Skip to main content Accessibility help
×
Home

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

  • JOHN A. MARINO (a1), MANJA P. HOLLAND (a1) and EARL E. WERNER (a1)

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.

Copyright

Corresponding author

*Corresponding author: Department of Biology, Bradley University, 06 Olin Hall, 1501 W. Bradley Ave., Peoria, IL 61625, USA. E-mail: jmarino@fsmail.bradley.edu

References

Hide All
Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. and Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters 9, 467484.
Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219247.
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. 7586. University California Press, Berkeley.
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, 289301.
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, 575583.
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, 511518.
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, 611620.
DeWitt, R. M. (1955). The ecology and life history of the pond snail Physa gyrina . Ecology 36, 4044.
Dobson, A. P. and Hudson, P. J. (1986). Parasites, disease and the structure of ecological communities. Trends in Ecology & Evolution 1, 1115.
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.
Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183190.
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, 122130.
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, 21582162.
Holland, M. P. (2010). Echinostome-induced mortality varies across amphibian species in the field. Journal of Parasitology 96, 851855.
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, 455462.
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, 10491058.
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, 288292.
Hudson, P., Dobson, A. P. and Newborn, D. (1998). Prevention of population cycles by parasite removal. Science 282, 22562258.
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, 90069011.
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, 230233.
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. 129. Kluwer Academic Publishers, Boston, Massachusetts, USA.
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, 724734.
Kiesecker, J. M. and Skelly, D. K. (2000). Choice of oviposition site by gray treefrogs: the role of potential parasitic infection. Ecology 81, 29392943.
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.
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, 16231629.
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, 641649.
Koprivnikar, J., Redfern, J. C. and Mazier, H. L. (2014). Variation in anti-parasite behaviour and infection among larval amphibian species. Oecologia 174, 11791185.
Lemly, A. and Esch, G. (1984). Population biology of the trematode Uvulifer ambloplitis (Hughes, 1927). Journal of Parasitology 70, 461465.
Marino, J. A. and Werner, E. E. (2013). Synergistic effects of predators and trematode parasites on larval green frog (Rana clamitans) survival. Ecology 94, 26972708.
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, 451460.
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, 621632.
May, R. M. and Anderson, R. M. (1978). Regulation and stability of host-parasite population interactions: II. Destabilizing processes. Journal of Animal Ecology 47, 249267.
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.
Minchella, D. J. and Scott, M. E. (1991). Parasitism: a cryptic determinant of animal community structure. Trends in Ecology & Evolution 6, 250254.
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, 29312940.
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, 5158.
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, 7582.
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.
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, 3749.
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, 19001907.
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, 10311042.
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, 854863.
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, 7082.
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, 12351239.
Rohr, J. R., Swan, A., Raffel, T. R. and Hudson, P. J. (2009). Parasites, info-disruption, and the ecology of fear. Oecologia 159, 447454.
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, 11101121.
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, 30083013.
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, 397404.
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, 91103.
Schell, S. C. (1985). Handbook of Trematodes of North America north of Mexico. University Press of Idaho, Moscow, Idaho.
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, 475482.
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. 153167. Oxford University Press, Cary, NC.
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, 17831786.
Tarr, T. L. and Babbitt, K. J. (2002). Effects of habitat complexity and predator identity on predation of Rana clamitans larvae. Amphibia-Reptilia 23, 1320.
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.
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, 115.
Vaughn, C. C. and Taylor, C. M. (2000). Macroecology of a host-parasite relationship. Ecography 23, 1120.
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, 325333.
Warkentin, K. M. (1992). Microhabitat use and feeding rate variation in green frog tadpoles (Rana clamitans). Copeia 1992, 731740.
Werner, E. E., Skelly, D. K., Relyea, R. A. and Yurewicz, K. L. (2007). Amphibian species richness across environmental gradients. Oikos 116, 16971712.
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, 503521.
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, 348354.
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.
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, 196199.
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, 2428.
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, 306311.

Keywords

Type Description Title
WORD
Supplementary materials

Marino supplementary material
Table S1 and Fig. S1

 Word (573 KB)
573 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed