Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-24T00:17:12.513Z Has data issue: false hasContentIssue false
  • English
  • Français

The diversity–disease relationship: evidence for and criticisms of the dilution effect

Published online by Cambridge University Press:  04 April 2016

Z. Y. X. HUANG ,
F. VAN LANGEVELDE ,
A. ESTRADA-PEÑA ,
G. SUZÁN  and
W. F. DE BOER
Z. Y. X. HUANG*
Affiliation:
College of Life Sciences, Nanjing Normal University, Nanjing, China Resource Ecology Group, Wageningen University, Wageningen, the Netherlands
F. VAN LANGEVELDE
Affiliation:
Resource Ecology Group, Wageningen University, Wageningen, the Netherlands
A. ESTRADA-PEÑA
Affiliation:
Department of Animal Pathology, Faculty of Veterinary Medicine, University of Zaragoza, Zaragoza, Spain
G. SUZÁN
Affiliation:
Facultad de Medicina Veterinaria Zootecnia, Universidad Nacional Autónoma de México, Mexico, Mexico
W. F. DE BOER
Affiliation:
Resource Ecology Group, Wageningen University, Wageningen, the Netherlands
*
*Corresponding author: College of Life Sciences, Nanjing Normal University, Nanjing, China and Resource Ecology Group, Wageningen University, Wageningen, the Netherlands. Tel: +86 13921431410. E-mail: zhengyxhuang@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

The dilution effect, that high host species diversity can reduce disease risk, has attracted much attention in the context of global biodiversity decline and increasing disease emergence. Recent studies have criticized the generality of the dilution effect and argued that it only occurs under certain circumstances. Nevertheless, evidence for the existence of a dilution effect was reported in about 80% of the studies that addressed the diversity–disease relationship, and a recent meta-analysis found that the dilution effect is widespread. We here review supporting and critical studies, point out the causes underlying the current disputes. The dilution is expected to be strong when the competent host species tend to remain when species diversity declines, characterized as a negative relationship between species’ reservoir competence and local extinction risk. We here conclude that most studies support a negative competence–extinction relationship. We then synthesize the current knowledge on how the diversity–disease relationship can be modified by particular species in community, by the scales of analyses, and by the disease risk measures. We also highlight the complex role of habitat fragmentation in the diversity–disease relationship from epidemiological, evolutionary and ecological perspectives, and construct a synthetic framework integrating these three perspectives. We suggest that future studies should test the diversity–disease relationship across different scales and consider the multiple effects of landscape fragmentation.

Keywords

competence–extinction relationshipidentity effectinfection prevalenceabundanceamplification effecthabitat fragmentation
Type
Review Article
Information
Parasitology , Volume 143 , Issue 9 , August 2016 , pp. 1075 - 1086
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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.)

Footnotes

†

Present address: Nanjing Normal University, Wenyuan Road 1, 210046 Nanjing, China.

