Biodiversity and Conservation

, Volume 22, Issue 6–7, pp 1391–1404 | Cite as

Impact of forest size on parasite biodiversity: implications for conservation of hosts and parasites

  • Sarah E. Bush
  • Michelle Reed
  • Sean Maher
Original Paper


Studies of biodiversity traditionally focus on charismatic megafauna. By comparison, little is known about parasite biodiversity. Recent studies suggest that co-extinction of host specific parasites with their hosts should be common and that parasites may even go extinct before their hosts. The few studies examining the relationship between parasite diversity and habitat quality have focused on parasites that require intermediate hosts and pathogens that require vectors to complete their life-cycles. Declines in parasite and pathogen richness in these systems could be due to the decline of any of the definitive hosts, intermediate hosts, or vectors. Here we focus on avian ectoparasites, primarily lice, which are host specific parasites with simple, direct, life-cycles. By focusing on these parasites we gain a clearer understanding of how parasites are linked to their hosts and their hosts’ environment. We compare parasite richness on birds from fragmented forests in southern China. We show that parasite richness correlates with forest size, even among birds that are locally common. The absence of some ectoparasite genera in small forests suggests that parasites can go locally extinct even if their hosts persist. Our data suggest that the conservation of parasite biodiversity may require preservation of habitat fragments that are sufficiently large to maintain parasite populations, not just their host populations.


Avian ectoparasites Bird Lice Species richness Forest fragmentation Coextinction China 



We thank B. W. Benz, R. L. Boyd, R. Brown, G. Chen, T. J. Davis, K. P. Johnson, B. Lim, R. Moyle, A. T. Peterson, A. Nyari and M. B. Robbins for various forms of assistance. We thank B. Newmark and C. Sekercioglu and an anonymous reviewer for helpful comments on the manuscript. We especially thank D. H. Clayton for his assistance in the field, and thoughtful comments on the manuscript. This work was supported by NSF DEB-0344430, DEB-0743491, DEB 1050706, and DEB 1050038.


