Ecosystems

, Volume 19, Issue 4, pp 737–748 | Cite as

Disease Ecology Meets Ecosystem Science

  • Daniel L. Preston
  • John A. Mischler
  • Alan R. Townsend
  • Pieter T. J. Johnson
Article

Abstract

Growing evidence indicates that parasites—when considered—can play influential roles in ecosystem structure and function, highlighting the need to integrate disease ecology and ecosystem science. To strengthen links between these traditionally disparate fields, we identified mechanisms through which parasites can affect ecosystems and used empirical literature searches to explore how commonly such mechanisms have been documented, the ecosystem properties affected, and the types of ecosystems in which they occur. Our results indicate that ecosystem-disease research has remained consistently rare, comprising less than 2% of disease ecology publications. Existing studies from terrestrial, freshwater, and marine systems, however, demonstrate that parasites can strongly affect (1) biogeochemical cycles of water, carbon, nutrients, and trace elements, (2) fluxes of biomass and energy, and (3) temporal ecosystem dynamics including disturbance, succession, and stability. Mechanistically, most studies have demonstrated density-mediated indirect effects, rather than trait-mediated effects, or direct effects of parasites, although whether this is representative remains unclear. Looking forward, we highlight the importance of applying traits-based approaches to predict when parasites are most likely to exert ecosystem-level effects. Future research should include efforts to extend host–parasite studies across levels of ecological organization, large-scale manipulations to experimentally quantify ecosystem roles of parasites, and the integration of parasites and disease into models of ecosystem functioning.

Keywords

parasite pathogen infection host ecosystem structure ecosystem function ecosystem dynamics biogeochemistry energy flow stability 

Notes

Acknowledgements

We thank S. Collinge, M. Joseph, V. McKenzie, J. Mihaljevic, Y. Springer, and two anonymous reviewers for comments that improved the manuscript. This research was supported by a fellowship from the David and Lucile Packard Foundation and funds from the University of Colorado and the National Science Foundation (DEB-0841758, DEB-1149308, DEB-1311467, and a Graduate Fellowship to DLP).

Supplementary material

10021_2016_9965_MOESM1_ESM.docx (199 kb)
Supplementary Material 1 (DOCX 200 kb).

