Skip to main content

Parasite abundance decreases with host density: evidence of the encounter-dilution effect for a parasite with a complex life cycle

Abstract

The relationship between host density and parasitism depends on a parasite’s life history. The abundance of a directly transmitted contagious parasite should increase with host density, whereas the abundance of a directly transmitted parasite that seeks its host might decrease due to the encounter-dilution effect. For parasites with complex life cycles, previous studies have found no association between parasite abundance and host density. We tested the relationship between host density and metacercarial abundance of a trematode parasite (Posthodiplostomum minimum) in two species of centrarchid fishes (Lepomis macrochirus and L. auritus) from eight small creeks. We found that host density was negatively associated with parasite abundance. Thus, our study represents the first evidence of the encounter-dilution effect for a parasite with complex life cycle in a natural system. We also report a positive association between total P. minimum population abundance and Lepomis spp. density, indicating that at low host density, cercarial mortality could moderate the encounter-dilution effect.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Anderson, R. M., 1978. Population dynamics of snail infection by miracidia. Parasitology 77: 201–224.

    CAS  Article  PubMed  Google Scholar 

  • Anderson, R. M. & R. M. May, 1978. Regulation and stability of host-parasite population interactions: I. Regulatory processes. Journal of Animal Ecology 47: 219–247.

    Article  Google Scholar 

  • Anderson, S. M., R. A. Fiorillo, T. J. Cook & W. I. Lutterschmidt, 2015. Helminth parasites of two species of Lepomis (Osteichthyes: Centrarchidae) from an urban watershed and their potential use in environmental monitoring. Georgia Journal of Science 73: 123–135.

    Google Scholar 

  • Arneberg, P., 2001. An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence. Ecography 24: 352–358.

    Article  Google Scholar 

  • Arneberg, P., A. Skorping, B. Grenfell & A. F. Read, 1998. Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society B: Biological Sciences 265: 1283–1289.

    Article  PubMed Central  Google Scholar 

  • Avault Jr., J. W. & R. O. Smitherman, 1965. Experimental host specificity of Posthodiplostomum minimum. Experimental Parasitology 17: 268–270.

    Article  PubMed  Google Scholar 

  • Bedinger Jr., C. A. & T. G. Meade, 1967. Biology of a new cercaria for Posthodiplostomum minimum (Trematoda: Diplostomidae). The Journal of Parasitology 53: 985–988.

    Article  PubMed  Google Scholar 

  • Bush, A. O., K. D. Lafferty, J. M. Lotz & A. W. Shostak, 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83: 575–583.

    CAS  Article  PubMed  Google Scholar 

  • Christensen, N. O., P. Nansen & F. Frandsen, 1976. Molluscs interfering with the capacity of Fasciola hepatica miracidia to infect Lymnaea truncatula. Parasitology 73: 161–167.

    CAS  Article  PubMed  Google Scholar 

  • Côté, I. M. & R. Poulin, 1995. Parasitism and group-size in social animals: a metaanalysis. Behavioral Ecology 6: 159–165.

    Article  Google Scholar 

  • Crofton, H. D., 1971. A quantitative approach to parasitism. Parasitology 62: 179–193.

    Article  Google Scholar 

  • Dobson, A. P., 1990. Models for multi-species parasite-host communities. In Esch, G. W., A. O. Bush & J. M. Aho (eds), Parasite communities: patterns and processes. Chapman and Hall, London: 261–288.

    Chapter  Google Scholar 

  • Fauchald, P., R. Rodven, B.-J. Bardsen, K. Langeland, T. Tveraa, N. G. Yoccoz & R. A. Ims, 2007. Escaping parasitism in the selfish herd: age, size and density-dependent warble fly infestation in reindeer. Oikos 116: 491–499.

    Article  Google Scholar 

  • Ferguson, M. S., 1943. Experimental studies on the fish hosts of Posthodiplostomum minimum (Trematoda: Strigeida). The Journal of Parasitology 29: 350–353.

    Article  Google Scholar 

  • Hoffman, G. L., 1958. Experimental studies on the cercaria and metacercaria of a strigeoid trematode, Posthodiplostomum minimum. Experimental Parasitology 7: 23–50.

    CAS  Article  PubMed  Google Scholar 

  • Hoffman, G. L., 1967. Parasites of North American Freshwater Fishes. University of California Press, Berkeley.

    Google Scholar 

  • Hunter III, G. W. & W. S. Hunter, 1940. Studies on the development of the metacercaria and the nature of the cyst of Posthodiplostomum minimum (MacCallum 1921) (Trematoda; Strigeata). Transactions of the American Microscopical Society 59: 52–63.

    Article  Google Scholar 

  • Johnson, P. T. J., D. L. Preston, J. T. Hoverman, J. S. Henderson, S. H. Paull, K. L. D. Richgels & M. D. Redmond, 2012. Species diversity reduces parasite infection through cross-generational effects on host abundance. Ecology 93: 56–64.

    Article  PubMed  Google Scholar 

  • Klak, G. E., 1940. Neascus infestation of black-head, blunt-nosed, and other forage minnows. Transactions of the American Fisheries Society 69: 273–278.