References

REFERENCES

Allan, B. F., Keesing, F. and Ostfeld, R. S. (2003). Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17, 267–272.CrossRefGoogle Scholar
Allan, B. F., Langerhans, 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, 699–708.Google Scholar
Altermatt, F. and Ebert, D. (2008). Genetic diversity of Daphnia magna populations enhances resistance to parasites. Ecology Letters 11, 918–928.CrossRefGoogle ScholarPubMed
Becker, C. G., Rodriguez, D., Toledo, L. F., Longo, A. V., Lambertini, C., Corrêa, D. T., Leite, D. S., Haddad, C. F. and Zamudio, K. R. (2014). Partitioning the net effect of host diversity on an emerging amphibian pathogen. Proceedings of the Royal Society B – Biological Sciences 281, 20141796.Google Scholar
Begon, M. (2008). Effects of host diversity on disease dynamics. In Infectious Disease Ecology: Effects of Ecosystems on Disease and of Disease on Ecosystems (eds. Ostfeld, R.S., Keesing, F. & Eviner, V.T.), pp. 12–29. Princeton University Press, Princeton, NJ.Google Scholar
Blackburn, T. M., Brown, V. K., Doube, B. M., Greenwood, J. J. D., Lawton, J. H. and Stork, N. E. (1993). The relationship between abundance and body-size in natural animal assemblages. Journal of Animal Ecology 62, 519–528.Google Scholar
Bonds, M. H., Dobson, A. P. and Keenan, D. C. (2012). Disease ecology, biodiversity, and the latitudinal gradient in income. PLoS Biology 10, e1001456.Google Scholar
Bouchard, C., Beauchamp, G., Leighton, P. A., Lindsay, R., Belanger, D. and Ogden, N. H. (2013). Does high biodiversity reduce the risk of Lyme disease invasion? Parasites & Vectors 6, 195.Google Scholar
Brownstein, J. S., Skelly, D. K., Holford, T. R. and Fish, D. (2005). Forest fragmentation predicts local scale heterogeneity of Lyme disease risk. Oecologia 146, 469–475.Google Scholar
Cardillo, M. (2003). Biological determinants of extinction risk: why are smaller species less vulnerable? Animal Conservation 6, 63–69.Google Scholar
Cardinale, B. J., Duffy, J. E., Gonzalez, A., Hooper, D. U., Perrings, C., Venail, P., Narwani, A., Mace, G. M., Tilman, D. and Wardle, D. A. (2012). Biodiversity loss and its impact on humanity. Nature 486, 59–67.Google Scholar
Carlsson-Granér, U. and Thrall, P. H. (2002). The spatial distribution of plant populations, disease dynamics and evolution of resistance. Oikos 97, 97–110.Google Scholar
Chen, L. and Zhou, S. (2015). A combination of species evenness and functional diversity is the best predictor of disease risk in multihost communities. The American Naturalist 186, 755–765.Google Scholar
Civitello, D. J., Cohen, J., Fatima, H., Halstead, N. T., Liriano, J., McMahon, T. A., Ortega, C. N., Sauer, E. L., Sehgal, T. and Young, S. (2015 a). Biodiversity inhibits parasites: broad evidence for the dilution effect. Proceedings of the National Academy of Sciences of the United States of America 112, 8667–8671.Google Scholar
Civitello, D. J., Cohen, J., Fatima, H., Halstead, N. T., McMahon, T. A., Ortega, C. N., Sauer, E. L., Young, S. and Rohr, J. R. (2015 b). Reply to Salkeld et al.: diversity-disease patterns are robust to study design, selection criteria, and publication bias. Proceedings of the National Academy of Sciences of the United States of America 112, E6262–E6262.Google Scholar
Clay, C. A., Lehmer, E. M., Jeor, S. S. and Dearing, M. D. (2009 a). Sin Nombre virus and rodent species diversity: a test of the dilution and amplification hypotheses. PLoS ONE 4, e6467.CrossRefGoogle ScholarPubMed
Clay, C. A., Lehmer, E. M., St Jeor, S. and Dearing, M. D. (2009 b). Testing mechanisms of the dilution effect: deer mice encounter rates, Sin Nombre virus prevalence and species diversity. EcoHealth 6, 250–259.Google Scholar
Cronin, J. P., Welsh, M. E., Dekkers, M. G., Abercrombie, S. T. and Mitchell, C. E. (2010). Host physiological phenotype explains pathogen reservoir potential. Ecology Letters 13, 1221–1232.Google Scholar
Cronin, J. P., Rúa, M. A. and Mitchell, C. E. (2014). Why is living fast dangerous? Disentangling the roles of resistance and tolerance of disease. The American Naturalist 184, 172–187.Google Scholar