References

  1. Amundsen PA, Lafferty KD, Knudsen R, Primicerio R, Klemetsen A, Kuris AM. 2009. Food web topology and parasites in the pelagic zone of a subarctic lake. Journal of Animal Ecology 78:563–72.CrossRefPubMedGoogle Scholar
  2. Anderson RM. 1978. The regulation of host population growth by parasitic species. Parasitology 76:119–57.CrossRefPubMedGoogle Scholar
  3. Balvanera P, Pfisterer AB, Buchmann N, He JS, Nakashizuka TB, Schmid Raffaelli D. 2006. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecology Letters 9:1146–56.CrossRefPubMedGoogle Scholar
  4. Baudoin M. 1975. Host castration as a parasitic strategy. Evolution 29:335–52.CrossRefGoogle Scholar
  5. Bernot RJ. 2013. Parasite-host elemental content and the effects of a parasite on host- consumer-driven nutrient recycling. Freshwater Science 32:299–308.CrossRefGoogle Scholar
  6. Castello JD, Leopold DJ, Smallidge PJ. 1995. Pathogens, patterns, and processes in forest ecosystems. Bioscience 45:16–24.CrossRefGoogle Scholar
  7. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naem S. 2012. Biodiversity loss and its impact on humanity. Nature 486:59–67.CrossRefPubMedGoogle Scholar
  8. Chapin FSIII, Matson PPA, Vitousek PM, Eds. 2011. Principles of terrestrial ecosystem ecology. New York: Springer.Google Scholar
  9. Cobb RC, Chan MN, Meentemeyer RK, Rizzo DM. 2012. Common factors drive disease and coarse woody debris dynamics in forests impacted by sudden oak death. Ecosystems 15:242–55.CrossRefGoogle Scholar
  10. Collinge SK, Ray C, Eds. 2006. Disease ecology: community structure and pathogen dynamics. Oxford, UK: Oxford University Press.Google Scholar
  11. Connelly S, Pringle CM, Bixby RJ, Brenes R, Whiles MR, Lips KR, Kilham S, Huryn AD. 2008. Changes in stream primary producer communities resulting from large-scale catastrophic amphibian declines: can small-scale experiments predict effects of tadpole loss? Ecosystems 11:1262–76.CrossRefGoogle Scholar
  12. Danovaro R, Corinaldesi C, DellAnno A, Fuhrman JA, Middelburg JJ, Noble RT, Suttle CA. 2011. Marine viruses and global climate change. FEMS Microbiology Reviews 35:993–1034.CrossRefPubMedGoogle Scholar
  13. De Bello F, Lavorel S, Díaz S, Harrington R, Cornelissen JH, Bardgett RD, Berg MP, Cipriotti P, Feld CK, Hering D, da Silva PM, Potts SG, Sandin L, Sousa JP, Storkey J, Wardle DA, Harrison PA. 2010. Towards an assessment of multiple ecosystem processes and services via functional traits. Biodiversity and Conservation 19:2873–93.CrossRefGoogle Scholar
  14. De Castro F, Bolker B. 2005. Mechanisms of disease-induced extinction. Ecology Letters 8:117–26.CrossRefGoogle Scholar
  15. Del Giorgio PA, Duarte CM. 2002. Respiration in the open ocean. Nature 420:379–84.CrossRefPubMedGoogle Scholar
  16. Dobson AP, Crawley M. 1994. Pathogens and the structure of plant communities. Trends in Ecology and Evolution 9:393–8.CrossRefPubMedGoogle Scholar
  17. Dobson AP, Hudson PJ. 1986. Parasites, disease and the structure of ecological communities. Trends in Ecology and Evolution 1:11–15.CrossRefPubMedGoogle Scholar
  18. Dunn RR, Harris NC, Colwell RK, Koh LP, Sodhi NS. 2009. The sixth mass coextinction: are most endangered species parasites and mutualists? Proceedings of the Royal Society B 276:3037–45.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Ellison AM, Bank MS, Clinton BD, Colburn EA, Elliott K, Ford CR, Foster DR, Kloeppel DL, Knoepp JD, Lovett GM, Mohan J, Orwig DA, Rodenhouse NL, Sobczak WV, Stinson KA, Stone JK, Swan CM, Thompson J, Von Holle B, Webster JR. 2005. Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment 3:479–86.CrossRefGoogle Scholar
  20. Elser JJ, Urabe J. 1999. The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80:735–51.CrossRefGoogle Scholar
  21. Eviner VT, Likens GE. 2008. Effects of pathogens on terrestrial ecosystem function. In: Ostfeld RS, Keesing F, Eviner V, Eds. Infectious disease ecology: effects of ecosystems on disease and of disease on ecosystems. Princeton, NJ: Princeton University Press. p 260–83.Google Scholar
