Verreaux’s sifaka (Propithecus verreauxi) and ring-tailed lemur (Lemur catta) endoparasitism at the Bezà Mahafaly Special Reserve

Authors

  • James E. Loudon Department of Anthropology East Carolina University Greenville, NC 27858 & Department of Anthropology University of Colorado-Boulder Boulder, CO 80309-0233
  • Michelle L. Sauther Department of Anthropology University of Colorado-Boulder Boulder, CO 80309-0233

DOI:

https://doi.org/10.4314/mcd.v8i1.4

Keywords:

endoparasites, Verreaux’s sifaka, ring-tailed lemur, socioecology, anthropogenic effects, Beza Mahafaly, socio-écologie, Lemur catta, Propithecus verreauxi, effets anthropologiques

Abstract

As hosts, primate behavior is responsible for parasite avoidance and elimination as well as parasite acquisition and transmission among conspecifics. Thus, host behavior is largely responsible for the distribution of parasites in free-ranging populations. We examined the importance of host behavior in acquiring and avoiding parasites that use oral routes by comparing the behavior of sympatric Verreaux’s sifaka (Propithecus verreauxi) and ring-tailed lemurs (Lemur catta) inhabiting the Bezà Mahafaly Special Reserve (BMSR) in Madagascar. For each species, two groups lived in a protected parcel and two groups lived in anthropogenically-disturbed forests. Analysis of 585 fecal samples revealed that the BMSR ring-tailed lemurs harbored six species of nematode worms and three species of protistan parasites. The sifaka harbored only two nematodes. Differences in richness and prevalence appear to be linked to host behavior and the ecological distribution of their parasites. To understand the interplay between behavioral mechanisms to avoid or transmit parasites, we analyzed 683 hours of behavioral observations. BMSR ring-tailed lemurs were observed on the ground significantly more than sifaka and this terrestrial substrate use provides greater opportunities for soil-transmitted parasites to acquire a host. Ring-tailed lemurs using the anthropogenically-disturbed forests harbored parasites not found in the groups inhabiting the protected parcel which they may be acquiring via coprophagy or contact with feces. The arboreality of sifaka allows them to evade most soil-transmitted endoparasites and the patterns of parasitism exhibited by sifaka living in the anthropogenically-disturbed forests did not deviate from the patterns observed among the sifaka living in the protected parcel.

 

RÉSUMÉ

En tant qu’hôtes, les lémuriens interviennent dans l’acquisition et la transmission de parasites entre les individus d’une population, mais aussi sur la prévention et l’élimination de ces parasites. Leur comportement est donc largement responsable de la distribution des parasites au sein d’une population non contrôlée. Dans notre étude, nous avons examiné l’importance des facteurs comportementaux lors de l’acquisition et l’évitement des parasites transmis par voie orale en comparant le comportement des Propithèques de Verreaux (Propithecus verreauxi) et des Makis (Lemur catta) se trouvant dans la Réserve Spéciale du Bezà Mahafaly (RSBM) à Madagascar. Deux groupes de chacune de ces espèces étaient distribués dans une parcelle protégée et deux autres dans des forêts dégradées par l’activité humaine. L’analyse de 585 échantillons fécaux a révélé que les makis de la RSBM étaient infestés par six espèces de nématodes et trois espèces de parasites protistes tandis que les Propithèques de Verreaux ne l’étaient que par deux espèces de nématodes. Les différences de densité et de fréquence auxquelles étaient trouvés les parasites semblaient être liées au comportement des hôtes et à la distribution écologique de leurs parasites. Pour comprendre la relation entre les mécanismes comportementaux et la transmission des parasites, nous avons analysé le comportement des Propithèques et des Makis lors de 683 heures d’observations. Les Makis de la RSBM ont été observés à terre beaucoup plus souvent que les Propithèques. Cette utilisation du substrat terrestre augmente les possibilités des parasites du sol de trouver un hôte. Les Makis se trouvant dans les forêts perturbées étaient infestés de parasites absents des excréments des lémuriens distribués dans la parcelle protégée. Il est possible que les parasites aient été transmis par coprophagie ou par contact avec des matières fécales. La tendance des Propithèques à vivre dans les arbres leur permet d’éviter la contagion par la plupart des parasites liés au sol et le comportement des Propithèques distribués dans les forêts perturbées ne diffère guère de celui des Propithèques distribués dans la parcelle protégée.