Dobson, A. (2004). Population dynamics of pathogens with multiple host species. The American Naturalist 164, S64–S78.Google Scholar
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, 714–718.CrossRefGoogle ScholarPubMed
Estrada-Peña, A. (2003). The relationships between habitat topology, critical scales of connectivity and tick abundance Ixodes ricinus in a heterogeneous landscape in northern Spain. Ecography 26, 661–671.Google Scholar
Estrada-Peña, A. (2009). Diluting the dilution effect: a spatial Lyme model provides evidence for the importance of habitat fragmentation with regard to the risk of infection. Geospatial Health 3, 143–155.Google Scholar
Estrada-Peña, A., Ostfeld, R. S., Peterson, A. T., Poulin, R. and de la Fuente, J. (2014). Effects of environmental change on zoonotic disease risk: an ecological primer. Trends in Parasitology 30, 205–214.Google 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 the Royal Society B – Biological Sciences 273, 109–117.Google Scholar
Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics 34, 487–515.Google Scholar
Glavanakov, S., White, D. J., Caraco, T., Lapenis, A., Robinson, G. R., Szymanski, B. K. and Maniatty, W. A. (2001). Lyme disease in New York State: spatial pattern at a regional scale. American Journal of Tropical Medicine and Hygiene 65, 538–545.Google Scholar
Gottdenker, N. L., Chaves, L. F., Calzada, J. E., Saldana, A. and Carroll, C. R. (2012). Host life history strategy, species diversity, and habitat influence Trypanosoma cruzi vector infection in Changing landscapes. PLoS Neglected Tropical Diseases 6, e1884.Google Scholar
Haas, S. E., Hooten, M. B., Rizzo, D. M. and Meentemeyer, R. K. (2011). Forest species diversity reduces disease risk in a generalist plant pathogen invasion. Ecology Letters 14, 1108–1116.CrossRefGoogle Scholar
Hantsch, L., Braun, U., Scherer-Lorenzen, M. and Bruelheide, H. (2013). Species richness and species identity effects on occurrence of foliar fungal pathogens in a tree diversity experiment. Ecosphere 4, 1–12.Google Scholar
Hardstaff, J. L., Marion, G., Hutchings, M. R. and White, P. C. (2013). Evaluating the tuberculosis hazard posed to cattle from wildlife across Europe. Research in Veterinary Science 97, S86–S93.Google 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 B – Biological Sciences 272, 1059–1066.Google Scholar
Hess, G. (1996). Disease in metapopulation models: implications for conservation. Ecology 77, 1617–1632.Google Scholar
Hily, J. M., García, A., Moreno, A., Plaza, M., Wilkinson, M. D., Fereres, A., Fraile, A. and García-Arenal, F. (2014). The relationship between host lifespan and pathogen reservoir potential: an analysis in the system Arabidopsis thaliana–Cucumber mosaic virus. PLoS Pathogens 10, e1004492.Google Scholar
Hooper, D. U., Chapin, F. S., Ewel, J. J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J. H., Lodge, D. M., Loreau, M., Naeem, S., Schmid, B., Setala, H., Symstad, A. J., Vandermeer, J. and Wardle, D. A. (2005). Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75, 3–35.Google Scholar
Huang, Z. Y. X., de Boer, W. F., van Langevelde, F., Olson, V., Blackburn, T. M. and Prins, H. H. T. (2013 a). Species’ life-history traits explain interspecific variation in reservoir competence: a possible mechanism underlying the dilution effect. PLoS ONE 8, e54341.Google Scholar
Huang, Z. Y. X., de Boer, W. F., van Langevelde, F., Xu, C., Ben Jebara, K., Berlingieri, F. and Prins, H. H. T. (2013 b). Dilution effect in bovine tuberculosis: risk factors for regional disease occurrence in Africa. Proceedings of the Royal Society B – Biological Sciences 280, 20130624.Google Scholar
Huang, Z. Y. X., Xu, C., van Langevelde, F., Prins, H. H. T., ben Jebara, K. and de Boer, W. F. (2014). Dilution effect and identity effect by wildlife in the persistence and recurrence of bovine tuberculosis. Parasitology 141, 981–987.Google Scholar
