Emerging fungal threats to animal, plant and ecosystem health

Abstract

The past two decades have seen an increasing number of virulent infectious diseases in natural populations and managed landscapes. In both animals and plants, an unprecedented number of fungal and fungal-like diseases have recently caused some of the most severe die-offs and extinctions ever witnessed in wild species, and are jeopardizing food security. Human activity is intensifying fungal disease dispersal by modifying natural environments and thus creating new opportunities for evolution. We argue that nascent fungal infections will cause increasing attrition of biodiversity, with wider implications for human and ecosystem health, unless steps are taken to tighten biosecurity worldwide.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Worldwide reporting trends in fungal EIDs.
Figure 2: Fungal disease dynamics leading to host extinction.

References

  1. 1

    The Institute of Medicine. Fungal Diseases: an Emerging Threat to Human Animal and Wildlife Health (National Academy of Sciences, 2011)The output of a key workshop assessing the risk of novel fungal diseases.

  2. 2

    Pennisi, E. Armed and dangerous. Science 327, 804–805 (2010)

    Google Scholar 

  3. 3

    Grünwald, N. J., Goss, E. M. & Press, C. M. Phytophthora ramorum: a pathogen with a remarkably wide host range causing sudden oak death on oaks and ramorum blight on woody ornamentals. Mol. Plant Pathol. 9, 729–740 (2008)

    Google Scholar 

  4. 4

    Anderson, P. K. et al. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19, 535–544 (2004)The first meta-analysis of emerging plant diseases. Reasons for this emergence are proposed and the cost to human welfare and biodiversity is estimated.

    Google Scholar 

  5. 5

    Brown, J. K. M. & Hovmoller, M. S. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297, 537–541 (2002)

    Google Scholar 

  6. 6

    Daszak, P., Cunningham, A. A. & Hyatt, A. D. Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287, 443–449 (2000)

    Google Scholar 

  7. 7

    Smith, K. F., Sax, D. F. & Lafferty, K. D. Evidence for the role of infectious disease in species extinction and endangerment. Conserv. Biol. 20, 1349–1357 (2006)

    Google Scholar 

  8. 8

    Blehert, D. S. et al. Bat white-nose syndrome: an emerging fungal pathogen? Science 323, 227 (2009)

    Google Scholar 

  9. 9

    Gargas, A., Trest, M. T., Christensen, M., Volk, T. J. & Blehert, D. S. Geomyces destructans sp. nov. associated with bat white-nose syndrome. Mycotaxon 108, 147–154 (2009)

    Google Scholar 

  10. 10

    Lorch, J. M. et al. Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature 480, 376–378 (2011)

    Google Scholar 

  11. 11

    Frick, W. F. et al. An emerging disease causes regional population collapse of a common North American bat species. Science 329, 679–682 (2010)Population viability analysis showing the high risk of extinction of little brown bats caused by the emergence of a pathogenic fungus.

    Google Scholar 

  12. 12

    Boyles, J. G., Cryan, P. M., McCracken, G. F. & Kunz, T. H. Economic importance of bats in agriculture. Science 332, 41–42 (2011)

    Google Scholar 

  13. 13

    Berger, L. et al. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc. Natl Acad. Sci. USA 95, 9031–9036 (1998)The first study describing the discovery of amphibian chytridiomycosis in the tropics.

    Google Scholar 

  14. 14

    Longcore, J. E., Pessier, A. P. & Nichols, D. K. Batrachochytrium dendrobatidis gen. et sp. Nov., a chytrid pathogenic to amphibians. Mycologia 91, 219–227 (1999)

    Google Scholar 

  15. 15

    Fisher, M. C., Garner, T. W. J. & Walker, S. F. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu. Rev. Microbiol. 63, 291–310 (2009)

    Google Scholar 

  16. 16

    Bd-Maps 〈http://www.bd-maps.net/〉 (accessed, February 2012)

  17. 17

    Cheng, T. L., Rovito, S. M., Wake, D. B. & Vredenburg, V. T. Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proc. Natl Acad. Sci. USA 108, 9502–9507 (2011)

    Google Scholar 

  18. 18

    Crawford, A. J., Lips, K. R. & Bermingham, E. Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proc. Natl Acad. Sci. USA 107, 13777–13782 (2010)

    Google Scholar 

  19. 19

    Colón-Gaud, C. et al. Assessing ecological responses to catastrophic amphibian declines: patterns of macroinvertebrate production and food web structure in upland Panamanian streams. Limnol. Oceanogr. 54, 331–343 (2009)

    Google Scholar 

  20. 20

    Stuart, S. N. et al. Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786 (2004)Analysis describing the high levels of amphibian extinctions caused by many environmental factors and disease.

