Biodiversity loss decreases parasite diversity: Theory and patterns

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1604, 2012, Pages 2814-2827

  Lafferty, Kevin D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biodiversity loss; Coextinction; Food web; Parasite

Indexed keywords

BIODIVERSITY; COEXISTENCE; FOOD CHAIN; FOOD WEB; HABITAT LOSS; HOST-PARASITE INTERACTION; LIFE CYCLE; SPECIALIST; SPECIES RICHNESS;

EID: 84866111170     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0110     Document Type: Review

References (71)

1. Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S. & Samuel, M. D. 2002 Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158-2162. (doi:10.1126/science.1063699)
2. Keesing, F. et al. 2010 Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647-652. (doi:10.1038/nature09575)
3. Swaddle, J. P. & 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. (doi:10.1371/journal.pone.0002488)
4. Keesing, F., Holt, R. D. & Ostfeld, R. S. 2006 Effects of species diversity on disease risk. Ecol. Lett. 9, 485-498. (doi:10.1111/j.1461-0248.2006.00885.x)
5. Pongsiri, M. J., Roman, J., Ezenwa, V. O., Goldberg, T. L., Koren, H. S., Newbold, S. C., Ostfeld, R. S., Pattanayak, S. K. & Salkeld, D. J. 2009 Biodiversity loss affects global disease ecology. Bioscience 59, 945-954. (doi:10.1525/bio.2009.59.11.6)
6. Dobson, A. P., Lafferty, K. D., Kuris, A. M., Hechinger, R. F. & Jetz, W. 2008 Homage to Linnaeus: how many parasites? How many hosts? Proc. Natl Acad. Sci. USA 105, 11482-11489. (doi:10.1073/pnas.0803232105)
7. Dunn, R. R., Harris, N. C., Colwell, R. K., Koh, L. P. & Sodhi, N. S. 2009 The sixth mass coextinction: are most endangered species parasites and mutualists? Proc. R. Soc. B 276, 3037-3045. (doi:10.1098/rspb.2009.0413)
8. Koh, L. P., Dunn, R. R., Sodhi, N. S., Colwell, R. K., Proctor, H. C. & Smith, V. S. 2004 Species coextinctions and the biodiversity crisis. Science 305, 1632-1634. (doi:10.1126/science.1101101)
9. Poulin, R. & Morand, S. 1997 Parasite body size distributions: interpreting patterns of skewness. Int. J. Parasitol. 27, 959-964. (doi:10.1016/S0020-7519(97)00055-6)
10. Sprent, J. F. A. 1992 Parasites lost. Int. J Parasitol. 22, 139-151. (doi:10.1016/0020-7519(92)90095-3)
11. Dobson, A. P. & May, R. M. 1987 The effects of parasites on fish populations - theoretical aspects. Int. J Parasitol. 17, 363-370. (doi:10.1016/0020-7519(87)90111-1)
12. Hechinger, R. F., Lafferty, K. D., Huspeni, T. C., Brooks, A. & Kuris, A. M. 2007 Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local fishes and benthos. Oecologia 151, 82-92. (doi:10.1007/s00442-006-0568-z)
13. Hudson, P. J., Dobson, A. P. & Lafferty, K. D. 2006 Parasites and ecological systems: is a healthy system one with many parasites?. Trends Ecol. Evol. 21, 381-385. (doi:10.1016/j.tree.2006.04.007)
14. Huspeni, T. C. & Lafferty, K. D. 2004 Using larval trematodes that parasitize snails to evaluate a salt-marsh restoration project. Ecol. Appl. 14, 795-804. (doi:10.1890/01-5346)
15. Lafferty, K. D. 1997 Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitol. Today 13, 251-255. (doi:10.1016/S0169-4758(97)01072-7)
16. Lafferty, K. D. & Kuris, A. M. 1999 How environmental stress affects the impacts of parasites? Limnol. Oceanogr. 44, 925-931. (doi:10.4319/lo.1999.44.3_part_2.0925)
17. Wood, C. L., Lafferty, K. D. & Micheli, F. 2010 Fishing out marine parasites? Impacts of fishing on rates of parasitism in the ocean. Ecol. Lett. 13, 761-775. (doi:10.1111/j.1461-0248.2010.01467.x)
18. Byers, J. E., Altman, I., Grosse, A. M., Huspeni, T. C. & Maerz, J. C. 2011 Using parasitic trematode larvae to quantify an elusive vertebrate host. Conserv. Biol. 25, 85-93. (doi:10.1111/j.1523-1739.2010.01583.x)
