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Habitat fragmentation and haemoparasites in the common fruit bat, Artibeus jamaicensis (Phyllostomidae) in a tropical lowland forest in Panamá

Published online by Cambridge University Press:  23 July 2009

V. M. COTTONTAIL*
Affiliation:
Institute of Experimental Ecology, University of Ulm, Albert-Einstein-Allee 11, 89069 Ulm, Germany Institute of Medical Microbiology and Hygiene, Robert-Koch-Strasse 8, 89081 Ulm, Germany
N. WELLINGHAUSEN
Affiliation:
Institute of Medical Microbiology and Hygiene, Robert-Koch-Strasse 8, 89081 Ulm, Germany
E. K. V. KALKO
Affiliation:
Institute of Experimental Ecology, University of Ulm, Albert-Einstein-Allee 11, 89069 Ulm, Germany Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Panamá
*
*Corresponding author: Institute of Experimental Ecology, University of Ulm, Albert-Einstein-Allee 11, 89069 Ulm, Germany. Tel: 0049 (0) 731 5022660. Fax: 0049 (0) 731 5022683. E-mail: [email protected].

Summary

Anthropogenic influence on ecosystems, such as habitat fragmentation, impacts species diversity and interactions. There is growing evidence that degradation of habitats favours disease and hence affects ecosystem health. The prevalence of haemoparasites in the Common Fruit Bat (Artibeus jamaicensis) in a tropical lowland forest in Panamá was studied. We assessed the relation of haemoparasite to the general condition of the animals and tested for possible association of haemoparasite prevalence to habitat fragmentation, with special focus on trypanosomes. Overall, a total of 250 A. jamaicensis sampled from fragmented sites, here man-made, forested islands in Lake Gatùn, and sites in the adjacent, continuous forest in and around the Barro Colorado Nature Monument were examined. Using microscopy and DNA-sequencing 2 dominant types of haemoparasite infections, trypanosomes and Litomosoides (Nematoda) were identified. Trypanosome prevalence was significantly higher in bats from forest fragments, than in bats captured in continuous forest. We attribute this to the loss of species richness in forest fragments and specific characteristics of the fragments favouring trypanosome transmission, in particular changes in vegetation cover. Interestingly, the effect of habitat fragmentation on the prevalence of trypanosomes as multi-host parasites could not be observed in Litomosoides which probably has a higher host specificity and might be affected less by overall diversity loss.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Allan, B. F., Keesing, F. and Ostfeld, R. S. (2003). Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17, 267272.Google Scholar
Apanius, V. (1998). Stress and immune response. In Stress and Behavior – Advances in the Study of Animal Behavior 27 (ed. Slater, P. J. B.), pp. 133153. Academic Press, San Diego, USA.Google Scholar
Aufderheide, A. C., Salo, W., Madden, M., Streitz, J., Buikstra, J., Guhl, F., Arriaza, B., Renier, C., Wittmers, L. E., Fornaciari, G. and Allison, M. (2003). A 9,000-year record of Chagas' disease. Proceedings of the National Academy of Sciences, USA 101, 20342039.CrossRefGoogle Scholar
Bower, S. M. and Woo, P. T. K. (1981). In vitro comparison of Trypanosoma spp. subgenus Schizoptrypanum in bats. Systematic Parasitology 3, 217236.CrossRefGoogle Scholar
Brant, S. V. and Gardner, S. L. (2000). Phylogeny of species of the genus Litomosoides (Nematoda: Onchocercidae): evidence of rampant host switching. Journal of Parasitology 86, 545554.Google Scholar
Brown, B. A. (1993). Hematology: Principles and Procedures. 6th Edn.Lea & Febiger, Malvern, UK.Google Scholar
