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Small alteration – big impacts: effects of small-scale riparian forest management on host–parasite dynamics in streams

Published online by Cambridge University Press:  18 January 2017

C. Lagrue*
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand
A.A. Besson
Affiliation:
Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand
A. Lecerf
Affiliation:
CNRS, INP, UPS, EcoLab – Université de Toulouse, 118 Route de Narbonne, 31062 Toulouse, France
*
*Fax: +64 3 479 7584 E-mail: clement.lagrue@gmail.com

Abstract

Environmental changes and ecological disturbances can have large and unpredictable effects on parasite dynamics. Increasing human impacts on freshwater ecosystems through land use may thus modify the distribution and abundance of parasites and have cascading effects on host populations. Here we tested the effects of small-scale riparian forest management on the nematode Cystidicoloides ephemeridarum and its insect intermediate host Ephemera danica in forested streams. We assessed the impacts of harvesting riparian trees on parasite prevalence and abundance concomitantly with host densities. We also looked at upstream and downstream reaches to document potential cascading effects on unaltered stream sections mediated by aerial dispersal of adult mayfly or downstream drift of E. danica larvae. We show that host densities and parasite levels (prevalence and abundance) increased significantly following riparian tree removal. Overall, parasite densities showed a 6- to 66-fold increase in harvested reaches compared to upstream, pristine reaches. Similar effects were also clear downstream of the disturbance. Thus, despite the small extent of riparian forest alteration along the study streams, both parasite and intermediate host were strongly affected. Small-scale riparian forest management may thus have large, unforeseen impacts on some aspects of freshwater ecosystem structure and functioning that are often ignored. Generally, understanding how human perturbations influence parasites is vital when trying to predict overall impacts on ecosystem structure and functioning, and how changes in infection dynamics may further affect host species.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

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References

Aho, J.M. & Kennedy, C.R. (1984) Seasonal population dynamics of the nematode Cystidicoloides tenuissima (Zeder) from the River Swincombe, England. Journal of Fish Biology 25, 473489.CrossRefGoogle Scholar
Aho, J.M. & Kennedy, C.R. (1987) Circulation pattern and transmission dynamics of the supra-population of the nematode Cystidicoloides tenuissima (Zeder) in the River Swincombe, England. Journal of Fish Biology 31, 123141.CrossRefGoogle Scholar
Arneberg, P., Skorping, A., Grenfell, B. & Read, A.F. (1998) Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London B: Biological Sciences 265, 12831289.CrossRefGoogle Scholar
Blanar, C.A., Munkittrick, K.R., Houlahan, J., MacLatchy, D.L. & Marcogliese, D.J. (2009) Pollution and parasitism in aquatic animals: a meta-analysis of effect size. Aquatic Toxicology 93, 1828.Google Scholar
Blasco-Costa, I., Koehler, A.V., Martin, A. & Poulin, R. (2013) Upstream–downstream gradient in infection levels by fish parasites: a common river pattern? Parasitology 140, 266274.Google Scholar
Brittain, J.E. (1982) Biology of mayflies. Annual Review of Entomology 27, 119147.CrossRefGoogle Scholar
Broadmeadow, S. & Nisbet, T.R. (2004) The effects of riparian forest management on the freshwater environment: a literature review of best management practice. Hydrology and Earth System Sciences Discussions 8, 286305.CrossRefGoogle Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Cézilly, F., Thomas, F., Médoc, V. & Perrot-Minnot, M.-J. (2010) Host-manipulation by parasites with complex life cycles: adaptive or not? Trends in Parasitology 26, 311317.CrossRefGoogle ScholarPubMed
