Effect of socio-ecological factors and parasite infection on body condition of Brown Mouse Lemur Microcebus rufus (Mammalia: Primates: Cheirogaleidae)

Authors

  • Andry Herman Rafalinirina University of Antananarivo, Mention Anthropobiology and Longterm Development, Study group and Research of Primates (GERP), Antananarivo 101, Madagascar. https://orcid.org/0000-0003-4856-7594 (unauthenticated)
  • Jeannot Randrianasy University of Antananarivo, Mention Anthropobiology and Longterm Development, Antananarivo 101, Madagascar.
  • Patricia C. Wright Stony Brook University, Departement of Anthropology, New York 11794-4364, USA.
  • Jonah Ratsimbazafy Study Group and Research of Primates (GERP), Antananarivo 101, Madagascar. https://orcid.org/0000-0002-7629-0476 (unauthenticated)

DOI:

https://doi.org/10.11609/jott.4799.11.6.13632-13643

Keywords:

Condition index, infectious disease, Ranomafana National Park, southeastern Madagascar, volume index

Abstract

Various studies in ecology have shown the relationship between body condition and parasitic loads in nonhuman primates, however, little information is available regarding prosimians such as lemurs.  In this study, the synergistic effect of parasite infection and socio-ecological factors on the body condition of Microcebus rufus in the family Cheirogaleidae was analyzed in Ranomafana National Park in southeastern Madagascar.  This lemur species is characterized by its ability to adapt to different types of forest, and by seasonal fattening.  Based on the factors considered, this species is, therefore, a good model for the study of body condition and ecology of infectious diseases in lemurs. Floatation and direct observation techniques were used for examination of parasite infection.  Two indices considering body condition were analyzed: volume index (VI) and condition index (CI), the residual between the mass observed and the corrected mass.  The generalized linear mixed model (GLMM) was used to model the synergistic effect of parasite infections and socio-ecological factors on variation in body condition, with the identity of individuals used as a random factor.  We identified five species of helminths, one species of protist, and one species of lice which infected the 204 mouse lemurs captured.  There was a sexual difference for all measures of the parasite infection.  The more parasite species an individual was infected with, the smaller was its body size according to the Volume Index that reflects deposits of subcutaneous fat.  Individuals with more positive Condition Index values, particularly females, excreted more parasite eggs or oocyst in their faecal matter.  The results suggest that an individual’s body condition constitutes an indicator of risk of parasite infection and transmission. 

Author Biographies

  • Andry Herman Rafalinirina, University of Antananarivo, Mention Anthropobiology and Longterm Development, Study group and Research of Primates (GERP), Antananarivo 101, Madagascar.

    Rafalinirina andry Herman is the coordinator of gerp's project, he is a membre of IUCN primate specialist group section Madagascar and a part-time lecture at the University of Antananarivo, mention Anthropobiology and Long term development

  • Jeannot Randrianasy, University of Antananarivo, Mention Anthropobiology and Longterm Development, Antananarivo 101, Madagascar.

    Randrianasy Jeannot is the director of primate laboratory at the University of Antananarivo, mention Anthropobiology and long term development

  • Patricia C. Wright, Stony Brook University, Departement of Anthropology, New York 11794-4364, USA.

    Dr. Patricia Wright is a distinguised service professorat département anthropologue  stony Brook University, she is also the founder and executive director of valbio research station ranomafana Madagascar and fonder and executive director of Institute for conservation of tropical environements

  • Jonah Ratsimbazafy, Study Group and Research of Primates (GERP), Antananarivo 101, Madagascar.

    Pr Jonah Ratsimbazafy is the président of GERP,vice co-chair of IUCN primate specialist group Madagascar section, director of Houston zoo Madagascar program, adjunct professorat at the faculty of sciences

References

Aivelo, T. (2015). Longitudinal Monitoring of Parasites in Individual Wild Primates. (Vol. 2). University of Helsinki, 52pp. https://doi.org/10.13140/RG.2.1.2218.0563.

Altizer, S., C.L. Nunn & P. Lindenfors, (2007). Do threatened hosts have fewer parasites? A comparative study in primates. Journal of Animal Ecology 76: 304–314.

Alzaga, V., J. Vicente, D. Villanua, P. Acevedo, F. Casas & C. Gortazar (2008). Body condition and parasite intensity correlates with escape capacity in Iberian hares (Lepus granatensis). Behavioral Ecology and Sociobiology 62: 769–775. https://doi.org/10.1007/s00265-007-0502-3.

Atsalis, S. (1999). Seasonal fluctuation in body fat and activity levels in a rain-forest species of Mouse lemur, Microcebus rufus. International Journal of Primatology 20(6): 883–910. https://doi.org/10.1023/A:1020826502103.

