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Chapter Nine - Infection and invasion: study cases from aquatic communities

from Part II - Understanding between-host processes

Published online by Cambridge University Press:  28 October 2019

Kenneth Wilson
Affiliation:
Lancaster University
Andy Fenton
Affiliation:
University of Liverpool
Dan Tompkins
Affiliation:
Predator Free 2050 Ltd
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Summary

Invasive species drive biodiversity loss and lead to changes in parasite–host associations. Parasites are linked to invasions and can mediate invasion success and outcomes. We review theoretical and empirical research into parasites in biological invasions, focusing on a freshwater invertebrate study system. We focus on the effects of parasitic infection on host traits (behaviour and life history) that can mediate native/invader trophic interactions. We review evidence from the field and laboratory of parasite-driven changes in predation, intraguild predation and cannibalism. Theoretical work shows that the trait-mediated effects of parasites can be as strong as classical density effects and their impact on the host’s trophic interactions merits more consideration. We also report on evidence of broader cascading effects warranting deeper study. Biological invasion can lead to altered parasite–host associations. Focusing on amphipod invasions, we find patterns of parasite introduction and loss that mirror host invasion pathways, but also highlight the risks of introducing invasive parasites. Horizon scanning and impact predictions are vital in identifying future disease risks, potential pathways of introduction and suitable management measures for mitigation.

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Chapter
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Wildlife Disease Ecology
Linking Theory to Data and Application
, pp. 262 - 295
Publisher: Cambridge University Press
Print publication year: 2019

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References

Adlard, R.D., Miller, T.L. & Smit, N.J. (2015) The butterfly effect: parasite diversity, environment, and emerging disease in aquatic wildlife. Trends in Parasitology, 31, 160166.CrossRefGoogle ScholarPubMed
Anderson, L.G., Dunn, A.M., Rosewarne, P.J. & Stebbing, P.D. (2015) Invaders in hot water: a simple decontamination method to prevent the accidental spread of aquatic invasive non-native species. Biological Invasions, 17, 22872297.CrossRefGoogle Scholar
Anderson, L.G., White, P.C.L., Stebbing, P.D., Stentiford, G.D. & Dunn, A.M. (2014) Biosecurity and vector behaviour: evaluating the potential threat posed by anglers and canoeists as pathways for the spread of invasive non-native species and pathogens. PLoS ONE, 9, e92788.Google Scholar
Arundell, K., Dunn, A., Alexander, J., et al. (2015) Enemy release and genetic founder effects in invasive killer shrimp populations of Great Britain. Biological Invasions, 17, 14391451.Google Scholar
Bandi, C., Dunn, A.M., Hurst, G.D.D. & Rigaud, T. (2001) Inherited microorganisms, sex-specific virulence and reproductive parasitism. Trends in Parasitology, 17, 8894.Google Scholar
Bass, D., Stentiford, G.D., Littlewood, D.T.J. & Hartikainen, H. (2015) Diverse applications of environmental DNA methods in parasitology. Trends in Parasitology, 31, 499513.CrossRefGoogle ScholarPubMed
Blackburn, T.M., Pysek, P., Bacher, S., et al. (2011) A proposed unified framework for biological invasions. Trends in Ecology & Evolution, 26, 333339.CrossRefGoogle ScholarPubMed
Bojko, J. (2017) Parasites of invasive crustacea: risks and opportunities for control. PhD thesis, University of Leeds, UK.Google Scholar
Bojko, J., Bacela-Spychalska, K., Stebbing, P.D., et al. (2017) Parasites, pathogens and commensals in the ‘low-impact’ non-native amphipod host Gammarus roeselii. Parasites & Vectors, 10, 193.Google Scholar
Bojko, J., Dunn, A.M., Stebbing, P.D., et al. (2015) Cucumispora ornata n. sp (Fungi: Microsporidia) infecting invasive ‘demon shrimp’ (Dikerogammarus haemobaphes) in the United Kingdom. Journal of Invertebrate Pathology, 128, 2230.Google Scholar