  1. Allan BF, Keesing F, Ostfeld RS (2003) Effects of habitat fragmentation on Lyme disease risk. Conserv Biol 17:267–272CrossRefGoogle Scholar
  2. Altizer S, Nunn CL, Lindenfors P (2007) Do threatened hosts have fewer parasites? A comparative study in primates. J Anim Ecol 76:301–314CrossRefGoogle Scholar
  3. Boyd RL, Nyari AS, Benz BW, Chen G (2008) Aves, province of Guizhou, China. Check List 4:107–114Google Scholar
  4. Chao A (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43:783–791PubMedCrossRefGoogle Scholar
  5. Clayton DH, Drown DM (2001) Critical evaluation of five methods for quantifying chewing lice (Insecta: Phthiraptera). J Parasitol 87:1291–1300PubMedGoogle Scholar
  6. Clayton DH, Tompkins DM (1994) Ectoparasite virulence is linked to mode of transmission. Proc Roy Soc Lond B 256:211–217CrossRefGoogle Scholar
  7. Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum, New JerseyGoogle Scholar
  8. Colwell RK (2006) EstimateS: Statistical estimation of species richness and shared species from samples. V.8.2.0.
  9. Colwell RK, Dunn RR, Harris NC (2012) Coextinction and extinction cascadees. Ann Rev Ecol Evol Syst 43:183–203CrossRefGoogle Scholar
  10. Connor EF, Courtney AC, Yoder JM (2000) Individuals-area relationships: the relationship between animal population density and area. Ecol 81:734–748Google Scholar
  11. Dunn RR (2009) Coextinction: anecdotes, models and speculation. In: Tuvey ST (ed) Holocene extinctions. Oxford University Press, Oxford, pp 167–180CrossRefGoogle Scholar
  12. Dunn RR, Harris NC, Colwell RK, Koh LP, Sodhi NS (2009) The sixth mass coextinction: are most endangered species parasites and mutualists? Proc Roy Soc Lond B 276:3037–3045CrossRefGoogle Scholar
  13. Durden LA, Keirans JE (1996) HostParasite coextinction and the plight of tick conservation. Am Entomol 42:87–91Google Scholar
  14. ESRI, Inc.: Environmental Systems Research Institute (2009) ArcGIS: Geographic information software, version 9.3. Redlands, CaliforniaGoogle Scholar
  15. Fair J, Paul E, Jones J (2010) Guidelines to the use of wild birds in research, 3rd edn. Ornithological Council, Washington, D.C.Google Scholar
  16. Harris NC, Dunn RR (2010) Using host associations to predict spatial patterns in the species richness of the parasites of North American carnivores. Ecol Lett 13:1411–1418PubMedCrossRefGoogle Scholar
  17. Hastriter MW, Bush SE (2010) Notes and new records of Fleas (Insecta: Siphonaptera) from small mammals and birds collected in Southern China. Proc Entomol Soc Wash 112:214–228CrossRefGoogle Scholar
  18. Hechinger RF, Lafferty KD (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proc Roy Soc Lond B 272:1059–1066CrossRefGoogle Scholar
  19. Hechinger RF, Lafferty KD, Huspeni TC, Brooks AJ, Kuris AM (2007) Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos fishes. Oecologia 151:82–92PubMedCrossRefGoogle Scholar
  20. Hechinger RF, Lafferty KD, Kuris AM (2008) Trematodes indicate animal biodiversity in the Chilean Intertidal and Lake Tanganyika. J Parasitol 94:966–968PubMedCrossRefGoogle Scholar
  21. Hijmans RJ, Cameron S, Parra J (2005) WorldClim—global climate data. Accessed 8 July 2009
  22. Hong Y, He F, Wirth R, Melville D, Pan-ji Z, Xia-zhi W, Gui-fu W, Zhi-yong L (2003) Little-known Oriental bird: Courtois’s Laughingthrush Garrulax galbanus courtoisi. Orient Bird Club Bull 38:35–40Google Scholar
  23. Hudson PJ, Dobson AP, Lafferty KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends Ecol Evol 21:381–385PubMedCrossRefGoogle Scholar
  24. IUCN: International Union for Conservation of Nature (2010) Garrulax courtoisi in IUCN (2010) IUCN red list of threatened species. Version 2010.3. Accessed 1 Oct 2012
  25. Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith VS (2004) Species coextinctions and the biodiversity crisis. Science 305:1632–1634PubMedCrossRefGoogle Scholar
  26. Kuris AM, Blaustein AR, Alio JJ (1980) Hosts as Islands. Am Nat 116:570–586CrossRefGoogle Scholar
  27. Lafferty KD, Holt RD (2003) How should environmental stress affect the population dynamics of disease? Ecol Lett 6:654–664CrossRefGoogle Scholar
  28. Lafferty KD, Kuris AM (1999) How environmental stress affects the impacts of parasites. Limnol Oceanogr 44:925–931CrossRefGoogle Scholar
  29. Lafferty KD, Shaw JC, Kuris AM (2008) Reef fishes have higher parasite richness at unfished Palmyra Atoll compared to fished Kiritimati Island. EcoHealth 5:338–345PubMedCrossRefGoogle Scholar
  30. Lampilla P, Mönkkönen M, Desrochers A (2005) Demographic responses by birds to forest fragmentation. Conserv Biol 19:1537–1546CrossRefGoogle Scholar
