Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-28T14:10:13.211Z Has data issue: false hasContentIssue false
  • English
  • Français

The influence of human settlements on the parasite community in two species of Peruvian tamarin

Published online by Cambridge University Press:  22 December 2009

A. WENZ ,
E. W. HEYMANN ,
T. N. PETNEY  and
H. F. TARASCHEWSKI
A. WENZ*
Affiliation:
University of Karlsruhe, Zoological Institute, Department of Ecology and Parasitology, Kornblumenstrasse 13, 76131Karlsruhe, Germany
E. W. HEYMANN
Affiliation:
German Primate Center, Department of Behavioural Ecology and Sociobiology, Kellnerweg 4, 37077Göttingen, Germany
T. N. PETNEY
Affiliation:
University of Karlsruhe, Zoological Institute, Department of Ecology and Parasitology, Kornblumenstrasse 13, 76131Karlsruhe, Germany
H. F. TARASCHEWSKI
Affiliation:
University of Karlsruhe, Zoological Institute, Department of Ecology and Parasitology, Kornblumenstrasse 13, 76131Karlsruhe, Germany
*
*Corresponding author: University of Karlsruhe, Zoological Institute, Department of Ecology and Parasitology, Kornblumenstrasse 13, 76131Karlsruhe, Germany. Tel: +49 721 6084717. Fax: +49 721 6087655. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Although there is a growing recognition that the transfer of diseases between humans and non-human primates can be of great significance for conservation biology, there have been only a few studies focusing on parasites. In this study, saddleback (Saguinus fuscicollis) and moustached tamarin (Saguinus mystax) from the rainforest of the Peruvian lowlands were used as models to determine helminth parasite associations between canopy-dwelling primate species and a nearby human settlement. The human population showed high prevalences of infestation with a number of nematodes, including Ascaris lumbricoides (88·9%), Trichuris trichiura (37%) and hookworms (55·6%). However, the ova of these geohelminths were not detectable in tamarin faeces. Thus, no direct parasite transfer from humans to non-human primates could be documented. However, tamarin groups with more frequent contact to humans and their facilities had significantly higher prevalences and egg output of Prosthenorchis elegans, an important primate pathogen, than a forest group. In contrast, a cestode was significantly more common with more egg output in sylvatic than in human-associated groups. Human alteration of the habitat is likely to play a major role in determining the occurrence, prevalence and intensity of helminth infestation of wild non-human primates.

Keywords

PeruprimatesparasitestamarinProsthenorchis eleganshumanssynanthropic transmission
Type
Research Article
Information
Parasitology , Volume 137 , Issue 4 , April 2010 , pp. 675 - 684
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

REFERENCES

Anderson, R. M. and Schad, G. A. (1985). Hookworm burdens and faecal egg counts: an analysis of the biological basis of varation. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 812–825.CrossRefGoogle Scholar
Ash, L. R. and Orihel, T. C. (1987). Parasites: a Guide to Laboratory Procedures and Identification. American Society of Clinical Pathologists Press, Chicago, IL, USA.Google Scholar
Ash, L. R., Orihel, T. C. and Savioli, L. (1994). Bench Aids for the Diagnosis of Intestinal Parasites. World Health Organisation, Geneva, Switzerland.Google Scholar
Basset, Y. (2001). Invertebrates in the canopy of tropical rain forests. How much do we really know? Plant Ecology 153, 87–107. doi: 10.1023/A:1017581406101.CrossRefGoogle Scholar
Bengis, R. G., Kock, R. A. and Fischer, J. (2002). Infectious animal diseases: the wildlife/livestock interface. Revue Scientifique et Technique 21, 53–65.Google ScholarPubMed
Boyer, S. and Rivault, C. (2006). Impact of human activity on the distribution of native and non-native cockroach species (Dictyoptera) in La Réunion and Mayotte. Bulletin of Entomological Research 96, 399–406.CrossRefGoogle Scholar