Bojko, J., Stebbing, P.D., Bateman, K.S., et al. (2013) Baseline histopathological survey of a recently invading island population of ‘killer shrimp’, Dikerogammarus villosus. Diseases of Aquatic Organisms, 106, 241253.CrossRefGoogle ScholarPubMed
Bovy, H.C., Barrios-O’Neill, D., Emmerson, M.C., Aldridge, D.C. & Dick, J.T.A. (2015) Predicting the predatory impacts of the ‘demon shrimp’ Dikerogammarus haemobaphes, on native and previously introduced species. Biological Invasions, 17, 597607.CrossRefGoogle Scholar
Bowers, R.G. & Turner, J. (1997) Community structure and the interplay between interspecific infection and competition. Journal of Theoretical Biology, 187, 95109.CrossRefGoogle ScholarPubMed
Bunke, M., Alexander, M.E., Dick, J.T.A., et al. (2015) Eaten alive: cannibalism is enhanced by parasites. Royal Society Open Science, 2, 140369.Google Scholar
Claessen, D., de Roos, A.M. & Persson, L. (2004) Population dynamic theory of size-dependent cannibalism. Proceedings of the Royal Society B-Biological Sciences, 271, 333340.CrossRefGoogle ScholarPubMed
Colautti, R.I., Ricciardi, A., Grigorovich, I.A. & MacIsaac, H.J. (2004) Is invasion success explained by the enemy release hypothesis? Ecology Letters, 7, 721733.Google Scholar
DAISIE (2017) DAISIE European Invasive Alien Species Gateway, accessed 2017.Google Scholar
Dick, J.T.A. (1996) Post-invasion amphipod communities of Lough Neagh, Northern Ireland: influences of habitat selection and mutual predation. Journal of Animal Ecology, 65, 756767.CrossRefGoogle Scholar
Dick, J.T.A., Alexander, M.E., Jeschke, J.M., et al. (2014) Advancing impact prediction and hypothesis testing in invasion ecology using a comparative functional response approach. Biological Invasions, 16, 735753.Google Scholar
Dick, J.T.A., Armstrong, M., Clarke, H.C., et al. (2010) Parasitism may enhance rather than reduce the predatory impact of an invader. Biology Letters, 6, 636638.CrossRefGoogle ScholarPubMed
Dick, J.T.A., Laverty, C., Lennon, J.J., et al. (2017) Invader Relative Impact Potential: a new metric to understand and predict the ecological impacts of existing, emerging and future invasive alien species. Journal of Applied Ecology, 54, 12591267.CrossRefGoogle Scholar
Dick, J.T.A., Montgomery, I. & Elwood, R.W. (1993) Replacement of the indigenous amphipod Gammarus duebeni celticus by the introduced Gammarus pulex – differential cannibalism and mutual predation. Journal of Animal Ecology, 62, 7988.Google Scholar
Dick, J.T.A., Montgomery, W.I. & Elwood, R.W. (1999) Intraguild predation may explain an amphipod replacement: evidence from laboratory populations. Journal of Zoology, 249, 463468.CrossRefGoogle Scholar
Dick, J.T.A. & Platvoet, D. (1996) Intraguild predation and species exclusions in amphipods: the interaction of behaviour, physiology and environment. Freshwater Biology, 36, 375383.Google Scholar
Dobson, A., Lafferty, K.D., Kuris, A.M., Hechinger, R.F. & Jetz, W. (2008) Homage to Linnaeus: how many parasites? How many hosts? Proceedings of the National Academy of Sciences of the United States of America, 105, 11,48211,489.CrossRefGoogle ScholarPubMed
Dudgeon, D., Arthington, A.H., Gessner, M.O., et al. (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews, 81, 163182.Google Scholar
Dunn, A.M. & Dick, J.T.A. (1998) Parasitism and epibiosis in native and non-native gammarids in freshwater in Ireland. Ecography, 21, 593598.CrossRefGoogle Scholar
Dunn, A.M. & Hatcher, M.J. (2015) Parasites and biological invasions: parallels, interactions, and control. Trends in Parasitology, 31, 189199.Google Scholar
Dunn, A.M., Torchin, M.E., Hatcher, M.J., et al. (2012) Indirect effects of parasites in invasions. Functional Ecology, 26, 12621274.Google Scholar
EU. (2014). Regulation (EU) No. 1143/2014 of the European Parliament and of the Council of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species. https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=celex%3A32014R1143Google Scholar
Farrer, R.A., Weinert, L.A., Bielby, J., et al. (2011) Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proceedings of the National Academy of Sciences of the United States of America, 108, 18,73218,736.CrossRefGoogle ScholarPubMed
