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Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm

Published online by Cambridge University Press:  16 February 2012

Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK
Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK British Trust for Ornithology Scotland, Cottrell Building, University of Stirling, Stirling SFK9 4LA, UK


The twin concepts of zooprophylaxis and the dilution effect originated with vector-borne diseases (malaria), were driven forward by studies on Lyme borreliosis and have now developed into the mantra “biodiversity protects against disease”. The basic idea is that by diluting the assemblage of transmission-competent hosts with non-competent hosts, the probability of vectors feeding on transmission-competent hosts is reduced and so the abundance of infected vectors is lowered. The same principle has recently been applied to other infectious disease systems – tick-borne, insect-borne, indirectly transmitted via intermediate hosts, directly transmitted. It is claimed that the presence of extra species of various sorts, acting through a variety of distinct mechanisms, causes the prevalence of infectious agents to decrease. Examination of the theoretical and empirical evidence for this hypothesis reveals that it applies only in certain circumstances even amongst tick-borne diseases, and even less often if considering the correct metric – abundance rather than prevalence of infected vectors. Whether dilution or amplification occurs depends more on specific community composition than on biodiversity per se. We warn against raising a straw man, an untenable argument easily dismantled and dismissed. The intrinsic value of protecting biodiversity and ecosystem function outweighs this questionable utilitarian justification.

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Copyright © Cambridge University Press 2012

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Allan, B. F., Dutra, H. P., Goessling, L. S., Barnett, K., Chase, J. M., Marquis, R. J., Pang, G., Storch, G. A., Thach, R. E. and Orrock, J. L. (2011). Invasive honeysuckle eradication reduces tick-borne disease risk by altering host dynamics. Proceedings of the National Academy of Sciences, USA 107, 1852318527.CrossRefGoogle Scholar
Allan, B. F., Goessling, L. S., Storch, G. A. and Thach, R. E. (2010). Identification of reservoir hosts for Amblyomma americanum-associated zoonoses using bloodmeal analysis. Emerging Infectious Diseases 16, 433440.CrossRefGoogle Scholar
Allan, B. F., Keesing, F. and Ostfeld, R. S. (2003). Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17, 267272.CrossRefGoogle Scholar
Allan, B. F., Langerhaus, R. B., Ryberg, W. A., Landesman, W. J., Griffin, N. W., Katz, R. S., Oberle, B. J., Schutzenhofer, M. R., Smyth, K. N., de St Maurice, A., Clark, L., Crooks, K. R., Hernandez, D. E., McLean, R. G., Ostfeld, R. S. and Chase, J. M. (2009). Ecological correlates of risk and incidence of West Nile virus in the United States. Oecologia 158, 699708.CrossRefGoogle ScholarPubMed
Apperson, C. S., Levine, J. F., Evans, T. L., Braswell, A. and Heller, J. (1993). Relative utilization of reptiles and rodents as hosts by immature Ixodes scapularis (Acari: Ixodidae) in the coastal plain of North Carolina, USA. Experimental and Applied Acarology 17, 719731.Google ScholarPubMed
Begon, M. (2008). Effects of host diversity on disease dynamics. In Infectious Disease Ecology: Effects of Ecosystems on Disease and of Disease on Ecosystems. (ed. Ostfeld, R. S., Keesing, F. and Eviner, V. T.), pp. 1229. Princeton University Press, Princeton. NJ, USA.Google Scholar
Bogh, C., Clarke, S. E., Walraven, G. E. L. and Lindsay, S. W. (2002). Zooprophylaxis, artefact or reality? A paired-cohort study of the effect of passive zooprophylaxis on malaria in The Gambia. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 593596.CrossRefGoogle ScholarPubMed
Borer, E. T., Mitchell, C. E., Power, A. G. and Seabloom, E. W. (2009). Consumers indirectly increase infection risk in grassland food webs. Proceedings of the National Academy of Sciences, USA 106, 503506.CrossRefGoogle ScholarPubMed
Bouma, M. J. and Rowland, M. (1995). Failure of passive zooprophylaxis: cattle ownership in Parkistan is associated with a higher prevalence of malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 351353.CrossRefGoogle Scholar