    Google Scholar 

  21. 21

    Kim, K. & Harvell, C. D. The rise and fall of a six-year coral-fungal epizootic. Am. Nat. 164, S52–S63 (2004)

    Google Scholar 

  22. 22

    Cameron, S. A. et al. Patterns of widespread decline in North American bumble bees. Proc. Natl Acad. Sci. USA 108, 662–667 (2011)

    Google Scholar 

  23. 23

    Byrnes, E. J., III et al. Emergence and pathogenicity of highly virulent Cryptococcus gattii genotypes in the northwest United States. PLoS Pathog. 6, e1000850 (2010)

    Google Scholar 

  24. 24

    Simwami, S. P. et al. Low diversity Cryptococcus neoformans variety grubii multilocus sequence types from Thailand are consistent with an ancestral African origin. PLoS Pathog. 7, e1001343 (2011)

    Google Scholar 

  25. 25

    Holdich, D. M., Reynolds, J. D., Souty-Grosset, C. & Sibley, P. J. A review of the ever increasing threat to European crayfish from non-indigenous crayfish species. Knowl. Managt. Aquat. Ecosyst. 394–395, 11 (2009)

    Google Scholar 

  26. 26

    Andrew, T. G., Huchzermeyer, K. D. A., Mbeha, B. C. & Nengu, S. M. Epizootic ulcerative syndrome affecting fish in the Zambezi river system in southern Africa. Vet. Rec. 163, 629–631 (2008)

    Google Scholar 

  27. 27

    Rizzo, D. M. & Garbelotto, M. Sudden oak death: endangering California and Oregon forest ecosystems. Front. Ecol. Environ. 1, 197–204 (2003)

    Google Scholar 

  28. 28

    Wills, R. T. The ecological impact of Phytophthora cinnamomi in the Stirling Range National Park, Western Australia. Aust. J. Ecol. 18, 145–159 (1993)

    Google Scholar 

  29. 29

    Jaenike, J. An hypothesis to account for the maintenance of sex within populations. Evol. Theor. 3, 191–194 (1978)

    Google Scholar 

  30. 30

    Paterson, S. et al. Antagonistic coevolution accelerates molecular evolution. Nature 464, 275–278 (2010)

    Google Scholar 

  31. 31

    McCallum, H. & Dobson, A. Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol. Evol. 10, 190–194 (1995)

    Google Scholar 

  32. 32

    De Castro, F. & Bolker, B. Mechanisms of disease-induced extinction. Ecol. Lett. 8, 117–126 (2005)Theoretical study outlining the conditions under which disease can cause extinction of its host species.

    Google Scholar 

  33. 33

    Altizer, S., Nunn, C. L. & Lindenfors, P. Do threatened hosts have fewer parasites? A comparative study in primates. J. Anim. Ecol. 76, 304–314 (2007)

    Google Scholar 

  34. 34

    Daszak, P., Cunningham, A. A. & Hyatt, A. D. Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287, 443–449 (2000)

    Google Scholar 

  35. 35

    Jones, K. E. et al. Global trends in emerging infectious diseases. Nature 451, 990–993 (2008)Macroecological analysis of recent patterns of EIDs worldwide in humans.

    Google Scholar 

  36. 36

    Casadevall, A. & Pirofski, L. A. The damage response framework of microbial pathogenesis. Nature Rev. Microbiol. 1, 17–24 (2003)

    Google Scholar 

  37. 37

    de Roode, J. C. et al. Virulence and competitive ability in genetically diverse malaria infections. Proc. Natl Acad. Sci. USA 102, 7624–7628 (2005)

    Google Scholar 

  38. 38

    Nowak, M. A. & May, R. M. Superinfection and the evolution of parasite virulence. Proc. R. Soc. Lond. B 255, 81–89 (1994)

    Google Scholar 

  39. 39

    Briggs, C. J., Knapp, R. A. & Vredenburg, V. T. Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proc. Natl Acad. Sci. USA 107, 9695–9700 (2010)

    Google Scholar 

  40. 40

    Stephens, P. A., Sutherland, W. J. & Freckleton, R. P. What is the Allee effect? Oikos 87, 185–190 (1999)

    Google Scholar 

  41. 41

    Mitchell, K. M., Churcher, T. S., Garner, T. W. G. & Fisher, M. C. Persistence of the emerging pathogen Batrachochytrium dendrobatidis outside the amphibian host greatly increases the probability of host extinction. Proc. R. Soc. B 275, 329–334 (2008)

