Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-24T16:45:09.366Z Has data issue: false hasContentIssue false
  • English
  • Français

The prevalence of avian Plasmodium is higher in undisturbed tropical forests of Cameroon

Published online by Cambridge University Press:  01 July 2009

Camille Bonneaud ,
Irem Sepil ,
Borja Milá ,
Wolfgang Buermann ,
John Pollinger ,
Ravinder N.M. Sehgal ,
Gediminas Valkiūnas ,
Tatjana A. Iezhova ,
Sassan Saatchi  and
Thomas B. Smith
Camille Bonneaud*
Affiliation:
Center for Tropical Research, Institute of the Environment, University of California at Los Angeles, Los Angeles, CA 90095, USA
Irem Sepil
Affiliation:
Center for Tropical Research, Institute of the Environment, University of California at Los Angeles, Los Angeles, CA 90095, USA
Borja Milá
Affiliation:
Department of Ecology and Evolutionary Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA
Wolfgang Buermann
Affiliation:
Center for Tropical Research, Institute of the Environment, University of California at Los Angeles, Los Angeles, CA 90095, USA
John Pollinger
Affiliation:
Center for Tropical Research, Institute of the Environment, University of California at Los Angeles, Los Angeles, CA 90095, USA
Ravinder N.M. Sehgal
Affiliation:
Center for Tropical Research, Institute of the Environment, University of California at Los Angeles, Los Angeles, CA 90095, USA Department of Biology, San Francisco State University, San Francisco CA USA
Gediminas Valkiūnas
Affiliation:
Institute of Ecology, Vilnius University, Akademijos 2, LT-08412 Vilnius, Lithuania
Tatjana A. Iezhova
Affiliation:
Institute of Ecology, Vilnius University, Akademijos 2, LT-08412 Vilnius, Lithuania
Sassan Saatchi
Affiliation:
Center for Tropical Research, Institute of the Environment, University of California at Los Angeles, Los Angeles, CA 90095, USA Jet Propulsion Laboratory, California Institute of Technology, Pasadena, CA 94132 USA
Thomas B. Smith
Affiliation:
Center for Tropical Research, Institute of the Environment, University of California at Los Angeles, Los Angeles, CA 90095, USA Department of Ecology and Evolutionary Biology, University of California at Los Angeles, Los Angeles, CA 90095, USA
*
1Corresponding author. Current address: Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, USA. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract:

Habitat fragmentation and deforestation are thought to disrupt host–parasite interactions and increase the risk of epizootic outbreaks in wild vertebrates. A total of 220 individuals from three species of African rain-forest bird (Andropadus latirostris, Andropadus virens, Cyanomitra obscura), captured in two pristine and two agroforests in Cameroon, were screened for the presence of avian haemosporidian parasites (species of Plasmodium and Haemoproteus) to test whether habitat differences were associated with differences in the prevalence of infectious diseases in natural populations. Thirteen mitochondrial lineages, including 11 Plasmodium and two Haemoproteus lineages were identified. Whereas levels of Haemoproteus spp. infections were too low to permit analysis, the prevalence of infections with Plasmodium spp. reached significantly greater levels in undisturbed mature forests. Importantly however, the significant association between forest type and parasite prevalence was independent of host density effects, suggesting that the association did not reflect changes in host species composition and abundance between forest types. Our results illustrate how characterizing land-cover differences, and hence changes, may be a prerequisite to understanding and predicting patterns of parasite infections in natural populations of rain-forest birds.

