EcoHealth

, Volume 8, Issue 3, pp 320–331 | Cite as

Effect of Forest Fragmentation on Tick Infestations of Birds and Tick Infection Rates by Rickettsia in the Atlantic Forest of Brazil

  • Maria Ogrzewalska
  • Alexandre Uezu
  • Clinton N. Jenkins
  • Marcelo B. Labruna
Original Contribution
First Online:
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Revised:
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Abstract

Habitat loss and modifications affect biodiversity, potentially contributing to outbreaks of infectious diseases. We evaluated if the patch sizeinfragmented areas of Atlantic Forest in southeastern Brazil influences the diversity of forest birds and consequently the prevalence of ticks on birds and the rickettsial infection of these ticks. During 2 years, we collected ticks from birds in 12 sites: four small forest patches (80–140 ha), four large ones (480–1,850 ha), and four forest control areas within the much larger Morro do Diabo State Park (~36,000 ha). A total of 1,725 birds were captured (81 species, 24 families), from which 223 birds were infested by 2,339 ticks of the genus Amblyomma, mostly by the species A. nodosum. Bird diversity and richness were higher in larger than smaller forest fragments. The prevalence of ticks on birds was inversely correlated with bird diversity and richness. Among 174 A. nodosum tested for rickettsial infection by polymerase chain reaction, 51 were found to be infected by Rickettsia bellii or Rickettsia parkeri. However, tick infection rates by Rickettsia spp. were not statistically different between forest patch sizes. The higher prevalence of ticks on birds in degraded patches might be caused by a dominance of a few generalist bird species in small patches, allowing an easier transmission of parasites among individuals. It could also be related to more favorable microclimatic conditions for the free-living stages of A. nodosum in smaller forest fragments.The higher burden of ticks on birds in smaller forest fragments is an important secondary effect of habitat fragmentation, possibly increasing the likelihood of Rickettsia contagion.

Keywords

ticks birds rickettsia Atlantic Forest fragmentation biodiversity 
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Notes

Acknowledgments

We thank the staff of Institute for Ecological Research (IPE), especially Cicero José da Silva Filho for valuable help during the field work, and Sheila Oliveira de Souza for technical support in DNA sequencing. This work was supported by FAPESP (grant to MBL and scholarship to MO and AU) and CNPq (Academic Career Scholarship to MBL).