  31. Lyles AM, Dobson AP (1993) Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites. J Zoo Wildl Med 3:315–326Google Scholar
  32. MacKinnon J (1997) Protected areas systems review of the Indo-Malayan realm. Asian Bureau for Conservation, CanterburyGoogle Scholar
  33. Malenke JR, Newbold N, Clayton DH (2011) Condition-specific competition governs the geographic distribution and diversity of ectoparasites. Am Nat 177:522–534PubMedCrossRefGoogle Scholar
  34. McGarigal K, Cushman SA, Neel MC, Ene E (2002) FRAGSTATS: Spatial pattern analysis program for categorical maps. Accessed 6 Feb 2009
  35. Moir ML, Vesk PA, Brennan KEC, Keith DA, Hughes L, McCarthy MA (2010) Current constraints and future directions in estimating coextinction. Conserv Biol 24:682–690PubMedCrossRefGoogle Scholar
  36. Myers N, Mittermeier RA, Mittermeier CG, da Fonesca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858PubMedCrossRefGoogle Scholar
  37. Olsson U, Alström P, Ericson PGP, Sundberg P (2005) Non-monophyletic taxa and cryptic species—evidence from a molecular phylogeny of leaf-warblers (Phylloscopus, Aves). Mol Phylo Evol 36:261–276CrossRefGoogle Scholar
  38. Pérez TM (1995) Seven species of Fainalges Gaud and Berla (Analgoidea, Xolalgidae) from Aratinga holochlora (Sclater) (Aves, Psittacidae). Zoo Scripta 24:203–223CrossRefGoogle Scholar
  39. Pérez TM (1997) Eggs of feather mite congeners (Acarina: Pterolichidae, Xolalgidae) from different species of new world parrots (Aves, Psittaciformes). Int J Acarol 23:103–106CrossRefGoogle Scholar
  40. Peterson AT, Bush SE, Spackman E, Swayne DE, Ip H (2008) Influenza A virus infections in land birds, People’s Republic of China. Emerg Infect Dis 14:1644–1646PubMedCrossRefGoogle Scholar
  41. Pimm SL, Raven P (2000) Extinction by numbers. Nature 403:843–845PubMedCrossRefGoogle Scholar
  42. Poulin R, Morand S (2004) Parasite biodiversity. Smithsonian Institution Scholarly Press, Washington D.C.Google Scholar
  43. Price PW (1980) Evolutionary biology of parasites. Princeton University Press, PrincetonGoogle Scholar
  44. Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton DH (2003) The chewing lice: world checklist and biological overview. Illinois Natural History Survey Special Publication 24, 501 ppGoogle Scholar
  45. Price RD, Arnold DC, Bush SE (2006) Five new species of Myrsidea (Phthiraptera: Menoponidae) from Asian Babblers (Passeriformes: Timaliidae). J Kansas Entomol Soc 79:369–377CrossRefGoogle Scholar
  46. Ralph CJ, Sauer JR, Droege S (1995) Monitoring bird populations by point counts. U.S. Department of Agriculture, Forest Service, General Technical Report PSW-149Google Scholar
  47. Robbins MB, Peterson AT, Nyari AS, Chen G, Davis TJ (2006) Ornithological surveys of two reserves in Guangxi province, China, 2004–2005. Forktail 22:140–146Google Scholar
  48. Roberts MG et al (2001) Parasite community ecology and biodiversity. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) The ecology of wildlife diseases. Oxford University Press, Oxford, pp 63–82Google Scholar
  49. Rolstad J (1991) Consequences of forest fragmentation for the dynamics of bird populations: conceptual issues and the evidence. Biol J Linn Soc 42:149–163CrossRefGoogle Scholar
  50. Rosenstock SS, Anderson DR, Giesen KM, Leukering T, Carter MF (2002) Landbird counting techniques: current practices and an alternative. Auk 119:46–53Google Scholar
  51. Thomas JA et al (2004) Comparative losses of British butterflies, birds and plants and the global extinction crisis. Science 303:1879–1881PubMedCrossRefGoogle Scholar
  52. Underhill LG, Gibbons DW (2002) Mapping and monitoring bird populations: their conservation uses. In: Norrisand K, Pain DJ (eds) Conserving bird biodiversity: general principles and their application. Cambridge University Press, Cambridge, pp 34–60CrossRefGoogle Scholar
  53. Vogeli MJ, Lemus A, Serrano D, Blanco G, Tella JL (2011) An island paradigm on the mainland: host population fragmentation impairs the community of avian pathogens. Proc Roy Soc Lond B. doi: 10.1098/rspb.2010.1227 Google Scholar
  54. Walther BA, Morand S (1998) Comparative performance of species richness estimation methods. Parasitol 116:395–405CrossRefGoogle Scholar
  55. Whiteman NK, Parker PG (2005) Using parasites to infer host population history: a new rationale for parasite conservation. Anim Conserv 8:175–181CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of BiologyUniversity of UtahSalt Lake CityUSA
  2. 2.University of MichiganAnn ArborUSA
  3. 3.Biodiversity Institute and Department of Ecology and Evolutionary BiologyUniversity of KansasLawrenceUSA
  4. 4.Museum of Vertebrate ZoologyUniversity of CaliforniaBerkeleyUSA

Personalised recommendations