Author Biography

James E. Loudon, Department of Anthropology East Carolina University Greenville, NC 27858 & Department of Anthropology University of Colorado-Boulder Boulder, CO 80309-0233

Instructor of Anthropology

References

Altizer, S., Nunn, C. L., Thrall, P. H., et al. 2003. Social organization and parasite risk in mammals: Integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics 34: 517–547. (doi:10.1146/annurev.ecolsys.34.030102.151725)

Altmann, J. 1974. Observational study of behavior: sampling methods. Behaviour 49, 3: 227–266. (doi:10.1163/156853974X00534)

Anderson, R. C. 2000. Nematode Parasites of Vertebrates: Their Development and Transmission. CABI Publishing, Wallingford, UK.

Anderson, R. M. and May, R. M. 1992. Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, Oxford.

Axel, A. C. and Maurer, B. A. 2010. Lemurs in a complex landscape: mapping species density in subtropical dry forests of southwestern Madagascar using data at multiple levels. American Journal of Primatology 73, 1: 38–52. (doi:10.1002/ajp.20872)

Brooks, D. R. and Glen, D. R. 1982. Pinworms and primates: a case study in coevolution. Proceedings of the Helminthological Society of Washington 49, 1: 76–85.

Chabaud, A. G., Petter, A. J. & Golvan, Y. 1961. Les nématodes parasites de lémuriens malgaches. III. Collections récoltées par M. et Mme Francis Petter. Annales de Parasitologie Humaine et Comparée 36, 1–2: 113–126.

Chabaud, A. G., Brygoo, E. R. & Petter A. J. 1965. Les nématodes parasites de lémuriens malgaches VI. Description de six espèces nouvelles et conclusions générales. Annales de Parasitologie Humaine et Comparée 40, 2: 181–214.

Chapman, C. A., Gillespie, T. R. and Goldber, T. L. 2005. Primates and the ecology of their infectious diseases: How will anthropogenic change affect host-parasite interactions? Evolutionary Anthropology 14, 4: 134–144. (doi:10.1002/evan.20068)

Combes, C. 2005. The Art of Being a Parasite. The University of Chicago Press, Chicago.

Dewar, R. E. and Richard, A. F. 2007. Evolution in the hypervariable environment of Madagascar. Proceedings of the National Academy of Sciences of the USA 104, 34: 13723–13727. (doi:10.1073/pnas.0704346104)

Drea, C. M. and Scordato, E. S. 2008.Olfactory communication in the ring-tailed lemur (Lemur catta): form and function of multimodal signals. In: Chemical Signals in Vertebrates 11. J. L Hurst, R. J. Beyon, S. C. Roberts and T. D. Wyatt (eds.), pp 91–102. New Springer, NY.

Dunn, J. J., Columbus, S. T., Aldeen, W. E., Davis, M. and Carroll, K. C. 2002. Trichuris vulpis recovered from a patient with chronic diarrhea and five dogs. Journal of Clinical Microbiology 40, 7: 2703–2704. (doi:10.1128/JCM.40.7.2703-2704.2002)

Fish, K. D., Sauther, M. L., Loudon, J. E. and Cuozzo F. P. 2007. Coprophagy by wild ring-tailed lemurs (Lemur catta) in human-disturbed locations adjacent to the Beza Mahafaly Special Reserve, Madagascar. American Journal of Primatology 69, 6: 713–718. (doi:10.1002/ajp.20392)

Gillespie, T. R. 2006. Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. International Journal of Primatology 27, 4: 1129–1143. (doi: 10.1007/s10764-006-9064-x)

Glen, D. R. and Brooks, D. R. 1985. Phylogenetic relationships of some strongylate nematodes of primates. Proceedings of the Helminthological Society of Washington 52: 227–236.