Huang, Z. Y. X., van Langevelde, F., Prins, H. H. T. and de Boer, W. F. (2015). Dilution versus facilitation: impact of connectivity on disease risk in metapopulations. Journal of Theoretical Biology 376, 66–73.Google Scholar
Johnson, P. T. J. and Hoverman, J. T. (2012). Parasite diversity and coinfection determine pathogen infection success and host fitness. Proceedings of the National Academy of Sciences of the United States of America 109, 9006–9011.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, 961–970.Google Scholar
Johnson, P. T., Ostfeld, R. S. and Keesing, F. (2015). Frontiers in research on biodiversity and disease. Ecology Letters 18, 1119–1133.Google Scholar
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 the Royal Society B – Biological Sciences 276, 1657–1663.Google Scholar
Johnson, P. T. J., Preston, D. L., Hoverman, J. T., Henderson, J. S., Paull, S. H., Richgels, K. L. D. and Redmond, M. D. (2012 a). Species diversity reduces parasite infection through cross-generational effects on host abundance. Ecology 93, 56–64.Google Scholar
Johnson, P. T. J., Rohr, J. R., Hoverman, J. T., Kellermanns, E., Bowerman, J. and Lunde, K. B. (2012 b). Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecology Letters 15, 235–242.Google Scholar
Johnson, P. T. J., Preston, D. L., Hoverman, J. T. and LaFonte, B. E. (2013 a). Host and parasite diversity jointly control disease risk in complex communities. Proceedings of the National Academy of Sciences of the United States of America 110, 16916–16921.Google Scholar
Johnson, P. T. J., Preston, D. L., Hoverman, J. T. and Richgels, K. L. D. (2013 b). Biodiversity decreases disease through predictable changes in host community competence. Nature 494, 230–233.Google Scholar
Joseph, M. B., Mihaljevic, J. R., Orlofske, S. A. and Paull, S. H. (2013). Does life history mediate changing disease risk when communities disassemble? Ecology Letters 16, 1405–1412.Google Scholar
Jousimo, J., Tack, A. J. M., Ovaskainen, O., Mononen, T., Susi, H., Tollenaere, C. and Laine, A. L. (2014). Ecological and evolutionary effects of fragmentation on infectious disease dynamics. Science 344, 1289–1293.Google Scholar
Kaltz, O. and Shykoff, J. A. (1998). Local adaptation in host–parasite systems. Heredity 81, 361–370.Google Scholar
Kamiya, T., O'Dwyer, K., Nakagawa, S. and Poulin, R. (2014). Host diversity drives parasite diversity: meta-analytical insights into patterns and causal mechanisms. Ecography 37, 689–697.CrossRefGoogle Scholar
Keeling, M. J. (2000). Metapopulation moments: coupling, stochasticity and persistence. Journal of Animal Ecology 69, 725–736.Google Scholar
Keesing, F., Holt, R. D. and Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecology Letters 9, 485–498.Google Scholar
Keesing, F., Brunner, J., Duerr, S., Killilea, M., LoGiudice, K., Schmidt, K., Vuong, H. and Ostfeld, R. (2009). Hosts as ecological traps for the vector of Lyme disease. Proceedings of the Royal Society B – Biological Sciences 276, 3911–3919.Google Scholar
Kilpatrick, A. 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 B – Biological Sciences 273, 2327–2333.Google Scholar
Lacroix, C., Jolles, A., Seabloom, E. W., Power, A. G., Mitchell, C. E. and Borer, E. T. (2014). Non-random biodiversity loss underlies predictable increases in viral disease prevalence. Journal of the Royal Society Interface 11, 20130947.Google Scholar
Lafferty, K. D. (2012). Biodiversity loss decreases parasite diversity: theory and patterns. Philosophical Transactions of the Royal Society B – Biological Sciences 367, 2814–2827.Google Scholar
Lajeunesse, M. J. and Forbes, M. R. (2002). Host range and local parasite adaptation. Proceedings of the Royal Society B – Biological Sciences 269, 703–710.Google Scholar
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 of the United States of America 100, 567–571.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, 2841–2849.Google Scholar
Loreau, M. and Hector, A. (2001). Partitioning selection and complementarity in biodiversity experiments. Nature 412, 72–76.Google Scholar
