Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-25T20:17:51.981Z Has data issue: false hasContentIssue false

How does human-induced environmental change influence host-parasite interactions?

Published online by Cambridge University Press:  05 December 2013

ALEXANDRE BUDRIA*
Affiliation:
Department of Biosciences, University of Helsinki, P.O. Box 65, FI-00014 Helsinki, Finland
ULRIKA CANDOLIN
Affiliation:
Department of Biosciences, University of Helsinki, P.O. Box 65, FI-00014 Helsinki, Finland
*
* Corresponding author: Department of Biosciences, University of Helsinki, P.O. Box 65, FI-00014 Helsinki, Finland. E-mail: [email protected]

Summary

Host-parasite interactions are an integral part of ecosystems that influence both ecological and evolutionary processes. Humans are currently altering environments the world over, often with drastic consequences for host-parasite interactions and the prevalence of parasites. The mechanisms behind the changes are, however, poorly known. Here, we explain how host-parasite interactions depend on two crucial steps – encounter rate and host-parasite compatibility – and how human activities are altering them and thereby host-parasite interactions. By drawing on examples from the literature, we show that changes in the two steps depend on the influence of human activities on a range of factors, such as the density and diversity of hosts and parasites, the search strategy of the parasite, and the avoidance strategy of the host. Thus, to unravel the mechanisms behind human-induced changes in host-parasite interactions, we have to consider the characteristics of all three parts of the interaction: the host, the parasite and the environment. More attention should now be directed to unfold these mechanisms, focusing on effects of environmental change on the factors that determine encounter rate and compatibility. We end with identifying several areas in urgent need of more investigations.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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

Adamo, S. A. and Lovett, M. M. (2011). Some like it hot: the effects of climate change on reproduction, immune function and disease resistance in the cricket Gryllus texensis . Journal of Experimental Biology 214, 19972004.CrossRefGoogle ScholarPubMed
Aho, J. M., Camp, J. W. and Esch, G. W. (1982). Long-term studies on the population biology of Diplostomulum scheuringi in a thermally altered reservoir. Journal of Parasitology 68, 695708.CrossRefGoogle Scholar
Alizon, S., Hurford, A., Mideo, N. and Van Baalen, M. (2009). Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. Journal of Evolutionary Biology 22, 245259. doi: 10.1111/j.1420-9101.2008.01658.x.CrossRefGoogle ScholarPubMed
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. doi: 10.1111/j.1461-0248.2005.00879.x.CrossRefGoogle ScholarPubMed
Altizer, S., Nunn, C. L. and Lindenfors, P. (2007). Do threatened hosts have fewer parasites? A comparative study in primates. Journal of Animal Ecology 76, 304314. doi: 10.1111/j.1365-2656.2007.01214.x.CrossRefGoogle ScholarPubMed
Alvarez-Pellitero, P. (2008). Fish immunity and parasite infections: from innate immunity to immunoprophylactic prospects. Veterinary Immunology and Immunopathology 126, 171198. doi: 10.1016/j.vetimm.2008.07.013.CrossRefGoogle ScholarPubMed
Amundsen, P. A. and Kristoffersen, R. (1990). Infection of whitefish (Coregonus lavaretus L. sl) by Triaenophorus crassus Forel (Cestoda: Pseudophyllidea): a case study in parasite control. Canadian Journal of Zoology 68, 11871192.CrossRefGoogle Scholar
Anderson, R. M. and May, R. (1979). Population biology of infectious diseases: part I. Nature 280, 361367.CrossRefGoogle ScholarPubMed
Arkush, K. D., Giese, A. R., Mendonca, H. L., McBride, A. M., Marty, G. D. and Hedrick, P. W. (2002). Resistance to three pathogens in the endangered winter-run chinook salmon (Oncorhynchus tshawytscha): effects of inbreeding and major histocompatibility complex genotypes. Canadian Journal of Fisheries and Aquatic Sciences 59, 966975.CrossRefGoogle Scholar
