszegi, L. Z. (2012). Do animals living in larger groups experience greater parasitism? A meta-analysis. American Naturalist 180, 70–82.Google Scholar
Rohr, J. R., Schotthoefer, A. M., Raffel, T. R., Carrick, H. J., Halstead, N., Hoverman, J. T., Johnson, C. M., Johnson, L. B., Lieske, C., Piwoni, M. D., Schoff, P. K. and Beasley, V. R. (2008). Agrochemicals increase trematode infections in a declining amphibian species. Nature 455, 1235–1239.Google Scholar
Rohr, J. R., Swan, A., Raffel, T. R. and Hudson, P. J. (2009). Parasites, info-disruption, and the ecology of fear. Oecologia 159, 447–454.Google Scholar
Rohr, J. R., Raffel, T. R. and Hall, C. A. (2010). Developmental variation in resistance and tolerance in a multi-host–parasite system. Functional Ecology 24, 1110–1121.Google Scholar
Rohr, J. R., Civitello, D. J., Crumrine, P. W., Halstead, N. T., Miller, A. D., Schotthoefer, A. M., Stenoien, C., Johnson, L. B. and Beasley, V. R. (2015). Predator diversity, intraguild predation, and indirect effects drive parasite transmission. Proceedings of the National Academy of Sciences of the United States of America 112, 3008–3013.Google Scholar
Saino, N., Moller, A. P. and Bolzern, A. M. (1995). Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rustica): an experimental test of the immunocompetence hypothesis. Behavioral Ecology 6, 397–404.CrossRefGoogle Scholar
Sapp, K. K. and Esch, G. W. (1994). The effects of spatial and temporal heterogeneity as structuring forces for parasite communities in Helisoma anceps and Physa gyrina . American Midland Naturalist 132, 91–103.Google Scholar
Schell, S. C. (1985). Handbook of Trematodes of North America north of Mexico. University Press of Idaho, Moscow, Idaho.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.Google Scholar
Skelly, D. K., Bolden, S. R., Holland, M. P., Freidenburg, L. K., Friedenfelds, N. A. and Malcolm, T. R. (2006). Urbanization and disease in amphibians. In Disease Ecology: Community Structure and Pathogen Dynamics (ed. Collinge, S. K. and Ray, C.), pp. 153–167. Oxford University Press, Cary, NC.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.Google Scholar
Tarr, T. L. and Babbitt, K. J. (2002). Effects of habitat complexity and predator identity on predation of Rana clamitans larvae. Amphibia-Reptilia 23, 13–20.Google Scholar
Thiemann, G. W. and Wassersug, R. J. (2000). Patterns and consequences of behavioural responses to predators and parasites in Rana tadpoles. Biological Journal of the Linnean Society 71, 513.Google Scholar
Tkach, V. V., Littlewood, D. T. J., Olson, P. D., Kinsella, J. M. and Swiderski, Z. (2003). Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 1–15.Google Scholar
Vaughn, C. C. and Taylor, C. M. (2000). Macroecology of a host-parasite relationship. Ecography 23, 11–20.CrossRefGoogle Scholar
Vonesh, J. R. and De la Cruz, O. (2002). Complex life cycles and density dependence: assessing the contribution of egg mortality to amphibian declines. Oecologia 133, 325–333.Google Scholar
Warkentin, K. M. (1992). Microhabitat use and feeding rate variation in green frog tadpoles (Rana clamitans). Copeia 1992, 731–740.Google Scholar
Werner, E. E., Skelly, D. K., Relyea, R. A. and Yurewicz, K. L. (2007). Amphibian species richness across environmental gradients. Oikos 116, 1697–1712.Google Scholar
Werner, E. E., Relyea, R. A., Yurewicz, K. L., Skelly, D. K. and Davis, C. J. (2009). Comparative landscape dynamics of two anuran species: climate-driven interaction of local and regional processes. Ecological Monographs 79, 503–521.Google Scholar
Wilson, D. S., Muzzall, P. M. and Ehlinger, T. J. (1996). Parasites, morphology, and habitat use in a bluegill sunfish (Lepomis macrochirus) population. Copeia 1996, 348–354.CrossRefGoogle Scholar
Wojdak, J. M., Edman, R. M., Wyderko, J. A., Zemmer, S. A. and Belden, L. K. (2014). Host density and competency determine the effects of host diversity on trematode parasite infection. PLoS ONE 9, e105059.Google Scholar
Zellmer, A. J., Richards, C. L. and Martens, L. M. (2008). Low prevalence of Batrachochytrium dendrobatidis across Rana sylvatica populations in southeastern Michigan, USA. Herpetological Review 39, 196–199.Google Scholar
Zelmer, D. A. and Arai, H. P. (1998). The contributions of host age and size to the aggregated distribution of parasites in yellow perch, Perca flavescens, from Garner Lake, Alberta, Canada. Journal of Parasitology 84, 24–28.Google Scholar
Zimmermann, M. R., Luth, K. E. and Esch, G. W. (2016). Microhabitat differences in the benthic substrata affect parasitism in a pulmonate snail host, Helisoma anceps . Journal of Parasitology 102, 306–311.CrossRefGoogle Scholar
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