Bradley, C. A. and Altizer, S. (2007). Urbanization and the ecology of wildlife diseases. Trends in Ecology and Evolution 22, 95–102. doi: 10.1016/j.tree.2006.11.001.CrossRefGoogle ScholarPubMed
Burgess, N. R. H., McDermott, S. N. and Whiting, J. (1973). Aerobic bacteria occurring in the hind-gut of the cockroach, Blatta orientalis. Journal of Hygiene 71, 1.CrossRefGoogle ScholarPubMed
Cabaret, J., Gasnier, N. and Jacquiet, P. (1998). Faecal egg counts are representative of digestive-tract strongyle worm burdens in sheep and goats. Parasite 5, 137–142.CrossRefGoogle ScholarPubMed
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, 134–144. doi: 10.1002/evan.20068.CrossRefGoogle Scholar
Chapman, C. A. and Peres, C. A. (2001). Primate conservation in the new millenium: the role of scientists. Evolutionary Anthropology 10, 16–33.3.0.CO;2-O>CrossRefGoogle Scholar
Chi, F., Leider, M., Leendertz, F., Bergmann, C., Boesch, C., Schenk, S., Pauli, G., Ellerbrok, H. and Hakenbeck, R. (2007). New Streptococcus pneumoniae clones in deceased wild chimpanzees. Journal of Bacteriology 189, 6085–6088. doi: 10.1128/JB.00468-07.CrossRefGoogle ScholarPubMed
Christensen, C. M., Barnes, E. H., Nansen, P., Roepstorff, A. and Slotved, H. C. (1995). Experimental Oesophagostomum dentatum infection in the pig: worm populations resulting from single infections with three doses of larvae. International Journal for Parasitology 25, 1491–1498.CrossRefGoogle ScholarPubMed
Crompton, D. W. T. (1970). An Ecological Approach to Acanthocephalan Physiology. Cambridge University Press, Cambridge, UK.Google Scholar
Cubas, Z. S. (1996). Special challenges of maintaining wild animals in captivity in South America. Revue Scientifique et Technique 15, 267–287.CrossRefGoogle ScholarPubMed
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2000). Emerging infectious diseases of wildlife – threats to biodiversity and human health. Science 287, 443–449. doi: 10.1126/science.287.5452.443.CrossRefGoogle ScholarPubMed
Daszak, P., Tabor, G. M., Kilpatrick, A. M., Epstein, J. and Plowright, R. (2004). Conservation medicine and a new agenda for emerging diseases. Annals of the New York Academy of Sciences 1026, 1–11. doi: 10.1196/annals.1307.001.CrossRefGoogle Scholar
de Gruijter, J. M., Gasser, R. B., Polderman, A. M., Asigri, V. and Dijkshoorn, L. (2005). High resolution DNA fingerprinting by AFLP to study the genetic variation among Oesophagostomum bifurcum (Nematoda) from human and non-human primates from Ghana. Parasitology 130, 229–237.CrossRefGoogle Scholar
Engels, D., Nahimana, S., DeVlas, S. J. and Gryseels, B. (1997 a). Variation in weight of stool samples prepared by the Kato-Katz method and its implications. Tropical Medicine & International Health 2, 265–271.CrossRefGoogle ScholarPubMed
Engels, D., Sinzinkayo, E., DeVlas, S. J. and Gryseels, B. (1997 b). Intraspecimen fecal egg count variation in Schistosoma mansoni infection. American Journal of Tropical Medicine and Hygiene 54, 572–577.Google Scholar
Engels, D., Sinzinkayo, E. and Gryseels, B. (1996). Day-to-day egg count fluctuation in Schistosoma mansoni infection and its operational implications. American Journal of Tropical Medicine and Hygiene 54, 3119–3324.CrossRefGoogle ScholarPubMed
Gasser, R. B., de Gruijter, J. M. and Polderman, A. M. (2009). The utility of molecular methods for elucidating primate-pathogen relationships-the Oesophagostomum bifurcum example. In Primate Parasite Ecology: The Dynamics and Study of Host-Parasite Relationships (ed. Huffman, M. A. and Chapman, C. A.), pp. 47–62. Cambridge Studies in Biological and Evolutionary Anthropology, Cambridge University Press, Cambridge.Google Scholar
Gillespie, T. R. and Chapman, C. A. (2006). Forest fragment attributes predict parasite infection dynamics in primate metapopulations. Conservation Biology 20, 441–448. doi: 10.1111/j.1523 1739.2006.00290.x.CrossRefGoogle ScholarPubMed
Gillespie, T. R., Greiner, E. C. and Chapman, C. A. (2005). Gastrointestinal parasites of the colobus monkeys of Uganda. Journal of Parasitology 91, 569–573.CrossRefGoogle ScholarPubMed