Arneberg, P., Skorping, A., Grenfell, B. and Read, A. F. (1998). Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London, Series B 265, 12831289.CrossRefGoogle Scholar
Banerjee, B. D. (1999). The influence of various factors on immune toxicity assessment of pesticide chemicals. Toxicology Letters 107, 2131. doi: 10.1016/s0378-4274(99)00028-4.CrossRefGoogle ScholarPubMed
Best, S. M. and Kerr, P. J. (2000). Coevolution of host and virus: the pathogenesis of virulent and attenuated strains of myxoma virus in resistant and susceptible European rabbits. Virology 267, 3648. doi: 10.1006/viro.1999.0104.CrossRefGoogle ScholarPubMed
Biagianti-Risbourg, S. (1990). Contribution à l’étude du foie de juvéniles de muges (Téléostéens, Mugilides), contaminés expérimentalement par l'atrazine (s-triazine herbicide): approche ultrastructurale et métabolique: intérêt en écotoxicologie. Doctoral thesis. Université de Perpignan, France.Google Scholar
Black, G. A. (1983). Taxonomy of a swimbladder nematode, Cystidicola stigmatura (Leidy), and evidence of its decline in the Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 40, 643647.CrossRefGoogle Scholar
Black, G. A. (1985). Reproductive output and population biology of Cystidicola stigmatura (Leidy) (Nematoda) in Arctic char, Salvelinus alpinus (L.) (Salmonidae). Canadian Journal of Zoology 63, 617622.CrossRefGoogle Scholar
Blakley, B., Brousseau, P., Fournier, M. and Voccia, I. (1999). Immunotoxicity of pesticides: a review. Toxicology and Industrial Health 15, 119132.CrossRefGoogle Scholar
Bols, N. C., Brubacher, J. L., Ganassin, R. C. and Lee, L. E. (2001). Ecotoxicology and innate immunity in fish. Developmental and Comparative Immunology 25, 853873.CrossRefGoogle ScholarPubMed
Bordes, F. and Morand, S. (2011). The impact of multiple infections on wild animal hosts: a review. Infection Ecology and Epidemiology 1. doi: 10.3402/iee.v1i0.7346.CrossRefGoogle ScholarPubMed
Bradley, J. and Jackson, J. (2008). Measuring immune system variation to help understand host–pathogen community dynamics. Parasitology 135, 807823.CrossRefGoogle ScholarPubMed
Carton, Y. and Sokolowski, M. (1992). Interactions between searching strategies of Drosophila parasitoids and the polymorphic behavior of their hosts. Journal of Insect Behavior 5, 161175.CrossRefGoogle Scholar
Chakrabarty, P. and Banerjee, V. (1988). Effect of organophosphorus pesticides on the peripheral hemogram of the fish Channa punctatus . Environment and Ecology 6, 390394.Google Scholar
Choisy, M. and de Roode, J. C. (2010). Mixed infections and the evolution of virulence: effects of resource competition, parasite plasticity, and impaired host immunity. American Naturalist 175, E105E118. doi: 10.1086/651587.CrossRefGoogle ScholarPubMed
Christin, M. S., Gendron, A. D., Brousseau, P., Ménard, L., Marcogliese, D. J., Cyr, D., Ruby, S. and Fournier, M. (2003). Effects of agricultural pesticides on the immune system of Rana pipiens and on its resistance to parasitic infection. Environmental Toxicology and Chemistry 22, 11271133.CrossRefGoogle ScholarPubMed
Christin, M., Menard, L., Gendron, A., Ruby, S., Cyr, D., Marcogliese, D., Rollins-Smith, L. and Fournier, M. (2004). Effects of agricultural pesticides on the immune system of Xenopus laevis and Rana pipiens . Aquatic Toxicology 67, 3343.CrossRefGoogle ScholarPubMed
Chubb, J. C. (1977). Seasonal occurrence of helminths in freshwater fishes. Part I. Monogenea. Advances in Parasitology 15, 133199.CrossRefGoogle ScholarPubMed
Chubb, J. C. (1979). Seasonal occurrence of helminths in freshwater fishes. Part II. Trematoda. Advances in Parasitology 17, 141313.CrossRefGoogle Scholar
Chubb, J. C. (1980). Seasonal occurrence of helminths in freshwater fishes. Part III. Larval Cestoda and Nematoda. Advances in Parasitology 18, 1120.CrossRefGoogle ScholarPubMed
Chubb, J. C. (1982). Seasonal occurrence of helminths in freshwater fishes. Part IV. Adult Cestoda, Nematoda and Acanthocephala. Advances in Parasitology 20, 1292.CrossRefGoogle ScholarPubMed