Combes, C. (1996) Parasites, biodiversity and ecosystem stability. Biodiversity and Conservation 5, 953962.Google Scholar
Delettre, Y.R. & Morvan, N. (2000) Dispersal of adult Chironomidae (Diptera) in agricultural landscapes. Freshwater Biology 44, 399411.CrossRefGoogle Scholar
De Nadaï-Monoury, E., Gilbert, F. & Lecerf, A. (2014) Forest canopy cover determines invertebrate diversity and ecosystem process rates in depositional zones of headwater streams. Freshwater Biology 59, 15321545.CrossRefGoogle Scholar
Dobson, A. & Foufopoulos, J. (2001) Emerging infectious pathogens of wildlife. Philosophical Transactions of the Royal Society of London B: Biological Sciences 356, 10011012.CrossRefGoogle ScholarPubMed
Evangelista, C., Boiche, A., Lecerf, A. & Cucherousset, J. (2014) Ecological opportunities and intraspecific competition alter trophic niche specialization in an opportunistic stream predator. Journal of Animal Ecology 83, 10251034.CrossRefGoogle Scholar
Frantova, D. & Moravec, F. (2003) Ultrastructure of the body wall of Cystidicoloides ephemeridarum (Nematoda, Cystidicolidae) in relation to the histopathology of this nematode in salmonids. Parasitology Research 91, 100108.CrossRefGoogle Scholar
Gyselman, E.C. (1980) The mechanisms that maintain population stability of selected species of Ephemeroptera in a temperate stream. pp. 309319 in Flannagan, J.F. & Marshall, K.E. (Eds) Advances in Ephemeroptera biology. New York, USA, Springer US.Google Scholar
Hauer, F.R. & Lamberti, G.A. (2011) Methods in stream ecology. San Diego, USA, Academic Press.Google Scholar
Holmes, J.C. (1996) Parasites as threats to biodiversity in shrinking ecosystems. Biodiversity & Conservation 5, 975983.CrossRefGoogle Scholar
Holt, R.D. & Roy, M. (2007) Predation can increase the prevalence of infectious disease. The American Naturalist 169, 690699.CrossRefGoogle ScholarPubMed
Hubbard, M.D. (1991) Theoretical and practical problems involved in determination of upstream flight compensation in lotic aquatic insects. pp. 359365 in Campell, I. (Ed.) Overview and strategies of Ephemeroptera and Plecoptera. Dordrecht, The Netherlands, Kluwer Academic Publishers.Google Scholar
Hudson, P.J., Dobson, A.P. & Lafferty, K.D. (2006) Is a healthy ecosystem one that is rich in parasites? Trends in Ecology & Evolution 21, 381385.CrossRefGoogle Scholar
Johnson, P.T. & Chase, J.M. (2004) Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecology Letters 7, 521526.CrossRefGoogle Scholar
Johnson, P.T., Chase, J.M., Dosch, K.L., Hartson, R.B., Gross, J.A., Larson, D.J., Sutherland, D.R. & Carpenter, S.R. (2007) Aquatic eutrophication promotes pathogenic infection in amphibians. Proceedings of the National Academy of Sciences, USA 104, 1578115786.CrossRefGoogle Scholar
Khan, R.A. & Hooper, R.G. (2007) Influence of a thermal discharge on parasites of a cold-water flatfish, Pleuronectes americanus, as a bioindicator of subtle environmental change. Journal of Parasitology 93, 12271230.CrossRefGoogle ScholarPubMed
Knudsen, R., Amundsen, P.A., Nilsen, R., Kristoffersen, R. & Klemetsen, A. (2008) Food borne parasites as indicators of trophic segregation between Arctic charr and brown trout. Environmental Biology of Fishes 83, 107116.CrossRefGoogle Scholar
Koprivnikar, J., Marcogliese, D.J., Rohr, J.R., Orlofske, S.A., Raffel, T.R. & Johnson, P.T. (2012) Macroparasite infections of amphibians: what can they tell us? EcoHealth 9, 342360.Google Scholar
Lafferty, K.D. (1997) Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitology Today 13, 251255.Google Scholar
Lafferty, K.D. (2008) Ecosystem consequences of fish parasites. Journal of Fish Biology 73, 20832093.CrossRefGoogle Scholar