Brisson, D., Dykhuizen, D. E. and Ostfeld, R. S. (2008). Conspicuous impacts of inconspicuous hosts on the Lyme disease epidemic. Proceedings of the Royal Society of London, B 275, 227235.CrossRefGoogle ScholarPubMed
Bruemmer, C. M., Rushton, S. P., Gurnell, J., Lurz, P. W. W., Nettleton, P., Sainsbury, A. W., Duff, J. P., Gilray, J. and McInnes, C. J. (2010). Epidemiology of squirrelpox in grey squirrels in the UK. Epidemiology & Infection 138, 941950.CrossRefGoogle ScholarPubMed
Brunner, J. L. and Ostfeld, R. S. (2008). Multiple causes of variable tick burdens on small-mammal hosts. Ecology 89, 22592272.CrossRefGoogle ScholarPubMed
Burri, C., Bastic, V., Maeder, G., Patalas, E. and Gern, L. (2011). Microclimate and the zoonotic cycle of tick-borne encephalitis virus in Switzerland. Journal of Medical Entomology 48, 615627.CrossRefGoogle ScholarPubMed
Carlson, J. C., Dyer, L. A., Omlin, F. X. and Beier, J. C. (2009). Diversity cascades and malaria vectors. Journal of Medical Entomology 46, 460464.CrossRefGoogle ScholarPubMed
Civitello, D. J., Flory, S. L. and Clay, K. (2008). Exotic grass invasion reduces survival of Amblyomma americanum and Dermacentor variabilis ticks (Acari: Ixodidae). Journal of Medical Entomology 45, 867872.CrossRefGoogle Scholar
Clover, J. R. and Lane, R. S. (1995). Evidence implicating nymphal Ixodes pacificus (Acari: Ixodidae) in the epidemiology of Lyme disease in California. American Journal of Tropical Medicine and Hygiene 53, 237240.CrossRefGoogle ScholarPubMed
Costello, A., Abbas, M., Allen, A., Ball, S., Bellamy, R., Friel, S., Grace, N., Johnson, A., Kett, M., Lee, M., Levy, C., Maslin, M., McCoy, D., McGuire, B., Montgomery, H., Napier, D., Pagel, C., Patel, J., de Oliveira, J. A. P., Redclift, N., Rees, H., Rogger, D., Scott, J., Stephenson, J., Twigg, J., Wolff, J. and Patterson, C. (2009). Managing the health effects of climate change. The Lancet 373, 16931733.CrossRefGoogle ScholarPubMed
Craine, N. G., Randolph, S. E. and Nuttall, P. A. (1995). Seasonal variation in the rôle of grey squirrels as hosts of Ixodes ricinus, the tick vector of the Lyme disease spirochaete, in a British woodland. Folia Parasitologica 42, 7380.Google Scholar
Dalkvist, T., Sibly, R. M. and Topping, C. J. (2011). How predation and landscape fragmentation affect vole population dynamics. PLoS ONE 6, e22834.CrossRefGoogle ScholarPubMed
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2001). Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78, 103116.CrossRefGoogle ScholarPubMed
Diaz, S., Fargione, J., Chapin, F. S. I. and Tilman, D. (2006). Biodiversity loss threatens human well-being. PLoS Biology 4, 13001305.CrossRefGoogle ScholarPubMed
Dizney, L. J. and Ruedas, L. A. (2009). Increased host species diversity and decreased prevalence of Sin Nombre virus. Emerging Infectious Diseases 15, 10121018.CrossRefGoogle ScholarPubMed
Dobson, A. P. (2004). Population dynamics of pathogens with multiple host species. The American Naturalist 164 (Suppl.) S64S78.CrossRefGoogle ScholarPubMed
Dobson, A., Cattadori, I., Holt, R. D., Ostfeld, R. S., Keesing, F., Krichbaum, K., Rohr, J. R., Perkins, S. E. and Hudson, P. J. (2006). Sacred cows and sympathetic squirrels: the importance of biological diversity to human health. PLoS Medicine 3, 714718.CrossRefGoogle ScholarPubMed
Dobson, A., Lafferty, K. D., Kuris, A. M., Hechinger, R. F. and Jetz, W. (2008). Homage to Linneaus: How many parasites? How many hosts? Proceedings of the National Academy of Sciences, USA 105, (Suppl. 1), 1148211489.Google Scholar
Dobson, A. D. M., Finnie, T. J. R. and Randolph, S. E. (2011). A modified matrix model to describe the seasonal population ecology of the European tick Ixodes ricinus. Journal of Applied Ecology 48, 10171028.CrossRefGoogle Scholar
Dobson, A. D. M. and Randolph, S. E. (2011). Modelling the effects of recent changes in climate, host density and acaricide treatments on population dynamics of Ixodes ricinus in the UK. Journal of Applied Ecology 48, 10291037.CrossRefGoogle Scholar
Dowling, D. K. and Simmons, L. W. (2009). Reactive oxygen species as universal constraints in life-history evolution. Proceedings of Royal Society of London, B 276, 17371745.CrossRefGoogle ScholarPubMed
Elias, S. P., Lubelczyk, C. B., Rand, P. W., Lacombe, E. H., Holman, M. S. and Smith, R. P. J. (2006). Deer browse resistant exotic-invasive understory: an indicator of elevated human risk of exposure to Ixodes scapularis (Acari: Ixodidae) in southern coastal Maine woodlands. Journal of Medical Entomology 43, 11421152.CrossRefGoogle ScholarPubMed