References

  1. Allan BF, Keesing F, Ostfeld, RS (2003).Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17: 267-272CrossRefGoogle Scholar
  2. Allan BF, Langerhans RB, Ryberg WA, Landesman WJ, Griffin NW, Katz RS, Oberle BJ, Schutzenhofer MR, Smyth KN, Maurice A, Clark L, Crooks KR, Hernandez DE, McLean RG, Ostfeld RS, Chase JM (2009) Ecological correlates of risk and incidence of West Nile virus in the United States. Oecologia 158:699–708PubMedCrossRefGoogle Scholar
  3. Anderson JF, Johnson RC, Magnarelli LA, Hyde FW (1986) Involvement of birds in the epidemiology of the Lyme disease agent Borreliaburgdofreri. Infection and Immunity 2: 394-396Google Scholar
  4. Andrén H (1994). Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos 71: 355-366CrossRefGoogle Scholar
  5. Aragão HB (1936) Ixodidas brasileiros e de alguns paizes limitrophes. Memorias do Instituto Oswaldo Cruz 31: 759-843CrossRefGoogle Scholar
  6. Bradley CA, Gibbs SE, Altizer S (2008) Urban land use predicts West Nile virus exposure in songbirds. Ecological Applications 18: 1083–1092PubMedCrossRefGoogle Scholar
  7. Clay CA, Lehmer EM, Jeor SS, Dearing MD (2009) Testing mechanisms of the dilution effect: deer mice encounter rates, Sin Nombre virus prevalence and species diversity. EcoHealth 6: 250–259PubMedCrossRefGoogle Scholar
  8. Conti-Díaz IA,Moraes-Filho J, Richard C. Pacheco RC, Labruna MB (2009) Serological evidence ofRickettsiaparkerias the etiological agent of rickettsiosis in Uruguay.Revista do Instituto de MedicinaTropical de São Paulo 51: 337-339CrossRefGoogle Scholar
  9. Daszak P, Cunningham AA (2003) Anthropogenic change, biodiversity loss, and a new agenda for emerging diseases. Journal of Parasitology 37-41: 2003Google Scholar
  10. Daszak P, Cunningham AA, Hayatt AD (2000) Emerging infectious diseases of wildlife.Threats to biodiversity and human health. Science 287: 443-449PubMedCrossRefGoogle Scholar
  11. Deblinger RD, Wilson ML, Rimmer DW, Spielman A (1993) Reduced abundance of immature Ixodesdammini (Acari: Ixodidae) following incremental removal of deer. Journal of Medical Entomology 30: 144-150PubMedGoogle Scholar
  12. Dias E, Martins AV (1939) Spotted fever in Brazil. A summary. Journal of Tropical Medicine and Hygiene 19:103-108Google Scholar
  13. Ditt EH (2002) Fragmentos florestais no Pontal do Paranapanema. 1. ed. São Paulo: AnnablumeGoogle Scholar
  14. Dobson A, Foufopoulus J (2001) Emerging infectious pathogens of wildlife. Philosophical Transaction of The Royal Society of London 356: 1001-1012CrossRefGoogle Scholar
  15. Elfving K, Olsen B, Bergstrom S, Waldenstrom J, Lundkvist A, Sjostedt A, Mejlon H, Nilsson K (2010) Dissemination of Spotted Fever Rickettsia agents in Europe by migrating birds. Plos One 5: e8572PubMedCrossRefGoogle Scholar
  16. Estrada-Pena A, Gugliemone AA, Mangold AJ (2004) The distribution and ecological ‘preferences’ of tick Amblyomma cajennense (Acari: Ixodidae), an ectoparasite of humans and other mammals in the Americas. Annals of Tropical Medicine and Parasitology 98: 283-292PubMedCrossRefGoogle Scholar
  17. Ezenwa VO, Godsey MS, King RJ, Gupthill SC (2006) Avian diversity and West Nile virus: Testing associations between biodiversity andinfectious disease risk. Proceedings of the Royal Society B: Biological Sciences 273: 109–117PubMedCrossRefGoogle Scholar
  18. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annual Review of Ecology and Systematics 34: 487–515CrossRefGoogle Scholar
  19. Ferraz G, Nichols, JD, Hines JE, Stouffer PC, BierregaardJr RO, Lovejoy TE (2007) A Large-Scale Deforestation Experiment: Effects of Patch Area and Isolation on Amazon Birds. Science 315:238-241PubMedCrossRefGoogle Scholar
  20. Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Global Ecology and Biogeography16: 265– 280CrossRefGoogle Scholar
  21. Hildebrandt A, Franke J, Meier F, Sachse S, Dorn W, Straube E (2010) The potential role of migratory birds in transmission cycles of Babesia spp., Anaplasmaphagocytophilum, and Rickettsia spp. Ticks and Tick-borne Diseases 1: 105–107PubMedCrossRefGoogle Scholar
  22. Hoogstraal H (1961) Migrating birds and their ectoparasites in realtion to disease. The East African Journal 38: 221-226Google Scholar
