The sixth mass coextinction: Are most endangered species parasites and mutualists?

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1670, 2009, Pages 3037-3045

  Dunn, Robert R ^a   Harris, Nyeema C ^a   Colwell, Robert K ^b   Koh, Lian Pin ^c   Sodhi, Navjot S ^d,e  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

^c ETH ZURICH   (Switzerland)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e HARVARD UNIVERSITY   (United States)

Author keywords

Chains of extinction; Climate change; Coextinction; Emerging diseases; Mass extinction; Secondary extinctions

Indexed keywords

BIODIVERSITY; CLIMATE CHANGE; ENDANGERED SPECIES; MASS EXTINCTION; MUTUALISM; PARASITE; POPULATION DECLINE; TROPHIC LEVEL;

BIODIVERSITY; CLIMATE CHANGE; ENDANGERED SPECIES; MASS COEXTINCTION; NONHUMAN; PARASITE; PRIORITY JOURNAL; REVIEW; SPECIES DIVERSITY; SPECIES EXTINCTION; SYMBIONT;

EID: 68849094696     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.0413     Document Type: Review

References (71)

1. 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)
2. Bascompte, J. & Jordano, P. 2007 Plant-animal mutualistic networks: the architecture of biodiversity. Annu. Rev. Ecol. Evol. Syst. 38, 567-593. (doi:10.1146/annurev.ecolsys.38.091206.095818)
3. Bond, W. J. 1994 Do mutualisms matter: assessing the impact of pollinator and disperser disruption on plant extinction. Phil. Trans. R. Soc. Lond. B 344, 83-90. (doi:10.1098/rstb.1994.0055)
4. Breitbart, M., Hewson, I., Felts, B., Mahaffy, J. M., Nulton, J., Salamon, P. & Rohwer, F. 2003 Metagenomic analyses of an uncultured viral community from human feces. J. Bacteriol. 185, 6220-6223. (doi:10.1128/JB.185.20.6220-6223.2003)
5. Brook, B. W., Sodhi, N. S. & Ng, P. K. L. 2003 Catastrophic extinctions follow deforestation in Singapore. Nature 424, 420-423. (doi:10.1038/nature01795)
6. Brook, B. W., Sodhi, N. S. & Bradshaw, C. J. A. 2008 Synergies among extinction drivers under global change. Trends Ecol. Evol. 23, 453-460. (doi:10.1016/j.tree.2008.03.011)
7. Bush, M. B. 2002 Distributional change and conservation on the Andean flank: a palaeoecological perspective. Global Ecol. Biogeogr. 11, 463-473. (doi:10.1046/j.1466-822X.2002.00305.x)
8. Bush, M. B. & Hooghiemstra, H. 2005 Tropical biota responses to climate change. In Climate change and biodiversity (eds T. E. Lovejoy & L. Hannah), pp. 125-137. New Haven, CT: Yale University Press.
9. Cardillo, M., Mace, G. M., Gittleman, J. L., Jones, K. E., Bielby, J. & Purvis, A. 2008 The predictability of extinction: biological and external correlates of decline in mammals. Proc. R. Soc. B 275, 1441-1448. (doi:10.1098/rspb.2008.0179)
10. Chen, I. C., Shiu, H. J., Benedick, S., Holloway, J. D., Cheye, V. K., Barlow, H. S., Hill, J. K. & Thomas, C. D. 2009 Elevation increases in moth assemblages over 42 years on a tropical mountain. Proc. Natl Acad. Sci. USA 106, 1479-1483. (doi:10.1073/pnas.0809320106)
11. Clayton, D. H. & Price, R. D. 1999 Taxonomy of NewWorld Columbicola (Phthiraptera: Philopteridae) from the Columbiformes (Aves), with descriptions of five new species. Ann. Entomol. Soc. Am. 92, 675-685.
12. Colwell, R. K., Brehm, G., Cardelus, C. L., Gilman, A. C. & Longino, J. T. 2008 Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science 322, 258-261. (doi:10.1126/science.1162547)
13. Darwin, C. 1862 The various contrivances by which orchids are fertilized by orchids. London, UK: John Murray.