Elton, C. S. (1958). The Ecology of Invasions by Animals and Plants. Methuen, London, UK.CrossRefGoogle Scholar
Ezenwa, V. O., Godsey, M. S., King, R. J. and Guptill, S. C. (2006). Avian diversity and West Nile virus: testing associations between biodiversity and infectious disease risk. Proceedings of Royal Society of London, B 273, 109117.CrossRefGoogle ScholarPubMed
Falco, R. C., McKenna, D. F., Daniels, T. J., Nadelman, R. B., Nowakowski, J., Fish, D. and Wormser, G. P. (1999). Temporal relation between Ixodes scapularis abundance and risk for Lyme disease associated with erythema migrans. American Journal of Epidemiology 149, 771776.CrossRefGoogle ScholarPubMed
Gern, L., Estrada-Peña, A., Frandsen, F., Gray, J., J. S., G., Jaenson, T. G. T., Jongejan, F., Kahl, O., Korenberg, E., Mehl, R. and Nuttall, P. A. (1998). European reservoir hosts of Borrelia burgdorferi sensu lato. Zentralblatt für Bakteriologie 287, 196204.CrossRefGoogle ScholarPubMed
Giardina, A. R., Schmidt, K. A., Schauber, E. M. and Ostfeld, R. S. (2000). Modeling the role of songbirds and rodents in the ecology of Lyme disease. Canadian Journal of Zoology 78, 21842197.CrossRefGoogle Scholar
Gilbert, L., Norman, R., Laurenson, M. K., Reid, H. W. and Hudson, P. J. (2001). Disease persistence and apparent competition in a three-host community: an empirical and analytical study of large-scale, wild populations. Journal of Animal Ecology 70, 10531061.CrossRefGoogle Scholar
Glass, G. E., Schwarz, B. S., Morgan III, J. M., Johnson, D. T., Noy, P. M. and Israel, E. (1995). Environmental risk factor for Lyme disease identified with geographic information systems. American Journal of Public Health 85, 944948.CrossRefGoogle ScholarPubMed
Gray, J. S., Kahl, O., Janetzki, C. and Stein, J. (1992). Studies on the ecology of Lyme disease in a deer forest in County Galway, Ireland. Journal of Medical Entomology 29, 915920.CrossRefGoogle Scholar
Guernier, V., Hochberg, M. E. and Guegan, J.-F. (2004). Ecology drives the worldwide distribution of human diseases. PLoS Biology 2, 0740.CrossRefGoogle ScholarPubMed
Hamer, G. L., Chaves, L. F., Anderson, T. K., Kitron, U. D., Brawn, J. D., Ruiz, M. O., Loss, S. R., Walker, E. D. and Goldberg, T. L. (2011). Fine-scale variation in vector host use and force of infection drive localized patterns of West Nile virus transmission. PLoS ONE 6, e23767.CrossRefGoogle ScholarPubMed
Hanincova, K., Ogden, N. H., Diuk-Wasser, M., Pappas, C. J., Iyer, R., Fish, D., Schwartz, I. and Kurtenbach, K. (2008). Fitness variation of Borrelia burgdorferi sensu stricto strains in mice. Applied and Environmental Microbiology 74, 153157.CrossRefGoogle ScholarPubMed
Hanski, I., Hansson, L. and Henttonen, H. (1991). Specialist predators, generalist predators, and the microtine rodent cycle. Journal of Animal Ecology 60, 353367.CrossRefGoogle Scholar
Hartemink, N. A., Davis, S. A., Reiter, P., Hubálek, Z. and Heesterbeek, J. A. P. (2007). Importance of bird-to-bird transmission for the establishment of West Nile virus. Vector-Borne and Zoonotic Diseases 7, 575584.CrossRefGoogle ScholarPubMed
Hawley, D. M. and Altizer, S. M. (2011). Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Functional Ecology 25, 4860.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.CrossRefGoogle ScholarPubMed
Hess, A. D. and Hayes, R. O. (1970). Relative potentials of domestic animals for zooprophylaxis against mosquito vectors of encephalitis. American Journal of Tropical Medicine and Hygiene 19, 327334.CrossRefGoogle ScholarPubMed
Holt, R. D. and Lawton, J. H. (1994). The ecological consequences of shared natural enemies. Annual Review of Ecology and Systematics 25, 495520.CrossRefGoogle Scholar
Hoodless, A. N., Kurtenbach, K., Nuttall, P. A. and Randolph, S. E. (2002). The impact of ticks on pheasant territoriality. Oikos 96, 245250.CrossRefGoogle Scholar
Hoogstraal, H. (1981). Changing patterns of tick-borne diseases in modern society. Annual Review of Entomology 26, 7599.CrossRefGoogle ScholarPubMed
Horobik, V., Keesing, F. and Ostfeld, R. S. (2007). Abundance and Borrelia burgdorferi-infection prevalence of nymphal Ixodes scapularis ticks along forest-field edges. EcoHealth 3, 262268.CrossRefGoogle Scholar
Horrocks, N. P. C., Matson, K. D. and Tieleman, B. I. (2011). Pathogen pressure puts immune defense into perspective. Integrative and Comparative Biology 51, 563576.CrossRefGoogle ScholarPubMed
