EcoHealth

, Volume 10, Issue 2, pp 145–158 | Cite as

Do Shade-Grown Coffee Plantations Pose a Disease Risk for Wild Birds?

  • Sonia M. Hernandez
  • Valerie E. Peters
  • P. Logan Weygandt
  • Carlos Jimenez
  • Pedro Villegas
  • Barry O’Connor
  • Michael J. Yabsley
  • Maricarmen Garcia
  • Sylva M. Riblet
  • C. Ron Carroll
Original Contribution

Abstract

Shade-grown coffee plantations are often promoted as a conservation strategy for wild birds. However, these agro-ecosystems are actively managed for food production, which may alter bird behaviors or interactions that could change bird health, compared to natural forest. To examine whether there is a difference between the health parameters of wild birds inhabiting shade-grown coffee plantations and natural forest, we evaluated birds in Costa Rica for (1) their general body condition, (2) antibodies to pathogens, (paramyxovirus and Mycoplasma spp.), and (3) the prevalence and diversity of endo-, ecto-, and hemoparasites. We measured exposure to Mycoplasma spp. and paramyxovirus because these are pathogens that could have been introduced with domestic poultry, one mechanism by which these landscapes could be detrimental to wild birds. We captured 1,561 birds representing 75 species. Although seasonal factors influenced body condition, we did not find bird general body condition to be different. A total of 556 birds of 31 species were tested for antibodies against paramyxovirus-1. Of these, five birds tested positive, four of which were from shade coffee. Out of 461 other tests for pathogens (for antibodies and nucleotide detection), none were positive. Pterolichus obtusus, the feather mite of chickens, was found on 15 birds representing two species and all were from shade-coffee plantations. Larvated eggs of Syngamus trachea, a nematode typically associated with chickens, were found in four birds captured in shade coffee and one captured in forest. For hemoparasites, a total of 1,121 blood smears from 68 bird species were examined, and only one species showed a higher prevalence of infection in shade coffee. Our results indicate that shade-coffee plantations do not pose a significant health risk to forest birds, but at least two groups of pathogens may deserve further attention: Haemoproteus spp. and the diversity and identity of endoparasites.