14. Davis, M. B. & Shaw, R. G. 2001 Range shifts and adaptive responses to Quaternary climate change. Science 292, 673-679. (doi:10.1126/science.292.5517.673)
15. de Castro, F. & Bolker, B. 2005 Mechanisms of diseaseinduced extinction. Ecol. Lett. 8, 117-126. (doi:10.1111/j.1461-0248.2004. 00693.x)
16. Diamond, J. M. 1989 Overview of recent extinctions. In conservation for the twenty-first century (eds D. Western & M.Pearl), pp. 37-41.Oxford,UK:Oxford University Press.
17. Diamond, J. M., Ashmole, N. P. & Purves, P. E. 1989 Present, past and future of human-caused extinctions [and discussion]. Proc. R. Soc. Lond. B 325, 469-477.
18. Dobson, A. & Foufopoulos, J. 2001 Emerging infectious pathogens of wildlife. Phil. Trans. R. Soc. Lond. B 356, 1001-1012.
19. Dunn, R. R. 2002 On parasites lost-and found: passenger pigeon lice rediscovered. Wild Earth 12, 28-31.
20. Dunn, R. R. 2005 Modern insect extinctions, the neglected majority. Conserv. Biol. 19, 1030-1036.
21. Dunn, R. R. In press Coextinction: anecdotes, models, and speculation. In Holocene extinctions (ed. S. Turvey). Oxford, UK: Oxford University Press.
22. Franco, A. M. A., Hill, J. K., Kitschke, C., Collingham, Y. C., Roy, D. B., Fox, R., Huntley, B. & Thomas, C. D. 2006 Impacts of climate warming and habitat loss on extinctions at species' low-latitude range boundaries. Global Change Biol. 12, 1545-1553. (doi:10.1111/j.1365-2486.2006. 01180.x)
23. Gage, K. L., Burkot, T. R., Eisen, R. J. & Hayes, E. B. 2008 Climate and vectorborne diseases. Am. J. Prevent. Med. 35, 436-450. (doi:10.1016/j.amepre.2008.08.030)
24. Gog, J., Woodroffe, R. & Swinton, J. 2002 Disease in endangered metapopulations: the importance of alternative hosts. Proc. R. Soc. Lond. B 269, 671-676. (doi:10.1098/rspb.2001.1667)
25. Harper, L. H. 1989 The persistence of ant-following birds in small Amazonian forest fragments. Acta Amazon. 19, 249-264.
26. IUCN 2008 An analysis of mammals on the 2008 IUCN Red List. Conservation International, Arizona State University, Texas A&M Unviersity, University of Rome, University of Virginia, Zoological Society of London.
27. Jaenike, J. 1990 Host specialization in phytophagous insects. Annu. Rev. Ecol. Syst. 243-273. (doi:10.1146/annurev.es.21.110190.001331)
28. Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman, J. L. & Daszak, P. 2008 Global trends in emerging infectious diseases. Nature 451, 990-994. (doi:10.1038/nature06536)
29. Joshi, A. & Thompson, J. N. 1995 Trade-offs and the evolution of host specialization. Evol. Ecol. 9, 82-92. (doi:10.1007/BF01237699)
30. 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)
31. Labandeira, C. C., Johnson, K. R. & Wilf, P. 2002 Impact of the terminal Cretaceous event on plant-insect associations. Proc. Natl Acad. Sci. USA 99, 2061-2066. (doi:10.1073/pnas.042492999)
32. Laurance, W. F. 2007 Have we overstated the tropical biodiversity crisis? Trends Ecol. Evol. 22, 65-70. (doi:10.1016/j.tree.2006.09.014)
33. Light, J. E. & Hafner,M. S. 2008 Codivergence in heteromyid rodents (Rodentia: Heteromyidae) and their sucking lice of the genus Fahrenholzia (Phthiraptera: Anoplura). Syst. Biol. 57, 449-465. (doi:10.1080/10635150802169610)
34. 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. Global Ecol. Biogeogr. 16, 496-509. (doi:10.1111/j.1466-8238.2006. 00301.x)