    Google Scholar 

  42. 42

    Rypien, K. L., Andras, J. P. & Harvell, C. D. Globally panmictic population structure in the opportunistic fungal pathogen Aspergillus sydowii. Mol. Ecol. 17, 4068–4078 (2008)

    Google Scholar 

  43. 43

    Jessup, D. A. e. t. a. l. Southern sea otter as a sentinel of marine ecosystem health. EcoHealth 1, 239–245 (2004)

    Google Scholar 

  44. 44

    Sarmiento-Ramírez, J. M. et al. Fusarium solani is responsible for mass mortalities in nests of loggerhead sea turtle, Caretta caretta, in Boavista, Cape Verde. FEMS Microbiol. Lett. 312, 192–200 (2010)

    Google Scholar 

  45. 45

    Lindner, D. L. et al. DNA-based detection of the fungal pathogen Geomyces destructans in soils from bat hibernacula. Mycologia 103, 241–246 (2011)

    Google Scholar 

  46. 46

    Holt, R. D., Dobson, A. P., Begon, M., Bowers, R. G. & Schauber, E. M. Parasite establishment in host communities. Ecol. Lett. 6, 837–842 (2003)

    Google Scholar 

  47. 47

    Hansen, E. M., Parke, J. L. & Sutton, W. Susceptibility of Oregon forest trees and shrubs to Phytophthora ramorum: a comparison of artificial inoculation and natural infection. Plant Dis. 89, 63–70 (2005)

    Google Scholar 

  48. 48

    Fröhlich-Nowoisky, J., Pickersgill, D. A., Despres, V. R. & Poschl, U. High diversity of fungi in air particulate matter. Proc. Natl Acad. Sci. USA 106, 12814–12819 (2009)

    Google Scholar 

  49. 49

    Henk, D. A. et al. Speciation despite globally overlapping distributions in Penicillium chrysogenum: the population genetics of Alexander Fleming's lucky fungus. Mol. Ecol. 20, 4288–4301 (2011)

    Google Scholar 

  50. 50

    Pringle, A., Baker, D. M., Platt, J. L., Latge, J. P. & Taylor, J. W. Cryptic speciation in the cosmopolitan and clonal human pathogenic fungus Aspergillus fumigatus. Evolution 59, 1886–1899 (2005)

    Google Scholar 

  51. 51

    Ellison, C. E. et al. Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc. Natl Acad. Sci. USA 108, 2831–2836 (2011)

    Google Scholar 

  52. 52

    Giraud, T., Gladieux, P. & Gavrilets, S. Linking the emergence of fungal plant diseases with ecological speciation. Trends Ecol. Evol. 25, 387–395 (2010)

    Google Scholar 

  53. 53

    Springer, D. J. & Chaturvedi, V. Projecting global occurrence of Cryptococcus gattii. Emerg. Infect. Dis. 16, 14–20 (2010)

    Google Scholar 

  54. 54

    Seimon, T. A. et al. Upward range extension of Andean anurans and chytridiomycosis to extreme elevations in response to tropical deglaciation. Glob. Change Biol. 13, 288–299 (2007)

    Google Scholar 

  55. 55

    Fisher, M. C. et al. Biogeographic range expansion into South America by Coccidioides immitis mirrors New World patterns of human migration. Proc. Natl Acad. Sci. USA 98, 4558–4562 (2001)

    Google Scholar 

  56. 56

    Stukenbrock, E. H. & McDonald, B. A. The origins of plant pathogens in agro-ecosystems. Annu. Rev. Phytopathol. 46, 75–100 (2008)

    Google Scholar 

  57. 57

    Brasier, C. M. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol. 57, 792–808 (2008)An analysis of the lack of biosecurity and of the risk of disease introduction associated with the international plant trade.

    Google Scholar 

  58. 58

    Milgroom, M. G., Wang, K. R., Zhou, Y., Lipari, S. E. & Kaneko, S. Intercontinental population structure of the chestnut blight fungus, Cryphonectria parasitica. Mycologia 88, 179–190 (1996)

    Google Scholar 

  59. 59

    Gonthier, P., Warner, R., Nicolotti, G., Mazzaglia, A. & Garbelotto, M. M. Pathogen introduction, as a collateral effect of military activity. Mycol. Res. 108, 468–470 (2004)

    Google Scholar 

  60. 60

    Goka, K. et al. Amphibian chytridiomycosis in Japan: distribution, haplotypes and possible route of entry into Japan. Mol. Ecol. 18, 4757–4774 (2009)

    Google Scholar 

  61. 61

    Garner, T. W. J. et al. The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biol. Lett. 2, 455–459 (2006)

    Google Scholar 

  62. 62

    Cunningham, A. A. et al. Emergence of amphibian chytridiomycosis in Britain. Vet. Rec. 157, 386–387 (2005)

    Google Scholar 

  63. 63

    Walker, S. F. et al. Invasive pathogens threaten species recovery programs. Curr. Biol. 18, R853–R854 (2008)

    Google Scholar 

  64. 64

    Farrer, R. A. et al. Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalised hypervirulent recombinant lineage. Proc. Natl Acad. Sci. USA 108, 18732–18736 (2011)Population genomics analysis of the generation, and spread, of a hypervirulent fungal lineage in amphibians worldwide.