Graczyk, T. K., DaSilva, A. J., Cranfield, M. R., Nizeyi, J. B., Kalema, G. R. N. N. and Pieniazek, N. J. (2001). Cryptosporidium parvum Genotype 2 infections in free-ranging mountain gorillas (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park Uganda. Parasitology Research 87, 368–370.CrossRefGoogle ScholarPubMed
Graczyk, T. K., Knight, R. and Tamang, L. (2005). Mechanical transmission of human protozoan parasites by insects. Clinical Microbiology Reviews 18, 128–132. doi: 10.1128/CMR.18.1.128-132.2005.CrossRefGoogle ScholarPubMed
Gurgel-Gonçalves, R., Palma, A. R. T., Motta, P. C., Bar, M. E. and Cuba, C. A. C. (2006). Arthropods associated with the crown of Mauritia flexuosa (Arecaceae) palm trees in three different environments from Brazilian Cerrado. Neotropical Entomology 35, 302–312. doi: 10.1590/S1519-566X2006000300003.CrossRefGoogle ScholarPubMed
Hahn, N. E., Proulx, D., Muruthi, P. M., Alberts, S. and Altmann, J. (2003). Gastrointestinal parasites in free-ranging Kenyan baboons (Papio cynocephalus and P. anubis). International Journal of Primatology 24, 271–279.CrossRefGoogle Scholar
Heydon, M. J. and Bulloh, P. (1997). Mousedeer densities in a tropical rainforest: the impacts of selective logging. Journal of Applied Ecology 36, 564–574.Google Scholar
Heymann, E. W. (1995). Sleeping habitats of tamarins, Saguinus mystax and Saguinus fuscicollis (Mammalia; Primates; Callitrichidae), in north-eastern Peru. Journal of Zoology 237, 211–226.CrossRefGoogle Scholar
Holland, C. V. and Kennedy, M. W. (2002). The Geohelminths: Ascaris, Trichuris and Hookworm (World Class Parasites, Vol. 2) Page xi. Kluwer Academic Publishers, Boston, MA, USA.CrossRefGoogle Scholar
Hudson, P. J., Rizzoli, A. P., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P. (2002). The Ecology of Wildlife Diseases. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman, J. L. and Daszak, P. (2008). Global trends in emerging infectious diseases. Nature, London 451, 990–994. doi: 10.1038/nature06536.CrossRefGoogle ScholarPubMed
Kageyama, T. (2000). New World monkey pepsinogens A and C, and Prochymosins. Purification, characterization of enzymatic properties, cDNA cloning, and molecular evolution. Journal of Biochemistry 127, 761–770.CrossRefGoogle Scholar
Keymer, A. E. and Hiorns, R. W. (1986). Faecal egg counts and nematode fecundity: Heligmosomoides polygyrus and laboratory mice. Parasitology 93, 189–203.CrossRefGoogle ScholarPubMed
Köndgen, S., Kühl, H., N'Goran, P. K., Walsh, P. D., Schenk, S., Ernst, N., Biek, R., Formenty, P., Mätz-Rensing, K., Schweiger, B., Junglen, S., Ellerbrok, H., Nitsche, A., Briese, T., Lipkin, W. I., Pauli, G., Boesch, C. and Leendertz, F. H. (2008). Pandemic human viruses cause decline of endangered Great Apes. Current Biology 18, 260–264. doi: 10.1016/j.cub.2008.01.012.CrossRefGoogle ScholarPubMed
Lafferty, K. D. (2003). Is disease increasing or decreasing, and does it impact or maintain biodiversity? Journal of Parasitology 89, 5101–5105.Google Scholar
Leendertz, F. H., Yumlu, S., Pauli, G., Boesch, C., Couacy-Hymann, E., Vigilant, L., Junglen, S., Schenk, S. and Ellerbrok, H. (2006). A new Bacillus anthracis found in wild chimpanzees and a gorilla from West and Central Africa. Public Library of Science: Pathogens 2, 1–4. doi: 10.1371/journal.ppat.0020008.Google Scholar
Lilly, A. A., Mehlman, P. T. and Doran, D. (2002). Intestinal parasites in gorillas, chimpanzees, and humans at Mondika Research Site, Dzanga-Ndoki National Park, Central African Republic. International Journal of Primatology 23, 555–573. doi: 10.1023/A:1014969617036.CrossRefGoogle Scholar
Löttker, P., Huck, M. and Heymann, E. W. (2004). Demographic parameters and events in wild moustached tamarins (Saguinus mystax). American Journal of Primatology 64, 425–449. doi: 10.1002/ajp.20090.CrossRefGoogle ScholarPubMed
Michaud, C., Tantaleán, M., Ique, C., Montoya, E. and Gozalo, A. (2003). A survey for helminth parasites in feral New World non-human primate populations and its comparison with parasitological data from man in the region. Journal of Medical Primatology 32, 341–345.CrossRefGoogle ScholarPubMed