35. Marris, E. 2007 The Escalator Effect. Nature Reports Climate Change. (doi:10.1038/climate.2007.70)
36. Maynard Smith, J. 1977 The limitations of evolution theory. In The encyclopaedia of ignorance (eds R. Duncan & M.Weston-Smith), pp. 235-242. London,UK: Pergamon.
37. Millan, J., Ruiz-Fons, F., Marquez, F. J., Viota, M., Lopez-Bao, J. V. & Mateo, M. P. M. 2007 Ectoparasites of the endangered Iberian lynx Lynx pardinus and sympatric wild and domestic carnivores in Spain. Med. Vet. Entomol. 21, 248-254.
38. Moritz, C., Patton, J. L., Conroy, C. J., Parra, J. L., White, G. C. & Beissinger, S. R. 2008 Impact of a century of climate change on small-mammal communities in Yosemite National Park, USA. Science 322, 261-264. (doi:10.1126/science.1163428)
39. Mouillot, D., Krasnov, B. R., Shenbrot, G. I., Gaston, K. J. & Poulin, R. 2006 Conservatism of host specificity in parasites. Ecography 29, 596-602. (doi:10.1111/j.0906-7590.2006.04507.x)
40. Nunn, C. L., Altizer, S., Sechrest, W., Jones, K. E., Barton, R. A. & Gittleman, J. L. 2004 Parasites and the evolutionary diversification of primate clades. Am. Nat. 164, S90-S103.
41. Parmesan, C. 2006 Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637-669. (doi:10.1146/annurev.ecolsys.37.091305.110100)
42. Parmesan, C. & Yohe, G. 2003 A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37-42. (doi:10.1038/nature01286)
43. Pedersen, A. B., Altizer, S., Poss, M., Cunningham, A. A. & Nunn, C. L. 2005 Patterns of host specificity and transmission among parasites of wild primates. Int. J. Parasitol. 35, 647-657. (doi:10.1016/j.ijpara. 2005.01.005)
44. Petchey, O. L., Eklof, A., Borrvall, C. & Ebenman, B. 2008 Trophically unique species are vulnerable to cascading extinction. Am. Nat. 171, 568-579.
45. Peterson, A. T., Soberon, J. & Sanchez-Cordero, V. 1999 Conservatism of ecological niches in evolutionary time. Science 285, 1265-1267. (doi:10.1126/science.285.5431.1265)
46. Pimm, S. L. & Raven, P. 2000 Biodiversity: extinction by numbers. Nature 403, 843-845. (doi:10.1038/35002708)
47. Poulin, R. & Keeney, D. B. 2008 Host specificity under molecular and experimental scrutiny. Trends Parasitol. 24, 24-28. (doi:10.1016/j.pt.2007.10.002)
48. Poulin, R. & Morand, S. 2000 The diversity of parasites. Q. Rev. Biol. 75, 277-293.
49. Poulin, R., Krasnov, B. R., Shenbrot, G. I., Mouillot, D. & Khokhlova, I. S. 2006 Evolution of host specificity in fleas: is it directional and irreversible? Int. J. Parasitol. 36, 185-191. (doi:10.1016/j.ijpara.2005.09.017)
50. Price, R. D. & Clayton, D. H. 1996 Revision of the chewing louse genus Formicaphagus (Phthiraptera: Philopteridae) from Neotropical antbirds and gnateaters (Aves: Passeriformes). J. Kansas Entomol. Soc. 69, 346-356.
51. 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.CO;2)
52. Price, R. D., Arnold, D. C. & Bush, S. E. 2006 Five new species of Myrsidea (Phthiraptera: Menoponidae) from Asian babblers (Passeriformes: Timaliidae). J. Kansas Entomol. Soc. 79, 369-377. (doi:10.2317/0602.14.1)
53. Purvis, A., Agapow, P. M., Gittleman, J. L. & Mace, G. M. 2000 Non-random extinction and the loss of evolutionary history. Science 288, 328-330. (doi:10.1126/science.288.5464.328)
54. Rausher, M. D. 1984 Tradeoffs in performance on different hosts: evidence from within- and between-site variation in the beetle Deloya guttata. Evolution 38, 582-595. (doi:10.2307/2408708)