  23. Hubalek Z (2004)An annotated checklist of pathogenic microorganisms associated with migratory birds. Journal of Wildlife Diseases 40: 639–659PubMedGoogle Scholar
  24. Johnson P, Lund TJP, Hartson RB, Yoshino T (2009) Community diversity reduces Schistosomamansoni transmission and human infectionrisk. Proceedings of the Royal Society B: Biological Sciences276: 1657–1663PubMedCrossRefGoogle Scholar
  25. Jones KE, Nikkita G., Patel NG, Marc A., Levy MA, Adam Storeygard A, Deborah BalkD, Gittleman JL, Peter Daszak P (2008) Global trends in emerging infectious diseases. Nature 451: 990-993PubMedCrossRefGoogle Scholar
  26. Jongejan G, Uilenberg G (2004) The global importance of ticks.Parasitology 129: 3–14CrossRefGoogle Scholar
  27. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468: 647–652PubMedCrossRefGoogle Scholar
  28. Labruna MB (2009) Ecology of Rickettsia in South America. Annals of New York Academy of Science 1166: 156–66CrossRefGoogle Scholar
  29. Labruna MB, Guglielmone AA (2009) Ticks of New World tapirs. Tapir Conservation, 18: 21–28Google Scholar
  30. Labruna MB, Camargo LMA, Terrassini FA, Ferreira F, Schumaker TTS, Camargo EP (2005) Ticks (Acari: Ixodidae) from the state of Rondônia, western Amazon, Brazil. Systematic & Applied Acarology10: 17–32Google Scholar
  31. Labruna MB, Sanfilippo LF, Demetrio C, Menezes AC, Pinter A, Guglielmone AA, Silveira LF (2007) Ticks collected on birds in the state of São Paulo. Experimental and Applied Acarology 43: 147-160CrossRefGoogle Scholar
  32. Leite FJ (1998) A ocupação do Pontal do Paranapanema. Sao Paulo: Hucitec, Fundação UNESPGoogle Scholar
  33. Lima F (2009) Estimativas de abundância e densidade populacional da jaguatirica através de modelos de marcação-recaptura: Estudo de caso nos remanescentes florestais do Pontal do Paranapanema. Dissertação (Mestrado em Zoologia dos Vertebrados), Pontifícia Universidade Católica de Minas Gerais: Belo HorizonteGoogle Scholar
  34. Mittermeier RA, Myers N, Gil PR, Mittermeier CG (1999) Hotspots: earth’s biologically richest and most endangered terrestrial ecoregions. CEMEX: Mexico CityGoogle Scholar
  35. Murcia C (1995) Edge effects in fragmented forests: implications for conservation. Trends in Ecology and Evolution 2: 58-62CrossRefGoogle Scholar
  36. Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403: 853-858PubMedCrossRefGoogle Scholar
  37. Nava AFD (2009) Espécies sentinelas para a Mata Atlântica: as conseqüências epidemiológicas da fragmentação florestal no Pontal do Paranapanema. PhD Thesis, Universidade de São Paulo: São PauloGoogle Scholar
  38. Noss RF, Csuti B, Groom MJ (2005) Habitat fragmentation. In: Principles of Conservation Biology, 3rd ed, Groom MJ, Meffe GK, Carroll CR (editors), Massachusetts: SinauerGoogle Scholar
  39. Ogrzewalska M, Pacheco RC, Uezu A, Richtzenhain LJ, Ferreira F, Labruna MB (2009a) Ticks (Acari: Ixodidae) Infesting Birds in an Atlantic Rain Forest Region of Brazil. Journal of Medical Entomology46: 1225-1229PubMedCrossRefGoogle Scholar
  40. Ogrzewalska M, Pacheco, RC, Uezu A, Richtzenhain LJ, Ferreira F, Labruna MB (2009b) Rickettsial infection in Amblyomma nodosum ticks (Acari: Ixodidae) from Brazil. Annals of Tropical Medicine and Parasitology 103: 413–425PubMedCrossRefGoogle Scholar
  41. Oliveira-Filho AT, Fontes MAL (2000) Patterns of floristic differentiation among Atlantic Forests in southeastern Brazil and influence of climate. Biotropica 32: 793-810Google Scholar
  42. Oliver Jr H (1989) Biology and systematics of ticks (Acari: Ixodida). Annual Review of Ecology and Systematics 20: 397-430CrossRefGoogle Scholar
  43. Ostfeld RS, Keesing F (2000) Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14: 722-728CrossRefGoogle Scholar
  44. Ostfeld RS, Logiudice K (2003) Community disassembly, biodiversity loss, and the erosion of an ecosystem service. Ecology 84: 1421–1427CrossRefGoogle Scholar
  45. Paddock CD, Summer JW, Comer JA, Zaki SR, Goldsmith CS, Goddard J, McLellan SLF, Tamminga CL, Ohl CA (2004) Rickettsia parkeri: Anewly recognized cause of spotted fever rickettsiosis in the United States. Clinical Infectious Diseases 38: 805-811PubMedCrossRefGoogle Scholar
  46. Pardini R, Bueno AA, Gardner TA, Prado PI, Metzger JP (2010) Beyond the Fragmentation Threshold Hypothesis: Regime Shifts in Biodiversity Across Fragmented Landscapes Plos One 5: e13666PubMedCrossRefGoogle Scholar