Lafferty, K.D. & Holt, R.D. (2003) How should environmental stress affect the population dynamics of disease? Ecology Letters 6, 654664.Google Scholar
Lafferty, K.D. & Kuris, A.M. (1999) How environmental stress affects the impacts of parasites. Limnology and Oceanography 44, 925931.CrossRefGoogle Scholar
Lafferty, K.D. & Kuris, A.M. (2005) Parasitism and environmental disturbances. pp. 113123 in Thomas, F., Guégan, J.F. & Renaud, F. (Eds) Parasitism and ecosystems. Oxford, Oxford University Press.Google Scholar
Lagrue, C., Kaldonski, N., Perrot-Minnot, M.-J., Motreuil, S. & Bollache, L. (2007) Modification of hosts’ behavior by a parasite: field evidence for adaptive manipulation. Ecology 88, 28392847.Google Scholar
Lagrue, C., Kominoski, J.S., Danger, M., Baudoin, J.-M., Lamothe, S., Lambrigot, D. & Lecerf, A. (2011) Experimental shading alters leaf litter breakdown in streams of contrasting riparian canopy cover. Freshwater Biology 56, 20592069.CrossRefGoogle Scholar
Lecerf, A., Dobson, M., Dang, C.K. & Chauvet, E. (2005) Riparian plant species loss alters trophic dynamics in detritus based-stream ecosystems. Oecologia 146, 432442.Google Scholar
Lecerf, A., Baudoin, J.-M., Besson, A.A., Lamothe, S. & Lagrue, C. (2012) Is smaller necessarily better? Effects of small riparian forest openings on stream ecosystems. International Journal for Limnology 48, 401409.CrossRefGoogle Scholar
Lecerf, A., Evangelista, C., Cucherousset, J. & Boiché, A. (2016) Riparian overstory–understory interactions and their potential implications for forest–stream linkages. Forest Ecology and Management 367, 112119.CrossRefGoogle Scholar
Macan, T.T. (1979) A key to the nymphs of the British species of Ephemeroptera with notes on their ecology. Freshwater Biological Association Scientific Publication 20, 164.Google Scholar
Mackie, G.L., Morton, W.B. & Ferguson, M.S. (1983) Fish parasitism in a new impoundment and differences upstream and downstream. Hydrobiologia 99, 197205.CrossRefGoogle Scholar
Málnás, K., Polyák, L., Prill, E., Hegedüs, R., Kriska, G., Dévai, G., Horváth, G. & Lengyel, S. (2011) Bridges as optical barriers and population disruptors for the mayfly Palingenia longicauda: an overlooked threat to freshwater biodiversity? Journal of Insect Conservation 15, 823832.Google Scholar
Marcogliese, D.J. & Cone, D.K. (1996) On the distribution and abundance of eel parasites in Nova Scotia: influence of pH. Journal of Parasitology 82, 389399.CrossRefGoogle ScholarPubMed
McKenzie, V.J. (2007) Human land use and patterns of parasitism in tropical amphibian hosts. Biological Conservation 137, 102116.CrossRefGoogle Scholar
Mladineo, I., Zrnčić, S. & Oraić, D. (2009) Severe helminthic infection of the wild brown trout (Salmo trutta) in Cetina River, Croatia. Bulletin of the European Association of Fish Pathologists 29, 8691.Google Scholar
Moravec, F. (1994) Parasitic nematodes of freshwater fishes of Europe. Dordrecht, The Netherlands, Kluwer Academic Publishers.Google Scholar
Moravec, F. & Frantova, D. (2003) Observations on the transmission and the seasonality of infection of the nematode Cystidicoloides ephemeridarum in Salmo trutta fario in a small trout stream in North Bohemia, the Czech Republic. Acta Parasitologica 48, 4146.Google Scholar
Morley, N.J. (2007) Anthropogenic effects of reservoir construction on the parasite fauna of aquatic wildlife. EcoHealth 4, 374383.Google Scholar
Morley, N.J. & Lewis, J.W. (2006) Anthropogenic pressure on a molluscan–trematode community over a long-term period in the Basingstoke Canal, UK, and its implications for ecosystem health. EcoHealth 3, 269280.CrossRefGoogle Scholar
Mouritsen, K.N. & Poulin, R. (2002) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124, S101S117.Google Scholar
Ostfeld, R.S. & Holt, R.D. (2004) Are predators good for your health? Evaluating evidence for top-down regulation of zoonotic disease reservoirs. Frontiers in Ecology and the Environment 2, 1320.Google Scholar