Castro-Luna, A. A., Sosa, V. J. and Castillo-Campos, G. (2007). Quantifying phyllostomid bats at different taxonomic levels as ecological indicators in disturbed tropical forest. Acta Chiropterologica 9, 219228.CrossRefGoogle Scholar
Chapman, C. A., Gillespie, T. R. and Goldberg, T. L. (2005). Primates and the ecology of their infectious diseases: How will anthropogenic change affect host-parasite interactions? Evolutionary Anthropology 14, 134144.CrossRefGoogle Scholar
Chapman, C. A., Saj, T. L. and Snaith, T. V. (2007). Temporal dynamics of nutrition, parasitism, and stress in colobus monkeys: implications for population regulation and conservation. American Journal of Physical Anthropology 134, 240250.CrossRefGoogle ScholarPubMed
Chivian, E. (2001). Environment and health: Species loss and ecosystem disruption – the implications for human health. Canadian Medical Association Journal 164, 6669.Google ScholarPubMed
Cook, A., Jardine, A. and Weinstein, P. (2004). Using human disease outbreaks as a guide to multilevel ecosystem interventions. Environmental Health Perspectives 112, 11431146.Google Scholar
Cosson, J.-F., Pons, J.-M. and Masson, D. (1999). Effects of forest fragmentation on frugivorous and nectarivorous bats in French Guiana. Journal of Tropical Ecology 15, 515534.CrossRefGoogle Scholar
Desjeux, P. (2001). The increase in risk factors for leishmaniasis worldwide. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 239243.Google Scholar
Diamond, J. (2001). Dammed experiments! Science 294, 18471848.CrossRefGoogle ScholarPubMed
Dobson, A., Cattadori, I., Holt, R. D., Ostfeld, R. S., Keesing, F., Krichbaum, K., Rohr, J. R., Perekins, S. E. and Hudson, P. J. (2006). Sacred cows and sympathetic squirrels: The importance of biological diversity to human health. PLOS Medicine 3, 714718.Google Scholar
Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics 34, 487515.Google Scholar
Fleming, T. H., Hooper, E. T. and Wilson, E. D. (1972). Three Central American bat communities: structure, reproductive cycles, and movement patterns. Ecology 53, 555569.Google Scholar
Gardner, A. L., Handley, C. O. and Wilson, D. E. (1991). Survival and relative abundance. In Demography and Natural History of the Common Fruit Bat Artibeus jamaicensis on Barro Colorado Island, Panamá (ed. Handley, C. O., Wilson, D. E. and Gardner, A. L.), pp. 5375. Smithsonian Institution Press, Washington DC, USA.Google Scholar
Gaunt, M. and Miles, M. (2000). The ecotopes and evolution of triatomine bugs (Triatominae) and their associated trypanosomes. Memorias do Instituto Oswaldo Cruz 95, 557565.CrossRefGoogle ScholarPubMed
Gillespie, T. R., Chapman, C. A and Greiner, E. C. (2005). Effects of logging on gastrointestinal parasite infections and infection risk in African primates. Journal of Applied Ecology 42, 699707.Google Scholar
Gillespie, T. R. and Chapman, C. A. (2006). Prediction of parasite infection dynamics in primate metapopulations based on attributes of forest fragmentation. Conservation Biology 29, 441448.CrossRefGoogle Scholar
Gillespie, T. R. and Chapman, C. A. (2007). Forest fragmentation, the decline of an endangered primate, and changes in host-parasite interactions relative to an unfragmented forest. American Journal of Primatology 69, 113.Google Scholar
Grisard, E. C., Sturm, N. R. and Campbell, D. A. (2003). A new species of trypanosome, Trypanosoma desterrensis sp. n., isolated from South American bats. Parasitology 127, 265271.Google Scholar
Guerrero, R., Martin, C., Gardner, S. L. and Bain, O. (2002). New and known species of Litomosoides (Nematoda: Filarioidea): Important adult and larval characters and taxonomic changes. Comparative Parasitology 69, 177195.CrossRefGoogle Scholar