Coeurdassier, M., De Vaufleury, A., Scheifler, R., Morhain, E. and Badot, P.-M. (2004). Effects of cadmium on the survival of three life-stages of the freshwater pulmonate Lymnaea stagnalis (Mollusca: Gastropoda). Bulletin of Environmental Contamination and Toxicology 72, 10831090.CrossRefGoogle ScholarPubMed
Combes, C. (2001). Parasitism: the Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago, IL, USA.Google Scholar
Costello, M. J. (2009). How sea lice from salmon farms may cause wild salmonid declines in Europe and North America and be a threat to fishes elsewhere. Proceedings of the Royal Society of London, Series B 276, 33853394.Google ScholarPubMed
Davies, J. and Davies, D. (2010). Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews 74, 417433.CrossRefGoogle ScholarPubMed
Desneux, N., Decourtye, A. and Delpuech, J. M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology 52, 81106.CrossRefGoogle ScholarPubMed
Dobson, A., Lafferty, K. D., Kuris, A. M., Hechinger, R. F. and Jetz, W. (2008). Homage to Linnaeus: how many parasites? How many hosts? Proceedings of the National Academy of Sciences USA 105 (Suppl. 1), 1148211489. doi: 10.1073/pnas.0803232105.CrossRefGoogle ScholarPubMed
Dunn, R. R., Harris, N. C., Colwell, R. K., Koh, L. P. and Sodhi, N. S. (2009). The sixth mass coextinction: are most endangered species parasites and mutualists? Proceedings of the Royal Society of London, Series B 276, 30373045. doi: 10.1098/rspb.2009.0413.Google ScholarPubMed
Ebert, D. and Bull, J. J. (2003). Challenging the trade-off model for the evolution of virulence: is virulence management feasible? Trends in Microbiology 11, 1520.CrossRefGoogle ScholarPubMed
Ebert, D. and Herre, E. (1996). The evolution of parasitic diseases. Parasitology Today 12, 96101.CrossRefGoogle ScholarPubMed
Eswarappa, S. M., Estrela, S. and Brown, S. P. (2012). Within-host dynamics of multi-species infections: facilitation, competition and virulence. PLoS ONE 7, e38730. doi: 10.1371/journal.pone.0038730.CrossRefGoogle ScholarPubMed
Ewald, P. W. (1983). Host-parasite relations, vectors, and the evolution of disease severity. Annual Review of Ecology and Systematics 14, 465485.CrossRefGoogle Scholar
Farnsworth, M. L., Wolfe, L. L., Hobbs, N. T., Burnham, K. P., Williams, E. S., Theobald, D. M., Conner, M. M. and Miller, M. W. (2005). Human land use influences chronic wasting disease prevalence in mule deer. Ecological Applications 15, 119126.CrossRefGoogle Scholar
Fenner, F. and Marshall, I. (1957). A comparison of the virulence for European rabbits (Oryctolagus cuniculus) of strains of myxoma virus recovered in the field in Australia, Europe and America. Journal of Hygiene 55, 149191.CrossRefGoogle ScholarPubMed
Gandon, S., Mackinnon, M., Nee, S. and Read, A. (2003). Imperfect vaccination: some epidemiological and evolutionary consequences. Proceedings of the Royal Society of London, Series B 270, 11291136.CrossRefGoogle ScholarPubMed
Garnett, G. P. and Holmes, E. C. (1996). The ecology of emergent infectious disease. BioScience 46, 127135.CrossRefGoogle Scholar
Garrigan, D. and Hedrick, P. W. (2001). Class I MHC polymorphism and evolution in endangered California Chinook and other Pacific salmon. Immunogenetics 53, 483489.CrossRefGoogle ScholarPubMed
Giese, A. R. and Hedrick, P. W. (2003). Genetic variation and resistance to a bacterial infection in the endangered Gila topminnow. Animal Conservation 6, 369377.CrossRefGoogle Scholar
Hedrick, P. W., Parker, K. M., Miller, E. L. and Miller, P. S. (1999). Major histocompatibility complex variation in the endangered Przewalski's horse. Genetics 152, 17011710.CrossRefGoogle ScholarPubMed
Hedrick, P. W., Parker, K. M., Gutiérrez-Espeleta, G. A., Rattink, A. and Lievers, K. (2000). Major histocompatibility complex variation in the Arabian oryx. Evolution 54, 21452151.Google ScholarPubMed