Keywords

disease pathogen wild bird Costa Rica shade coffee conservation 

References

  1. Alexander DJ, Senne DA (2008). Newcastle disease virus and other avian paramyxoviruses. In: A laboratory manual for the isolation, identification, and characterization of avian pathogens, Dufour-Zavala DESL, Glisson JR, Pearson, JE, Reed WM, Jackwood MW, Woolcock PR (editors). American Association of Avian Pathologists, Athens, pp 135-141.Google Scholar
  2. Atkinson CT (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon and Haemproteus. In: Bird-Parasite interactions: Ecology, evolution and behaviour, Loye, MZ (editor), New York: Oxford University Press, pp 19-43.Google Scholar
  3. Barton JT, Bickford AA, Cooper GL, Charlton BR, Cardona CJ (1992) Avian Paramyxovirus Type 1 Infections in Racing Pigeons in California I: Clinical Signs, Pathology, and Serology. Avian Diseases 36:463-468.PubMedCrossRefGoogle Scholar
  4. Bennett GF, Caines JR, Bishop MA (1988) Influence of blood parasites on the body mass of passeriform birds. Journal of Wildlife Diseases 24:339-343.PubMedGoogle Scholar
  5. Bibby CJ, Burgess ND, Hill DA, Mustoe SH (2000) Birds census techniques. Academic Press 2nd edn. London: Academic Press.Google Scholar
  6. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulson JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24:127-135.PubMedCrossRefGoogle Scholar
  7. Callison SA, Riblet SM, Sun S, Ikuta N, Hilt D, Leiting V, Kleven SH, Suarez DL, Garcia M (2006) Development and validation of a real-time Taqman (R) polymerase chain reaction assay for the detection of Mycoplasma gallisepticum in naturally infected birds. Avian Diseases 50:537-544.PubMedCrossRefGoogle Scholar
  8. Cohen EB, Lindell CA (2004) Survival, habitat use, and movements of fledgling White-throated Robins (Turdus assimilis) in a Costa Rican agricultural landscape. Auk 121:404-414.CrossRefGoogle Scholar
  9. D’Souza PE, Jagannath MS, Murthy KMS (2001) Feather mite infestation in a broiler breeder farm. Vet Rec. 149:777a.Google Scholar
  10. DeGroote LW, Rodewald PG (2010) Blood parasites in migrating wood-warblers (Parulidae): effects on refueling, energetic condition, and migration timing. Journal of Avian Biology 41:147-153.CrossRefGoogle Scholar
  11. Dimitrov DP, Zehtindjie, Bensch S (2010) Genetic diversity of avian blood parasites in SE Europe: Cytochrome b lineages of the genera Plasmodium and Haemoproteus (Haemosporida) from Bulgaria. Acta Parasitologica 55:201-209.CrossRefGoogle Scholar
  12. Dowling DK, Richardson DS, Blaakmeer K (2001) Feather mite loads influenced by salt exposure, age and reproductive stage in the Seychelles Warbler Acrocephalus sechellensis. Journal of Avian Biology 32:364-369.CrossRefGoogle Scholar
  13. Dubinin VB (1951) Feather mites (Analgesoidea). Part 1. Introduction to their study. Fauna USSR 6:1-363.Google Scholar
  14. Floch H, Fauran P (1956) Two species of the genus Trombicula (Acariens, Trombiculidae) new for the fauna of French Guiana: Trombicula alfreddugesi (Oudemans, 1910) and Trombicula sinnamaryi n. sp. Publication. Cayenne, French Guiana. Institut Pasteur de la Guyane française et de l’Inini. 17:1-7.Google Scholar
  15. Friend M, Franson JC (1999–2001) Field manual of wildlife diseases: general field procedures and diseases of birds. Biological Resources Division, Information and Technology Report.Google Scholar
  16. Gillespie TR, Chapman CA, Greiner EC (2005) Effects of logging on gastrointestinal parasite infections and infection risk in African primates. Journal of Applied Ecology 42:699-707.CrossRefGoogle Scholar
  17. Goodman BB, Hanson RP (1988) Isolation of avian paramyxovirus-2 from domestic and wild birds in Costa Rica. Avian Diseases 32:713-717.PubMedCrossRefGoogle Scholar
  18. Gosler A (2004) Birds in the hand. In: Bird Ecology and Conservation, Sutherland WJ, Newton I, Green RE (editors), New York: Oxford University Press, pp 85-119.CrossRefGoogle Scholar
  19. Groom MJ (2006) Threats to Biodiversity. In: Principles of Conservation Biology, Groom MJ, Meffe GK, Carroll CR (editors) Sinauer Associates Inc., Sunderland, pp 63-111.Google Scholar
  20. Hartup BK, Oberc A, Stott-Messick B, Davis AK, Swarthout ECH (2008) Blood parasites of House Finches (Carpodacus mexicanus) from Georgia and New York. Journal of Wildlife Diseases 44:469-474.PubMedGoogle Scholar
  21. Hansbauer MM, Storch I, Pimentel RG, Metzger JP (2008) Comparative range use by three Atlantic Forest understorey bird species in relation to forest fragmentation. Journal of Tropical Ecology 24:291-299.CrossRefGoogle Scholar
  22. Hernandez-Divers SM, Villegas P, Jimenez C, Hernandez-Divers SJ, Garcia MC, Riblet SM, Carroll CR, O’Connor BM, Webb JL, Yabsley MJ, Williams SM, Sanchez S (2008) Backyard chicken flocks pose a disease risk for neotropical birds in Costa Rica. Avian Diseases 52:558-566.PubMedCrossRefGoogle Scholar
  23. Hilton-Taylor, C (2000) 2000 IUCN red list of threatened species. International Union for the Conservation of Nature.Google Scholar
  24. Hofle U, Blanco JM, Kaleta EF (2002) Seroprevalence of avian paramyxovirus 1,2, and 3 in captive and free-living birds of prey in Spain. Annals of the NY Academy of Sciences 969:213-216.PubMedCrossRefGoogle Scholar
  25. Jha S, Bacon CM, Philpott SM, Rice RA, Ernesto Mendez V, Laderach P (2011) A review of ecosystem services, farmer livelihoods, and value chains in shade coffee agroecosystems. In: Integrating Agriculture, Conservation and Ecotourism: Examples From the Field, Campbell WB, Lopez Ortiz S (editors), Dordrecht: Springer, pp 141–208Google Scholar
  26. Komar O (2006) Ecology and conservation of birds in coffee plantations: a critical review. Bird Conservation International 16:1-23.CrossRefGoogle Scholar
  27. Leighton FA, Heckert RA (2007) Viral Diseases. In: Infectious Diseases of Wild Birds, Thomas J, Hunter DB, Atkinson CT (editors), Ames: Blackwell Publishing Professional, pp 1–16Google Scholar
  28. Lindell CT, Gavin TA, Price RD, Sanders AL (2002) Chewing louse distributions on two Neotropical thrush species. Comparative Parasitology 69:212–217.CrossRefGoogle Scholar