Graczyk, T. K. and Cranfield, M. R. 2003. Coprophagy and intestinal parasites: implications to human-habituated mountain gorillas (Gorilla gorilla beringei) of the Virunga Mountains and Bwindi Impenetrable Forest. Primate Conservation 9: 58–64.

Hausfater, G. and Meade B. J. 1982. Alternation of sleeping groves by yellow baboons (Papio cynocephalus) as a strategy for parasite avoidance. Primates 23, 2: 287–297. (doi:10.1007/BF02381167)

Huffman, M. A. and Chapman, C. A. 2009. Primate Parasite Ecology: The Dynamics and Study of Host-parasite Relationships. Cambridge University Press, Cambridge.

Junge, R. E., Barrett, M. A. and Yoder, A. D. 2011. Effects of anthropogenic disturbance on indri (Indri indri) health in Madagascar. American Journal of Primatology 73, 7: 632–642. (doi:10.1002/ajp.20938)

Kagei, N., Hayashi, S. and Kato, K. 1986. Human cases of infection with canine whipworms, Trichuris vulpis (Froelich 1789), in Japan. Japanese Journal of Medical Science and Biology 39: 177–184.

Loudon, J. E. 2009. The parasite ecology and socioecology of ring-tailed lemurs (Lemur catta) and Verreaux’s sifaka (Propithecus verreauxi) inhabiting the Beza Mahafaly Special Reserve. Unpubl. Ph.D. thesis, University of Colorado Boulder, Boulder.

Loudon, J. E., Sauther, M. L., Fish, K. D., Hunter-Ishikawa, M. and Ibrahim, Y. J. 2006. One reserve, three primates: applying a holistic approach to understand the interconnections among ring-tailed lemurs (Lemur catta), Verreaux’s sifaka (Propithecus verreauxi), and humans (Homo sapiens) at Beza Mahafaly Special Reserve, Madagascar. Ecological and Environmental Anthropology 2: 54–74.

Moore, J. 2002. Parasites and the Behavior of Animals. Oxford University Press, Oxford.

Muehlenbein, M. P., Schwartz, M. and Richard, A. 2003. Parasitological analysis of the sifaka (Propithecus verreauxi verreauxi) at Beza Mahafaly, Madagascar. Journal of Zoo and Wildlife Medicine 34, 3: 274–277.

Nunn C. L. and Altizer, S. 2006. Infectious Diseases in Primates: Behavior, Ecology, and Evolution. Oxford University Press, Oxford.

Nunn, C. L., Thrall, P. H., Leendertz, F. H. and Boesch, C. 2011. The spread of focally transmitted parasites in socially-structured populations. PLoS ONE 6, 6: e21677. (doi:10.1371/journal.pone.0021677)

Pedersen, A. B., Altizer, S., Poss, M., Cunningham, A. A. and Nunn, C. L. 2005. Patterns of host specificity and transmission among parasites of wild primates. International Journal of Parasitology 35, 6: 647–657. (doi:10.1016/j.ijpara.2005.01.005)

Petter, J. J. 1962. Ecological and behavioral studies of Madagascar lemurs in the field. Annals of the New York Academy of Sciences 102: 267–281. (doi:10.1111/j.1749-6632.1962.tb13645.x)

Raharivololona, B. M. and Ganzhorn, J. U. 2009. Gastrointestinal parasite infection of the Gray mouse lemur (Microcebus murinus) in the littoral forest of Mandena, Madagascar: Effects of forest fragmentation and degradation. Madagascar Conservation & Development 4: 103–112. (doi:10.4314/mcd.v4i2.48650)

Ratsirarson, J. 2003. Réserve Spéciale de Bezà Mahafaly. In: The Natural History of Madagascar. S. M. Goodman and J. P. Benstead (eds.) pp 1520-1525. The University of Chicago Press, Chicago.

Richard, A. F., Dewar, R. E., Schwartz, M. and Ratsirarson, J. 2002. Life in the slow lane? Demography and life histories of male and female sifaka (Propithecus verreauxi verreauxi). Journal of Zoology 256, 4: 421–436. (doi:10.1017/S0952836902000468)

Roberts, L. and Janovy Jr., J. 2008. Foundations of Parasitology. McGraw-Hill, Boston.