Patz, J.A., Graczyk, T.K., Geller, N. & Vittor, A.Y. (2000) Effects of environmental change on emerging parasitic diseases. International Journal for Parasitology 30, 13951405.Google Scholar
Petersen, I., Masters, Z., Hildrew, A.G. & Ormerod, S.J. (2004) Dispersal of adult aquatic insects in catchments of differing land use. Journal of Applied Ecology 41, 934950.Google Scholar
Poulin, R. (1995) ‘Adaptive’ changes in the behaviour of parasitized animals: a critical review. International Journal for Parasitology 25, 13711383.Google Scholar
Richardson, J.S. & Béraud, S. (2014) Effects of riparian forest harvest on streams: a meta-analysis. Journal of Applied Ecology 51, 17121721.Google Scholar
Rincón, P.A. & Lobón-Cerviá, J. (1999) Prey-size selection by brown trout (Salmo trutta L.) in a stream in northern Spain. Canadian Journal of Zoology 77, 755765.CrossRefGoogle Scholar
Ringler, N.H. (1979) Selective predation by drift-feeding brown trout (Salmo trutta). Journal of the Fisheries Board of Canada 36, 392403.Google Scholar
Smith, K.F., Sax, D.F. & Lafferty, K.D. (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20, 13491357.CrossRefGoogle ScholarPubMed
Stamps, J.A., Buechner, M. & Krishnan, V.V. (1987) The effects of edge permeability and habitat geometry on emigration from patches of habitat. The American Naturalist 129, 533552.CrossRefGoogle Scholar
Surber, E.W. (1937) Rainbow trout and bottom fauna production in one mile of stream. Transactions of the American Fisheries Society 66, 193202.Google Scholar
Sures, B. (2001) The use of fish parasites as bioindicators of heavy metals in aquatic ecosystems: a review. Aquatic Ecology 35, 245255.CrossRefGoogle Scholar
Sures, B. (2004) Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends in Parasitology 20, 170177.Google Scholar
Sweeney, B.W., Bott, T.L., Jackson, J.K., Kaplan, L.A., Newbold, J.D., Standley, L.J., Hession, W.C. & Horwitz, R.J. (2004) Riparian deforestation, stream narrowing, and loss of stream ecosystem services. Proceedings of the National Academy of Sciences, USA 101, 1413214137.CrossRefGoogle Scholar
Thompson, K.G. & Nehring, R.B. (2000) A simple technique used to filter and quantify the actinospore of Myxobolus cerebralis and determine its seasonal abundance in the Colorado River. Journal of Aquatic Animal Health 12, 316323.2.0.CO;2>CrossRefGoogle Scholar
Tokeshi, M. (1985) Life-cycle and production of the burrowing mayfly, Ephemera danica: a new method for estimating degree-days required for growth. Journal of Animal Ecology 54, 919930.Google Scholar
Vidal-Martínez, V.M. & Wunderlich, A.C. (2016) Parasites as bioindicators of environmental degradation in Latin America: a meta-analysis. Journal of Helminthology. doi:10.1017/S0022149X16000432.Google Scholar
Vidal-Martinez, V.M., Pech, D., Sures, B., Purucker, S.T. & Poulin, R. (2010) Can parasites really reveal environmental impact? Trends in Parasitology 26, 4451.CrossRefGoogle ScholarPubMed
Williams, J.K., Townsend, C.R. & Poulin, R. (2001) Mermithid nematode infections and drift in the mayfly Deleatidium spp. (Ephemeroptera). Journal of Parasitology 87, 12251227.Google Scholar
Winterbourn, M.J., Chadderton, W.L., Entrekin, S.A., Tank, J.L. & Harding, J.S. (2007) Distribution and dispersal of adult stream insects in a heterogeneous montane environment. Fundamental and Applied Limnology/Archiv für Hydrobiologie 168, 127135.Google Scholar
Wood, C.L., Byers, J.E., Cottingham, K.L., Altman, I., Donahue, M.J. & Blakeslee, A.M. (2007) Parasites alter community structure. Proceedings of the National Academy of Sciences, USA 104, 93359339.CrossRefGoogle Scholar
Zhang, Y., Richardson, J.S. & Pinto, X. (2009) Catchment-scale effects of forestry practices on benthic invertebrate communities in Pacific coastal streams. Journal of Applied Ecology 46, 12921303.Google Scholar