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The Effects of Habitat Disturbance on Lemurs at Ranomafana National Park, Madagascar

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Abstract

The alarming rate of deforestation in Madagascar is driving some endemic primates to extinction. Surprisingly, anthropogenic habitat disturbance is not always deleterious. The effect of disturbance on lemur abundance may be related to diet, with frugivorous species more prone to population declines than folivores or insectivores. To test the effects of disturbance on lemur abundance and group size, we surveyed 2 sites within contiguous forest at Ranomafana National Park, 1 lightly disturbed primary forest (Vato) and 1 heavily logged forest (Tala). We quantified forest structure variables along 6 survey routes and conducted 68 diurnal and 42 nocturnal lemur surveys. Canopy closure, canopy height, and understory visibility were greater in Vato than in Tala. We encountered 2 frugivorous lemurs (Eulemur rufifrons, Varecia variegata) and 1 folivore (Avahi peyrierasi) significantly more frequently in Vato than in Tala, whereas the opposite was true for the insectivorous Microcebus rufus. Rates did not differ statistically for 1 frugivore (Eulemur rubriventer) and 2 folivores (Propithecus edwardsi, Hapalemur griseus). Comparisons across the 6 survey routes suggest that the abundance was heterogeneous within as well as between sites. Neither group size nor composition differed between sites. Encounter rates for Varecia variegata were positively related to canopy closure, and encounter rates for Avahi peyrierasi were positively related to canopy height. Encounter rates for Microcebus rufus were negatively related to canopy closure, height, and understory visibility. Similar to other studies, the results suggest that some lemurs, including folivores, may cope with anthropogenic disturbance better than others, including some frugivores. Lemur abundance is heterogeneous, though, even on small spatial scales.

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References

  • Arrigo-Nelson, S. J. (2006). The impact of habitat disturbance on the feeding ecology of the Milne-Edwards' sifaka (Propithecus edwardsi) in Ranomafana National Park, Madagascar. Ph.D. dissertation, State University of New York, Stony Brook.

  • Arrigo-Nelson, S. J., & Wright, P. C. (2004). Survey results from Ranomafana National Park: new evidence for the effects of habitat preference and disturbance on the distribution of Hapalemur. Folia Primatologica, 75, 331–334.

    Article  Google Scholar 

  • Atsalis, S. (2007). A natural history of the brown mouse lemur. Upper Saddle River, NJ: Pearson Prentice-Hall.

    Google Scholar 

  • Balko, E. A. (1998). A behaviorally plastic response to forest composition and logging disturbance by Varecia variegata variegata in Ranomafana National Park, Madagascar. Ph.D. dissertation, State University of New York, Syracuse.

  • Balko, E. A., & Underwood, H. (2005). Effects of forest structure and composition on food availability for Varecia variegata at Ranomafana National Park, Madagascar. American Journal of Primatology, 66, 45–70.

    Article  PubMed  Google Scholar 

  • Buckland, S. T., Anderson, D. R., Burnham, K. P., Laake, J. L., Borchers, D. L., & Thomas, L. (2001). Introduction to distance sampling: Estimating abundance of biological populations. Oxford: Oxford University Press.

    Google Scholar 

  • Buckland, S., Plumptre, A., Thomas, L., & Rexstad, E. (2010). Design and analysis of line transect surveys for primates. International Journal of Primatology, 31, 833–847.

    Article  Google Scholar 

  • Chapman, C. A., & Chapman, L. J. (2000a). Constraints on group size in red colobus and red-tailed guenons: Examining the generality of the ecological constraints model. International Journal of Primatology, 21, 565–585.

    Article  Google Scholar 

  • Chapman, C. A., & Chapman, L. J. (2000b). Determinants of group size in social primates: The importance of travel costs. In S. Boinski & P. Garber (Eds.), Group movement in social primates and other animals: Patterns, processes, and cognitive implications (pp. 24–42). Chicago: University of Chicago Press.

    Google Scholar 

  • Chapman, C. A., Chapman, L. J., Bjorndal, K. A., & Onderdonk, D. A. (2002). Application of protein-to-fiber ratios to predict colobine abundance on different spatial scales. International Journal of Primatology, 23, 283–310.

    Article  Google Scholar 

  • Chapman, C. A., Struhsaker, T., & Lambert, J. (2005). Thirty years of research in Kibale National Park, Uganda, reveals a complex picture for conservation. International Journal of Primatology, 26, 539–555.

    Article  Google Scholar 

  • Dehgan, A. (2003). The behavior of extinction: Predicting the incidence and local extinction of lemurs in fragmented habitats of southeastern Madagascar. Ph.D. dissertation, University of Chicago.

  • Duckworth, J. W. (1998). The difficulty of estimating population densities of nocturnal forest mammals from transect counts of animals. Journal of Zoology (London), 246, 443–486.

    Article  Google Scholar 

  • Dufils, J. (2003). Remaining forest cover. In S. Goodman & J. Benstead (Eds.), The natural history of Madagascar (pp. 88–96). Chicago: University of Chicago Press.

    Google Scholar 

  • Erhart, E. M., & Overdorff, D. J. (2008). Population demography and social structure changes in Eulemur fulvus rufus from 1988 to 2003. American Journal of Physical Anthropology, 136, 183–193.

    Article  PubMed  Google Scholar 

  • Faulkner, A. L., & Lehman, S. M. (2006). Feeding patterns in a small-bodied nocturnal folivore (Avahi laniger) and the influence of leaf chemistry: a preliminary study. Folia Primatologica, 77, 218–227.