Roos, C., Schmitz, J. and Zischler, H. 2004. Primate jumping genes elucidate strepsirrhine phylogeny. Proceedings of the National Academy of Sciences of the USA 101, 29:10650–10654. (doi:10.1073/pnas.0403852101)

del Rosario Robles, M., Loudon, J. E., Kinsella, J. M., et al. 2010. Redescription of Lemuricola (Madoxyuris) bauchoti (Nematoda: Oxyuridae) from Lemur catta in Madagascar. Acta Parasitologica 55: 270–275. (doi:10.2478/s11686-010-0040-4)

Sauther, M. L. 1994. Wild plant use by pregnant and lactating ring-tailed lemurs, with implications for early hominid foraging. In: Eating on the Wild Side. N. L. Etkin (ed.), pp 240–256. The University of Arizona Press, Tuscon.

Sauther, M. L. 1998. Interplay of phenology and reproduction in ring-tailed lemurs: Implications for ring-tailed lemur conservation. Folia Primatologica 69, S1: 309–332. (doi:10.1159/000052719)

Sauther, M. L., Sussman, R. W. and Gould, L. 1999. The socioecology of the ringtailed lemur: Thirty-five years of research. Evolutionary Anthropology 8, 4: 120–132. (doi:10.1002/(SICI)1520-6505(1999)8:4<120::AID-EVAN3>3.0.CO;2-O)

Schwitzer, N., Clough, D., Zahner, H., Kaumanns, W., Kappeler, P. and Schwitzer, C. 2010. Parasite prevalence in blue-eyed black lemurs Eulemur flavifrons in differently degraded forest fragments. Endangered Species Research 12, 3: 215–225. (doi:10.3354/esr00304)

Sengbusch, H. G. 1970. Studies of enterobiasis III: The incidence of pinworm infection in a Mysore school. The Indian Journal of Pediatrics 37, 6: 229–238. (doi:10.1007/BF02807265)

Shahar, R., Horowitz, I. H. and Aizenberg, I. 1995. Disseminated hydatidosis in a ring-tailed lemur (Lemur catta): A case report. Journal of Zoo and Wildlife Medicine 26, 1: 119–122.

Soave, O. and Brand, C. D. 1991. Coprophagy in animals: a review. Cornell Veterinarian 81: 357–364.

Sussman, R. W. 1991. Demography and social organization of free-ranging Lemur catta in the Beza Mahafaly Reserve, Madagascar. American Journal of Physical Anthropology 84, 1: 43–58. (doi:10.1002/ajpa.1330840105)

Sussman, R. W. and Rakotozafy, A. 1994. Plant diversity and structural analysis of a tropical dry forest in southwestern Madagascar. Biotropica 26, 3: 241–254. (doi:10.2307/2388845)

Vitone, N. D., Altizer, S. and Nunn, C. L. 2004. Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates. Evolutionary Ecology Research 6: 183–189.

Whitelaw, D., Sauther, M. L., Loudon, J. E. and Cuozzo, F. 2005. Abstracts of AAPA poster and podium presentations. Anthropogenic change in and around Beza-Mahafaly reserve: methodology and results. American Journal of Physical Anthropology 126, S40: 222. (doi:10.1002/ajpa.20217)

Wright, P. C., Arrigo-Nelson, S. J., Hogg, K. L., et al. 2009. Habitat disturbance and seasonal fluctuations of lemur parasites in the rain forest of Ranomafana National Park, Madagascar. In: Primate Parasite Ecology: The Dynamics and Study of Host-parasite relationships. M.A. Huffman and C.A. Chapman (eds.), pp 311–330. Cambridge University Press, Cambridge.

Zajac, A. M. and Conboy, G. A. 2006. Veterinary Clinical Parasitology. Blackwell Publishing, West Sussex.

Verreaux’s sifaka (Propithecus verreauxi) and ring-tailed lemur (Lemur catta) endoparasitism at the Bezà Mahafaly Special Reserve; Journal Madagascar Conservation & Development

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18-06-2013

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