    Article  Google Scholar 

  • Lane, B., T. Spier, J. Wiederholt & S. Meagher, 2015. Host specificity of a parasitic fluke: is Posthodiplostomum minimum a centrarchid-infecting generalist or specialist? The Journal of Parasitology 101: 6–17.

    Article  PubMed  Google Scholar 

  • Lutterschmidt, W. I., J. F. Schaefer & R. A. Fiorillo, 2007. The ecological significance of helminth endoparasites on the physiological performance of two sympatric fishes. Comparative Parasitology 74: 194–203.

    Article  Google Scholar 

  • Martin, S. L. & W. I. Lutterschmidt, 2013. A checklist to the common cyprinid and centrarchid fishes of the Bull and Upatoi creeks watershed of Georgia with a brief glimpse of correlative urban influences and land use. Southeastern Naturalist 12: 769–780.

    Article  Google Scholar 

  • May, R. M. & R. M. Anderson, 1978. Regulation and stability of host-parasite population interactions: II. Destabilizing processes. Journal of Animal Ecology 47: 249–267.

    Article  Google Scholar 

  • Mettee, M. F., P. E. O’Neil & J. M. Pierson, 1996. Fishes of Alabama and the Mobile Basin. Oxmoor House, Birmingham, Ala.

    Google Scholar 

  • Miller, J. H., 1954. Studies on the life history of Posthodiplostomum minimum (MacCallum 1921). The Journal of Parasitology 40: 255–270.

    CAS  Article  PubMed  Google Scholar 

  • Moore, J., D. Simberloff & M. Freehling, 1988. Relationships between bobwhite quail social-group size and intestinal helminth parasitism. American Naturalist 131: 22–32.

    Article  Google Scholar 

  • Mooring, M. S. & B. L. Hart, 1992. Animal grouping for protection from parasites: selfish herd and encounter-dilution effects. Behaviour 123: 173–193.

    Article  Google Scholar 

  • Page, L. M. & B. M. Burr, 1991. A Field Guide to Freshwater Fishes of North America North of Mexico. Houghton Mifflin Company, Boston, Massachusetts.

    Google Scholar 

  • Pflieger, W. L., 1997. The Fishes of Missouri. Missouri Dept. of Conservation, Jefferson City.

    Google Scholar 

  • Rifkin, J. L., C. L. Nunn & L. Z. Garamszegi, 2012. Do animals living in larger groups experience greater parasitism? A meta-analysis. American Naturalist 180: 70–82.

    Article  PubMed  Google Scholar 

  • Ross, S. T., 2002. Inland Fishes of Mississippi. University Press of Mississippi, Jackson.

    Google Scholar 

  • Sonnenholzner, J. I., K. D. Lafferty & L. B. Ladah, 2011. Food webs and fishing affect parasitism of the sea urchin Eucidaris galapagensis in the Galapagos. Ecology 92: 2276–2284.

    Article  PubMed  Google Scholar 

  • Strona, G. & K. D. Lafferty, 2012. How to catch a parasite: Parasite Niche Modeler (PaNic) meets Fishbase. Ecography 35: 481–486.

    Article  Google Scholar 

  • Stumbo, A. D., C. T. James, C. P. Goater & B. D. Wisenden, 2012. Shoaling as an antiparasite defence in minnows (Pimephales promelas) exposed to trematode cercariae. Journal of Animal Ecology 81: 1319–1326.

    Article  PubMed  Google Scholar 

  • Turner, G. F. & T. J. Pitcher, 1986. Attack abatement: a model for group protection by combined avoidance and dilution. The American Naturalist 128: 228–240.

    Article  Google Scholar 

Download references

Acknowledgments

We thank S.M. Anderson, R.A. Fiorillo L. Dent, D.S. Millican, and D.K. Wasco for assistance related to this research. We thank K.D. Lafferty, A.M. Kuris, A. Smith-Herron, T.J. Cook, and two anonymous reviewers for useful discussions and comments on the manuscript. This work was supported by a grant from the Engineer Research and Development Center (ERDC) and the Civil Engineering Research Lab (CERL) of the US Army Corps of Engineers (ERDC-CERL Contract #DACA 42-00-C-0047) to W.I.L. We acknowledge the assistance provided by Gordon A. Plishker and all personnel of the Texas Research Institute for Environmental Studies (TRIES) at Sam Houston State University. We also thank Hugh Westbury of the Strategic Environmental Research and Development Program (SERDP), Ecosystem Management Project (SEMP), and Harold (Hal) Balbach of the US Army ERDC and CERL for their sincere interest in and support of this project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julia C. Buck.

Additional information

Handling editor: Lee B. Kats.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Buck, J.C., Lutterschmidt, W.I. Parasite abundance decreases with host density: evidence of the encounter-dilution effect for a parasite with a complex life cycle. Hydrobiologia 784, 201–210 (2017). https://doi.org/10.1007/s10750-016-2874-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-016-2874-8

Keywords

  • Encounter-dilution
  • Lepomis
  • Posthodiplostomum minimum
  • Sunfish
  • Trematode