Horrocks, N. P., Matson, K. D. and Tieleman, B. I. (2011). Pathogen pressure puts immune defense into perspective. Integrative and Comparative Biology 51, 563576. doi: 10.1093/icb/icr011.CrossRefGoogle ScholarPubMed
Hutton, F. W. (1881). Art. XIX. – Notes on some pulmonate Mollusca. Transactions and Proceedings of the Royal Society of New Zealand 14, 150158.Google Scholar
Jakobsen, P. J., Johnsen, G. H. and Larsson, P. (1988). Effects of predation risk and parasitism on the feeding ecology, habitat use, and abondance of lacustrine threespine stickleback (Gasterosteus aculeatus). Canadian Journal of Fisheries and Aquatic Sciences 45, 426431.CrossRefGoogle Scholar
Johnson, P. T. and Thieltges, D. W. (2010). Diversity, decoys and the dilution effect: how ecological communities affect disease risk. Journal of Experimental Biology 213, 961970. doi: 10.1242/jeb.037721.CrossRefGoogle ScholarPubMed
Johnson, P. T., Chase, J. M., Dosch, K. L., Hartson, R. B., Gross, J. A., Larson, D. J., Sutherland, D. R. and Carpenter, S. R. (2007). Aquatic eutrophication promotes pathogenic infection in amphibians. Proceedings of the National Academy of Sciences, USA 104, 1578115786. doi: 10.1073/pnas.0707763104.CrossRefGoogle ScholarPubMed
Johnson, P. T. J. and Chase, J. M. (2004). Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecology Letters 7, 521526. doi: 10.1111/j.1461-0248.2004.00610.x.CrossRefGoogle Scholar
Jorgensen, E. (2010). Ecotoxicology. Elsevier, Amsterdam, the Netherlands.Google Scholar
Keeling, M. and Grenfell, B. (1997). Disease extinction and community size: modeling the persistence of measles. Science 275, 6567.CrossRefGoogle ScholarPubMed
Keesing, F., Holt, R. D. and Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecology Letters 9, 485498. doi: 10.1111/j.1461-0248.2006.00885.x.CrossRefGoogle ScholarPubMed
Kelly, D. W., Paterson, R. A., Townsend, C. R., Poulin, R. and Tompkins, D. M. (2009 a). Has the introduction of brown trout altered disease patterns in native New Zealand fish? Freshwater Biology 54, 18051818. doi: 10.1111/j.1365-2427.2009.02228.x.CrossRefGoogle Scholar
Kelly, D. W., Paterson, R. A., Townsend, C. R., Poulin, R. and Tompkins, D. M. (2009 b). Parasite spillback: a neglected concept in invasion ecology? Ecology 90, 20472056.CrossRefGoogle ScholarPubMed
Kelly, D. W., Poulin, R., Tompkins, D. M. and Townsend, C. R. (2010). Synergistic effects of glyphosate formulation and parasite infection on fish malformations and survival. Journal of Applied Ecology 47, 498504.CrossRefGoogle Scholar
Khan, R. (1990). Parasitism in marine fish after chronic exposure to petroleum hydrocarbons in the laboratory and to the Exxon Valdez oil spill. Bulletin of Environmental Contamination and Toxicology 44, 759763.CrossRefGoogle Scholar
Khan, R. and Kiceniuk, J. (1988). Effect of petroleum aromatic hydrocarbons on monogeneids parasitizing Atlantic cod, Gadus morhua L. Bulletin of Environmental Contamination and Toxicology 41, 94100.CrossRefGoogle ScholarPubMed
Køie, M. (1991). Swimbladder nematodes (Anguillicola spp.) and gill monogeneans (Pseudodactylogyrus spp.) parasitic on the European eel (Anguilla anguilla). Journal du Conseil: ICES Journal of Marine Science 47, 391398.CrossRefGoogle Scholar
Konkel, M. E. and Tilly, K. (2000). Temperature-regulated expression of bacterial virulence genes. Microbes and Infection 2, 157166.CrossRefGoogle ScholarPubMed
Kopp, K. and Jokela, J. (2007). Resistant invaders can convey benefits to native species. Oikos 116, 295301. doi: 10.1111/j.2006.0030-1299.15290.x.CrossRefGoogle Scholar
Krkošek, M., Ford, J. S., Morton, A., Lele, S., Myers, R. A. and Lewis, M. A. (2007). Declining wild salmon populations in relation to parasites from farm salmon. Science 318, 17721775.CrossRefGoogle ScholarPubMed
Kunttu, H. M., Valtonen, E. T., Jokinen, E. I. and Suomalainen, L.-R. (2009). Saprophytism of a fish pathogen as a transmission strategy. Epidemics 1, 96100.CrossRefGoogle ScholarPubMed
Lafferty, K. D. (2009). The ecology of climate change and infectious diseases. Ecology 90, 888900.CrossRefGoogle ScholarPubMed