Middleton, C. C. (1966). Acanthocephala (Prostenorchis elegans) infection in squirrel monkeys (Saimiri sciureus). Laboratory Animal Digest 2, 2.Google Scholar
Moore, J. G. (1970). Epizootic of acanthocephaliasis among primates. Journal of the American Veterinary Medical Association 157, 703–705.Google ScholarPubMed
Mudakikwa, A. B., Sleeman, J., Foster, J., Meader, L. and Patton, S. (1998). An indicator of human impact: Gastrointestinal parasites of mountain gorillas (Gorilla gorilla beringei) from the Virunga Volcanoes Region, Central Africa. In Proceedings of the American Association of Zoo Veterinarians/American Association of Wildlife Veterinarians Joint Conference (ed. Baer, C. K.), pp. 436–437.Google Scholar
Müller, B. (2007). Determinants of the diversity of intestinal parasite communities in sympatric New World primates (Saguinus mystax, Saguinus fuscicollis, Callicebus cupreus). Ph.D. thesis, Tierärztliche Hochschule Hannover, Germany.Google Scholar
Mul, I. F., Paembonan, W., Singleton, I., Wich, S. A. and van Bolhuis, H. G. (2007). Intestinal parasites of free-ranging, semicaptive and captive Pongo abelii in Sumatra, Indonesia. International Journal of Primatology 28, 407–420. doi: 10.1007/s10764-007-9119-7.CrossRefGoogle Scholar
Neusser, M., Stanyon, R., Bigoni, F., Wienberg, J. and Müller, S. (2001). Molecular cytotaxonomy of New World monkeys (Platyrrhini) – comparative analysis of five species by multi-color chromosome painting gives evidence for a classification of Callimico goeldii within the familiy of Callitrichidae. Cytogenetic Cell Genetics 94, 206–215. doi: 10.1159/000048818.CrossRefGoogle Scholar
Nickle, D. A. and Heymann, E. W. (1996). Predation on Orthoptera and other orders in insects by tamarin monkeys, Saguinus mystax mystax and Saguinus fuscicollis nigrifrons (Primates: Callitrichidae), in north-eastern Peru. Journal of Zoology 239, 799–819.CrossRefGoogle Scholar
Nunn, C. and Altizer, S. (2006). Infectious Diseases in Primates: Behaviour, Ecology and Evolution. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Nunn, C., Altizer, S., Jones, K. E. and Sechrest, W. (2003). Comparative tests of parasite species richness in primates. American Naturalist 162, 597–614. doi: 10.1086/378721.CrossRefGoogle ScholarPubMed
Nunn, C., Gittleman, J. L. and Antonovics, J. (2000). Promiscuity and the primate immune system. Science 290, 1168–1170. doi: 10.1126/science.290.5494.1168.CrossRefGoogle ScholarPubMed
Olupot, W., Chapman, C. A., Brown, C. H. and Waser, P. M. (1994). Mangabey (Cercocebus albigena) population density, group size, and ranging: a twenty-year comparison. American Journal of Primatology 21, 587–611.Google Scholar
Patriquin, K. J. and Barclay, R. M. R. (2003). Foraging by bats in cleared, thinned and unharvested boreal forest. Journal of Applied Ecology 40, 646–657.CrossRefGoogle Scholar
Perpens, S., Kreuzer, K. A., Leendertz, F. H., Nitsche, A. and Ehlers, B. (2007). Discovery of herpesviruses in multi-infected primates using locked nucleic acids (LNA) and a bigenic PCR approach. Virology Journal 4, 84. doi: 10.1186/1743-422X-4-84.CrossRefGoogle Scholar
Phillips, K. A., Haas, M. E., Grafton, B. W. and Yrivarren, M. (2004). Survey of the gastrointestinal parasites of the primate community at Tambopata National Reserve, Peru. Journal of Zoology 264, 149–151. doi: 10.1017/S0952836904005680.CrossRefGoogle Scholar
Pritchard, D. I., Quinnell, R. J., Slater, A. F., McKean, P. G., Dale, D. D. S., Raiko, A. and Keymer, A. E. (1990). Epidemiology and immunology of Necator americanus infection in a community in Papua New Guinea: humoral responses to excretory-secretory and cuticular collagen antigens. Parasitology 100, 317–326.CrossRefGoogle Scholar
Roepstorff, A., Bjørn, H., Nansen, P., Barnes, E. H. and Christensen, C. M. (1996). Experimental Oesophagostomum dentatum infections in the pig: worm populations resulting from trickle infections with three dose levels of larvae. International Journal for Parasitology 26, 399–408.CrossRefGoogle ScholarPubMed
