Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-28T04:31:20.709Z Has data issue: false hasContentIssue false

Abiotic versus biotic hierarchies in the assembly of parasite populations

Published online by Cambridge University Press:  22 December 2009

T. K. ANDERSON*
Affiliation:
Graduate Program in Ecology and Evolution, Rutgers University, 14 College Farm Road, New Brunswick, NJ08901, USA
M. V. K. SUKHDEO
Affiliation:
Department of Ecology, Evolution and Natural Resources, Rutgers University, 14 College Farm Road, New Brunswick, NJ08901, USA
*
*Corresponding author: 1656 Linden Drive, University of Wisconsin–Madison, Madison, WI53706, USA. Tel: +608 890 3156. Fax: +608 262 7420. E-mail: [email protected]

Summary

The presence or absence of parasites within host populations is the result of a complex of factors, both biotic and abiotic. This study uses a non-parametric classification tree approach to evaluate the relative importance of key abiotic and biotic drivers controlling the presence/absence of parasites with complex life cycles in a sentinel, the common killifish Fundulus heteroclitus. Parasite communities were classified from 480 individuals representing 15 fish from 4 distinct marsh sites in each of 4 consecutive seasons between 2006 and 2007. Abiotic parameters were recorded at continuous water monitoring stations located at each of the 4 sites. Classification trees identified the presence of benthic invertebrate species (Gammarus sp. and Littorina sp.) as the most important variables in determining parasite presence: secondary splitters were dominated by abiotic variables including conductance, pH and temperature. Seventy percent of hosts were successfully classified into the correct category (infected/uninfected) based on only these criteria. The presence of competent definitive hosts was not considered to be an important explanatory variable. These data suggest that the most important determinant of the presence of these parasite populations in the common killifish is the availability of diverse communities of benthic invertebrates.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Allesina, S. and Pascual, M. (2008). Network structure, predator-prey modules, and stability in large food webs. Journal of Theoretical Ecology 1, 5564.Google Scholar
Allison, G. (2004). The influence of species diversity and stress intensity on community resistance and resilience. Ecological Monographs 74, 117134.CrossRefGoogle Scholar
Anderson, R. C., Chabaud, A. G. and Willmott, S. (1974). CIH Keys to the Nematode Parasites of Vertebrates. Commonwealth Agricultural Bureaux, England.Google Scholar
Bagge, A. M., Poulin, R. and Valtonen, E. T. (2004). Fish population size, and not density, as the determining factor of parasite infection: a case study. Parasitology 128, 305313.Google Scholar
Biserkov, V. and Kostadinova, A. (1998). Intestinal helminth communities in the green lizard, Lacerta viridis, from Bulgaria. Journal of Helminthology 72, 267271.CrossRefGoogle ScholarPubMed
Bragin, A. B., Misuik, J., Woolcott, C. A., Barrett, K. R. and Jusino-Atresino, R. J. (2005). A Fisheries Resource Inventory of the Lower Hackensack River Within the Hackensack Meadowlands District. New Jersey Meadowlands Commission: Meadowlands Environmental Research Institute, New Jersey, USA.Google Scholar
Breiman, L., Friedman, J. H., Olshen, R. A. and Stone, C. G. (1984). Classification and Regression Trees. Wadsworth International Group, California, USA.Google Scholar
Brown, J. H. (1995). Macroecology. University of Chicago Press, Chicago, USA.Google Scholar
Bush, A. O. and Holmes, J. C. (1986). Intestinal helminthes of lesser scaup ducks: source communities. Canadian Journal of Zoology 71, 13581363.Google Scholar
Byrnes, J. E., Stachowicz, J. J., Hultgren, K., Hughes, A. R., Olyarnik, S. V. and Thornber, C. S. (2006). Predator diversity enhances kelp forest trophic cascades by modifying herbivore behavior. Ecology Letters 9, 6171.Google Scholar
Chubb, J. C. (1963). On the characterization of the parasite fauna of the fish of Lynn Tegid. Proceedings of the Zoological Society of London 141, 609621.Google Scholar
Chubb, J. C. (1979). Seasonal occurence of helminths in freshwater fishes. Advances in Parasitology 17, 141313.CrossRefGoogle Scholar