  29. Loye JE, Zuck M (1991) Bird-Parasite Interactions: Ecology, Evolution, and Behavior. New York: Oxford University Press.Google Scholar
  30. Luttrell MP, Fischer JR, Stallknecht DE, Kleven SH (1996) Field investigation of Mycoplasma gallisepticum infections in house finches (Carpodacus mexicanus) from Maryland and Georgia. Avian Diseases 40:335-341.PubMedCrossRefGoogle Scholar
  31. Luttrell MP, Stallknecht DE, Kleven SH, Kavanaugh DM, Corn JL, Fischer JR (2001) Mycoplasma gallisepticum in house finches (Carpodacus mexicanus) and other wild birds associated with poultry production facilities. Avian Diseases 45:321-329.PubMedCrossRefGoogle Scholar
  32. Luttrell MP, Fischer JR (2007) Mycoplasmosis. In: Infectious diseases of wild birds, Thomas J, Hunter DB, Atkinson CT (editors), Ames: Blackwell Publishing Professional, pp 317-331.CrossRefGoogle Scholar
  33. Martinez-de la Puente J, Gustavo-Tomas SM, Moreno J, Morales J, Lobato E, García-Fraile S, Belda EJ (2010) The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment. Biology Letters 6:663-665.CrossRefGoogle Scholar
  34. Moguel P, Toledo M (1999) Review: Biodiversity conservation in traditional coffee systems of Mexico. Conservation Biology 13:11-21.CrossRefGoogle Scholar
  35. Morishita TY, Aye PP, Ley EC, Harr BS (1999) Survey of pathogens and blood parasites in free-living passerines. Avian Diseases 43:549-552.PubMedCrossRefGoogle Scholar
  36. Norte AC, Araujo PM, Sampaio HL, Sousa JP, Ramos JA (2009) Haematozoa infections in a Great Tit Parus major population in Central Portugal: relationships with breeding effort and health. Ibis 151:677-688.CrossRefGoogle Scholar
  37. Nuttall GHF (1916) Notes on Ticks. IV. Relating to the genus Ixodes and including a description of three new species and two new varieties. Parasitology 8:294-337.CrossRefGoogle Scholar
  38. Perfecto I, Rice RA, Greenberg R, Van der Voort ME (1996) Shade coffee: A disappearing refuge for biodiversity. Bioscience 46:598-608.CrossRefGoogle Scholar
  39. Perfecto I, Armbrecht I, Philpott SM, Dietsch T, Soto-Pinto L (2007) Shaded coffee and the stability of rainforest margins in Latin America. In: The stability of tropical rainforest margins: linking ecological, economic, and social constraints of land use and conservation, Tscharntke LT, Zeller M, Guhudja E, Bidin A (editors), Heidelberg: Springer, Environmental Science Series pp 227–264.Google Scholar
  40. Perfecto I, Vandermeer J (2008) Biodiversity conservation in tropical agroecosystems: A new conservation paradigm. Ann. NY Acad. Sci. 1134:173-200.PubMedCrossRefGoogle Scholar
  41. Perfecto I, Vandermeer JH, Gustavo López Bautista GL, Nuñez GI, Greenberg R, Bichier P, Langridge S (2004) Greater predation in shaded coffee farms: The role of resident neotropical birds. Ecology 85:2677-2681.CrossRefGoogle Scholar
  42. Perozo F, Villegas P, Estevez C, Alvarado I, Purvis LB (2006) Use of FTA (R) filter paper for the molecular detection of Newcastle disease virus. Avian Pathology 35:93-95.PubMedCrossRefGoogle Scholar
  43. Peters VE, Greenberg R (2012) Fruit supplementation affects birds but not arthropod predation by birds in Costa Rican agroforestry systems. Biotropica DOI: 10.1111/j.1744-7429.2012.00891.x.Google Scholar
  44. Philpott SM, Armbrecht I (2006) Biodiversity in tropical agroforests and the ecological role of ants and ant diversity in predatory function. Ecological Entomology 31:369-377.CrossRefGoogle Scholar
  45. Philpott SM, Bichier P, Rice R, Greenberg R (2007) Field-Testing Ecological and Economic Benefits of Coffee Certification Programs. Conservation Biology 21:975-985.PubMedCrossRefGoogle Scholar
  46. Proctor HC (2003). Feather mites (Acari: Astigmata): Ecology, behavior, and evolution. Annual Review of Entomology 48:185-209.PubMedCrossRefGoogle Scholar
  47. Rappole JH, King DI, Vega Rivera JH (2003) Coffee and conservation. Conservation Biology 17:334-336.CrossRefGoogle Scholar
  48. Rice RA, Ward JR (1996) Coffee, conservation and commerce in the Western Hemisphere. Washington, Smithsonian National Zoological Park, pp 1–40.Google Scholar
  49. Romagnano A (1999) Examination and preventive medicine protocols in psittacines. Vet Clin North Am Exot Anim Pract 2:333-355.PubMedGoogle Scholar
  50. Roy P, Dhillon AS, Lauerman L, Shivaprasad HL (2003) Detection of pigeon circovirus by polymerase chain reaction. Avian Diseases 47:218-222.PubMedCrossRefGoogle Scholar
  51. Sanchez-Azofeifa GA, Pfaff A, Robalino JA, Boomhower JP (2007) Costa Rica’s payment for environmental services program: Intention, implementation, and impact. Conservation Biology 21:1165-1173.PubMedCrossRefGoogle Scholar
  52. Schnebel B, Dierschke V, Rautenschlein S, Ryll M (2005) No detection of avian influenza A viruses of the subtypes H5 and H7 and isolation of lentogenic avian paramyxovirus serotype 1 in passerine birds during stopover in the year 2001 on the island Helgoland (North Sea). Deutsche Tierarztliche Wochenschrift 112:456-460.PubMedGoogle Scholar
  53. Sekercioglu CH, Loarie SR, Brenes FO, Ehrlich PR, Daily GC (2007) Persistence of forest birds in the Costa Rican agricultural countryside. Conservation Biology 21:482-494.PubMedCrossRefGoogle Scholar
  54. Stanislawek WL, Meers J, Wilks C, Horner GW, Morgan C, Alexander DJ (2001). A survey for paramyxoviruses in caged birds, wild birds, and poultry in New Zealand. New Zealand Veterinary Journal 49:18-23.PubMedCrossRefGoogle Scholar
  55. Stiles GF, Skutch AF (1989) A guide to the birds of Costa Rica. Cornell University Press, Ithaca.Google Scholar
  56. Taylor M, Coop B, Wall R (2007) The Laboratory Diagnosis of Parasitism. In: Veterinary Parasitology, Taylor M, Coop B, Wall R (editors), Ames: Blackwell Publishing, pp 895-900.Google Scholar
  57. Wobeser GA (2007) Disease in Wild Animals: Investigation and Management. Springer, Heidelberg.CrossRefGoogle Scholar
  58. Yabsley MJ (2008). Capillarid Nematodes. In: Parasitic Diseases of Wild Birds, Atkinson CT, Thomas N, Hunter DB (editors), Ames: Wiley-Blackwell.Google Scholar
  59. Young BE, McDonald DB (2000) Birds. In: Monteverde: ecology and conservation of a tropical cloud forest, Nadkarni N, Wheelwright N (editors), New York: Oxford University Press, pp 179-222.Google Scholar