Ross, A. G. P., Yuesheng, LI, Sleigh, A. C., Williams, G. M. and McManus, D. P. (1998). Faecal egg aggregation in humans infected with Schistosoma japonicum in China. Acta Tropica 70, 205–210.CrossRefGoogle ScholarPubMed
Schmidt, G. D. (1972). Acanthocephala of captive primates. In Pathology of Simian Primates Part II (ed. Fiennes, R. N. T. N.), pp. 144–156. Karger, Basel, Switzerland.CrossRefGoogle Scholar
Schmidt, G. D. and Roberts, L. S. (1981). Foundations of Parasitology, 2nd Edn. Mosby, St Louis, MO, USA.Google Scholar
Sithithaworn, P., Tesana, S., Pipitgool, V., Kaewkes, S., Pairojkul, C., Sripa, B., Paupairoj, A. and Thaiklar, K. (1991). Relationship between faecal egg count and worm burden of Opisthorchis viverrini in human autopsy cases. Parasitology 103, 277–281.CrossRefGoogle Scholar
Smith, A. C. (2000). Interspecific differences in prey captured by associating saddleback (Saguinus fuscicollis) and moustached (Saguinus mystax) tamarins. Journal of Zoology 251, 315–324. doi: 10.1017/S0952836900007056.CrossRefGoogle Scholar
Smith, K. F., Sax, D. F. and Lafferty, K. D. (2006). Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20, 1349–1357. doi: 10.1111/j.15231739.2006.00524.x.CrossRefGoogle ScholarPubMed
St-Amour, V., Wong, W. M., Garner, T. W. J. and Lesbarrères, D. (2008). Anthropogenic influence on prevalence of 2 amphibian pathogens. Emerging Infectious Diseases 14, 1175–1176. doi: 10.3201/eid1407.070602.CrossRefGoogle ScholarPubMed
Stear, M. J., Bishop, S. C., Doligalska, M., Duncan, J. L., Holmes, P. H., Irvine, J., McCririe, L., McKellar, Q. A., Sinski, E. and Murray, M. (1995). Regulation of egg production, worm burden, worm lenght and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunology 17, 643–652.CrossRefGoogle Scholar
Stuart, M. D. and Strier, K. B. (1995). Primates and parasites: a case for a multidisciplinary approach. International Journal of Primatology 15, 577–593. doi: 10.1007/BF02735282.CrossRefGoogle Scholar
Tantaleán, M., Sánchez, L., Gómez, L. and Huiza, A. (2005). Acanthocéfalos del Perú (in Spanish). Revista Peruana de Biología 12, 83–92.CrossRefGoogle Scholar
Taraschewski, H. F. (2000). Host-parasite interactions in Acanthocephala: a morphological approach. Advances in Parasitology 46, 1–179.CrossRefGoogle ScholarPubMed
Vickers, J. H. (1969). Diseases of primates affecting the choice of species for toxicologic studies. Annals of the New York Academy of Sciences 162, 659–672.CrossRefGoogle ScholarPubMed
Vitazkova, S. K. and Wade, S. E. (2007). Effects of ecology on the gastrointestinal parasites of Alouatta pigra. International Journal of Primatology 28, 1327–1343.CrossRefGoogle Scholar
Warnick, L. D. (1992). Daily variability of equine fecal strongyle egg counts. Cornell Veterinarian 82, 453–463.Google ScholarPubMed
Weyher, A. H., Ross, C. and Semple, S. (2006). Gastrointestinal parasites in crop raiding and wild foraging Papio anubis in Nigeria. International Journal of Primatology 27, 2519–1534.CrossRefGoogle Scholar
Wolfe, N. D., Escalante, A. A., Karesh, W. B., Kilbourn, A., Spielman, A. and Lal, A. A. (1998). Wild primate populations in emerging infectious disease research: the missing link? Emerging Infectious Diseases 4, 149–158.CrossRefGoogle ScholarPubMed
Wolfe, N. D., Prosser, T. A., Carr, J. K., Tamoufe, U., Mpoudi-Ngole, E., Torimiro, J. N., LeBreton, M., McCutchan, F. E., Birx, D. L. and Burke, D. S. (2004). Exposure to nonhuman primates in rural Cameroon. Emerging Infectious Diseases 10, 2094–2099.CrossRefGoogle ScholarPubMed
Woodford, M. H., Butynski, T. M. and Karesh, W. B. (2002). Habituating the great apes: the disease risks. Oryx 36, 153–160. doi: 10.1017/S0030605302000224.CrossRefGoogle Scholar
Young, T. P. (1994). Natural die-offs of large mammals: implications for conservation. Conservation Biology 8, 410–418. doi: 10.1046/j.1523-1739.1994.08020410.x.CrossRefGoogle Scholar