Handley, C. O. and Morrison, D. W. (1991). Roosting behavior. In Demography and Natural History of the Common Fruit Bat Artibeus jamaicensis on Barro Colorado Island, Panamá (ed. Handley, C. O., Wilson, D. E. and Gardner, A. L.), pp. 131136. Smithsonian Institution Press, Washington DC, USA.Google Scholar
Handley, C. O., Wilson, D. E. and Gardner, A. L. (1991). Demography and Natural history of the Common Fruit Bat Artibeus jamaicensis on Barro Colorado Island, Panamá. Smithsonian Institution Press, Washington DC, USA.Google Scholar
Hoare, C. A. (1972). The Trypanosomes of Mammals. A Zoological Monograph. Blackwell Scientific Publications, Oxford and Edinburgh, UK.Google Scholar
Hoerauf, A., Satoguina, J., Saeftel, M. and Specht, S. (2005). Immunomodulation by filarial nematodes. Parasite Immunology 27, 417429.CrossRefGoogle ScholarPubMed
Hoffmann, W. H., Pfaff, A. W., Schulz-Key, H. and Soboslav, P. T. (2001). Determinants for resistance and susceptibility to microfilaraemia in Litomosoides sigmodontis filariasis. Parasitology 122, 641649.CrossRefGoogle ScholarPubMed
Houwen, B. (2000). Blood film preparation and staining procedures. Laboratory Hematology 6, 17.Google Scholar
Ilmonen, P., Taarna, T. and Hasselquist, D. (2000). Experimentally activated immune defense in female pied flycatchers results in reduced breeding success. Proceedings of the Royal Society of London, B 267, 655670.Google Scholar
Kalko, E. K. V., Handley, C. O. and Handley, D. (1996). Organisation, diversity and long-term dynamics of a neotropical bat community. In Long-Term Studies of Vertebrate Communities (ed. Smallwood, J.), pp. 503553. Academic Press, San Diego, USA.Google Scholar
Keesing, F., Holt, R. D. and Ostfeld, R. S. (2006). Effects of species diversity on disease risk. Ecology Letters 9, 485498.CrossRefGoogle ScholarPubMed
Lafferty, K. D. and Holt, R. D. (2003). How should environmental stress affect the population dynamics of disease? Ecology Letters 6, 654664.Google Scholar
Laurance, W. F., Lovejoy, T. E., Vasconcelos, H. L., Bruna, E. M., Didham, R. K., Stouffer, P. C., Gascon, C., Bierregaard, R. O., Laurance, S. G. and Sampaio, E. M. (2002). Ecosystem decay of Amazonian forest fragments: a 22-year investigation. Conservation Biology 16, 605618.CrossRefGoogle Scholar
Le Goff, L., Marechal, P., Petit, G., Taylor, W. D., Hoffmann, W. and Bain, O. (1997). Early reduction of the challenge recovery rate following immunisation with irradiated infective larvae in a filaria mouse system. Tropical Medicine and International Health 2, 11701174.CrossRefGoogle Scholar
Leigh, E. G. (1999). Tropical Forest Ecology. A View from Barro Colorado Island. Oxford University Press, New York, USA and Oxford, UK.CrossRefGoogle Scholar
LoGiudice, K., Ostfeld, R. S., Schmidt, K. A. and Keesing, F. (2003). The ecology of infectious disease: Effects of host diversity and community composition on lyme disease risk. Proceedings of the National Academy of Sciences, USA 100, 567571.CrossRefGoogle ScholarPubMed
Lüllmann-Rauch, R. (2003). Histologie. Georg Thieme Verlag, Stuttgart and Berlin, Germany.Google Scholar
Lyles, A. M. and Dobson, A. P. (1993). Infectious disease and intensive management: Population dynamics, threatened hosts, and their parasites. Journal of Zoo and Wildlife Medicine 24, 315326.Google Scholar
Marinkelle, C. J. (1976). Biology of trypanosomes of bats. In Biology of the Kinetoplastida Vol 1 (ed. Lumsden, W. H. R. and Evans, D. A.), pp. 175216. Academic Press, London, UK.Google Scholar
Marinkelle, C. J. (1982). Prevelance of Trypanosoma cruzi-like infection of colombian bats. Annals of Tropical Medicine and Parasitology 76, 125134.CrossRefGoogle Scholar