Beldomenico, P.M. & M. Begon (2010). Disease spread, susceptibility and infection intensity: vicious circles? Trends in Ecology and Evolution 25(1): 21–27. https://doi.org/10.1016/j.tree.2009.06.015

Bize, P., C. Jeanneret, A. Klopfenstein & A. Roulin (2008). What makes a host profitable? Parasites balance host nutritive resources against immunity. American Naturalist 171(1):107–118; http://doi.org/10.1086/523943

Chapman, C.A., M.D. Wasserman, T.R. Gillespie, M.L. Speirs, M.J. Lawes, T.L. Saj & T.E. Ziegler (2006). Do food avalaibility, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments? American Journal of Physical Anthropology 131(4): SN 1096–8644. https://doi.org/10.1002/ajpa.20477

Coop, R.L., & P.H. Holmes (1996). Nutrition and parasite interaction. International Journal for Parasitology 26, 8–9:951–962. https://doi.org/10.1016/S0020-7519(96)80070-1

Dryden, M.W., P.A. Payne, R. Ridley & V. Smith (2005). Comparison of Common Fecal Flotation Techniques for the Recovery of Parasite Eggs and Oocysts. Spring Veterinary Therapeutics 6(1): 15–28.

Durden, L.A., S. Zohdy, J. Laakkonen (2010). Lice and Ticks of the Eastern Rufous Mouse Lemur, Microcebus rufus, with Descriptions of the Male and Third Instar Nymph of Lemurpediculus verruculosus (Phthiraptera: Anoplura). Journal of Parasitology 96(5): 874–878. https://doi.org/10.1645/GE-2512.1

Esch, G. & J.C. Fernandez (1993). A Functional Biology of Parasitism: Ecological and Evolutionary Implications. Chapman and Hall, London, 289pp.

Ezenwa, V.O., R.S. Etienne, G. Luikart, A. Beja-Pereira & A. E. Jolles, (2010). Hidden consequences of living in a wormy World: Nematode-induced immune suppression facilitates tuberculosis invasion in African buffalo. The American Naturalist 176(5): 613–624. https://doi.org/10.1086/656496

Gillespie, T.R. (2006). Non-invasive Assessment of Gastrointestinal Parasite Infections in Free Ranging Primates. International Journal of Primatology 27: 1129. https://doi.org/10.1007/s10764-006-9064-x

Gillespie, T.R., E.C. Greiner & C.A. Chapman (2005). Gastrointestinal parasites of the colobus monkeys of Uganda. Journal of Parasitology 92: 569–573.

Gillespie, T.R. & C.A. Chapman (2008). Forest fragmentation, the decline of an endangered primate, and changes in host-parasite interactions relative to an unfragmented forest. American Journal of Primatology 70: 222–230.

Green, A.J. (2001). Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82(5):1473–1483. https://doi.org/10.1890/0012-9658(2001)082[1473:MLRMOB]2.0.CO;2

Hochachka, V.W. & A.A. Dhondt, (2000). Density-dependent decline of host abundance resulting from a new infectious disease. Proceedings of the National Academy of Science 97: 5303–5306.

Hudson, P.J., A.P. Dobson, & D. Newborn (1998). Prevention of population cycles by parasite removal. Science 282: 2256–2258.

Hudson, P.J., A. Rizzoli, B.T. Grenfell, H. Heesterbeek & A.P. Dobson (2002). The Ecology of Wildlife Disease. Oxford University Press, 240pp.

Kappeler, P.M. & C.P. Van Schaik (2002). Evolution of primate social systems. International Journal of Primatology, 23(4): 707-740.

Kappeler, P.M., S. Cremer & C.L. Nunn (2015). Sociality and health: impacts of sociality on disease susceptibility and transmission in animal and human societies. Philosophical Transaction of the Royal Society B: Biological Sciences 370(1669) https://doi.org/10.1098/rstb.2014.0116

Kessler, S.E., U. Radespiel, K. Schaber & C. Strube (2015). Tiny samples from tiny lemurs: methodological considerations for endoparasite analyses in mouse lemurs, pp210–219. In: Lehman S.M., Radespiel U., Zimmermann E. (eds.). Biology, Behavior, and Conservation Biogeography of the Cheirogaleidae. Cambridge University Press, Cambridge, 570pp.

Labocha, M.K., H. Schutz, & J.P. Hayes (2014). Which body condition index is best? (June 2013): 111–119. https://doi.org/10.1111/j.1600-0706.2013.00755

Loudon, J., M. Howell & A. Fuentes (2006). The importance of integrative anthropology: a preliminary investigation employing primatological and cultural anthropological data collection methods in assessing human-monkey co-existence in Bali, Indonesia. Ecological and Environmental Anthropology 2(1): 2–13.