Combes, C. (2001). Parasitism: the Ecology and Evolution of Intimate Interactions, 1st Edn.The University of Chicago Press, London, UK.Google Scholar
De'Ath, G. and Fabricius, K. E. (2000). Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81, 31783192.Google Scholar
Duffy, J. E., Richardson, J. P. and Canuel, E. A. (2003). Grazer diversity effects on ecosystem functioning in seagrass beds. Ecology Letters 6, 637645.Google Scholar
Esch, G. W. (1971). Impact of ecological succession on the parasite fauna in centrarchids from oligotrophic and eutrophic systems. American Midland Naturalist 86, 160168.CrossRefGoogle Scholar
Esch, G. W., Hazen, T. C., Marcogliese, D. J., Goater, T. M. and Crews, A. E. (1986). A long-term study on the population biology of Crepidostomum cooperi (Trematoda: Allocreadidae) in the burrowing mayfly, Hexagenia limbata (Emphemeroptera). American Midland Naturalist 116, 304314.CrossRefGoogle Scholar
Esch, G. W., Kennedy, C. R., Bush, A. O. and Aho, J. M. (1988). Patterns of helminth communities in freshwater fish in Great Britain: alternative strategies for colonization. Parasitology 96, 519532.Google Scholar
Galaktionov, K. V. (1993). Life cycles and distribution of seabird helminthes in Arctic and sub-arctic regions. Bulletin of the Scandinavian Society of Parasitology 6, 3149.Google Scholar
Gasith, A. and Resh, V. H. (1999). Streams in Mediterranean climate regions: abiotic influences and biotic responses to predictable seasonal events. Annual Review of Ecology and Systematics 30, 5181.Google Scholar
Harris, C. E. and Vogelbein, W. K. (2006). Parasites of mummichogs, Fundulus heteroclitus, from the York River, Virginia, U.S.A., with a checklist of parasites of Atlantic Coast Fundulus spp. Comparative Parasitology 73, 72–110.CrossRefGoogle Scholar
Hart, D. D. and Finelli, C. M. (1999). Physical-biological coupling in streams: the pervasive effects of flow on benthic organisms. Annual Review of Ecology and Systematics 30, 363395.CrossRefGoogle Scholar
Hechinger, R. F. and Lafferty, K. D. (2005). Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society of London, B 272, 10591066.Google ScholarPubMed
Hechinger, R. F., Lafferty, K. D., Huspeni, T. C., Brooks, A. J. and Kuris, A. M. (2007). Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and fishes. Oecologia 151, 8292.CrossRefGoogle ScholarPubMed
Holmes, J. C. (1990). Helminth communities in marine fishes. In Parasite Communities: Patterns and Processes (ed. Esch, G., Bush, A. O. and Aho, J.),pp.101113. Chapman and Hall, New York, USA.Google Scholar
Hudson, P. J., Dobson, A. P. and Lafferty, K. D. (2006). Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 21, 381385.CrossRefGoogle Scholar
Huspeni, T. C. and Lafferty, K. D. (2004). Using larval trematodes that parasitize snails to evaluate a saltmarsh restoration project. Ecological Applications 14, 795804.CrossRefGoogle Scholar
Hutchinson, G. E. (1959). Homage to Santa Rosalia, or, why are there so many kinds of animals? American Naturalist 93, 145159.Google Scholar
Janovy, J., Snyder, S. D. and Clopton, R. E. (1997). Evolutionary constraints on population structure: the parasites of Fundulus zebrinus (Pisces: Cyprinodontidae) in the South Platte River of Nebraska. Journal of Parasitology 83, 584592.CrossRefGoogle ScholarPubMed
Karvonen, A., Paukku, S., Valtonen, E. T. and Hudson, P. J. (2003). Transmission, infectivity and survival of Diplostomum spathaceum cercariae. Parasitology 127, 217224.CrossRefGoogle ScholarPubMed
Kennedy, C. R. (1978). An analysis of the metazoan parasitocoenoses of brown trout Salmo trutta from British lakes. Journal of Fish Biology 13, 255263.CrossRefGoogle Scholar
Kennedy, C. R. and Bush, A. O. (1994). The relationship between pattern and scale in parasite communities: a stranger in a strange land. Parasitology 109, 187196.Google Scholar
Khan, R. A. and Thulin, J. (1991). Influence of pollution on parasites of aquatic animals. Advances in Parasitology 30, 201238.Google Scholar
Lafferty, K. D., Allesina, S., Arim, M., Briggs, C. J., DeLeo, G., Dobson, A. P., Dunne, J. A., Johnson, P. T. J., Kuris, A. M., Marcogliese, D. J., Martinez, N. D., Memmott, J., Marquet, P. A., McLaughlin, J. P., Mordecai, E. A., Pascual, M., Poulin, R. and Thieltges, D. W. (2008). Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533546.Google Scholar