Copyright information

© International Association for Ecology and Health 2013

Authors and Affiliations

  • Sonia M. Hernandez
    • 1
    • 6
  • Valerie E. Peters
    • 1
    • 9
  • P. Logan Weygandt
    • 2
    • 10
  • Carlos Jimenez
    • 3
    • 8
  • Pedro Villegas
    • 4
  • Barry O’Connor
    • 5
    • 7
  • Michael J. Yabsley
    • 6
  • Maricarmen Garcia
    • 4
  • Sylva M. Riblet
    • 4
  • C. Ron Carroll
    • 1
  1. 1.Odum School of EcologyUniversity of GeorgiaAthensUSA
  2. 2.John Hopkins School of MedicineBaltimoreUSA
  3. 3.Escuela de Medicina VeterinariaUniversidad Nacional de Costa RicaHerediaCosta Rica
  4. 4.Department of Population Health, Poultry Diagnostic and Research Center, College of Veterinary MedicineUniversity of GeorgiaAthensUSA
  5. 5.Insect Division, Museum of ZoologyUniversity of MichiganAnn ArborUSA
  6. 6.Daniel B. Warnell School of Forestry and Natural Resources and the Southeastern Cooperative Wildlife Disease StudyUniversity of GeorgiaAthensUSA
  7. 7.Department of Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA
  8. 8.Programa de Investigacion en Enfermedades Tropicales, Escuela de Medicina VeterinariaUniversidad NacionalHerediaCosta Rica
  9. 9.Department of ZoologyMiami UniversityOxfordUSA
  10. 10.BaltimoreUSA

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