Lafferty, K. D. and Kuris, A. M. (2005). Parasitism and environmental disturbances. In Parasitism and Ecosystems (ed. Thomas, F., Guégan, J.-F. and Renaud, F.), pp. 113123. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Lewis, E. E., Campbell, J. F. and Sukhdeo, M. V. K. (2002). The Behavioural Ecology of Parasites. CABI, Wallingford, UK.CrossRefGoogle Scholar
Lipsitch, M. and Moxon, E. R. (1997). Virulence and transmissibility of pathogens: what is the relationship? Trends in Microbiology 5, 3137.CrossRefGoogle ScholarPubMed
Louhi, K. R., Karvonen, A., Rellstab, C. and Jokela, J. (2010). Is the population genetic structure of complex life cycle parasites determined by the geographic range of the most motile host? Infection, Genetics and Evolution 10, 12711277. doi: 10.1016/j.meegid.2010.08.013.CrossRefGoogle ScholarPubMed
Lyles, A. M. and Dobson, A. P. (1993). Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites. Journal of Zoo and Wildlife Medicine 24, 315326.Google Scholar
Macnab, V. i. and Barber, I. (2012). Some (worms) like it hot: fish parasites grow faster in warmer water, and alter host thermal preferences. Global Change Biology 18, 15401548. doi: 10.1111/j.1365-2486.2011.02595.x.CrossRefGoogle Scholar
Marcogliese, D. J. (2001). Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 13311352. doi: 10.1139/cjz-79-8-1331.CrossRefGoogle Scholar
Marcogliese, D. J. (2004). Parasites: small players with crucial roles in the ecological theater. Ecohealth 1, 151164. doi: 10.1007/s10393-004-0028-3.CrossRefGoogle Scholar
Marcogliese, D. J., Goater, T. M. and Esch, G. W. (1990). Crepidostomum cooperi (Allocreadidae) in the burrowing mayfly, Hexagenia limbata (Ephemeroptera) related to trophic status of a lake. American Midland Naturalist 124, 309317.CrossRefGoogle Scholar
Marshall, I. and Fenner, F. (1960). Studies in the epidemiology of infectious myxomatosis of rabbits: VII. The virulence of strains of myxoma virus recovered from Australian wild rabbits between 1951 and 1959. Journal of Hygiene 58, 485488.Google ScholarPubMed
Martin, L. B., Hopkins, W. A., Mydlarz, L. D. and Rohr, J. R. (2010). The effects of anthropogenic global changes on immune functions and disease resistance. Annals of the New York Academy of Sciences 1195, 129148. doi: 10.1111/j.1749-6632.2010.05454.x.CrossRefGoogle ScholarPubMed
Massad, E. (1987). Transmission rates and the evolution of pathogenicity. Evolution 41, 11271130.CrossRefGoogle ScholarPubMed
May, R. M. and Anderson, R. M. (1979). Population biology of infectious diseases: part II. Nature 280, 455461.CrossRefGoogle ScholarPubMed
Mbora, D. N. and McPeek, M. A. (2009). Host density and human activities mediate increased parasite prevalence and richness in primates threatened by habitat loss and fragmentation. Journal of Animal Ecology 78, 210218. doi: 10.1111/j.1365-2656.2008.01481.x.CrossRefGoogle ScholarPubMed
Mbora, D. and Meikle, D. (2004 a). The value of unprotected habitat in conserving endangered species: case study of the Tana River red colobus in eastern Kenya. Biological Conservation 120, 9199.CrossRefGoogle Scholar
Mbora, D. N. M. and Meikle, D. B. (2004 b). Forest fragmentation and the distribution, abundance and conservation of the Tana River red colobus (Procolobus rufomitratus). Biological Conservation 118, 6777.CrossRefGoogle Scholar
McCallum, H. and Dobson, A. (2002). Disease, habitat fragmentation and conservation. Proceedings of the Royal Society of London, Series B 269, 20412049. doi: 10.1098/rspb.2002.2079.CrossRefGoogle ScholarPubMed
Mennerat, A., Nilsen, F., Ebert, D. and Skorping, A. (2010). Intensive farming: evolutionary implications for parasites and pathogens. Evolutionary Biology 37, 5967. doi: 10.1007/s11692-010-9089-0.CrossRefGoogle ScholarPubMed
Mennerat, A., Hamre, L., Ebert, D., Nilsen, F., Davidova, M. and Skorping, A. (2012). Life history and virulence are linked in the ectoparasitic salmon louse Lepeophtheirus salmonis . Journal of Evolutionary Biology 25, 856861. doi: 10.1111/j.1420-9101.2012.02474.x.CrossRefGoogle ScholarPubMed