Loreau, M. and Mouquet, N. (1999). Immigration and the maintenance of local species diversity. The American Naturalist 154, 427–440.Google Scholar
Mace, G. M., Norris, K. and Fitter, A. H. (2012). Biodiversity and ecosystem services: a multilayered relationship. Trends in Ecology & Evolution 27, 19–26.Google Scholar
McCallum, H., Barlow, N. and Hone, J. (2001). How should pathogen transmission be modelled? Trends in Ecology & Evolution 16, 295–300.Google Scholar
Mihaljevic, J. R., Joseph, M. B., Orlofske, S. A. and Paull, S. H. (2014). The scaling of host density with richness affects the direction, shape, and detectability of diversity-disease relationships. PLoS ONE 9, e97812.Google Scholar
Mitchell, M. G. E., Suarez-Castro, A. F., Martinez-Harms, M., Maron, M., McAlpine, C., Gaston, K. J., Johansen, K. and Rhodes, J. R. (2015). Reframing landscape fragmentation's effects on ecosystem services. Trends in Ecology & Evolution 30, 190–198.Google Scholar
Moore, S. M. and Borer, E. T. (2012). The influence of host diversity and composition on epidemiological patterns at multiple spatial scales. Ecology 93, 1095–1105.Google Scholar
Morand, S. and Harvey, P. (2000). Mammalian metabolism, longevity and parasite species richness. Proceedings of the Royal Society B – Biological Sciences 267, 1999–2003.Google Scholar
Mundt, C. (2002). Use of multiline cultivars and cultivar mixtures for disease management. Annual Review of Phytopathology 40, 381–410.Google 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, 299–306.Google Scholar
Norman, R., Bowers, R., Begon, M. and Hudson, P. J. (1999). Persistence of tick-borne virus in the presence of multiple host species: tick reservoirs and parasite mediated competition. Journal of Theoretical Biology 200, 111–118.Google Scholar
Ogden, N. H. and Tsao, J. I. (2009). Biodiversity and Lyme disease: dilution or amplification? Epidemics 1, 196–206.Google Scholar
Ostfeld, R. S. (2013). A Candide response to Panglossian accusations by Randolph and Dobson: biodiversity buffers disease. Parasitology 140, 1196–1198.Google Scholar
Ostfeld, R. and Keesing, F. (2000). The function of biodiversity in the ecology of vector-borne zoonotic diseases. Canadian Journal of Zoology – Revue Canadienne De Zoologie 78, 2061–2078.Google Scholar
Ostfeld, R. S. and Keesing, F. (2012). Effects of host diversity on infectious disease. Annual Review of Ecology Evolution and Systematics 43, 157–182.Google Scholar
Ostfeld, R. S., Levi, T., Jolles, A. E., Martin, L. B., Hosseini, P. R. and Keesing, F. (2014). Life history and demographic drivers of reservoir competence for three tick-borne zoonotic pathogens. PLoS ONE 9, e107387.Google Scholar
Piudo, L., Monteverde, M. J., Walker, R. S. and Douglass, R. J. (2011). Rodent community structure and Andes virus infection in sylvan and peridomestic habitats in northwestern Patagonia, Argentina. Vector-Borne and Zoonotic Diseases 11, 315–324.Google Scholar
Plantegenest, M., Le May, C. and Fabre, F. (2007). Landscape epidemiology of plant diseases. Journal of the Royal Society Interface 4, 963–972.Google Scholar
Previtali, M. A., Ostfeld, R. S., Keesing, F., Jolles, A. E., Hanselmann, R. and Martin, L. B. (2012). Relationship between pace of life and immune responses in wild rodents. Oikos 121, 1483–1492.Google Scholar
Randolph, S. E. and Dobson, A. D. M. (2012). Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139, 847–863.Google Scholar
Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 1099–1102.Google Scholar
Reich, P. B., Knops, J., Tilman, D., Craine, J., Ellsworth, D., Tjoelker, M., Lee, T., Wedin, D., Naeem, S. and Bahauddin, D. (2001). Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition. Nature 410, 809–810.Google Scholar
Roche, B., Dobson, A. P., Guegan, J. F. and Rohani, P. (2012). Linking community and disease ecology: the impact of biodiversity on pathogen transmission. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 2807–2813.Google Scholar