Martínez-Mota, R., Valdespino, C., Sánchez-Ramos, M. A., and Serio-Silva, J. C. (2007). Effects of forest fragmentation on the physiological stress response of black howler monkeys. Animal Conservation 10, 374379. doi:10.1111/j.1469-1795.2007.00122.X.CrossRefGoogle Scholar
McCallum, H. and Dobson, A. (2002). Disease, habitat fragmentation and conservation. Proceedings of the Royal Society of London, B 269, 20412049.CrossRefGoogle ScholarPubMed
Medellin, R. A., Equihua, M. and Amin, M. A. (2000). Bat diversity and abundance as indicators of disturbance in neotropical rainforests. Conservation Biology 14, 16661675.CrossRefGoogle ScholarPubMed
Meyer, C. F. J., Fründ, J., Lizano, W. P. and Kalko, E. K. V. (2008). Ecological correlates of vulnerability to fragmentation in neotropical bats. Journal of Applied Ecology 45, 381391.CrossRefGoogle Scholar
Meyer, C. F. J. and Kalko, E. K. V. (2008 a). Bat assemblages on neotropical landbridge islands: nested subsets and null model analyses of species co-occurrence patterns. Diversity and Distributions 14, 644654.Google Scholar
Meyer, C. F. J. and Kalko, E. K. V. (2008 b). Assemblage-level responses of phyllostomid bats to tropical forest fragmentation: land-bridge islands as a model system. Journal of Biogeography 35, 17111726.Google Scholar
Molyneux, D. H. (1991). Trypanosomes of bats. In Parasitic Protozoa, 2nd Edn. (ed. Kreier, J. P. and Baker, J. R.), pp. 195223. Academic Press, New York, USA.Google Scholar
Noyes, H. A., Stevens, J. R., Teixeira, M., Phelan, J. and Holz, P. (1999). A nested PCR for the ssrRNA gene detects Trypanosoma binneyi in the platypus and Trypanosoma sp. in wombats and kangaroos in Australia. International Journal for Parasitology 29, 331339.CrossRefGoogle ScholarPubMed
Ostfeld, R. S. and Keesing, F. (2000 a). Biodiversity and disease risk: the case of lyme disease. Conservation Biology 14, 722728.CrossRefGoogle Scholar
Ostfeld, R. S. and Keesing, F. (2000 b). The function of biodiversity in the ecology of vector-borne diseases. Canadian Journal of Zoology 78, 20612078.CrossRefGoogle Scholar
Palmer, P. E. S. and Reeder, M. M. (2001). The Imaging of Tropical Diseases. Vol. 1. Springer Verlag. Berlin, Germany.Google Scholar
Patterson, B. D., Willig, M. R. and Stevens, R. D. (2003). Trophic strategies, niche partitioning, and patterns of ecological organization. In Bat Ecology (ed. Kunz, T. H. and Fenton, M. B.), pp. 536579. University of Chicago Press, Chicago, USA.Google Scholar
Patz, J. A., Graczyk, T. K., Geller, N. and Vittor, A. Y. (2000). Effects of environmental change on emerging parasitic diseases. International Journal for Parasitology 30, 13951405.Google Scholar
Patz, J. A., Daszak, P., Tabor, G. A., Aguirre, A. A., Pearl, M., Epstein, J., Wolfe, N. D., Kilpatrick, A. M., Foufopoulos, J., Molyneux, D., Bradley, D. J. and Members of the Working Group on Land Use Change and Disease Emergence (2004). Unhealthy landscapes: Policy recommendations on land use change and infectious disease emergence. Environmental Health Perspectives 112, 10921098.Google Scholar
Pichler, W. J., Peter, H. and Hänsch, M. G. (1996). Prinzipien des Immunsystems. In Klinische Immunologie, 2nd Edn. (ed. Peter, H. and Pichler, W. J.), pp. 351. Urban & Schwarzenberg, Munich, Germany.Google Scholar
Precht, M. (1982). Biostatistik Teil 1. Oldenbourg Verlag, Munich, Germany.Google Scholar
Reid, F. (1997). A field guide to mammals of Central America and southeast Mexico. Oxford University Press, New York, USA and Oxford, UK.Google Scholar
Ruedas, L. A., Salazar-Bravo, J., Tinnin, D. S., Armien, B., Caceres, L., Garcia, A., Avila Diaz, M., Garcia, G., Suzan, G., Peters, C. J., Yates, T. L. and Mills, J. M. (2004). Community ecology of small mammal populations in Panama following an outbreak of hantavirus pulmonary syndrome. Journal of Vector Ecology 29, 177191.Google Scholar