19. Guernier, V., Hochberg, M. E. & Guegan, J. F. O. 2004 Ecology drives the worldwide distribution of human diseases. PLoS Biol. 2, 740-746. (doi:10.1371/journal.pbio.0020141)
20. Dunn, R. R., Davies, T. J., Harris, N. C. & Gavin, M. C. 2010 Global drivers of human pathogen richness and prevalence. Proc. R. Soc. B 277, 2587-2595. (doi:10.1098/rspb.2010.0340)
21. Harris, N. C. & Dunn, R. R. 2010 Using host associations to predict spatial patterns in the species richness of the parasites of North American carnivores. Ecol. Lett. 13, 1411-1418. (doi:10.1111/j.1461-0248.2010.01527.x)
22. Hechinger, R. F. & Lafferty, K. D. 2005 Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proc. R. Soc. B 272, 1059-1066. (doi:10.1098/rspb.2005.3070)
23. Lafferty, K. D. & Dunham, E. J. 2005 Trematodes in snails near raccoon latrines suggest a final host role for this mammal in California salt marshes. J Parasitol. 91, 474-476. (doi:10.1645/GE-390R1)
24. Whitney, K. L., Hechinger, R. F., Kuris, A. M. & Lafferty, K. D. 2007 Endangered light-footed clapper rail affects parasite community structure in coastal wetlands. Ecol. Appl. 17, 1694-1702. (doi:10.1890/06-1325.17)
25. Lafferty, K. D., Shaw, J. C. & Kuris, A. M. 2008 Reef fishes have higher parasite richness at unfished Palmyra Atoll compared to fished Kiritimati Island. EcoHealth 5, 338-345. (doi:10.1007/s10393-008-0196-7)
26. Loot, G., Aldana, M. & Navarrete, S. A. 2005 Effects of human exclusion on parasitism in intertidal food webs of central Chile. Conserv. Biol. 19, 203-212. (doi:10.1111/j.1523-1739.2005.00396.x)
27. McIntyre, P. B., Michel, E., France, K., Rivers, A., Hakizimana, P. & Cohen, A. S. 2005 Individual- and assemblage-level effects of anthropogenic sedimentation on snails in Lake Tanganyika. Conserv. Biol. 19, 171-181. (doi:10.1111/j.1523-1739.2005.00456.x)
28. Rudolf, V. & Lafferty, K. D. 2011 Stage structure alters how complexity affects stability of ecological networks. Ecol. Lett. 14, 75-79. (doi:10.1111/j.1461-0248.2010.01558.x)
29. Dunne, J. A. & Williams, R. J. 2009 Cascading extinctions and community collapse in model food webs. Phil. Trans. R. Soc. B 364, 1711-1723. (doi:10.1098/rstb.2008.0219)
30. Dunne, J. A., Williams, R. J. & Martinez, N. D. 2002 Food-web structure and network theory: the role of connectance and size. Proc. Natl Acad. Sci. USA 99, 12917-12922. (doi:10.1073/pnas.192407699)
31. Sole, R. V. & Montoya, J. M. 2001 Complexity and fragility in ecological networks. Proc. R. Soc. Lond. B 268, 2039-2045. (doi:10.1098/rspb.2001.1767)
32. Price, R. D., Clayton, D. H. & Adams, R. J. 2000 Pigeon lice down under: taxonomy of Australian Campanulotes (Phthiraptera: Philopteridae), with a description of C. durdeni n. sp. J. Parasitol. 86, 948-950. (doi:10.1645/0022-3395(2000)086[0948:PLDUTO]2.0.C0;2)
33. Chen, H.-W., Shao, K. T., Liu, C. W.-J., Lin, W.-H. & Liu, W. C. 2011 The reduction of food web robustness by parasitism: fact and artefact. Int. J. Parasitol. 4, 627-634. (doi:10.1016/j.ijpara.2010.12.013)
34. Lafferty, K. D. & Kuris, A. M. 2009 Parasites reduce food web robustness because they are sensitive to secondary extinction as illustrated by an invasive estuarine snail. Phil. Trans. R. Soc. B 364, 1659-1663. (doi:10.10l98/rstb2000800220)
35. Altizer, S., Nunn, C. L. & Lindenfors, P. 2007 Do threatened hosts have fewer parasites? A comparative study in primates. J. Anim. Ecol. 76, 304-314. (doi:10.1111/j.1365-2656.2007.01214.x)
36. Purvis, A., Gittleman, J. L., Cowlishaw, G. & Mace, G. M. 2000 Predicting extinction risk in declining species. Proc. R. Soc. Lond. B 267, 1947-1952. (doi:10.1098/rspb.2000.1234)