  22. Filbee-Dexter K, Scheibling RE. 2014. Sea urchin barrens as alternative stable states of collapsed kelp ecosystems. Marine Ecology Progress Series 495:1–25.CrossRefGoogle Scholar
  23. Fuhrman JA. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399:541–8.CrossRefPubMedGoogle Scholar
  24. Gessner MO, Swan CM, Dang CK, McKie BG, Bardgett RD, Wall DH, Hattenschwiler S. 2010. Diversity meets decomposition. Trends in Ecology and Evolution 25:372–80.CrossRefPubMedGoogle Scholar
  25. Hall RO Jr, Tank JL, Dybdahl MF. 2003. Exotic snails dominate nitrogen and carbon cycling in a highly productive stream. Frontiers in Ecology and the Environment 1:407–11.CrossRefGoogle Scholar
  26. Hernandez AD, Sukhdeo MV. 2008a. Parasite effects on isopod feeding rates can alter the host’s functional role in a natural stream ecosystem. International Journal of Parasitology 38:683–90.CrossRefPubMedGoogle Scholar
  27. Hernandez AD, Sukhdeo MV. 2008b. Parasites alter the topology of a stream food web across seasons. Oecologia 156:613–24.CrossRefPubMedGoogle Scholar
  28. Holah JC, Wilson MV, Hansen EM. 1997. Impacts of a native root-rotting pathogen on successional development of old-growth Douglas fir forests. Oecologia 111:429–33.CrossRefGoogle Scholar
  29. Holdo RM, Sinclair AR, Dobson AP, Metzger KL, Bolker BM, Ritchie ME, Holt RD. 2009. A disease-mediated trophic cascade in the Serengeti and its implications for ecosystem C. PLoS Biology 7:e1000210.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hooper DU, Chapin FSIII, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setala H, Symstad AJ, Vandermeer J, Wardle DA. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75:3–35.CrossRefGoogle Scholar
  31. Hudson PJ, Dobson AP, Newborn D. 1998. Prevention of population cycles by parasite removal. Science 282:2256–58.CrossRefPubMedGoogle Scholar
  32. Johnson PTJ, Dobson AP, Lafferty KD, Marcogliese DJ, Memmott J, Orlofske SA, Poulin R, Thieltges DW. 2010. When parasites become prey: ecological and epidemiological significance of eating parasites. Trends in Ecology and Evolution 25:362–71.CrossRefPubMedGoogle Scholar
  33. Kagami M, de Bruin A, Ibelings BW, Van Donk E. 2007. Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiologia 587:113–29.CrossRefGoogle Scholar
  34. Kohler SL, Wiley MJ. 1997. Pathogen outbreaks reveal large-scale effects of competition in stream communities. Ecology 78:2164–76.CrossRefGoogle Scholar
  35. Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP, Dunham EJ, Fredensborg BL, Huspeni TC, Lorda J, Mababa L, Mancini FT, Mora AB, Pickering M, Talhouk NL, Torchin ME, Lafferty KD. 2008. Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515–18.CrossRefPubMedGoogle Scholar
  36. Lafferty KD, Dobson AP, Kuris AM. 2006. Parasites dominate food web links. Proceedings of the National Academy of Sciences of the United States of America 103:11211–16.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Lafferty KD, Kuris AM. 2002. Trophic strategies, animal diversity and body size. Trends in Ecology and Evolution 17:507–13.CrossRefGoogle Scholar
  38. Lessios HA. 1988. Mass mortality of Diadema antillarum in the Caribbean: what have we learned? Annual Review of Ecology, Evolution and Systematics 19:371–93.CrossRefGoogle Scholar
  39. Loo JA. 2009. Ecological impacts of non-indigenous invasive fungi as forest pathogens. Biological Invasions 11:81–96.CrossRefGoogle Scholar
  40. Loreau M, Roy J, Tilman D. 2005. Linking ecosystem and parasite ecology. In: Thomas F, Renaud F, Guegan JF, Eds. Parasitism and ecosystems. Oxford, UK: Oxford University Press. p 13–21.CrossRefGoogle Scholar
  41. Lovett GM, Arthur MA, Weathers KC, Griffin JM. 2010. Long-term changes in forest carbon and nitrogen cycling caused by an introduced pest/pathogen complex. Ecosystems 13:1188–200.CrossRefGoogle Scholar
