Letter | Published:

Biodiversity decreases disease through predictable changes in host community competence

Nature volume 494, pages 230233 (14 February 2013) | Download Citation

Abstract

Accelerating rates of species extinctions and disease emergence underscore the importance of understanding how changes in biodiversity affect disease outcomes1,2,3. Over the past decade, a growing number of studies have reported negative correlations between host biodiversity and disease risk4,5,6,7,8, prompting suggestions that biodiversity conservation could promote human and wildlife health9,10. Yet the generality of the diversity–disease linkage remains conjectural11,12,13, in part because empirical evidence of a relationship between host competence (the ability to maintain and transmit infections) and the order in which communities assemble has proven elusive. Here we integrate high-resolution field data with multi-scale experiments to show that host diversity inhibits transmission of the virulent pathogen Ribeiroia ondatrae and reduces amphibian disease as a result of consistent linkages among species richness, host composition and community competence. Surveys of 345 wetlands indicated that community composition changed nonrandomly with species richness, such that highly competent hosts dominated in species-poor assemblages whereas more resistant species became progressively more common in diverse assemblages. As a result, amphibian species richness strongly moderated pathogen transmission and disease pathology among 24,215 examined hosts, with a 78.4% decline in realized transmission in richer assemblages. Laboratory and mesocosm manipulations revealed an approximately 50% decrease in pathogen transmission and host pathology across a realistic diversity gradient while controlling for host density, helping to establish mechanisms underlying the diversity–disease relationship and their consequences for host fitness. By revealing a consistent link between species richness and community competence, these findings highlight the influence of biodiversity on infection risk and emphasize the benefit of a community-based approach to understanding infectious diseases.

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References

  1. 1.

    et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012)

  2. 2.

    et al. Global trends in emerging infectious diseases. Nature 451, 990–993 (2008)

  3. 3.

    , & The functions of biological diversity in an age of extinction. Science 336, 1401–1406 (2012)

  4. 4.

    , , & Sin Nombre virus and rodent species diversity: a test of the dilution and amplification hypotheses. PLoS ONE 4, e6467 (2009)

  5. 5.

    , , & Forest species diversity reduces disease risk in a generalist plant pathogen invasion. Ecol. Lett. 14, 1108–1116 (2011)

  6. 6.

    , , & The ecology of infectious disease: Effects of host diversity and community composition on Lyme disease risk. Proc. Natl Acad. Sci. USA 100, 567–571 (2003)

  7. 7.

    et al. Ecological correlates of risk and incidence of West Nile virus in the United States. Oecologia 158, 699–708 (2009)

  8. 8.

    , , & Avian diversity and West Nile virus: testing associations between biodiversity and infectious disease risk. Proc. R. Soc. B. 273, 109–117 (2006)

  9. 9.

    et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647–652 (2010)

  10. 10.

    & Effects of host diversity on infectious disease. Annu. Rev. Ecol. Evol. Syst. 43, 157–182 (2012)

  11. 11.

    & Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139, 847–863 (2012)

  12. 12.

    et al. Fine-scale variation in vector host use and force of infection drive localized patterns of West Nile virus transmission. PLoS ONE 6, e23767 (2011)

  13. 13.

    & Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends Ecol. Evol.. (23 November 2012)

  14. 14.

    , , & Functionally diverse reef-fish communities ameliorate coral disease. Proc. Natl Acad. Sci. USA 106, 17067–17070 (2009)

  15. 15.

    Globalization, land use, and the invasion of West Nile virus. Science 334, 323–327 (2011)

  16. 16.

    , & Effects of species diversity on disease risk. Ecol. Lett. 9, 485–498 (2006)

  17. 17.

    et al. Experimental evidence for reduced rodent diversity causing increased Hantavirus prevalence. PLoS ONE 4, e5461 (2009)

  18. 18.

    , , & A dilution effect in the emerging amphibian pathogen Batrachochytrium dendrobatidis. Proc. Natl Acad. Sci. USA 108, 16322–16326 (2011)

  19. 19.

    et al. Species diversity reduces parasite infection through cross-generational effects on host abundance. Ecology 93, 56–64 (2012)

  20. 20.

    & Community disassembly, biodiversity loss, and the erosion of an ecosystem service. Ecology 84, 1421–1427 (2003)

  21. 21.

    Community diversity: relative roles of local and regional processes. Science 235, 167–171 (1987)

  22. 22.