    Google Scholar 

  65. 65

    Wibbelt, G. et al. White-nose syndrome Fungus (Geomyces destructans) in Bats, Europe. Emerg. Infect. Dis. 16, 1237–1243 (2010)

    Google Scholar 

  66. 66

    Richards, T. A. et al. Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc. Natl Acad. Sci. USA 108, 15258–15263 (2011)

    Google Scholar 

  67. 67

    Fraser, J. A. et al. Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 437, 1360–1364 (2005)Analysis of the evolution of a hypervirulent lineage of human-infecting fungus that invaded British Columbia.

    Google Scholar 

  68. 68

    Turner, E., Jacobson, D. J. & Taylor, J. W. Genetic architecture of a reinforced, postmating, reproductive isolation barrier between Neurospora species indicates evolution via natural selection. PLoS Genet. 7, e1002204 (2011)

    Google Scholar 

  69. 69

    Coyne, J. A. & Orr, H. A. Speciation (Sinauer Associates, 2004)

    Google Scholar 

  70. 70

    Mallet, J. Hybrid speciation. Nature 446, 279–283 (2007)

    Google Scholar 

  71. 71

    Brasier, C. M., Rose, J. & Gibbs, J. N. An unusual phytophthora associated with widespread alder mortality in Britain. Plant Pathol. 44, 999–1007 (1995)

    Google Scholar 

  72. 72

    Inderbitzin, P., Davis, R. M., Bostock, R. M. & Subbarao, K. V. The ascomycete Verticillium longisporum is a hybrid and a plant pathogen with an expanded host range. PLoS One 6, e18260 (2011)

    Google Scholar 

  73. 73

    Gange, A. C., Gange, E. G., Sparks, T. H. & Boddy, L. Rapid and recent changes in fungal fruiting patterns. Science 316, 71 (2007)

    Google Scholar 

  74. 74

    Pachauri, R. K., Resinger, A., eds. Climate change 2007: Synthesis report. (Intergovernmental Panel on Climate Change, 2007)

  75. 75

    Newton, A. C., Johnson, S. N. & Gregory, P. J. Implications of climate change for diseases, crop yields and food security. Euphytica 179, 3–18 (2011)This paper highlights the importance of understanding the impact of climate change on crops and disease.

    Google Scholar 

  76. 76

    Lake, J. A. & Wade, R. N. Plant–pathogen interactions and elevated CO2: morphological changes in favour of pathogens. J. Exp. Bot. 60, 3123–3131 (2009)

    Google Scholar 

  77. 77

    Chakraborty, S. et al. Impacts of global change on diseases of agricultural crops and forest trees. CAB Rev. 3, 1–5 (2008)

    Google Scholar 

  78. 78

    Kobayashi, T. et al. Effects of elevated atmospheric CO2 concentration on the infection of rice blast and sheath blight. Phytopathology 96, 425–431 (2006)

    Google Scholar 

  79. 79

    Madgwick, J. W. et al. Impacts of climate change on wheat anthesis and fusarium ear blight in the UK. Eur. J. Plant Pathol. 130, 117–131 (2011)

    Google Scholar 

  80. 80

    Gregory, P. J., Johnson, S. N., Newton, A. C. & Ingram, J. S. I. Integrating pests and pathogens into the climate change/food security debate. J. Exp. Bot. 60, 2827–2838 (2009)

    Google Scholar 

  81. 81

    Pounds, J. A. et al. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439, 161–167 (2006)

    Google Scholar 

  82. 82

    Bosch, J., Carrascal, L. M., Duran, L., Walker, S. & Fisher, M. C. Climate change and outbreaks of amphibian chytridiomycosis in a montane area of Central Spain; is there a link? Proc. R. Soc. B 274, 253–260 (2007)

    Google Scholar 

  83. 83

    Rohr, J. R., Raffel, T. R., Romansic, J. M., McCallum, H. & Hudson, P. J. Evaluating the links between climate, disease spread, and amphibian declines. Proc. Natl Acad. Sci. USA 105, 17436–17441 (2008)