  42. March WA, Watson DM. 2010. The contribution of mistletoes to nutrient returns: evidence for a critical role in nutrient cycling. Austral Ecology 35:713–21.CrossRefGoogle Scholar
  43. Maron JL, Marler M, Klironomos JN, Cleveland CC. 2011. Soil fungal pathogens and the relationship between plant diversity and productivity. Ecology Letters 14:36–41.CrossRefPubMedGoogle Scholar
  44. McCann K, Hastings A, Huxel GR. 1998. Weak trophic interactions and the balance of nature. Nature 395:794–8.CrossRefGoogle Scholar
  45. McCormick JF, Platt RB. 1980. Recovery of an Appalachian forest following the chestnut blight or Catherine Keever-you were right!. American Midland Naturalist 104:264–73.CrossRefGoogle Scholar
  46. McGill BJ, Enquist BJ, Weiher E, Westoby M. 2006. Rebuilding community ecology from functional traits. Trends in Ecology and Evolution 21:178–85.CrossRefPubMedGoogle Scholar
  47. Metz MR, Varner JM, Frangioso KM, Meentemeyer RK, Rizzo DM. 2013. Unexpected redwood mortality from synergies between wildfire and emerging infectious disease. Ecology 94:2152–9.CrossRefPubMedGoogle Scholar
  48. Mitchell CE. 2003. Trophic control of grassland production and biomass by pathogens. Ecology Letters 6:147–55.CrossRefGoogle Scholar
  49. Paine RT. 1966. Food web complexity and species diversity. The American Naturalist 100:65–75.CrossRefGoogle Scholar
  50. Pedersen AB, Antonovics J. 2013. Anthelmintic treatment alters the parasite community in a wild mouse host. Biology Letters 9:20130205.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Petermann JS, Fergus AJF, Turnbull LA, Schmid B. 2008. Janzen-Connell effects are widespread and strong enough to maintain diversity in grasslands. Ecology 89:2399–406.CrossRefPubMedGoogle Scholar
  52. Poulin R. 2010. Parasite manipulation of host behavior: an update and frequently asked questions. Advances in the Study of Host Behavior 41:151–86.CrossRefGoogle Scholar
  53. Preisser EL, Bolnick DI, Benard MF. 2005. Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–9.CrossRefGoogle Scholar
  54. Press MC, Phoenix GK. 2005. Impacts of parasitic plants on natural communities: Tansley review. New Phytologist 166:737–51.CrossRefPubMedGoogle Scholar
  55. Preston DL, Jacobs AZ, Orlofske SA, Johnson PTJ. 2014. Complex life cycles in a pond food web: effects of life stage structure and parasites on network properties, trophic positions and the fit of a probabilistic niche model. Oecologia 174:953–65.CrossRefPubMedGoogle Scholar
  56. Preston DL, Orlofske SA, Lambden JP, Johnson PTJ. 2013. Biomass and productivity of trematode parasites in pond ecosystems. Journal of Animal Ecology 82:509–17.CrossRefPubMedGoogle Scholar
  57. Price PW. 1977. General concepts on the evolutionary biology of parasites. Evolution 31:405–20.CrossRefGoogle Scholar
  58. Quested HM, Press MC, Callaghan TV, Cornelissen HJ. 2002. The hemiparasitic angiosperm Bartsia alpina has the potential to accelerate decomposition in sub-arctic communities. Oecologia 130:88–95.CrossRefGoogle Scholar
  59. Rasconi S, Jobard M, Sime-Ngando T. 2011. Parasitic fungi of phytoplankton: ecological roles and implications for microbial food webs. Aquatic Microbial Ecology 62:123–37.CrossRefGoogle Scholar
  60. Rudolf VHW, Lafferty KD. 2011. Stage structure alters how complexity affects stability of ecological networks. Ecology Letters 14:75–9.CrossRefPubMedGoogle Scholar
  61. Ruess RW, McFarland JM, Trummer LM, Rohrs-Richey JK. 2009. Disease-mediated declines in N-fixation inputs by Alnus tenuifolia to early-successional floodplains in interior and south-central Alaska. Ecosystems 12:489–502.CrossRefGoogle Scholar
  62. Sato T, Egusa T, Fukushima K, Oda T, Ohte N, Tokuchi N, Watanabe K, Kanaiwa M, Murakami I, Lafferty KD. 2012. Nematomorph parasites indirectly alter the food web and ecosystem function of streams through behavioural manipulation of their cricket hosts. Ecology Letters 15:786–93.CrossRefPubMedGoogle Scholar