Keywords

agroforestAndropadus latirostrisAndropadus virensCyanomitra obscuraHaemoproteushost–parasite interactionPlasmodiumprimary forestrain-forest birds
Type
Research Article
Information
Journal of Tropical Ecology , Volume 25 , Issue 4 , July 2009 , pp. 439 - 447
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ALLAN, B. F., KEESING, F. & OSTFELD, R. S. 2003. Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17:267–272.CrossRefGoogle Scholar
ATKINSON, C. T. & VAN RIPER, C. 1991. Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. Pp. 19–48 in Loye, E. & Zuk, M. (eds.). Bird–parasite interactions: ecology, evolution, and behavior. Oxford University Press, New York.CrossRefGoogle Scholar
BEADELL, J. S., COVAS, R., GEBHARD, C., ISHTIAQ, F., MELO, M., SCHMIDT, B. K., PERKINS, S. L., GRAVES, G. R. & FLEISCHER, R. C. 2009. Host associations and evolutionary relationships of avian blood parasites from West Africa. International Journal for Parasitology 39:257–266.CrossRefGoogle ScholarPubMed
BEQUAERT, J. C. 1954. The Hippoboscidae or louse-flies (Diptera) of mammals and birds. Part II. Taxonomy, evolution and revision of American genera and species. Entomologica Americana 34:1–232.Google Scholar
BORROW, N. & DEMEY, R. 2005. Birds of Western Africa. Princeton Field Guides, New Jersey. 512 pp.Google Scholar
DESJEUX, P. 2001. The increase in risk factors for leishmaniasis worldwide. Transactions of the Royal Society of Tropical Medicine and Hygiene 95:239–243.CrossRefGoogle ScholarPubMed
FRY, C. H., KEITH, S. & URBAN, E. K. 1988. The birds of Africa. Academic Press, New York. 611 pp.Google Scholar
GAGER, A. B., LOAIZA, J. D. R., DEARBORN, D. C. & BERMINGHAM, E. 2008. Do mosquitoes filter the access of Plasmodium cytochrome b lineages to an avian host? Molecular Ecology 17:2552–2561.CrossRefGoogle Scholar
GILLESPIE, T. R. & CHAPMAN, C. A. 2006. Prediction of parasite infection dynamics in primate metapopulations based on attributes of forest fragmentation. Conservation Biology 20:441–448.CrossRefGoogle ScholarPubMed
GILLESPIE, T. R., CHAPMAN, C. A. & GREINER, E. C. 2005. Effects of logging on gastrointestinal parasite infections and infection risk in African primates. Journal of Applied Ecology 42:699–707.CrossRefGoogle Scholar
GUERRA, C. A., SNOW, R. W. & HAY, S. I. 2006. A global assessment of closed forests, deforestation and malaria risk. Annals of Tropical Medicine and Parasitology 100:189–204.CrossRefGoogle ScholarPubMed
HANSEN, M. C., DEFRIES, R. S., TOWNSHEND, J. R. G., SOHLBERG, R. A., DIMICELI, C. & CARROLL, M. 2002. Towards an operational MODIS continuous field of percent tree cover algorithm: examples using AVHRR and MODIS data. Remote Sensing of the Environment 83:303–319.CrossRefGoogle Scholar
HELLGREN, O., WALDENSTROM, J., PEREZ-TRIS, J., SZOLLOSI, E., HASSELQUIST, D., KRIŽANAUSKIENĖ, A., OTTOSSON, U. & BENSCH, S. 2007. Detecting shifts of transmission areas in avian blood parasites – a phylogenetic approach. Molecular Ecology 16:1281–1290.CrossRefGoogle ScholarPubMed
HELLGREN, O., BENSCH, S. & MALMQVIST, B. 2008. Bird hosts, blood parasites and their vectors – associations uncovered by molecular analyses of blackfly blood meals. Molecular Ecology 17:1605–1613.CrossRefGoogle ScholarPubMed
HUELSENBECK, J. P., RONQUIST, F., NIELSEN, R. & BOLLBACK, J. P. 2001. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310–2314.CrossRefGoogle ScholarPubMed
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 451:990–993.CrossRefGoogle ScholarPubMed
JULIANO, S. A. & LOUNIBOS, L. P. 2005. Ecology of invasive mosquitoes: effect on resident species and on human health. Ecological Letters 8:558–574.CrossRefGoogle ScholarPubMed
KEITH, S., URBAN, E. K. & FRY, C. H. 1992. The birds of Africa. Academic Press, New York. 609+ pp.Google Scholar
KETTLE, D. S. 1982. Medical and veterinary entomology. Wiley and Sons, New York. 658 pp.Google Scholar
KRIŽANAUSKIENĖ, A., HELLGREN, O., KOSAREV, V., SOKOLOV, L., BENSCH, S. & VALKIŪNAS, G. 2006. Variation in host specificity between species of avian hemosporidian parasites: evidence from parasite morphology and cytochrome B gene sequences. Journal of Parasitology 92:1319–1324.CrossRefGoogle ScholarPubMed