55. Raxworthy, C. J., Pearson, R. G., Rabibisoa, N., Rakotondrazafy, A. M., Ramanamanjato, J. B., Raselimanana, A. P., Wu, S., Nussbaum, R. A. & Stone, D. A. 2008 Extinction vulnerability of tropical montane endemism from warming and upslope displacement: a preliminary appraisal for the highest massif in Madagascar. Global Change Biol. 14, 1703-1720. (doi:10.1111/j.1365-2486.2008.01596.x)
56. Rezende, E. L., Lavabre, J. E., Guimaraes, P. R. J., Jordano, P. & Bascompte, J. 2007 Random coextinctions in phylogenetically structured mutualistic networks. Nature 448, 925-928. (doi:10.1038/ nature05956)
57. Schipper, J. et al. 2008 The status of the world's land and marine mammals: diversity, threat, and knowledge. Science 322, 225-230. (doi:10.1126/science.1165115)
58. Sekercioglu, C. H., Ehrlich, P. R., Daily, G. C., Aygen, D., Goehring, D. & Sandi, R. F. 2002 Disappearance of insectivorous birds from tropical forest fragments. Proc. Natl Acad. Sci. USA 99, 263-267. (doi:10.1073/pnas.012616199)
59. Shaw, M. R. 1994 Parasitoid host ranges. In Parasitoid community ecology (eds B. A. Hawkins & W. Sheehan), pp. 111-114. Oxford, UK: Oxford University Press.
60. Smith, T. B. & Bernatchez, L. 2008 Evolutionary change in human-altered environments. Mol. Ecol. 17, 1-8. (doi:10.1111/j.1365-294X.2007.03607.x)
61. Stireman, J. O. 2005 The evolution of generalization? Parasitoid flies and the perils of inferring host range evolution from phylogenies. J. Evol. Biol. 18, 325-336. (doi:10.1111/j.1420-9101.2004.00850.x)
62. Stork, N. & Lyal, C. H. C. 1993 Extinction or 'co-extinction' rates?. Nature 366, 307.
63. Thacker, J. I., Hopkins, G. W. & Dixon, A. F. G. 2006 Aphids and scale insects on threatened trees: coextinction is a minor threat. Oryx 40, 233-236. (doi:10.1017/S0030605306000123)
64. Tompkins, D. M. & Clayton, D. H. 1999 Host resources govern the specificity of swiftlet lice: size matters. J. Anim. Ecol. 68, 489-500. (doi:10.1046/j.1365-2656.1999.00297.x)
65. Walther, G. R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T. J. C., Fromentin, J. M., Hoegh-Guldberg, O. & Bairlein, F. 2002 Ecological responses to recent climate change. Nature 416, 389-395. (doi:10.1038/416389a)
66. Whiteman, N. K. & Parker, P. G. 2005 Using parasites to infer host population history: a new rationale for parasite conservation. Anim. Conserv. 8, 175-181. (doi:10.1017/S1367943005001915)
67. Wilson, R. J., Gutierrez, D., Gutierrez, J., Martinez, D., Agudo, R. & Monserrat, V. J. 2005 Changes to the elevational limits and extent of species ranges associated with climate change. Ecol. Lett. 8, 1138-1146.
68. Wilson, R. J., Gutierrez, D., Gutierrez, J. & Monserrat, V. J. 2007 An elevational shift in butterfly species richness and composition accompanying recent climate change. Global Change Biol. 13, 1873-1887. (doi:10.1111/j.1365-2486.2007.01418.x)
69. Woolhouse, M. E. J. & Gowtage-Sequeria, S. 2005 Host range and emerging and re-emerging pathogens. Emerg. Infect. Dis. 11, 1842-1847.
70. Woolhouse, M. E. J., Haydon, D. T. & Antia, R. 2005 Emerging pathogens: the epidemiology and evolution of species jumps. Trends Ecol. Evol. 20, 238-244. (doi:10.1016/j.tree.2005.02.009)
71. Zaffarano, P. L., McDonald, B. A. & Linde, C. C. 2008 Rapid speciation following recent host shifts in the plant pathogenic fungus Rhynchosporium. Evolution 62, 1418-1436. (doi:10.1111/j.1558-5646. 2008.00390.x)