  63. Sato T, Watanabe K, Kanaiwa M, Niizuma Y, Harada Y, Lafferty KD. 2011. Nematomorph parasites drive energy flow through a riparian ecosystem. Ecology 92:201–7.CrossRefPubMedGoogle Scholar
  64. Scott ME, Dobson AP. 1989. The role of parasites in regulating host abundance. Parasitology Today 5:176–83.CrossRefPubMedGoogle Scholar
  65. Sumption KJ, Flowerdew JR. 1985. The ecological effects of the decline in rabbits (Oryctolagus cuniculus L.) due to myxomatosis. Mammal Review 15:151–86.CrossRefGoogle Scholar
  66. Suttle CA. 2005. Viruses in the sea. Nature 437:356–61.CrossRefPubMedGoogle Scholar
  67. Suttle CA. 2007. Marine viruses—major players in the global ecosystem. Nature Reviews Microbiology 5:801–12.CrossRefPubMedGoogle Scholar
  68. Thieltges DW, Amundsen PA, Hechinger RF, Johnson PTJ, Lafferty KD, Mouritsen KN, Preston DL, Reise K, Zander CD, Poulin R. 2013. Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission. Oikos 10:1473–82.Google Scholar
  69. Thomas F, Bonsall MB, Dobson AP. 2005. Parasitism, biodiversity, and conservation. In: Thomas F, Renaud F, Guegan JF, Eds. Parasitism and ecosystems. Oxford, UK: Oxford University Press. p 124–39.CrossRefGoogle Scholar
  70. Tompkins DM, Dunn AM, Smith MJ, Telfer S. 2011. Wildlife diseases: from individuals to ecosystems. Journal of Animal Ecology 80:19–38.CrossRefPubMedGoogle Scholar
  71. Tsao JI, Wootton JT, Bunikis J, Luna MG, Fish D, Barbour AG. 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 of the United States of America 101:18159–64.CrossRefPubMedPubMedCentralGoogle Scholar
  72. Valachovic YS, Lee CA, Scanlon H, Varner JM, Glebocki R, Graham BD, Rizzo DM. 2011. Sudden oak death-caused changes to surface fuel loading and potential fire behavior in Douglas-fir-tanoak forests. Forest Ecology and Management 261:1973–86.CrossRefGoogle Scholar
  73. Van der Putten WH, Vet LEM, Harvey JA, Wackers FL. 2001. Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends in Ecology and Evolution 16:547–54.CrossRefGoogle Scholar
  74. Van der Putten WH, Van Dijk C, Peters BAM. 1993. Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362:53–6.CrossRefGoogle Scholar
  75. Vredenburg VT. 2004. Reversing introduced species effects: experimental removal of introduced fish leads to rapid recovery of a declining frog. Proceedings of the National Academy of Sciences of the United States of America 101:7646–50.CrossRefPubMedPubMedCentralGoogle Scholar
  76. Webb CT, Hoeting JA, Ames GM, Pyne MI, Poff NL. 2010. A structured and dynamic framework to advance traits-based theory and prediction in ecology. Ecology Letters 13:267–83.CrossRefPubMedGoogle Scholar
  77. Werner EE, Peacor SD. 2003. A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–100.CrossRefGoogle Scholar
  78. Whiles MR, Hall RO, Dodds WK, Verburg P, Huryn AD, Pringle CM, Lips KR, Kilham SS, Colon-Gaud C, Rugenski AT, Peterson S, Connelly S. 2012. Disease-driven amphibian declines alter ecosystem processes in a tropical stream. Ecosystems 16:146–57.CrossRefGoogle Scholar
  79. Wilhelm SW, Suttle CA. 1999. Viruses and nutrient cycles in the sea. Bioscience 49:781–8.CrossRefGoogle Scholar
  80. Worrall JJ, Lee TD, Harrington TC. 2005. Forest dynamics and agents that initiate and expand canopy gaps in Picea-Abies forests of Crawford Notch, New Hampshire, USA. Journal of Ecology 93:178–90.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Daniel L. Preston
    • 1
    • 2
  • John A. Mischler
    • 3
  • Alan R. Townsend
    • 4
  • Pieter T. J. Johnson
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA
  2. 2.Department of Integrative BiologyOregon State UniversityCorvallisUSA
  3. 3.Department of BiologyKings CollegeWilkes-BarreUSA
  4. 4.Nicholas School of the EnvironmentDuke UniversityDurhamUSA

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