37. Vitone, N. D., Altizer, S. & Nunn, C. L. 2004 Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates. Evol. Ecol. Res. 6, 183-199.
38. Lafferty, K. D., Dobson, A. P. & Kuris, A. M. 2006 Parasites dominate food web links. Proc. Natl Acad. Sci. USA 103, 11211-11216. (doi:10.1073/pnas.0604755103)
39. Chen, H. W., Liu, W. C., Davis, A. J., Jordan, F., Hwang, M. J. & Shao, K. T. 2008 Network position of hosts in food webs and their parasite diversity. Oikos 117, 1847-1855. (doi:10.1111/j.1600-0706.2008.16607.x)
40. Gerber, L. R., Lafferty, K. D., McCallum, H. I., Sabo, J. L. & Dobson, A. P. 2005 Exposing extinction risk analysis to pathogens: is disease just another form of density dependence?. Ecol. Appl. 15, 1402-1414. (doi:10.1890/04-0880)
41. Srinivasan, U. T., Dunne, J. A., Harte, J. & Martinez, N. D. 2007 Response of complex food webs to realistic extinction sequences. Ecology 88, 671-682. (doi:10.1890/06-0971)
42. Lafferty, K. D. & Dunne, J. A. 2010 Stochastic ecological network occupancy (SENO) models: a new tool for modeling ecological networks across spatial scales. Theor. Ecol. 3, 123-135. (doi:10.1007/s12080-010-0082-0)
43. Hernandez, A. D. & Sukhdeo, M. V. K. 2008 Parasites alter the topology of a stream food web across seasons. Oecologia 156, 613-624. (doi:10.1007/s00442-008-0999-9)
44. Amundsen, P. A., Lafferty, K. D., Knudsen, R., Primicerio, R., Klemetsen, A. & Kuris, A. M. 2009 Food web topology and parasites in the pelagic zone of a subarctic lake. J. Anim. Ecol. 78, 563-572. (doi:10.1111/j.1365-2656.2008.01518.x)
45. Huxham, M. & Raffaelli, D. 1995 Parasites and food-web patterns. J Anim. Ecol. 64, 168-176. (doi:10.2307/5752)
46. Mouritsen, K. N., Poulin, R., McLaughlin, J. P. & Thieltges, D. W. 2011 Food web including metazoan parasites for an intertidal ecosystem in New Zealand. Ecology 92, 2006. (doi:10.1890/11-0371.1)
47. Thieltges, D. W., Reise, K., Mouritsen, K. N., McLaughlin, J. P. & Poulin, R. 2011 Food web including metazoan parasites for a tidal basin in Germany/Denmark. Ecology 92, 2005. (doi:10.1890/11-0351.1)
48. Zander, C. D., Josten, N., Detloff, K. C., Poulin, R., McLaughlin, J. P. & Thieltges, D. W. 2011 Food web including metazoan parasites for a brackish shallow water ecosystem in Germany and Denmark. Ecology 92, 2007. (doi:10.1890/11-0374.1)
49. Hechinger, R. F. et al. 2011 Food webs including parasites, biomass, body sizes, and life stages for three California/Baja California estuaries. Ecology 92, 791-792. (doi:10.1890/10-1383.1)
50. Byers, J. E. 1999 The distribution of an introduced mollusc and its role in the long-term demise of a native confamilial species. Biol. Invasions 1, 339-352. (doi:10.1023/A:1010038001768)
51. Torchin, M. E., Byers, J. E. & Huspeni, T. C. 2005 Differential parasitism of native and introduced snails: replacement of a parasite fauna. Biol. Invasions 7, 885-894. (doi:10.1007/s10530-004-2967-6)
52. Cardillo, M., Mace, G. M., Jones, K. E., Bielby, J., Bininda-Emonds, O. R. P., Sechrest, W., Orme, C. D. L. & Purvis, A. 2005 Multiple causes of high extinction risk in large mammal species. Science 309, 1239-1241. (doi:10.1126/science.1116030)
53. Lee, T. M. & Jetz, W. 2011 Range size is a common factor associated with risk of extinction in a range of organisms. Proc. R. Soc. B 278, 1329-1338. (doi:10.1098/rspb.2010.1877)
54. Lindenfors, P., Nunn, C. L., Jones, K. E., Cunningham, A. A., Sechrest, W. & Gittleman, J. L. 2007 Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density. Glob. Ecol. Biogeogr. 16, 496-509. (doi:10.1111/j.1466-8238.2006.00301.x)