Rottstock, T., Joshi, J., Kummer, V. and Fischer, M. (2014). Higher plant diversity promotes higher diversity of fungal pathogens, while it decreases pathogen infection per plant. Ecology 95, 1907–1917.Google Scholar
Roy, M. and Pascual, M. (2006). On representing network heterogeneities in the incidence rate of simple epidemic models. Ecological Complexity 3, 80–90.Google Scholar
Rubio, A. V., Ávila-Flores, R. and Suzán, G. (2014). Responses of small mammals to habitat fragmentation: epidemiological considerations for rodent-borne Hantaviruses in the Americas. EcoHealth 11, 1–8.Google Scholar
Rudolf, V. H. W. and Antonovics, J. (2005). Species coexistence and pathogens with frequency-dependent transmission. The American Naturalist 166, 112–118.Google Scholar
Salkeld, D. J., Padgett, K. A. and Jones, J. H. (2013). A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecology Letters 16, 679–686.Google Scholar
Salkeld, D. J., Padgett, K. A., Jones, J. H. and Antolin, M. F. (2015). Public health perspective on patterns of biodiversity and zoonotic disease. Proceedings of the National Academy of Sciences of the United States of America 112, E6261–E6261.Google Scholar
Schmidt, K. A. and Ostfeld, R. S. (2001). Biodiversity and the dilution effect in disease ecology. Ecology 82, 609–619.Google Scholar
States, S., Brinkerhoff, R., Carpi, G., Steeves, T., Folsom-O'Keefe, C., DeVeaux, M. and Diuk-Wasser, M. (2014). Lyme disease risk not amplified in a species-poor vertebrate community: similar Borrelia burgdorferi tick infection prevalence and OspC genotype frequencies. Infection, Genetics and Evolution 26, 566–575.Google 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.Google Scholar
Suzán, G., Esponda, F., Carrasco-Hernández, R. and Aguirre, A. (2012). Habitat fragmentation and infectious disease ecology. In New Directions in Conservation Medicine: Applied Cases of Ecological Health (eds. Aguirre, A., Ostfeld, R. and Daszak, P.), pp. 135–150. Oxford University Press, New York.Google Scholar
Suzán, G., García-Peña, G. E., Castro-Arellano, I., Rico, O., Rubio, A. V., Tolsá, M. J., Roche, B., Hosseini, P. R., Rizzoli, A. and Murray, K. A. (2015). Metacommunity and phylogenetic structure determine wildlife and zoonotic infectious disease patterns in time and space. Ecology and Evolution 5, 865–873.Google Scholar
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.Google Scholar
Turney, S., Gonzalez, A. and Millien, V. (2014). The negative relationship between mammal host diversity and Lyme disease incidence strengthens through time. Ecology 95, 3244–3250.Google Scholar
Venesky, M., Liu, X., Sauer, E. and Rohr, J. (2014). Linking manipulative experiments to field data to test the dilution effect. Journal of Animal Ecology 83, 557–565.Google Scholar
Werden, L., Barker, I. K., Bowman, J., Gonzales, E. K., Leighton, P. A., Lindsay, L. R. and Jardine, C. M. (2014). Geography, deer, and host biodiversity shape the pattern of Lyme disease emergence in the Thousand Islands archipelago of Ontario, Canada. PLoS ONE 9, e85640.Google Scholar
Wood, C. L. and Lafferty, K. D. (2013). Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends in Ecology & Evolution 28, 239–247.Google Scholar
Wood, C. L., Lafferty, K. D., DeLeo, G., Young, H. S., Hudson, P. J. and Kuris, A. M. (2014). Does biodiversity protect humans against infectious disease? Ecology 95, 817–832.Google Scholar
Young, H., Griffin, R. H., Wood, C. L. and Nunn, C. L. (2013). Does habitat disturbance increase infectious disease risk for primates? Ecology Letters 16, 656–663.Google Scholar
Young, H. S., Dirzo, R., Helgen, K. M., McCauley, D. J., Billeter, S. A., Kosoy, M. Y., Osikowicz, L. M., Salkeld, D. J., Young, T. P. and Dittmar, K. (2014). Declines in large wildlife increase landscape-level prevalence of rodent-borne disease in Africa. Proceedings of the National Academy of Sciences of the United States of America 111, 7036–7041.Google Scholar
Zhu, Y., Chen, H., Fan, J., Wang, Y., Li, Y., Chen, J., Fan, J., Yang, S., Hu, L. and Leung, H. (2000). Genetic diversity and disease control in rice. Nature 406, 718–722.Google Scholar