Fielding, N.J., MacNeil, C., Robinson, N., et al. (2005) Ecological impacts of the microsporidian parasite Pleistophora mulleri on its freshwater amphipod host Gammarus duebeni celticus. Parasitology, 131, 331336.CrossRefGoogle ScholarPubMed
Filipova, L., Petrusek, A., Matasova, K., Delaunay, C. & Grandjean, F. (2013) Prevalence of the crayfish plague pathogen Aphanomyces astaci in populations of the signal crayfish Pacifastacus leniusculus in France: evaluating the threat to native crayfish. PLoS ONE, 8, e70157.CrossRefGoogle ScholarPubMed
Fisher, M.C., Henk, D.A., Briggs, C.J., et al. (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature, 484, 186194.Google Scholar
GBNNSS (2015) The Great Britain Invasive Non Native Species Strategy.Google Scholar
Grabner, D.S., Weigand, A.M., Leese, F., et al. (2015) Invaders, natives and their enemies: distribution patterns of amphipods and their microsporidian parasites in the Ruhr Metropolis, Germany. Parasites & Vectors, 8, 419.Google Scholar
Hatcher, M.J., Dick, J.T.A. & Dunn, A.M. (2006) How parasites affect interactions between competitors and predators. Ecology Letters, 9, 12531271.Google Scholar
Hatcher, M.J., Dick, J.T.A. & Dunn, A.M. (2008) A keystone effect for parasites in intraguild predation? Biology Letters, 4, 534537.Google Scholar
Hatcher, M.J., Dick, J.T.A. & Dunn, A.M. (2012a) Disease emergence and invasions. Functional Ecology, 26, 12751287.Google Scholar
Hatcher, M.J., Dick, J.T.A. & Dunn, A.M. (2012b) Diverse effects of parasites in ecosystems: linking interdependent processes. Frontiers in Ecology and the Environment, 10, 186194.Google Scholar
Hatcher, M.J., Dick, J.T.A. & Dunn, A.M. (2014) Parasites that change predator or prey behaviour can have keystone effects on community composition. Biology Letters, 10.Google Scholar
Hatcher, M.J., Dick, J.T.A., Paterson, R.A., et al. (2015) Trait-mediated effects of parasites on invader–native interactions. In: Mehlhorn, H. (ed.), Host Manipulations by Parasites and Viruses (pp. 2947). Cham: Springer.CrossRefGoogle Scholar
Hatcher, M.J. & Dunn, A.M. (2011) Parasites in Ecological Communities; From Interactions to Ecosystems. Cambridge: Cambridge University Press.Google Scholar
Holt, R.D. & Dobson, A.P. (2006) Extending the principles of community ecology to address the epidemiology of host–pathogen systems. In: Collinge, S.K.R. (ed.), Disease Ecology: Community Structure and Pathogen Dynamics (pp. 627). Oxford: Oxford University Press.CrossRefGoogle Scholar
Holt, R.D., Dobson, A.P., Begon, M., Bowers, R.G. & Schauber, E.M. (2003) Parasite establishment in host communities. Ecology Letters, 6, 837842.Google Scholar
Holt, R.D. & Pickering, J. (1985) Infectious-disease and species coexistence – a model of Lotka–Volterra form. American Naturalist, 126, 196211.Google Scholar
Holt, R.D. & Polis, G.A. (1997) A theoretical framework for intraguild predation. American Naturalist, 149, 745764.Google Scholar
Hudson, P. & Greenman, J. (1998) Competition mediated by parasites: biological and theoretical progress. Trends in Ecology & Evolution, 13, 387390.CrossRefGoogle ScholarPubMed
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.Google Scholar
IUCN (2017) Global invasive species database. www.iucngisd.org/gisd/, accessed November 2017.Google Scholar
Keane, R.M. & Crawley, M.J. (2002) Exotic plant invasions and the enemy release hypothesis. Trends in Ecology & Evolution, 17, 164170.Google Scholar
Keesing, F., Belden, L.K., Daszak, P., et al. (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature, 468, 647652.Google Scholar
Kelly, D.W. & Dick, J.T.A. (2005) Introduction of the non-indigenous amphipod Gammarus pulex alters population dynamics and diet of juvenile trout Salmo trutta. Freshwater Biology, 50, 127140.Google Scholar
Kelly, D.W., Dick, J.T.A. & Montgomery, W.I. (2002) The functional role of Gammarus (Crustacea, Amphipoda): shredders, predators, or both? Hydrobiologia, 485, 199203.Google Scholar
Kenna, D., Fincham, W.N., Dunn, A.M., Brown, L.E. & Hassall, C. (2017) Antagonistic effects of biological invasion and environmental warming on detritus processing in freshwater ecosystems. Oecologia, 183, 875886.Google Scholar