Lawlor, L. R. (1980). Structure and stability in natural and randomly constructed competitive communities. American Naturalist 116, 394408.Google Scholar
Levin, S. A. (1999). Fragile Dominion: Complexity and the Commons. Perseus Books, Reading, MA, USA.Google Scholar
Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J. P., Hector, A., Hooper, D. U., Huston, M. A., Raffaelli, D., Schmid, B., Tilman, D. and Wardle, D. A. (2001). Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804808.CrossRefGoogle ScholarPubMed
Lotrich, V. A. (1975). Summer home range and movements of Fundulus heteroclitus (Pisces: Cyprinodontidae) in a tidal creek. Ecology 56, 191198.CrossRefGoogle Scholar
MacArthur, R. H. (1955). Fluctuation of animal populations and a measure of community stability. Ecology 36, 533536.CrossRefGoogle Scholar
MacArthur, R. H. and Levins, R. (1967). The limiting similarity, convergence, and divergence of coexisting species. American Naturalist 101, 377385.CrossRefGoogle Scholar
MacKenzie, K., Williams, H. H., Williams, B., McVicar, A. H. and Sidall, R. (1995). Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Advances in Parasitology 35, 85–114.Google Scholar
Marcogliese, D. J. (2001). Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 13311352.Google Scholar
Marcogliese, D. J. (2002). Food webs and the transmission of parasites to marine fish. Parasitology 124 (Suppl.), S83S99.Google Scholar
Marcogliese, D. J. (2004). Parasites: small players with crucial roles in the ecological theatre. EcoHealth 1, 151164.Google Scholar
Marcogliese, D. J. (2005). Parasites of the superorganism: are they indicators of ecosystem health? International Journal for Parasitology 35, 705716.Google Scholar
Marcogliese, D. J. and Cone, D. K. (1996). On the distribution and abundance of eel parasites in Nova Scotia: influences of pH. Journal of Parasitology 82, 389399.Google Scholar
Marcogliese, D. J. and Cone, D. K. (1997). Food webs: a plea for parasites. Trends in Ecology and Evolution 12, 320325.Google Scholar
Marcogliese, D. J. and Cone, D. K. (1998). Comparison of richness and diversity of macroparasite communities among eels from Nova Scotia, the United Kingdom and Australia. Parasitology 116, 7383.Google Scholar
Marcogliese, D. J., Dumont, P., Gendron, A. D., Mailhot, Y., Bergeron, E. and McLaughlin, J. D. (2001). Spatial and temporal variation in abundance of Diplostomum spp. in walleye (Stizostedion vitreum) and white suckers (Catstomus commersoni) from the St. Lawrence River. Canadian Journal of Zoology 79, 355369.CrossRefGoogle Scholar
Marcogliese, D. J., Goater, T. M. and Esch, G. W. (1990). Crepidostomum cooperi (Allocreadidae) in the burrowing mayfly, Hezagenia limbata (Ephemeroptera) related to the trophic status of a lake. American Midland Naturalist 124, 309317.Google Scholar
McCune, B. and Grace, J. B. (2002). Analysis of Ecological Communities. MjM Software Design, Gleneden Beach, USA.Google Scholar
Moller, H. (1987). Pollution and parasitism in the aquatic environment. International Journal for Parasitology 17, 353361.Google Scholar
Murdoch, W. W., Evans, F. C. and Peterson, C. H. (1972). Diversity and pattern in plants and insects. Ecology 53, 819829.Google Scholar
Naeem, S. and Li, S. (1997). Biodiversity enhances ecosystem reliability. Nature, London 390, 507509.CrossRefGoogle Scholar
Ondrackova, M., Simkova, A., Gelnar, M. and Jurajda, P. (2004). Posthodiplostomum cuticola (Digenea: Diplostomatidae) in intermediate fish hosts: factors contributing to the parasite infection and prey selection by the definitive bird host. Parasitology 129, 761770.CrossRefGoogle Scholar
Paine, R. T. (1966). Food web complexity and species diversity. American Naturalist 100, 6575.Google Scholar
Poulin, R. (1992). Toxic pollution and parasitism in freshwater fish. Parasitology Today 8, 5861.CrossRefGoogle ScholarPubMed
Poulin, R. (2007). Evolutionary Ecology of Parasites. Princeton University Press, Princeton, NJ, USA.Google Scholar
Relyea, K. (1983). A systematic study of two species complexes of the genus Fundulus (Pisces: Cyprinodontidae). Bulletin of the Florida State Museum, Biological Sciences 29, 164.Google Scholar
Rohde, K. (1993). Ecology of Marine Parasites, 2nd Edn.CAB International, Bristol, UK.CrossRefGoogle Scholar