Hubálek, Z. and Halouzka, J. (1998). Prevalence rates of Borrelia burgdorferi sensu lato in host-seeking Ixodes ricinus ticks in Europe. Parasitology Research 84, 167172.Google Scholar
Hubálek, Z. and Halouzka, J. (1999). West Nile virus – a reemerging mosquito-borne viral disease in Europe. Emerging Infectious Diseases 5, 643650.CrossRefGoogle Scholar
Hudson, P. J., Rizzoli, A., Rosa, R., Chemini, C., Jones, L. D. and Gould, E. A. (2001). Tick-borne encephalitis virus in northern Italy: molecular analysis, relationships with density and seasonal dynamics of Ixodes ricinus. Medical and Veterinary Entomology 15, 304313.CrossRefGoogle ScholarPubMed
Humair, P.-F. and Gern, L. (1998). Relationship between Borrelia burgdorferi sensu lato species, red squirrels (Sciurus vulgaris) and Ixodes ricinus in enzootic areas in Switzerland. Acta Tropica 69, 213227.CrossRefGoogle ScholarPubMed
Humair, P.-F., Postic, D., Wallich, R. and Gern, L. (1998). An avian reservoir (Turdus merula) of the Lyme borreliosis spirochetes. Zentralblatt für Bakteriologie 287, 521538.Google ScholarPubMed
Jensen, P. M. and Frandsen, F. (2000). Temporal risk assessment for Lyme borreliosis in Denmark. Scandinavian Journal of Infectious Diseases 35, 539544.Google Scholar
Jensen, P. M., Hansen, H. and Frandsen, F. (2000). Spatial risk assessment for Lyme borreliosis in Denmark. Scandinavian Journal of Infectious Diseases 35, 545550.Google Scholar
Johnson, P. T. J., Hartson, R. B., Larson, D. J. and Sutherland, D. R. (2008). Diversity and disease: community structure drives parasite transmission and host fitness. Ecology Letters 11, 10171026.CrossRefGoogle ScholarPubMed
Johnson, P. T. J., Lund, P. J., Hartson, R. B. and Yoshino, T. P. (2009). Community diversity reduces Schistosoma mansoni transmission, host pathology and human infection risk. Proceedings of Royal Society of London, B 276, 16571663.CrossRefGoogle ScholarPubMed
Johnson, P. T. J. and Thieltges, D. W. (2010). Diversity, decoys and the dilution effect: how ecological communities affect disease risk. Journal of Experimental Biology 213, 961970.CrossRefGoogle ScholarPubMed
Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman, J. L. and Daszak, P. (2008). Global trends in emerging infectious diseases. Nature, London 451, 990994.CrossRefGoogle ScholarPubMed
Keesing, F., Belden, L. K., Daszak, P., Dobson, A., Harvell, C. D., Holt, R. D., Hudson, P., Jolles, A., Jones, K. E., Mitchell, C. E., Myers, S. S., Bogich, T. and Ostfeld, R. S. (2010). Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature, London 468, 647652.CrossRefGoogle ScholarPubMed
Keesing, F., Brunner, J., Duerr, S., Killilea, M., LoGiudice, K., Schmidt, K., Vuong, H. and Ostfeld, R. S. (2009). Hosts as ecological traps for the vector of Lyme disease. Proceedings of the Royal Society, B 276, 39113919.CrossRefGoogle ScholarPubMed
Keesing, F., Holt, R. D. and Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecology Letters 9, 485498.CrossRefGoogle ScholarPubMed
Kilpatrick, M., Daszak, P., Jones, M. J., Marra, P. P. and Kramer, L. D. (2006). Host heterogeneity dominates West Nile virus transmission. Proceedings of the Royal Society of London, B 273, 23272333.CrossRefGoogle ScholarPubMed
Kimura, K., Isogal, E., Isogal, H., Kamewaka, Y., Nishikawa, T., Ishii, N. and Fujii, N. (1995). Detection of Lyme disease spirochetes in the skin of naturally infected wild sika deer (Cervus nippon yesoensis) by PCR. Applied and Environmental Microbiology 61, 16411642.Google ScholarPubMed
Komar, N., Langevin, S., Hinten, S., Nemeth, N., Edwards, E., Hettler, D., Davis, B., Bowen, R. and Bunning, M. (2003). Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerging Infectious Diseases 9, 311322.CrossRefGoogle ScholarPubMed
Kostiukov, M. A., Alekseev, A. N., Bulychev, V. P. and Gordeeva, Z. E. (1986). [Experimental evidence for infection of Culex pipiens L. mosquitoes by West Nile fever virus from Rana ridibunda Pallas and its transmission by bites]. Meditsinskaya Parazitologiya i Parazitarnye Bolezni 6, 7678.Google Scholar
Kurtenbach, K., Carey, D., Hoodless, A. N., Nuttall, P. A. and Randolph, S. E. (1998 a). Competence of pheasants as reservoirs for Lyme disease spirochetes. Journal of Medical Entomology 35, 7781.CrossRefGoogle ScholarPubMed
Kurtenbach, K., Hanincova, K., Tsao, J. I., Margos, G., Fish, D. and Ogden, N. H. (2006). Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nature Reviews Microbiology 4, 660669.CrossRefGoogle ScholarPubMed