    Google Scholar 

  84. 84

    Garner, T. W. J., Rowcliffe, J. M. & Fisher, M. C. Climate change, chytridiomycosis or condition: an experimental test of amphibian survival. Glob. Change Biol. 17, 667–675 (2011)

    Google Scholar 

  85. 85

    Becker, C. G. & Zamudio, K. R. Tropical amphibian populations experience higher disease risk in natural habitats. Proc. Natl Acad. Sci. USA 108, 9893–9898 (2011)

    Google Scholar 

  86. 86

    Harvell, C. D. et al. Review: Emerging marine diseases - Climate links and anthropogenic factors. Science 285, 1505–1510 (1999)

    Google Scholar 

  87. 87

    vanEngelsdorp, D. et al. Colony collapse disorder: a descriptive study. PLoS One 4, e6481 (2009)

    Google Scholar 

  88. 88

    Ratnieks, F. L. W. & Carreck, N. L. Clarity on honey bee collapse? Science 327, 152–153 (2010)

    Google Scholar 

  89. 89

    Verweij, P. E., Mellado, E. & Melchers, W. J. G. Multiple-triazole-resistant aspergillosis. N. Engl. J. Med. 356, 1481–1483 (2007)

    Google Scholar 

  90. 90

    Klaassen, C. H. W., Gibbons, J. G., Fedorova, N. D., Meis, J. F. & Rokas, A. Evidence for genetic differentiation and variable recombination rates among Dutch populations of the opportunistic human pathogen Aspergillus fumigatus. Mol. Ecol. 21, 57–70 (2012)

    Google Scholar 

  91. 91

    Miraglia, M. et al. Climate change and food safety: an emerging issue with special focus on Europe. Food Chem. Toxicol. 47, 1009–1021 (2009)

    Google Scholar 

  92. 92

    Stokstad, E. The famine fighter’s last battle. Science 324, 710–712 (2009)

    Google Scholar 

  93. 93

    Loo, J. A. Ecological impacts of non-indigenous invasive fungi as forest pathogens. Biol. Invasions 11, 81–96 (2009)

    Google Scholar 

  94. 94

    Kurz, W. A. et al. Mountain pine beetle and forest carbon feedback to climate change. Nature 452, 987–990 (2008)Study describing pest- and pathogen-induced loss of forest carbon sinks.

    Google Scholar 

  95. 95

    Mazzoni, R. et al. Emerging pathogen of wild amphibians in frogs (Rana catesbeiana) farmed for international trade. Emerg. Infect. Dis. 9, 995–998 (2003)

    Google Scholar 

  96. 96

    Byrnes, E. J., III, Bildfell, R. J., Dearing, P. L., Valentine, B. A. & Heitman, J. Cryptococcus gattii with bimorphic colony types in a dog in western Oregon: additional evidence for expansion of the Vancouver Island outbreak. J. Vet. Diagn. Invest. 21, 133–136 (2009)

    Google Scholar 

  97. 97

    Lubick, N. Emergency medicine for frogs. Nature 465, 680–681 (2010)

    Google Scholar 

  98. 98

    Harris, R. N. et al. Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME J. 3, 818–824 (2009)

    Google Scholar 

  99. 99

    U.S. Fish and Wildlife Service A national plan for assisting states, federal agencies, and tribes in managing white-nose syndrome in bats. 〈http://www.fws.gov/WhiteNoseSyndrome/pdf/WNSnationalplanMay2011.pdf〉 (2011)

Download references

Acknowledgements

M.C.F. was supported by grants from the Wellcome Trust, Natural Environment Research Council (NERC), and the European Research Area (ERA)-net project BiodivERsA. D.A.H. was supported by a grant from the Leverhulme Trust, C.J.B. was supported by the US National Science Foundation (NSF) Ecology of Infectious Disease grant EF-0723563. S.J.G. was supported by grants from the UK Biotechnology and Biological Sciences Research Council (BBSRC) and the John Fell Fund of the University of Oxford, and S.L.M. was supported by a graduate scholarship from Magdalen College, University of Oxford. J.S.B. was supported by Google.org and the National Institutes of Health grant 5R01LM010812-02. N. Knowlton and J. Heitman provided impetus to develop this review.

Author information

Affiliations

Authors

Contributions

M.C. F., D.A.H., C.J.B., S.L.M. and S.J.G designed, analysed and wrote the paper. Data were collected and analysed by J.S.B. and L.C.M.

Corresponding authors

Correspondence to Matthew C. Fisher or Sarah J. Gurr.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Tables 1-5 and additional references. (PDF 343 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Fisher, M., Henk, D., Briggs, C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012). https://doi.org/10.1038/nature10947

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.