KRONE, O., WALDENSTROM, J., VALKIUNAS, G., LESSOW, O., MULLER, K., IEZHOVA, T. A., FICKEL, J. & BENSCH, S. 2008. Haemosporidian blood parasites in European birds of prey and owls. Journal of Parasitology 94:709–715.CrossRefGoogle ScholarPubMed
KUMAR, S., TAMURA, K. & NEI, M. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics 5:150–163.CrossRefGoogle ScholarPubMed
KUTZ, S. J., HOBERG, E. P., POLLEY, L. & JENKINS, E. J. 2005. Global warming is changing the dynamics of Arctic host–parasite systems. Proceedings of the Royal Society B-Biological Sciences 272:2571–2576.CrossRefGoogle ScholarPubMed
LAURANCE, W. F. 1999. Reflections on the tropical deforestation crisis. Biological Conservation 91:109–117.CrossRefGoogle Scholar
LOUETTE, M. 1981. The birds of Cameroon. An annotated checklist. Verhandelingen van de Koniklijke Academie voor Wetenschappen, Letteren Schone Kunsten van Belgie. Klasse de Wetenschappen 43:1–295.Google Scholar
LOUETTE, M. & BIJNENS, L. 1995. The utility of birds as bioindicators – case-studies in Equatorial Africa. Belgian Journal of Zoology 125:157–165.Google Scholar
MERCER, D. R., SHEELEY, S. L. & BROWN, E. J. 2005. Mosquito (Diptera: Culicidae) development within microhabitats of an Iowa wetland. Journal of Medical Entomology 42:685–693.CrossRefGoogle ScholarPubMed
MERINO, S., MORENO, J., SANZ, J. J. & ARRIERO, E. 2000. Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proceedings of the Royal Society of London Series B, Biological Sciences 267:2507–2510.CrossRefGoogle Scholar
MORAND, S. & POULIN, R. 1998. Density, body mass and parasite species richness of terrestrial mammals. Evolutionary Ecology 12:717–727.CrossRefGoogle Scholar
OSTFELT, R. S. & KEESING, F. 2000. Biodiversity and disease risk: the case of Lyme disease. Conservation Biology 14:722–728.CrossRefGoogle Scholar
OSTFELD, R. S., GLASS, G. & KEESING, F. 2005. Spatial epidemiology: an emerging (or re-emerging) discipline. Trends in Ecology and Evolution 20:328–336.CrossRefGoogle ScholarPubMed
PACKER, C., ALTIZER, S., APPEL, M., BROWN, E., MARTENSON, J., O'BRIEN, S. J., ROELKE-PARKER, M., HOFMANN-LEHMANN, R. & LUTZ, H. 1999. Viruses of the Serengeti: patterns of infection and mortality in African lions. Journal of Animal Ecology 68:1161–1178.CrossRefGoogle Scholar
PATZ, J. A., GRACZYK, T. K., GELLER, N. & VITTOR, A. Y. 2000. Effects of environmental change on emerging parasitic diseases. International Journal of Parasitology 30:1395–1405.CrossRefGoogle ScholarPubMed
PATZ, J. A., DASZAK, P., TABOR, G. M., AGUIRRE, A. A., PEARL, M., EPSTEIN, J., WOLFE, N. D., KILPATRICK, A. M., FOUFOPOULOS, J., MOLYNEUX, D. & BRADLEY, D. J. 2004. Unhealthy landscapes: policy recommendations on land use change and infectious disease emergence. Environmental Health Perspectives 112:1092–1098.CrossRefGoogle ScholarPubMed
PÉREZ-TRIS, J. & BENSCH, S. 2005. Diagnosing genetically diverse avian malarial infections using mixed-sequence analysis and TA-cloning. Parasitology 131:15–23.CrossRefGoogle ScholarPubMed
PÉREZ-TRIS, J., HELLGREN, O., KRIŽANAUSKIENĖ, A., WALDENSTRÖM, J., SECONDI, J., BONNEAUD, C., FJELDSÅ, J., HASSELQUIST, D. & BENSCH, S. 2007. Within-host speciation of malaria parasites. PLoS ONE 2:e235.CrossRefGoogle ScholarPubMed
RICKLEFS, R. E. & FALLON, S. M. 2002. Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society of London Series B, Biological Sciences 269:885–892.CrossRefGoogle ScholarPubMed
SAATCHI, S., NELSON, B., PODEST, E. & HOLT, J. 2000. Mapping land cover types in the Amazon Basin using 1 km JERS-1 mosaic. International Journal of Remote Sensing 21:1201–1234.CrossRefGoogle Scholar
SCHMIDT, K. A. & OSTFELD, R. S. 2001. Biodiversity and the dilution effect in disease ecology. Ecology 82:609–619.CrossRefGoogle Scholar
SEHGAL, R. N. M., JONES, H. I. & SMITH, T. B. 2005. Blood parasites of some West African rainforest birds. Journal of Veterinary Medical Science 67:295–301.CrossRefGoogle ScholarPubMed