Kurtenbach, K., Peacey, M. F., Rijpkema, S. G. T., Hoodless, A. N., Nuttall, P. A. and Randolph, S. E. (1998 b). Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Applied and Environmental Microbiology 64, 11691174.Google ScholarPubMed
Kurtenbach, K., Sewell, H., Ogden, N. H., Randolph, S. E. and Nuttall, P. A. (1998 c). Serum complement as a key factor in Lyme disease ecology. Infection and Immunity 66, 12481251.Google ScholarPubMed
Lane, R. S. and Quistad, G. B. (1998). Borreliacidal factor in the blood of the western fence lizard (Sceloporus occidentalis). Journal of Parasitology 84, 2934.CrossRefGoogle Scholar
Larigauderie, A. and Mooney, H. A. (2010). The Intergovernmental science-policy Platform on Biodiversity and Ecosystems Services: moving a step closer to an IPCC-like mechanism for biodiversity. Current Opinion in Environmental Sustainability 2, 914.CrossRefGoogle Scholar
Lee, K. A., Martin, L. B., Hasselquist, D., Ricklefs, R. E. and Wikelski, M. (2006). Contrasting adaptive immune defenses and blood parasite prevalence in closely related Passer sparrows. Oecologia 150, 383392.CrossRefGoogle ScholarPubMed
Lee, K. A., Wikelski, M., Robinson, W. D., Robinson, T. R. and Klasing, K. C. (2008). Constitutive immune defences correlate with life-history variables in tropical birds. Journal of Animal Ecology 77, 356363.CrossRefGoogle ScholarPubMed
Linard, C., Lamarque, P., Heyman, P., Ducoffre, G., Lutasu, V., Tersago, K., Vanwambeke, S. O. and Lambin, E. F. (2007). Determinants of the geographic distribution of Puumala virus and Lyme borreliosis infections in Belgium. International Journal of Health Geographics 6, 1529.CrossRefGoogle ScholarPubMed
LoGiudice, K., Duerr, S. T. K., Newhouse, M. J., Schmidt, K. A., Killilea, M. E. and Ostfeld, R. S. (2008). Impact of host community composition on Lyme disease risk. Ecology 89, 28412849.CrossRefGoogle ScholarPubMed
LoGiudice, K., Ostfeld, R. S., Schmidt, K. A. and Keesing, F. (2003). The ecology of infectious disease: Effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences, USA 100, 567571.CrossRefGoogle ScholarPubMed
Loss, S. R., Hamer, G. L., Walker, E. D., Ruiz, M. O., Goldberg, T. L., Kitron, U. and Brawn, J. D. (2009). Avian host community structure and prevalence of West Nile virus in Chicago, Illinois. Oecologia 159, 415424.CrossRefGoogle ScholarPubMed
Macdonald, G. (1956). Epidemiological basis of malaria control. Bulletin of the World Health Organization 15, 613626.Google ScholarPubMed
Marina, C. F., Bond, J. G., Casas, M., Munoz, J., Orozco, A., Valle, J. and Williams, T. (2011). Spinosad as an effective larvicide for control of Aedes albopictus and Aedes aegypti, vectors of dengue in southern Mexico. Pest Management Science 67, 114121.CrossRefGoogle ScholarPubMed
Marris, E. (2010). UN body will assess ecosystems and biodiversity. Nature, London 465, 859859.CrossRefGoogle ScholarPubMed
Martin, L. B., Hasselquist, D. and Wikelski, M. (2006). Investment in immune defense is linked to pace of life in house sparrows. Oecologia 147, 565575.CrossRefGoogle ScholarPubMed
Martin, L. B., Weil, Z. M. and Nelson, R. J. (2007). Immune defense and reproductive pace of life in Peromyscus mice. Ecology 88, 25162528.CrossRefGoogle ScholarPubMed
Matuschka, F.-R., Fischer, P., Heiler, M., Richter, D. and Spielman, A. (1992). Capacity of European animals as reservoir hosts for the Lyme disease spirochete. Journal of Infectious Diseases 165, 479483.CrossRefGoogle ScholarPubMed
Matuschka, F.-R., Heiler, M., Eiffert, H., Fischer, P., Lotter, H. and Spielman, A. (1993). Diversionary role of hoofed game in the transmission of Lyme-disease spirochetes. American Journal of Tropical Medicine and Hygiene 48, 693699.CrossRefGoogle ScholarPubMed
Matuschka, F.-R., Schinkel, T. W., Klug, B., Spielman, A. and Richter, D. (2000). Relative importance of European rabbits for Lyme disease spirochaetes. Parasitology 121, 297302.CrossRefGoogle Scholar
Miller, D. L., Mauel, M. J., Baldwin, C. L., Burtle, G., Ingram, D., Hines, M. E. and Frazier, K. S. (2003). West Nile virus in farmed alligators. Emerging Infectious Diseases 9, 794799.CrossRefGoogle ScholarPubMed
Murgue, B., Murri, S., Zientara, S., Durand, B., Durand, J.-P. and Zeller, H. (2001). West Nile outbreak in horses in southern France, 2000: the return after 35 years. Emerging Infectious Diseases 7, 692696.CrossRefGoogle Scholar
Nah, K., Kim, Y. and Lee, J. M. (2010). The dilution effect of the domestic animal population on the transmission of P. vivax malaria. Journal of Theoretical Biology 266, 299306.CrossRefGoogle ScholarPubMed