Salzer, J. S., Rwego, I. B., Goldberg, T. L., Kuhlenschmidt, M. S. and Gillespie, T. R. (2007). Giardia sp. and Cryptosporidium sp. infections in primates in fragmented and undisturbed forest in western Uganda. Journal of Parasitology 93, 439440.Google Scholar
Sehgal, R. N. M., Jones, H. I. and Smith, T. B. (2001). Host specificity and incidence of Trypanosoma in some African rainforest birds: a molecular approach. Molecular Ecology 10, 23192327.CrossRefGoogle ScholarPubMed
Sih, A., Johnson, B. G. and Luikart, G. (2000). Habitat loss: ecological, evolutionary and genetic consequences. Trends in Ecology & Evolution 15, 132134.Google Scholar
Sousa, O. E. (1972). Annotaciones sobre la Enfermidad de Chagas en Panama. Frecuencia y distribution de Trypanosoma cruzi y Trypanosoma rangeli. Revista de Biologia Tropical 20, 167169.Google Scholar
Stevens, J. R. and Brisse, S. (2004). Systematics of trypanosomes of medical and veterinary importance. In The Trypanosomiases (ed. Maudlin, I., Holmes, P. H. and Miles, M. A.), pp. 123. CABI Publishing, Wallingford, UK.Google Scholar
Steindel, M., Grisard, E. C., Carvalhopinto, C. J., Cordeiro, F. D., Ribeiro-Rodrigues, R. and Romanha, H. A. (1998). Characterization of trypanosomes from the subgenus Schizotrypanum isolated from bats Eptisicus sp. (Chiroptera: Vespertilionidae), captured in Florianopolis, Santa Catarina State, Brazil. Journal of Parasitology 84, 601607.Google Scholar
Tabarelli, M., Cardoso da Silva, J. M. and Gascon, C. (2004). Forest fragmentation, synergisms and the impoverishment of Neotropical forests. Biodiversity and Conservation 13, 14191425.CrossRefGoogle Scholar
Terborgh, J., Lopez, L., Nuñez, V. P., Rao, M., Shahabuddin, G., Oriheula, G., Riveros, R., Adler, G. H., Lambert, T. D. and Balbas, L. (2001). Ecological meltdown in predator-free forest fragments. Science 294, 19231926.CrossRefGoogle ScholarPubMed
Travi, B. L., Jaramillo, C., Montoya, J., Segura, I., Zea, A., Concalves, A. and Velez, I. D. (1994). Didelphis marsupialis, an important reservoir of Trypanosoma (Schizotrypanum) cruzi and Leishmania (Leishmania) chagasi in Colombia. American Journal of Tropical Medicine and Hygiene 50, 557565.CrossRefGoogle ScholarPubMed
Ubelaker, G. E., Spezian, R. D. and Duzynski, D. W. (1977). Endoparasites. In Biology of the Bats of the New World Family Phyllostomidae Part II. (ed. Baker, R. J., Jones, J. K. and Carter, D. C.) 13, 756. Special Publications, The Museum of Texas Tech, Lubbock University Press, Lubbock, USA.Google Scholar
Vaz, V. C., D' Andrea, P. S. and Jansen, A. M. (2007). Effects of habitat fragmentation on wild mammal infection by Trypanosoma cruzi. Parasitology 134, 17851793.Google Scholar
Verhoeven, K. J. F., Simonsen, K. L. and McIntyre, L. M. (2005). Implementing false discovery rate: increasing your power. OIKOS 108, 643647.CrossRefGoogle Scholar
Wade, T. G., Ritters, K. H., Wickham, J. D. and Jones, K. B. (2003). Distribution and causes of global forest fragmentation. Conservation Ecology 7, 7.CrossRefGoogle Scholar
Walsh, J. F., Molyneux, D. H. and Birley, M. H. (1993). Deforestation: effects on vector-borne disease. Parasitology 106 (Suppl.) S55S75.Google Scholar
Whitlaw, J. T. and Chaniotis, B. N. (1978). Palm trees and Chagas' disease in Panama. American Journal of Tropical Medicine and Hygiene 27, 873881.Google Scholar
Whitlaw, J. T. (1980). Palm trees and disease. International Journal of Dermatology 19, 142143.Google Scholar
Willig, M. R., Presley, S. J., Bloch, C. P., Hice, C. A., Yanoviak, S. P., Diaz, M. M., Chauca, L. A., Pacheco, V. and Weaver, S. C. (2007). Phyllostomid bats of lowland Amazonia: Effects of habitat alteration on abundance. Biotropica 39, 737746.Google Scholar