Kumschick, S., Gaertner, M., Vila, M., et al. (2015) Ecological impacts of alien species: quantification, scope, caveats, and recommendations. Bioscience, 65, 5563.Google Scholar
Laverty, C., Brenner, D., McIlwaine, C., et al. (2017) Temperature rise and parasitic infection interact to increase the impact of an invasive species. International Journal for Parasitology, 47, 291296.CrossRefGoogle ScholarPubMed
Ledger, M.E. & Milner, A.M. (2015) Extreme events in running waters. Freshwater Biology, 60, 24552460.Google Scholar
Lefevre, T., Lebarbenchon, C., Gauthier-Clerc, M., et al. (2009) The ecological significance of manipulative parasites. Trends in Ecology & Evolution, 24, 4148.Google Scholar
MacLeod, C.J., Paterson, A.M., Tompkins, D.M. & Duncan, R.P. (2010) Parasites lost – do invaders miss the boat or drown on arrival? Ecology Letters, 13, 516527.Google Scholar
MacNeil, C., Dick, J.T. & Elwood, R.W. (1997) The trophic ecology of freshwater Gammarus spp. (Crustacea: Amphipoda): problems and perspectives concerning the functional feeding group concept. Biological Reviews of the Cambridge Philosophical Society, 72, 349364.Google Scholar
MacNeil, C., Dick, J.T.A., Hatcher, M.J., et al. (2003a) Parasite-mediated predation between native and invasive amphipods. Proceedings of the Royal Society of London Series B, 270, 13091314.Google Scholar
MacNeil, C., Dick, J.T.A., Platvoet, D. & Briffa, M. (2011) Direct and indirect effects of species displacements: an invading freshwater amphipod can disrupt leaf-litter processing and shredder efficiency. Journal of the North American Benthological Society, 30, 3848.Google Scholar
MacNeil, C., Elwood, R.W. & Dick, J.T.A. (1999) Predator–prey interactions between brown trout Salmo trutta and native and introduced amphipods; their implications for fish diets. Ecography, 22, 686696.Google Scholar
MacNeil, C., Fielding, N.J., Dick, J.T.A., et al. (2003b) An acanthocephalan parasite mediates intraguild predation between invasive and native freshwater amphipods (Crustacea). Freshwater Biology, 48, 20852093.CrossRefGoogle Scholar
MacNeil, C., Fielding, N.J., Hume, K.D., et al. (2003c) Parasite altered micro-distribution of Gammarus pulex (Crustacea: Amphipoda). International Journal for Parasitology, 33, 5764.Google Scholar
MacNeil, C., Platvoet, D., Dick, J.T.A., et al. (2010) The Ponto-Caspian ‘killer shrimp’, Dikerogammarus villosus (Sowinsky, 1894), invades the British Isles. Aquatic Invasions, 5, 441445.CrossRefGoogle Scholar
Mitchell, C.E. & Power, A.G. (2003) Release of invasive plants from fungal and viral pathogens. Nature, 421, 625627.Google Scholar
Mouritsen, K.N. & Poulin, R. (2010) Parasitism as a determinant of community structure on intertidal flats. Marine Biology, 157, 201213.CrossRefGoogle Scholar
Ohgushi, T., Schmitz, O. & Holt, R.D. (2012) Trait-mediated Indirect Interactions: Ecological and Evolutionary Perspectives. Cambridge: Cambridge University Press.Google Scholar
Okamura, B. & Feist, S.W. (2011) Emerging diseases in freshwater systems. Freshwater Biology, 56, 627637.Google Scholar
Ovcharenko, M.O., Bacela, K., Wilkinson, T., et al. (2010) Cucumispora dikerogammarz n. gen. (Fungi: Microsporidia) infecting the invasive amphipod Dikerogammarus villosus: a potential emerging disease in European rivers. Parasitology, 137, 191204.Google Scholar
Parker, J.D., Torchin, M.E., Hufbauer, R.A., et al. (2013) Do invasive species perform better in their new ranges? Ecology, 94, 985994.Google Scholar
Paterson, R.A., Dick, J.T.A., Pritchard, D.W., et al. (2015) Predicting invasive species impacts: a community module functional response approach reveals context dependencies. Journal of Animal Ecology, 84, 453463.Google Scholar
Pimentel, D., Zuniga, R. & Morrison, D. (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics, 52, 273288.Google Scholar
Polis, G.A., Myers, C.A. & Holt, R.D. (1989) The ecology and evolution of intraguild predation – potential competitors that eat each other. Annual Review of Ecology and Systematics, 20, 297330.Google Scholar
Poulin, R. (2010) Network analysis shining light on parasite ecology and diversity. Trends in Parasitology, 26, 492498.CrossRefGoogle ScholarPubMed