Nupp, T. E. and Swihart, R. K. (1996). Effect of forest patch area on population attributes of white-footed mice (Peromyscus leucopus) in fragmented landscapes. Canadian Journal of Zoology 74, 467472.CrossRefGoogle Scholar
Nupp, T. E. and Swihart, R. K. (1998). Effects of forest fragmentation on population attributes of white-footed mice and eastern chipmunks. Journal of Mammalogy 79, 12341243.CrossRefGoogle Scholar
Ogden, N. H., Nuttall, P. A. and Randolph, S. E. (1997). Natural Lyme disease cycles maintained via sheep by co-feeding ticks. Parasitology 115, 591599.CrossRefGoogle ScholarPubMed
Ogden, N. H. and Tsao, J. I. (2009). Biodiversity and Lyme disease: dilution or amplification? Epidemics 1, 196206.CrossRefGoogle ScholarPubMed
Orrock, J. L., Allan, B. F. and Drost, C. A. (2011). Biogeographic and ecological regulation of disease: prevalence of Sin Nombre virus in island mice is related to island area, precipitation, and predator richness. American Naturalist 177, 691697.CrossRefGoogle ScholarPubMed
Ostfeld, R. S. (2009). Biodiversity loss and the rise of zoonotic pathogens. Clinical Infectious Diseases 15, 4043.Google ScholarPubMed
Ostfeld, R. S., Canham, C. D., Oggenfuss, K., Winchcombe, R. J. and Keesing, F. (2006). Climate, deer, rodents, and acorns as determinants of variation in Lyme-disease risk. PLoS Biology 4, e145.CrossRefGoogle ScholarPubMed
Ostfeld, R. S. and 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.CrossRefGoogle Scholar
Ostfeld, R. S. and Keesing, F. (2000 a). Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14, 722728.CrossRefGoogle Scholar
Ostfeld, R. S. and Keesing, F. (2000 b). The function of biodiversity in the ecology of vector-borne zoonotic diseases. Canadian Journal of Zoology 78, 20612078.CrossRefGoogle Scholar
Ostfeld, R. S. and LoGiudice, K. (2003). Community disassembly, biodiversity loss, and the erosion of an ecosystem service. Ecology 84, 14211427.CrossRefGoogle Scholar
Packer, C., Holt, R. D., Hudson, P. J., Lafferty, K. D. and Dobson, A. P. (2003). Keeping herds healthy and alert: implications of predator control for infectious disease. Ecology Letters 6, 797802.CrossRefGoogle Scholar
Paddock, C. D. and Yabsley, M. J. (2007). Ecological havoc, the rise of white-tailed deer, and the emergence of Amblyomma americanum-associated zoonoses in the United States. Current Topics in Microbiology and Immunology 315, 289324.Google ScholarPubMed
Peixoto, I. D. and Abramson, G. (2006). The effect of biodiversity on the hantavirus epizootic. Ecology 87, 873879.CrossRefGoogle ScholarPubMed
Perkins, S. E., Cattadori, I. M., Tagliapietra, V., Rizzoli, A. and Hudson, P. J. (2006). Localized deer absence leads to tick amplification. Ecology 87, 19811986.CrossRefGoogle ScholarPubMed
Piesman, J. (2002). Ecology of Borrelia burgdorferi sensu lato in North America. In Lyme Borreliosis Biology, Epidemiology and Control (ed. Gray, J. S., Kahl, O., Lane, R. S. and Stanek, G.), pp. 223250. CABI, Wallingford, UK.CrossRefGoogle Scholar
Piesman, J. and Gern, L. (2008). Lyme borreliosis in Europe and North America. In Ticks: Biology, Disease and Control (ed. Bowman, A. S. and Nuttall, P. A.), pp. 220252. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Plyusnina, A., Krajinovic, L. C., Margaletic, J., Niemimaa, J., Nemirov, K., Lundkvist, A., Markotic, A., Miletic-Medved, M., Avsic-Zupanc, T., Henttonen, H. and Plyusnin, A. (2011). Genetic evidence for the presence of two distinct hantaviruses associated with Apodemus mice in Croatia and analysis of local strains. Journal of Medical Virology 83, 108114.CrossRefGoogle ScholarPubMed
Pongsiri, M. J. and Roman, J. (2007). Examining the links between biodiversity and human health: an interdisciplinary research intiative at the U.S. Environmental Protection Agency. EcoHealth 4, 8285.CrossRefGoogle Scholar
Pongsiri, M. J., Roman, J., Ezenwa, V. O., Goldberg, T. L., Koren, H. S., Newbold, S. C., Ostfeld, R. S., Pattanayak, S. K. and Salkeld, D. J. (2009). Biodiversity loss affects global disease ecology. BioScience 59, 945954.CrossRefGoogle Scholar
Power, A. G. and Mitchell, C. E. (2004). Pathogen spillover in disease epidemics. American Naturalist 164, S79S89.CrossRefGoogle ScholarPubMed
Pugliese, A. and Rosa, R. (2008). Effect of host populations on the intensity of ticks and the prevalence of tick-borne pathogens: how to interpret the results of deer exclosure experiments. Parasitology 135, 15311544.CrossRefGoogle ScholarPubMed