SMITH, T. B. 1990. Resource use by bill morphs of an African finch: evidence for intraspecific competition. Ecology 71:1246–1257.CrossRefGoogle Scholar
SMITH, T. B., WAYNE, R. K., GIRMAN, D. J. & BRUFORD, M. W. 1997. A role for ecotones in generating rainforest biodiversity. Science 276:1855–1857.CrossRefGoogle Scholar
SMITH, T. B., MILÁ, B., GRETHER, G. F., SLABBEKOORN, H., SEPIL, I., BUERMANN, W., SAATCHI, S. & POLLINGER, J. P. 2008. Evolutionary consequences of human disturbance in a rainforest bird species from central Africa. Molecular Ecology 17:58–71.CrossRefGoogle Scholar
SZYMANSKI, M. M. & LOVETTE, I. J. 2005. High lineage diversity and host sharing of malarial parasites in a local avian assemblage. Journal of Parasitology 91:768–774.CrossRefGoogle Scholar
TADEI, W. P., THATCHER, B. D., SANTOS, J. M. H., SCARPASSA, V. M., RODRIGUES, I. B. & RAFAEL, M. S. 1998. Ecologic observations on anopheline vectors of malaria in the Brazilian Amazon. American Journal of Tropical Medicine and Hygiene 59:325–335.CrossRefGoogle ScholarPubMed
TURNER, W., SPECTOR, S., GARDINER, N., FLADELAND, M., STERLING, E. & STEININGER, M. 2003. Remote sensing for biodiversity science and conservation. Trends in Ecology and Evolution 18:306–314.CrossRefGoogle Scholar
TYLIANALIS, J. M., TSCHARNTKE, T. & LEWIS, O. T. 2007. Habitat modification alters the structure of tropical host–parasitoid food webs. Nature 445:202–205.CrossRefGoogle Scholar
VALKIŪNAS, G. 2005. Avian malaria parasites and other haemosporidia. CRC Press, Boca Raton. 932 pp.Google Scholar
VALKIŪNAS, G. & IEZHOVA, T. A. 2004. The transmission of Haemoproteus belopolskyi (Haemosporida: Haemoproteidae) of blackcap by Culicoides impunctatus (Diptera: Ceratopogonidae). Journal of Parasitology 90:196–198.CrossRefGoogle ScholarPubMed
VALKIŪNAS, G., BENSCH, S., IEZHOVA, T. A., KRIŽANAUSKIENĖ, A., HELLGREN, O. & BOLSHAKOV, C. V. 2006a. Nested cytochrome B polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: microscopy is still essential. Journal of Parasitology 92:418–422.CrossRefGoogle ScholarPubMed
VALKIŪNAS, G., ŽIČKUS, T., SHAPOVAL, A. P. & IEZHOVA, T. A. 2006b. Effect of Haemoproteus belopolskyi (Haemosporida: Haemoproteidae) on body mass of the blackcap Sylvia atricapilla. Journal of Parasitology 92:1123–1125.CrossRefGoogle ScholarPubMed
VALKIŪNAS, G., IEZHOVA, T. A., KRIŽANAUSKIENĖ, A., PALINAUSKAS, V., SEHGAL, R. N. M. & BENSCH, S. 2008a. A comparative analysis of microscopy and PCR-based detection methods for blood parasites. Journal of Parasitology 94:1395–1401.CrossRefGoogle ScholarPubMed
VALKIŪNAS, G., IEZHOVA, T. A., LOISEAU, C., CHASAR, A., SMITH, T. B. & SEHGAL, R. N. M. 2008b. New species of haemosporidian parasites (Haemosporida) from African rainforest birds, with remarks on their classification. Parasitology Research 103:1213–1228.CrossRefGoogle ScholarPubMed
VALKIŪNAS, G., IEZHOVA, T. A., LOISEAU, C., CHASAR, A., SMITH, T. B. & SEHGAL, R. N. M. 2009. New malaria parasites of the subgenus Novyella in African rainforest birds, with remarks on their high prevalence, classification and diagnostics. Parasitology Research 104:1061–1077.CrossRefGoogle ScholarPubMed
VAZ, V. C., D'ANDREA, P. S. & JANSEN, A. M. 2007. Effects of habitat fragmentation on wild mammal infection by Trypanosoma cruzi. Parasitology 134:1785–1793.CrossRefGoogle ScholarPubMed
VITTOR, A. Y., GILMAN, R. H., TIELSCH, J., GLASS, G., SHIELDS, T., LOZANO, W. S., PINEDO-CANCINO, V. & PATZ, J. A. 2006. The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon. American Journal of Tropical Medicine and Hygiene 74:3–11.CrossRefGoogle ScholarPubMed
WALSH, J. F., MOLYNEAUX, D. H. & BIRLEY, M. H. 1993. Deforestation: effects on vector-borne disease. Parasitology 106:S55–S75.CrossRefGoogle ScholarPubMed
WOOD, M. J., COSGROVE, C. L., WILKIN, T. A., KNOWLES, S. C. L., DAY, K. P. & SHELDON, B. C. 2007. Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology 16:3263–3273.CrossRefGoogle ScholarPubMed
YAHNER, R. H. 1988. Changes in wildlife communities near edges. Conservation Biology 2:333–339.CrossRefGoogle Scholar