  47. Parola P, Paddock CD, Raoult D (2005) Tick-borne rickettsioses around the world: emerging diseases challenging old concepts. Clinical Microbiology Reviews 18: 719-756PubMedCrossRefGoogle Scholar
  48. Perlman SJ, Hunter MS, Zchori-Fein E (2006)The emerging diversity of Rickettsia. Proceedings of the Royal Society B: Biological Sciences 273:2097-2106PubMedCrossRefGoogle Scholar
  49. Randolph SE (2004) Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129: 37– 65CrossRefGoogle Scholar
  50. Raoult D, Roux V (1997) Rickettsioses as paradigms of new or emerging infectious diseases. Clinical Microbiology Reviews 10: 694-719PubMedGoogle Scholar
  51. Redford KH, Eisenberg JF (1989) Mammals of the Neotropics.The Central Neotropics. Ecuador, Peru, Bolivia, Brazil. London: The University of Chicago Press: Chicago and LondonGoogle Scholar
  52. Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 142: 1141–1153CrossRefGoogle Scholar
  53. Ribon R, Simon JE, Mattos GT (2003) Bird extinctions in Atlantic Forest fragments of Viçosa Region, Southeastern Brazil. Conservation Biology 17: 1827-1839CrossRefGoogle Scholar
  54. Rizzoli A, Hauffe HC, Tagliapietra V, Neteler M, Rosa R (2009) Forest structure and Roe deer abundance predict tick- borne encephalitis risk in Italy. PLoS ONE 4: e4336PubMedCrossRefGoogle Scholar
  55. Spolidorio MG, Labruna M, Mantovani E, Brandao P, RichtzenhainL, Yoshinari N. (2010) Novel spotted fever group rickettsiosis, Brazil.Emerging Infectious Diseases 16:521–523PubMedCrossRefGoogle Scholar
  56. Sutherst RW (2004) Global Change and human vulnerability to vector-borne diseases. Clinical Microbiology Review 17: 136–173CrossRefGoogle Scholar
  57. Suzán G, Marcé E, Giermakowski JT, Mills JN, Ceballos G, Ostfeld RS, Armién B, Juan M, Pascale JM, Yates TL (2009) Experimental evidence for reduced rodent diversity causing increased hantavirus prevalence. PLoS ONE 4(5):e5461. doi: 10.1371/journal.pone.0005461 Google Scholar
  58. Swaddle J, Calos P (2008) Increased avian diversity is associated with lower incidence of human West Nile infection: observation of the dilution effect. PLoS ONE 3: e2488PubMedCrossRefGoogle Scholar
  59. Szabo MPJ, Labruna MB, Garcia MV, Pinter A, Castagnolli KC, Pacheco RC, Castro MB, Veronez VA, Magalha GM, Vogliotti ESA, Duarte JMB (2009) Ecological aspects of the free-living ticks (Acari: Ixodidae) on animal trails within Atlantic rainforest in south-eastern Brazil. Annals of Tropical Medicine and Parasitology 103: 57–72PubMedCrossRefGoogle Scholar
  60. Tischendorf L, Fahrig L (2000) On the usage and measurement of landscape connectivity. Oikos 90: 7–19CrossRefGoogle Scholar
  61. Uezu A, Metzger JPW (2011) Vanishing bird species in the Atlantic Forest: relative importance of landscape configuration, forest structure and species characteristics. Biodiversity and Conservation. doi: 10.1007/s10531-011-0154-5
  62. Uezu A, Metzger JPW, Vielliard JM (2005) The effect of structural and functional connectivity and patch size on the abundance of seven Atlantic Forest bird species. Biological 123: 507-519Google Scholar
  63. Veloso HP, Rangel-Filho AL, Lima LCA (1991) Classificação da vegetação brasileira, adaptada a um sistema universal. Rio de Janeiro: Fundação Instituto Brasileiro de Geografia e EstatísticaGoogle Scholar
  64. Willis EO (1979) The composition of avian communities in the remanescent woodlots in southern Brazil. PapéisAvulsos de Zoologia 33: 1-25Google Scholar
  65. Yasuoka J, Levins R (2007) Impact of deforestation and agricultural development on anopheline ecology and malaria epidemiology. American Journal of TropicalMedicine and Hygiene 76: 450–460PubMedGoogle Scholar

Copyright information

© International Association for Ecology and Health 2011

Authors and Affiliations

  • Maria Ogrzewalska
    • 1
    • 4
  • Alexandre Uezu
    • 2
  • Clinton N. Jenkins
    • 3
  • Marcelo B. Labruna
    • 1
  1. 1.Faculty of Veterinary MedicineUniversity of São PauloSão PauloBrazil
  2. 2.Instituto de Pesquisas Ecológicas (IPÊ)PaulistaBrazil
  3. 3.Department of BiologyNorth Carolina State UniversityRaleighUSA
  4. 4.Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e ZootecniaUniversidade de São PauloSão PauloBrazil

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