Randolph, S. E. (2004). Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129, S3766.CrossRefGoogle Scholar
Randolph, S. E. and Steele, G. M. (1985). An experimental evaluation of conventional control measures against the sheep tick Ixodes ricinus (L) (Acari: Ixodidae). II. The dynamics of the tick-host interaction. Bulletin of Entomological Research 75, 501518.CrossRefGoogle Scholar
Randolph, S. E. and Storey, K. (1999). Impact of microclimate on immature tick-rodent interactions (Acari: Ixodidae): implications for parasite transmission. Journal of Medical Entomology 36, 741748.CrossRefGoogle ScholarPubMed
Reiter, P. (2008). Global warming and malaria: knowing the horse before hitching the cart. Malaria Journal 7, S3.CrossRefGoogle ScholarPubMed
Rizzoli, A., Hauffe, H. C., Tagliapietra, V., Neteler, M. and Rosa, R. (2009). Forest structure and roe deer abundance predict tick-borne encephalitis risk in Italy. PLoS ONE 4, e4336.CrossRefGoogle ScholarPubMed
Roche, B. and Guégan, J.-F. (2011). Ecosystem dynamics, biological diversity and emerging infectious diseases. Comptes Rendus Biologies 334, 385392.CrossRefGoogle ScholarPubMed
Rosa, R., Pugliese, A., Norman, R. and Hudson, P. J. (2003). Thresholds for disease persistence in models for tick-borne infections including non-viraemic transmission, extended feeding and tick aggregation. Journal of Theoretical Biology 224, 359376.CrossRefGoogle ScholarPubMed
Ruedas, L. A., Salazar-Bravo, J., Tinnin, D. S., Armien, B., Caceres, L., Garcia, A., Diaz, M. A., Gracia, F., Suzán, G., Peters, C. J., Yates, T. L. and Mills, J. N. (2004). Community ecology of small mammal populations in Panama following an outbreak of Hantavirus pulmonary syndrome. Journal of Vector Ecology 29, 177191.Google ScholarPubMed
Saul, A. (2003). Zooprophylaxis or zoopotentiation: the outcome of introduced animals on vector transmission is highly dependent on the mosquito mortality while searching. Malaria Journal 2, 32.CrossRefGoogle ScholarPubMed
Sbrana, E., Tonry, J. H., Xiao, S. Y., da Rosa, A. P., Higgs, S. and Tesh, R. B. (2005). Oral transmission of West Nile virus in a hamster model. American Journal of Tropical Medicine and Hygiene 72, 325329.Google Scholar
Sota, T. and Mogi, M. (1989). Effectiveness of zooprophylaxis in malaria control – a theoretical enquiry, with a model for mosquito populations with two bloodmeal hosts. Medical and Veterinary Entomology 3, 337345.CrossRefGoogle Scholar
Spielman, A., Wilson, M. L., Levine, J. F. and Piesman, J. (1985). Ecology of Ixodes dammini-borne human babesiosis and Lyme disease. Annual Review of Entomology 30, 439460.CrossRefGoogle ScholarPubMed
Stafford, K. C. (III), Cartter, M. L., Magarelli, L. A., Ertel, S.-H. and Mshar, P. A. (1998). Temporal correlations between tick abundance and prevalence of ticks infected with Borrelia burgdorferi and increasing incidence of Lyme disease. Journal of Clinical Microbiology 36, 12401244.Google ScholarPubMed
Steinbach Elwell, L. C., Kerans, B. L. and Zickovich, J. (2009). Host-parasite interactions and competition between tubificid species in a benthic community. Freshwater Biology 54, 16161628.CrossRefGoogle Scholar
Suzán, G., Armien, N., Mills, J. N., Marce, E., Ceballos, G., Avila, M., Salazar-Bravo, J., Ruedas, L. A., Armien, B. and Yates, T. L. (2008). Epidemiological considerations of rodent community composition in fragmented landsacpes in Panama. Journal of Mammalogy 89, 634690.CrossRefGoogle Scholar
Suzán, G., Marce, E., Giermakowski, J. T., Mills, J. N., Ceballos, G., Ostfeld, R. S., Armien, B., Pascale, J. M. and Yates, T. L. (2009). Experimental evidence for reduced rodent diversity causing increased hantavirus prevalence. PLoS ONE 4, e5461.CrossRefGoogle ScholarPubMed
Swaddle, J. P. and Calos, S. E. (2008). Increased avian diversity is associated with lower incidence of human West Nile infection: observation of the dilution effect. PLoS ONE 3, e2488.CrossRefGoogle ScholarPubMed
Swei, A., Ostfeld, R. S., Lane, R. S. and Briggs, C. J. (2011). Impact of the experimental removal of lizards on Lyme disease risk. Proceedings of the Royal Society of London, B 278, 29702978.CrossRefGoogle ScholarPubMed
Talleklint, L. and Jaenson, T. G. T. (1994). Transmission of Borrelia burgdorferi s.l. from mammal reservoirs to the primary vector of Lyme borreliosis, Ixodes ricinus (Acari: Ixodidae), in Sweden. Journal of Medical Entomology 31, 880886.CrossRefGoogle Scholar