Price, P.W., Westoby, M., Rice, B., et al. (1986) Parasite mediation in ecological interactions. Annual Review of Ecology and Systematics, 17, 487505.CrossRefGoogle Scholar
Rewicz, T., Grabowski, M., MacNeil, C. & Bacela-Spychalska, K. (2014) The profile of a ‘perfect’ invader – the case of killer shrimp, Dikerogammarus villosus. Aquatic Invasions, 9, 267288.Google Scholar
Rewicz, T., Wattier, R., Grabowski, M., Rigaud, T. & Bacela-Spychalska, K. (2015) Out of the Black Sea: phylogeography of the invasive killer shrimp Dikerogammarus villosus across Europe. PLoS ONE, 10, e0118121.Google Scholar
Ricciardi, A. & MacIsaac, H.J. (2011) Impacts of Biological Invasions on Freshwater Ecosystems. Malden, MA: Wiley-Blackwell.Google Scholar
Roy, H. (2016) Invasive species: control wildlife pathogens too. Nature, 530, 281281.Google Scholar
Roy, H.E., Hesketh, H., Purse, B.V., et al. (2016) Alien pathogens on the horizon: opportunities for predicting their threat to wildlife. Conservation Letters, 10, 477484.Google Scholar
Rudolf, V.H.W. (2007) The interaction of cannibalism and omnivory: consequences for community dynamics. Ecology, 88, 26972705.CrossRefGoogle ScholarPubMed
Sanchez, M.I., Rode, N.O., Flaven, E., et al. (2012) Differential susceptibility to parasites of invasive and native species of Artemia living in sympatry: consequences for the invasion of A. franciscana in the Mediterranean region. Biological Invasions, 14, 18191829.Google Scholar
Selakovic, S., de Ruiter, P.C. & Heesterbeek, H. (2014) Infectious disease agents mediate interaction in food webs and ecosystems. Proceedings of the Royal Society of London B, 281, 20132709.Google Scholar
Shannon, C., Quinn, C.H., Sutcliffe, C., et al. (2019) Exploring knowledge, perception of risk and biosecurity practices among researchers in the UK: a quantitative survey. Biological Invasions, 21, 303314.CrossRefGoogle Scholar
Slothouber Galbreath, J.G.M., Smith, J.E., Becnel, J.J., Butlin, R.K. & Dunn, A.M. (2010) Reduction in post-invasion genetic diversity in Crangonyx pseudogracilis (Amphipoda: Crustacea): a genetic bottleneck or the work of hitchhiking vertically transmitted microparasites? Biological Invasions, 12, 191209.Google Scholar
Slothouber Galbreath, J.G.M., Smith, J.E., Terry, R.S., Becnel, J.J. & Dunn, A.M. (2004) Invasion success of Fibrillanosema crangonycis, n.sp., n.g.: a novel vertically transmitted microsporidian parasite from the invasive amphipod host Crangonyx pseudogracilis. International Journal for Parasitology, 34, 235244.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.Google Scholar
Sutcliffe, C., Quinn, C.H., Shannon, C., Glover, A. & Dunn, A.M. (2018) Exploring the attitudes to and uptake of biosecurity practices for invasive non-native species: views amongst stakeholder organisations working in UK natural environments. Biological Invasions, 20, 399411.Google Scholar
Terry, R.S., MacNeil, C., Dick, J.T.A., Smith, J.E. & Dunn, A.M. (2003) Resolution of a taxonomic conundrum: an ultrastructural and molecular description of the life cycle of Pleistophora mulleri (Pfeiffer 1895; Georgevitch 1929). Journal of Eukaryotic Microbiology, 50, 266273.Google Scholar
Terry, R.S., Smith, J.E., Sharpe, R.G., et al. (2004) Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum Microspora. Proceedings of the Royal Society of London Series B, 271, 17831789.Google Scholar
Torchin, M.E., Lafferty, K.D., Dobson, A.P., McKenzie, V.J. & Kuris, A.M. (2003) Introduced species and their missing parasites. Nature, 421, 628630.Google Scholar
Torchin, M.E., Lafferty, K.D. & Kuris, A.M. (2002) Parasites and marine invasions. Parasitology, 124, S137S151.Google Scholar
Wattier, R.A., Haine, E.R., Beguet, J., et al. (2007) No genetic bottleneck or associated microparasite loss in invasive populations of a freshwater amphipod. Oikos, 116, 19411953.Google Scholar
Wilkinson, T.J., Rock, J., Whiteley, N.M., Ovcharenko, M.O. & Ironside, J.E. (2011) Genetic diversity of the feminising microsporidian parasite Dictyocoela: new insights into host-specificity, sex and phylogeography. International Journal for Parasitology, 41, 959966.Google Scholar

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