55. Gregory, R. D., Keymer, A. E. & Harvey, P. H. 1996 Helminth parasite richness among vertebrates. Biodivers. Conserv. 5, 985-997. (doi:10.1007/BF00054416)
56. Poulin, R. 1995 Phylogeny, ecology and the richness of parasite communities in vertebrates. Ecol. Monogr. 65, 283-302. (doi:10.2307/2937061)
57. Smith, K. E., Sax, D. E. & Lafferty, K. D. 2006 Evidence for the role of infectious disease in species extinction and endangerment. Conserv. Biol. 20, 1349-1357. (doi:10.1111/j.1523-1739.2006.00524.x)
58. Amundsen, P. A., Lafferty, K. D., Knudsen, R., Primicerio, R., Kristoffersen, R., Klemetsen, A. & Kuris, A. M. In press. New parasites and predators follow the introduction of two fish species to a subarctic lake: implications for food-web structure and functioning. Oecologia.
59. Henson, K. S. E., Craze, P. G. & Memmott, J. 2009 The restoration of parasites, parasitoids, and pathogens to heathland communities. Ecology 90, 1840-1851. (doi:10.1890/07-2108.1)
60. Lafferty, K. D. 2004 Fishing for lobsters indirectly increases epidemics in sea urchins. Ecol. Appl. 14, 1566-1573. (doi:10.1890/03-5088)
61. Marcogliese, D. J. 2005 Parasites of the superorganism: are they indicators of ecosystem health? Int. J Parasitol. 35, 705-716. (doi:10.1016/j.ijpara.2005.01.015)
62. Heleno, R. H., Ceia, R. S., Ramos, J. A. & Memmott, J. 2009 Effects of alien plants on insect abundance and biomass: a food-web approach. Conserv. Biol. 23, 410-419. (doi:10.1111/j.1523-1739.2008.01129.x)
63. Marcogliese, D., Ball, M. & Lankester, M. W. 2001 Potential impacts of clearcutting on parasites of minnows in small boreal lakes. Folia Parasitol. 48, 269-274.
64. Marcogliese, D., Gendron, A., Plante, C., Fournier, M. & Cyr, D. 2006 Parasites of spottail shiners (Notropis hudsonius) in the St. Lawrence River: effects of municipal effluents and habitat. Can. J Zool. 84, 1461-1481. (doi:10.1139/z06-088)
65. Marcogliese, D. J. & Cone, D. K. 1996 On the distribution and abundance of eel parasites in Nova Scotia: influence of pH. Parasitol. 82, 389-399. (doi:10.2307/3284074)
66. Huspeni, T. C., Hechinger, R. F. & Lafferty, K. D. 2005 Trematode parasites as estuarine indicators: opportunities, applications and comparisons with conventional community approaches. In Estuarine indicators (ed. S. A. Bortone), pp. 297-314. Boca Raton, FL: CRC Press.
67. Lafferty, K. D., Hechinger, R. F., Lorda, J. & Soler, L. 2005 Trematodes associated with mangrove habitat in Puerto Rican salt marshes. J. Parasitol. 91, 697-699. (doi:10.1645/GE-427R)
68. Williams, R. J., Brose, U. & Martinez, N. D. 2007 Homage to Yodzis and Innes 1992: scaling up feeding-based population dynamics to complex ecological networks. In From energetics to ecosystems: the dynamics and structure of ecological systems (eds N. Rooney, K. S. McCann & D. L. G. Noakes), pp. 37-52. Berlin, Germany: Springer.
69. Clay, K., Reinhart, K., Rudgers, J., Tintjer, Tammy, Koslow, J. & Flory, S. L. 2008 Red queen communities. In Infectious disease ecology: effects of disease on ecosystems and of ecosystems on disease (eds R. Ostfeld, F. Keesing & V. Eviner), pp. 145-178. Millbrook, NY: Institute for Ecosystem Studies.
70. Tompkins, D. M., Greenman, J. V., Robertson, P. A. & Hudson, P. J. 2000 The role of shared parasites in the exclusion of wildlife hosts: Heterakis gallinarum in the ring-necked pheasant and the grey partridge. J Anim. Ecol. 69, 829-840. (doi:10.1046/j.1365-2656.2000.00439.x)
71. Lloyd-Smith, J. O., Cross, P. C., Briggs, C. J., Daugherty, M., Getz, W. M., Latto, J., Sanchez, M. S., Smith, A. B. & Swei, A. 2005 Should we expect population thresholds for wildlife disease?. Trends Ecol. Evol. 20, 511-519. (doi:10.1016/j.tree.2005.07.004)