Talleklint, L. and Jaenson, T. G. T. (1996). Relationship between Ixodes ricinus density and prevalence of infection with Borrelia-like spirochetes and density of infected ticks. Journal of Medical Entomology 33, 805811.CrossRefGoogle ScholarPubMed
Tersago, K., Schreurs, A., Linard, C., Verhagen, R., Van Dongen, S. and Leirs, H. (2008). Population, environmental, and community effects on local bank vole (Myodes glareolus) Puumala virus infection in an area with low human incidence. Vector-Borne and Zoonotic Diseases 8, 235244.CrossRefGoogle Scholar
Tersago, K., Verhagen, R. and Leirs, H. (2011 a). Temporal variation in individual factors associated with hantavirus infection in bank voles during an epizootic: implications for Puumala virus transmission dynamics. Vector-Borne and Zoonotic Diseases 11, 715721.CrossRefGoogle ScholarPubMed
Tersago, K., Verhagen, R., Servais, A., Heyman, P., Ducoffre, G. and Leirs, H. (2009). Hantavirus disease (nephropathia epidemica) in Belgium: effects of tree seed production and climate. Epidemiology and Infection 137, 250256.CrossRefGoogle ScholarPubMed
Tersago, K., Verhagen, R., Vapalahti, O., Heyman, P., Ducoffre, G. and Leirs, H. (2011 b). Hantavirus outbreak in Western Europe: reservoir host infection dynamics related to human disease patterns. Epidemiology and Infection 139, 381390.CrossRefGoogle ScholarPubMed
Thieltges, D. W., Bordalo, M. D., Cabalerro Hernandez, A., Prinz, K. and Jensen, K. T. (2009 a). Ambient fauna impairs parasite transmission in a marine parasite-host system. Parasitology 135, 11111116.Google Scholar
Thieltges, D. W., Reise, K., Prinz, K. and Jensen, K. T. (2009 b). Invaders interfere with native parasite-host interactions. Biological Invasions 11, 14211429.CrossRefGoogle Scholar
Tilman, D., Knops, J. M. H., Wedin, D., Reich, P. B., Ritchie, S. A. and Siemann, E. (1997). Influence of functional diversity and composition on ecosystem processes. Science 277, 13001302.CrossRefGoogle Scholar
Tilman, D., Reich, P. B. and Knops, J. M. H. (2006). Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature, London 441, 629632.CrossRefGoogle Scholar
Tsao, J. I., Wootton, J. T., Bunikis, J., Luna, M. G., Fish, D. and Barbour, A. G. (2004). An ecological approach to preventing human infection: vaccinating wild mouse reservoirs intervenes in the Lyme disease cycle. Proceedings of the National Academy of Sciences, USA 101, 1815918164.CrossRefGoogle ScholarPubMed
Turell, M. J., Dohm, D. J., Sardelis, M. R., O'Guinn, M. L., Andreadis, T. G. and Blow, J. A. (2005). An update on the potential of North American mosquitoes (Diptera: Culicidae) to transmit West Nile virus. Journal of Medical Entomology 42, 5762.CrossRefGoogle Scholar
van Buskirk, J. and Ostfeld, R. S. (1995). Controlling Lyme disease by modifying the density and species composition of tick hosts,. Ecological Applications 5, 11331140.CrossRefGoogle Scholar
Vapalahti, O., Mustonen, J., Lundkvist, A., Henttonen, H., Plyusnin, A. and Vaheri, A. (2003). Hantavirus infections in Europe. Lancet Infectious Diseases 3, 653661.CrossRefGoogle Scholar
Voltaire (1759). Candide (edn. L, Bair.), Bantam Dell, New York, USA.Google Scholar
Ward, J. S. and Mervosh, T. L. (2008). Strategies to reduce browse damage on eastern white pine (Pinis strobus) in southern New England, USA. Forest Ecology and Management 255, 15591567.CrossRefGoogle Scholar
Williams, S. C., Ward, J. S., Worthley, T. E. and Stafford, K. C. (III) (2009). Managing Japanese barberry (Ranunculales: Berberidaceae) infestations reduces black-legged tick (Acari: Ixodidae) abundance and infection prevalence with Borrelia burgdorferi (Spirochaetales: Spirochaetaceae). Environmental Entomology 38, 977984.CrossRefGoogle Scholar
Wilson, M. L., Litwin, T. S., Gavin, T. A., Capkanis, M. C., Maclean, D. C. and Spielman, A. (1990). Host-dependent differences in feeding and reproduction of Ixodes dammini (Acari: Ixodidae). Journal of Medical Entomology 27, 945954.CrossRefGoogle Scholar
Woolhouse, M. E. J. and Gowtage-Sequeria, S. (2005). Host range and emerging and reemerging pathogens. Emerging Infectious Diseases 11, 18421847.CrossRefGoogle ScholarPubMed
Zeman, P. and Januska, J. (1999). Epizootiologic background of dissimilar distribution of human cases of Lyme borreliosis and tick-borne encephalitis in a joint endemic area. Comparative Immunology, Microbiology and Infectious Diseases 22, 247260.CrossRefGoogle Scholar

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