Mideo, N. (2009). Parasite adaptations to within-host competition. Trends in Parasitology 25, 261268. doi: 10.1016/j.pt.2009.03.001.CrossRefGoogle ScholarPubMed
Mitchell, S. E., Rogers, E. S., Little, T. J. and Read, A. F. (2005). Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen. Evolution 59, 7080.Google ScholarPubMed
Møller, A. P. (2010). Host-parasite interactions and vectors in the barn swallow in relation to climate change. Global Change Biology 16, 11581170. doi: 10.1111/j.1365-2486.2009.02035.x.CrossRefGoogle Scholar
Morand, S. and Poulin, R. (1998). Density, body mass and parasite species richness of terrestrial mammals. Evolutionary Ecology 12, 717727.CrossRefGoogle Scholar
Moravec, F. (1996). Aquatic invertebrates (snails) as new paratenic hosts of Anguillicola crassus (Nematoda: Dracunculoidea) and the role of paratenic hosts in the life cycle of this parasite. Diseases of Aquatic Organisms 27, 237239.CrossRefGoogle Scholar
Moravec, F. and Škoriková, B. (1998). Amphibians and larvae of aquatic insects as new paratenic hosts of Anguillicola crassus (Nematoda: Dracunculoidea), a swimbladder parasite of eels. Diseases of Aquatic Organisms 34, 217222.CrossRefGoogle ScholarPubMed
Morley, N., Crane, M. and Lewis, J. (2002). Toxicity of cadmium and zinc to cercarial tail loss in Diplostomum spathaceum (Trematoda: Diplostomidae). Parasitology 125, 293301.CrossRefGoogle ScholarPubMed
Morley, N. J., Crane, M. and Lewis, J. W. (2005). Toxicity of cadmium and zinc mixtures to cercarial tail loss in Diplostomum spathaceum (Trematoda: Diplostomidae). Ecotoxicology and Environmental Safety 60, 5360. doi: 10.1016/j.ecoenv.2003.12.018.CrossRefGoogle ScholarPubMed
Munson, L., Terio, K. A., Kock, R., Mlengeya, T., Roelke, M. E., Dubovi, E., Summers, B., Sinclair, A. R. and Packer, C. (2008). Climate extremes promote fatal co-infections during canine distemper epidemics in African lions. PLoS ONE 3, e2545.CrossRefGoogle ScholarPubMed
Murray, A. G. and Peeler, E. J. (2005). A framework for understanding the potential for emerging diseases in aquaculture. Preventive Veterinary Medicine 67, 223235. doi: 10.1016/j.prevetmed.2004.10.012.CrossRefGoogle ScholarPubMed
Ostfeld, R. S. (2009). Climate change and the distribution and intensity of infectious diseases. Ecology 90, 903905.CrossRefGoogle ScholarPubMed
Ouellet, M., Mikaelian, I., Pauli, B. D., Rodrigue, J. and Green, D. M. (2005). Historical evidence of widespread chytrid infection in North American amphibian populations. Conservation Biology 19, 14311440.CrossRefGoogle Scholar
Palumbi, S. R. (2001). Humans as the world's greatest evolutionary force. Science 293, 17861790.CrossRefGoogle ScholarPubMed
Paterson, R. A., Townsend, C. R., Poulin, R. and Tompkins, D. M. (2011). Introduced brown trout alter native acanthocephalan infections in native fish. Journal of Animal Ecology 80, 990998. doi: 10.1111/j.1365-2656.2011.01834.x.CrossRefGoogle ScholarPubMed
Paull, S. H. and Johnson, P. T. J. (2011). High temperature enhances host pathology in a snail–trematode system: possible consequences of climate change for the emergence of disease. Freshwater Biology 56, 767778. doi: 10.1111/j.1365-2427.2010.02547.x.CrossRefGoogle Scholar
Pietrock, M. and Marcogliese, D. J. (2003). Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293299. doi: 10.1016/s1471-4922(03)00117-x.CrossRefGoogle ScholarPubMed
Poulin, R. (2003). Information about transmission opportunities triggers a life-history switch in a parasite. Evolution 57, 28992903.Google Scholar
Poulin, R. (2006). Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143151. doi: 10.1017/S0031182005008693.CrossRefGoogle ScholarPubMed
Prenter, J., MacNeil, C., Dick, J. T. A. and Dunn, A. M. (2004). Roles of parasites in animal invasions. Trends in Ecology and Evolution 19, 385390.CrossRefGoogle ScholarPubMed