Rosenzweig, M. L. (1995). Species Diversity in Space and Time. Cambridge University Press, Cambridge, UK.Google Scholar
Rothwell, J. J., Futter, M. N. and Dise, N. B. (2008). A classification and regression tree model of controls on dissolved inorganic nitrogen leaching from European forests. Environmental Pollution 156, 544552.Google Scholar
Sala, E. and Knowlton, N. (2006). Global marine biodiversity trends. Annual Review of Environment and Resources 31, 93–122.CrossRefGoogle Scholar
Sandland, G. J., Goater, C. P. and Danylchuk, A. J. (2001). Population dynamics of Ornithodiplostomum ptychocheilus metacercaria in fathead minnows (Pimephales promelas) from four northern-Alberta lakes. Journal of Parasitology 87, 744748.CrossRefGoogle ScholarPubMed
Schell, S. C. (1970). The Trematodes. Wm. C. Brown Company, Dubuque, Iowa, USA.Google Scholar
Schmidt, G. D. (1970). The Tapeworms. Wm. C. Brown Company, Dubuque, Iowa, USA.Google Scholar
Seigel, A. B. (2006). Avian Response to Urban Tidal Marsh Restoration. Masters thesis, Rutgers University, New Brunswick, NJ, USA.Google Scholar
Seigel, A. B., Hatfield, C. and Hartman, J. M. (2005). Avian response to restoration of urban tidal marshes in the Hackensack Meadowlands, New Jersey. Urban Habitats 3, 87–116.Google Scholar
Simkova, A., Sitko, J., Okulewicz, J. and Morand, S. (2003). Occurrence of intermediate hosts and structure of digenean communities of the black-headed gull, Larus ridibundus (L.). Parasitology 126, 6978.CrossRefGoogle ScholarPubMed
Smith, N. F. (2001). Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts. Oecologia 127, 115122.Google Scholar
Stables, J. N. and Chappell, L. H. (1986). Diplostomum spathaceum (Rud. 1819): effects of physical factors on the infection of rainbow trout (Salmo gairdneri) by cercariae. Parasitology 93, 7179.CrossRefGoogle ScholarPubMed
Stachowicz, J. J., Fried, H., Osman, R. W. and Whitlack, R. B. (2002). Biodiversity, invasion resistance, and marine ecosystem function: reconciling pattern and process. Ecology 83, 25752590.Google Scholar
Sukhdeo, M. V. K. and Hernandez, A. D. (2005). Food web patterns and the parasite's perspective. In Parasitism and Ecosystems (ed. Thomas, F., Guegan, J. F. and Renaud, F.),pp.5467. Oxford University Press, Oxford, UK.Google Scholar
Thang, N. D., Erhart, A., Speybroeck, N., Hung, L. X., Thuan, L.K, Hung, C. T., Ky, P. V., Coosemans, M. and D'Alessandro, U. (2008). Malaria in central Vietnam: analysis of risk factors by multivariate analysis and classification tree models. Malaria Journal 7, 28.Google Scholar
Tilman, D., Reich, P. and Knops, J. M. (2006). Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature, London 441, 629632.Google Scholar
Valtonen, E. T., Holmes, J. C. and Koskivaara, M. (1997). Eutrophication, pollution, and fragmentation: effects on parasite communities in roach (Rutilus rutilus) and perch (Perca fluviatilis) in four lakes in central Finland. Canadian Journal of Fisheries and Aquatic Sciences 54, 572585.CrossRefGoogle Scholar
Whittaker, R. H. (1972). Evolution and measurement of species diversity. Taxon 21, 213251.Google Scholar
Whittaker, R. H. (1975). Communities and Ecosystems, 2nd Edn.Macmillan. New York, NY, USA.Google Scholar
Wilson, J. B., Gitay, H. and Agnew, A. D. Q. (1987). Does niche limitation exist? Functional Ecology 1, 391397.Google Scholar
Wisniewski, W. L. (1958). Characterization of the parasitofauna of an eutrophic lake. Acta Parasitologica Polonica 6, 164.Google Scholar
Yachi, S. and Loreau, M. (1999). Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proceedings of the National Academy of Sciences, USA 96, 14631468.Google Scholar
Yamaguti, S. (1958). Systema Helminthum: the Digenetic Trematodes of Vertebrates. Interscience Publishers, New York, USA.Google Scholar
Yuhas, C. E. (2001). Benthic Communities in Spartina alterniflora and Phragmites australis Dominated Salt Marshes. Masters thesis, New Jersey Institute of Technology/Rutgers University, New Brunswick, NJ, USA.Google Scholar
Yuhas, C. E., Hartman, J. M. and Weis, J. S. (2005). Benthic communities in Spartina alterniflora and Phragmites australis dominated salt marshes in the Hackensack Meadowlands, New Jersey. Urban Habitats 3, 158191.Google Scholar
Zander, C. D. and Reimer, L. W. (2002). Parasitism at the ecosystem level in the Baltic Sea. Parasitology 124, S119S135.CrossRefGoogle ScholarPubMed