Martin, L.B., A. Scheurlein II & M. Wikelski, (2003). Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proceedings of the Royal Society of London, B 270:153–158. https://doi.org/10.1 098/rspb.2002.2185

May, R.M. (1988). Conservation and disease. Conservation Biology 2(1): 28–30. https://doi.org/10.1111/j.1 523-1739.1988.tb00332.x

Munyeme, M., H.M. Munang’andu, J.B. Muma, A.M. Nambota, D. Biffa & V.M. Siamudaala (2010). Investigating effects of parasite infection on body condition of the Kafue lechwe (Kobus leche kafuensis) in the Kafue basin. BMC Research Notes 3: #346. https://doi.org/10.11 86/1756-0500-3-346

Murray, D.L., L.B. Keith & J.R. Cary (1998). Do parasitism and nutritional status interact to affect production in snowshoe hares? Ecology 79: 1209–1222.

Neuhaus, P. (2003). Parasite removal and its impact on litter size and body condition in Columbian ground squirrels (Spermophilus columbianus). Biology Letters 270(2): 213–215. https://doi.org/10.1098/rsbl.2003.0073

Peig, J., A.J. Green & C. Ame (2009). New perspectives for estimating body condition from mass / length data: the scaled mass index as an alternative method, (May). https://doi.org/10.1111/j.1600-0706.2009.17643

Radespiel U., K. Schaber & S.E. Kessler (2015). Variations in the excretion patterns of helminth eggs in two sympatric mouse lemur species (Microcebus murinus and Microcebus ravelobensis) in northwestern Madagascar: 941–954.

Rafalinirina, A.H., T. Aivelo, J. Randrianasy & P.C. Wright (2015). Comparison of parasitic infections and body condition in rufous mouse lemurs (Microcebus rufus) at Ranomafana National Park, southeast Madagascar. Madagascar Conservation & Development 10(2): 60–66. https://doi.org/10.4314/mcd.v10i2.4

Raharivololona, B.M. (2009). Parasites gastro-intestinaux de Microcebus murinus de la forêt littorale de Mandena, Madagascar. Madagascar Conservation & Development 4: 52-62.

Rodriguez-Zaragoza, S. (1994). Ecology of free-living amoebas. Crit Rev Microbiol 20: 225–241.

Sánchez-Villagra M.R., T.R. Pope & V. Salas (1998). Relation of intergroup variation in allogrooming to group social structure and ectoparasite loads in red howlers (Alouatta seniculus). International Journal of Primatology 19(3): 473-491.

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

Seppälä, O., K. Liljeroos, A. Karvonen & J. Jokela (2008). Host condition as a constraint for parasite reproduction. Oikos 117(5): 749–753; https://doi.org/10.1111/j.0030-1299.2008.1 6396.x

Sheldon, B.C. & S. Verhulst (1996). Ecological immunity: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution 1: 317–321.

Silk, J.B. (1986). Social behavior in evolutionary perspective, pp318–329. In: Smuts, B.B., D.L. Cheney, R.M. Seyfarth, R.W. Wrangham & T.T. Struhsaker (eds.). Primate Societies. University of Chicago Press, Chicago, xi+578pp.

Stevenson, R.D. & W.A.Jr. Woods (2006). Condition indices for conservation: new uses for evolving tools. Integrative and Comparative Biology 46: 1169–1190.

Tompkins, D.M., A.M. Dunn, M.J. Smith & S. Telfer (2011). Wildlife diseases: from individuals to ecosystems. Journal of Animal Ecology 80(1): 19–38. https://doi.org/10.1111/j.1365-2656.2010.01742.x

Wilford, O. (1986). Animal Parasites: Their Life Cycles and Ecology. Dover Publications, New York, 564pp.

Willis, C. & R. Poulin (1999). Effects of the tapeworm Hymenolepis diminuta on maternal investement in rats. Canadian Journal of Zoology 77(6): 1001–1005. https://doi.org/10.11 39/z99-075

Wright, P. C. & B.A. Andriamihaja (2002). Making a rain forest national park work in Madagascar: Ranomafana National Park and its long-term research commitment, pp112–136. In: Terborgh, J., C. van Schaik, M. Rao & L. Davenport (eds.). Making Parks Work: Strategies for Preserving Tropical Nature Island Press, Washington D.C., 511pp.

Wright, P.C. (1992). Primate ecology, rainforest conservation and economic development: Building a national park in Madagascar. Evolutionary Anthropology 1(1): 25–33. https://doi.org/10.1002/evan.1360010108

Wright, P.C., S.J. Arrigo-Nelson, K.L. Hogg, B. Bannon, T.L. Morelli et al. (2009). Habitat disturbance and seasonal fluctuations of lemur parasites in the rainforest of Ranomafana National Park, Madagascar, pp 311–330 In: Huffman, M.A. & C.A. Chapman (eds.) Primate Parasite Ecology: The Dynamics and Study of Host-Parasite Relationships. Cambridge University Press, London, 548pp.

Zuur, A.F., E.N. Leno & C.S. Elphick (2010). A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1: 3–14. https://doi.org/10.1111/j.2041-210X.2009.00001.x

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26-04-2019

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