Pulkkinen, K., Suomalainen, L. R., Read, A. F., Ebert, D., Rintamaki, P. and Valtonen, E. T. (2010). Intensive fish farming and the evolution of pathogen virulence: the case of columnaris disease in Finland. Proceedings of the Royal Society of London, Series B 277, 593600. doi: 10.1098/rspb.2009.1659.Google ScholarPubMed
Purse, B. V., Mellor, P. S., Rogers, D. J., Samuel, A. R., Mertens, P. P. and Baylis, M. (2005). Climate change and the recent emergence of bluetongue in Europe. Nature Reviews Microbiology 3, 171181.CrossRefGoogle ScholarPubMed
Rachowicz, L. J., Hero, J., Alford, R. A., Taylor, J. W., Morgan, J. A. T., Vredenburg, V. T., Collins, J. P. and Briggs, C. J. (2005). The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conservation Biology 19, 14411448.CrossRefGoogle Scholar
Raffel, T. R., Martin, L. B. and Rohr, J. R. (2008). Parasites as predators: unifying natural enemy ecology. Trends in Ecology and Evolution 23, 610618. doi: 10.1016/j.tree.2008.06.015.CrossRefGoogle ScholarPubMed
Reiter, P. (2001). Climate change and mosquito-borne disease. Environmental Health Perspectives 109 (Suppl. 1), 141.Google ScholarPubMed
Rigaud, T., Perrot-Minnot, M. J. and Brown, M. J. (2010). Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proceedings of the Royal Society of London, Series B 277, 36933702. doi: 10.1098/rspb.2010.1163.Google ScholarPubMed
Rogers, D. J. and Randolph, S. E. (2006). Climate change and vector-borne diseases. Advances in Parasitology 62, 345381.CrossRefGoogle ScholarPubMed
Rohr, J. R. and McCoy, K. A. (2010). A qualitative meta-analysis reveals consistent effects of atrazine on freshwater fish and amphibians. Environmental Health Perspectives 118, 2032.CrossRefGoogle ScholarPubMed
Rohr, J. R., Swan, A., Raffel, T. R. and Hudson, P. J. (2009). Parasites, info-disruption, and the ecology of fear. Oecologia 159, 447454. doi: 10.1007/s00442-008-1208-6.CrossRefGoogle ScholarPubMed
Rosenberg, E. and Ben-Haim, Y. (2002). Microbial diseases of corals and global warming. Environmental Microbiology 4, 318326.CrossRefGoogle ScholarPubMed
Rosenberg, E. and Falkovitz, L. (2004). The Vibrio shiloi/Oculina patagonica model system of coral bleaching. Annual Review of Microbiology 58, 143159.CrossRefGoogle ScholarPubMed
Rymuszka, A., Siwicki, A. K. and Sieroslawska, A. (2007). Determination of the modulatory potential of atrazine on selected functions of immune cells isolated from rainbow trout (Oncorhynchus mykiss). Central European Journal of Immunology 32, 97100.Google Scholar
Schuurman, H. J., Frieke Kuper, C. and Vos, J. G. (1994). Histopathology of the immune system as a tool to assess immunotoxicity. Toxicology 86, 187212.CrossRefGoogle ScholarPubMed
Schweiger, O., Settele, J., Kudrna, O., Klotz, S. and Kühn, I. (2008). Climate change can cause spatial mismatch of trophically interacting species. Ecology 89, 34723479.CrossRefGoogle ScholarPubMed
Shephard, K. L. (1994). Functions for fish mucus. Reviews in Fish Biology and Fisheries 4, 401429.CrossRefGoogle Scholar
Sih, A. (2013). Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview. Animal Behaviour 85, 10771088.CrossRefGoogle Scholar
Sonnenholzner, J. I., Lafferty, K. D. and Ladah, L. B. (2011). Food webs and fishing affect parasitism of the sea urchin Eucidaris galapagensis in the Galápagos. Ecology 92, 22762284.CrossRefGoogle ScholarPubMed
Sures, B. (2006). How parasitism and pollution affect the physiological homeostasis of aquatic hosts. Journal of Helminthology 80, 151157. doi: 10.1079/joh2006346.CrossRefGoogle ScholarPubMed
Sures, B. (2008). Host-parasite interactions in polluted environments. Journal of Fish Biology 73, 21332142.CrossRefGoogle Scholar
Telfer, S., Bown, K. J., Sekules, R., Begon, M., Hayden, T. and Birtles, R. (2005). Disruption of a host-parasite system following the introduction of an exotic host species. Parasitology 130, 661668. doi: 10.1017/s0031182005007250.CrossRefGoogle ScholarPubMed
Thieltges, D. W. and Poulin, R. (2008). Parasites and pathogens: avoidance. In Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Chichester, UK.Google Scholar