    , , & Functional consequences of realistic biodiversity changes in a marine ecosystem. Proc. Natl Acad. Sci. USA 105, 924–928 (2008)

  23. 23.

    et al. Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecol. Lett. 15, 235–242 (2012)

  24. 24.

    , , , & Nestedness of ectoparasite-vertebrate host networks. PLoS ONE 4, e7873 (2009)

  25. 25.

    & The physiology/life-history nexus. Trends Ecol. Evol. 17, 462–468 (2002)

  26. 26.

    , , , & Constitutive immune defences correlate with life-history variables in tropical birds. J. Anim. Ecol. 77, 356–363 (2008)

  27. 27.

    , , & Predicting extinction risk in declining species. Proc. R. Soc. Lond. B. 267, 1947–1952 (2000)

  28. 28.

    & Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proc. R. Soc. B. 272, 1059–1066 (2005)

  29. 29.

    & Parasite diversity and coinfection determine pathogen infection success and host fitness. Proc. Natl Acad. Sci. USA 109, 9006–9011 (2012)

  30. 30.

    & Parasite competition hidden by correlated coinfection: using surveys and experiments to understand parasite interactions. Ecology 92, 535–541 (2011)

  31. 31.

    & All hosts are not equal: explaining differential patterns of malformations in an amphibian community. J. Anim. Ecol. 78, 191–201 (2009)

  32. 32.

    et al. Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecol. Lett. 15, 235–242 (2012)

  33. 33.

    A simplified table for staging anuran embryos and larvae with notes and identification. Herpetologica 16, 183–190 (1960)

  34. 34.

    & Limb developmental stages of the newt Notophthalmus viridescens. Int. J. Dev. Biol. 49, 375–389 (2005)

  35. 35.

    & Phylogeny of the New World true frogs (Rana). Mol. Phylogenet. Evol. 34, 299–314 (2005)

  36. 36.

    , & When molecules and morphology clash: a phylogenetic analysis of the North American ambystomatid salamanders (Caudata: Ambystomatidae). Syst. Zool. 40, 284–303 (1991)

  37. 37.

    , , & Effects of elevated CO2, nitrogen deposition, and decreased species diversity on foliar fungal plant disease. Glob. Change Biol. 9, 438–451 (2003)

  38. 38.

    & Improving the analyses of nestedness for large sets of matrices. Environ. Modell. Softw. 21, 1512–1513 (2006)

  39. 39.

    & The measure of order and disorder in the distribution of species in fragmented habitat. Oecologia 96, 373–382 (1993)

  40. 40.

    et al. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol. Evol. 24, 127–135 (2009)

  41. 41.

    , , , & Mixed Effects Models and Extensions in Ecology with R (Springer, 2009)

  42. 42.

    Measuring Biological Diversity (Blackwell Publishing, 2004)

  43. 43.

    & Model Selection and Multimodel Inference (Springer, 2002)

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Acknowledgements

We thank B. Hoye, J. Koprivnikar, K. Medley, J. Rohr and especially Y. Springer for editorial suggestions; S. Johnson for valuable statistical advice; M. Baragona, I. Buller, K. Gietzen, B. Goodman, J. Jenkins, E. Kellermanns, B. LaFonte, T. McDevitt-Galles, J. McFarland and S. Paull for assistance in collecting data; and East Bay Regional Parks, East Bay Municipal Utility District, Santa Clara County Parks, Hopland Research and Extension Center, Blue Oak Ranch Reserve, California State Parks, The Nature Conservancy, Open Space Authority and Mid-peninsula Open Space for access to properties and logistical support. This work was supported through funds from the US National Science Foundation (DEB-0841758, DEB-1149308), the National Geographic Society, and the David and Lucile Packard Foundation.

Author information

Affiliations

  1. Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309, USA

    • Pieter T. J. Johnson
    • , Daniel L. Preston
    •  & Katherine L. D. Richgels
  2. Department of Forestry and Natural Resources, Purdue University, West Lafayette, Indiana 47907, USA

    • Jason T. Hoverman

Authors

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Contributions

P.T.J.J. designed the study, D.L.P., K.L.D.R. and P.T.J.J. collected the data, P.T.J.J. and J.T.H. analysed the data, and all authors wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Pieter T. J. Johnson.

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    Supplementary Information

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https://doi.org/10.1038/nature11883

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