Thieltges, D. W., Jensen, K. T. and Poulin, R. (2008 a). The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology 135, 407426. doi: 10.1017/S0031182007000248.CrossRefGoogle ScholarPubMed
Thieltges, D. W., Reise, K., Prinz, K. and Jensen, K. T. (2008 b). Invaders interfere with native parasite–host interactions. Biological Invasions 11, 14211429. doi: 10.1007/s10530-008-9350-y.CrossRefGoogle Scholar
Thomas, F., Brown, S. P., Sukhdeo, M. V. and Renaud, F. (2002). Understanding parasite strategies: a state-dependent approach? Trends in Parasitology 18, 387390.CrossRefGoogle ScholarPubMed
Thompson, J. N. (1994). The Coevolutionary Process. University of Chicago Press, Chicago, IL, USA.CrossRefGoogle Scholar
Thompson, J. N. (2005). The Geographic Mosaic of Coevolution. University of Chicago Press, Chicago, IL, USA.CrossRefGoogle Scholar
Tierney, J. F. and Crompton, D. W. T. (1992). Infectivity of plerocercoids of Schistocephalus solidus (Cestoda: Ligulidae) and fecundity of the adults in an experimental definitive host, Gallus gallus . Journal of Parasitology 78, 10491054.CrossRefGoogle Scholar
Tolonen, A. and Kjellman, J. (2001). Post-stocking perturbations in a population of subarctic whitefish, Coregonus lavaretus (L.): effects on growth, condition and cestode infection. Hydrobiologia 445, 5766.CrossRefGoogle Scholar
Torchin, M. E. and Lafferty, K. D. (2008). Escape from parasites. In Marine Bioinvasions: Ecology, Conservation and Management Perspectives (ed. Rilov, G. and Crooks, J.), pp. 203214. Springer-Verlag, Berlin, Germany.Google Scholar
Torchin, M. E., Lafferty, K. D. and Kuris, A. M. (2002). Parasites and marine invasions. Parasitology 124, S137S151. doi: 10.1017/s0031182002001506.CrossRefGoogle Scholar
Torchin, M. E., Lafferty, K. D., Dobson, A. P., McKenzie, V. J. and Kuris, A. M. (2003). Introduced species and their missing parasites. Nature 421, 628630. doi: 10.1038/nature01346.CrossRefGoogle ScholarPubMed
Tschirren, B., Bischoff, L. L., Saladin, V. and Richner, H. (2007). Host condition and host immunity affect parasite fitness in a bird–ectoparasite system. Functional Ecology 21, 372378. doi: 10.1111/j.1365-2435.2007.01235.x.CrossRefGoogle Scholar
Tseng, M. (2006). Interactions between the parasite's previous and current environment mediate the outcome of parasite infection. American Naturalist 168, 565571.CrossRefGoogle ScholarPubMed
Turner, B. L. II, Kasperson, R. E., Meyer, W. B., Dow, K. M., Golding, D., Kasperson, J. X., Mitchell, R. C. and Ratick, S. J. (1990). Two types of global environmental change: definitional and spatial-scale issues in their human dimensions. Global Environmental Change 1, 1422.CrossRefGoogle Scholar
Wajnberg, E., Bernstein, C. and Van Alphen, J. (2008). Behavioural Ecology of Insect Parasitoids: from Theoretical Approaches to Field Applications. Wiley-Blackwell, Oxford, UK.CrossRefGoogle Scholar
Ward, J. R. and Lafferty, K. D. (2004). The elusive baseline of marine disease: are diseases in ocean ecosystems increasing? PLoS Biology 2, e120.CrossRefGoogle ScholarPubMed
Weldon, C., Du Preez, L. H., Hyatt, A. D., Muller, R. and Speare, R. (2004). Origin of amphibian chytrid fungus. Emerging Infectious Diseases 10, 21002105.CrossRefGoogle ScholarPubMed
Wieczkowski, J. and Mbora, D. (2000). Increasing threats to the conservation of endemic endangered primates and forests of the lower Tana River, Kenya. African Primates 4, 3240.Google Scholar
Wolinska, J. and King, K. C. (2009). Environment can alter selection in host-parasite interactions. Trends in Parasitology 25, 236244. doi: 10.1016/j.pt.2009.02.004.CrossRefGoogle ScholarPubMed
Wood, C. L., Lafferty, K. D. and Micheli, F. (2010). Fishing out marine parasites? Impacts of fishing on rates of parasitism in the ocean. Ecology Letters 13, 761775. doi: 10.1111/j.1461-0248.2010.01467.x.CrossRefGoogle ScholarPubMed
Zhao, J., Neher, D. A., Fu, S., Li, Z. A. and Wang, K. (2013). Non-target effects of herbicides on soil nematode assemblages. Pest Management Science 69, 679684.CrossRefGoogle ScholarPubMed