    Article  CAS  Google Scholar 

  • Ganzhorn, J. U. (1992). Leaf chemistry and the biomass of folivorous primates in tropical forests. Oecologia, 91, 540–547.

    Article  Google Scholar 

  • Ganzhorn, J. U. (1995). Low-level forest disturbance effects on primary production, leaf chemistry, and lemur populations. Ecology, 76, 2084–2096.

    Article  Google Scholar 

  • Ganzhorn, J. U. (2003). Habitat description and phenology. In J. Setchell & D. Curtis (Eds.), Field and laboratory methods in primatology (pp. 40–56). Cambridge: Cambridge University Press.

    Google Scholar 

  • Ganzhorn, J. U., Langrand, O., Wright, P. C., O’Connor, S., Rakotosamimanana, B., Feistner, A. T. C., et al. (1997). The state of lemur conservation in Madagascar. Primate Conservation, 17, 70–86.

    Google Scholar 

  • Ganzhorn, J. U., Malcomber, S., Adrianantoanina, O., & Goodman, S. M. (1997). Habitat characteristics and lemur species richness in Madagascar. Biotropica, 29, 331–343.

    Article  Google Scholar 

  • Ganzhorn, J. U., Wright, P. C., & Ratsimbazafy, J. (1999). Primate communities: Madagascar. In J. Fleagle, C. Janson, & K. Reed (Eds.), Primate communities (pp. 75–89). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Ganzhorn, J. U., Lowry, P. P., Schatz, G. E., & Sommer, S. (2001). The biodiversity of Madagascar: one of the world’s hottest hotspots on its way out. Oryx, 35, 346–348.

    Google Scholar 

  • Ganzhorn, J. U., Goodman, S. M., & Dehgan, A. (2003). Effects of forest fragmentation on small mammals and lemurs. In S. Goodman & J. Benstead (Eds.), The natural history of Madagascar (pp. 1228–1234). Chicago: University of Chicago Press.

    Google Scholar 

  • Garbutt, N. (2007). Mammals of Madagascar: a complete guide. New Haven: Yale University Press, p. 177.

  • Grassi, C. (2001). The behavioral ecology of Hapalemur griseus griseus: The influence of microhabitat and population density on this small-bodied prosimian folivore. Ph.D. dissertation, University of Texas, Austin.

  • Grassi, C. (2006). Variability in habitat, diet, and social structure of Hapalemur griseus in Ranomafana National Park, Madagascar. American Journal of Physical Anthropology, 131, 50–63.

    Article  PubMed  Google Scholar 

  • Groeneveld, L. F., Blanco, M. B., Raharison, J. L., Rahalinarivo, V., Rasoloarison, R. M., Kappeler, P. M., et al. (2010). MtDNA and nDNA corroborate existence of sympatric dwarf lemur species at Tsinjoarivo, eastern Madagascar. Molecular Phylogenetics and Evolution, 55, 833–845.

    Article  PubMed  Google Scholar 

  • Harper, G. J., Steininger, M. K., Tucker, C. J., Juhn, D., & Hawkins, F. (2007). Fifty years of deforestation and forest fragmentation in Madagascar. Environmental Conservation, 34, 325–333.

    Article  Google Scholar 

  • Irwin, M. T. (2008). Diademed sifaka (Propithecus diadema) ranging and habitat use in continuous and fragmented forest: higher density but lower viability in fragments? Biotropica, 40, 231–240.

    Article  Google Scholar 

  • Irwin, M. T., Johnson, S. E., & Wright, P. C. (2005). The state of lemur conservation in south-eastern Madagascar: population and habitat assessments for diurnal and cathemeral lemurs using surveys, satellite imagery and GIS. Oryx, 39, 204–218.

    Article  Google Scholar 

  • Irwin, M. T., Raharison, J. L., & Wright, P. C. (2009). Spatial and temporal variability in predation on rainforest primates: do forest fragmentation and predation act synergistically? Animal Conservation, 12, 220–230.

    Article  Google Scholar 

  • Irwin, M. T., Wright, P. C., Birkinshaw, C., Fisher, B. L., Gardner, C. J., Glos, J., et al. (2010). Patterns of species change in anthropogenically disturbed forests of Madagascar. Biological Conservation, 143, 2351–2362.

    Article  Google Scholar 

  • Johns, A., & Skorupa, J. (1987). Responses of rain-forest primates to habitat disturbance: a review. International Journal of Primatology, 8, 157–191.

    Article  Google Scholar 

  • Johnson, S. E., & Overdorff, D. J. (1999). Census of brown lemurs (Eulemur fulvus sspp.) in southeastern Madagascar: methods-testing and conservation implications. American Journal of Primatology, 47, 51–60.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, S. E., Irwin, M. T., Wright, P. C., Arrigo-Nelson, S. J., Grassi, C., Samonds, K. E., et al. (2003). Natural and anthropogenic influences on lemur population structure in southeastern Madagascar. American Journal of Physical Anthropology, 120, 123.

    Article  Google Scholar 

  • Keppel, G., & Wickens, T. (2004). Design and analysis: A researcher’s handbook. Pearson Prentice-Hall: Upper Saddle River, NJ.

    Google Scholar 

  • Lehman, S. M. (2007). Spatial variations in Eulemur fulvus rufus and Lepilemur mustelinus densities in Madagascar. Folia Primatologica, 78, 46–55.

    Article  Google Scholar 

  • Lehman, S. M., Rajaonson, A., & Day, S. (2006a). Edge effects on the density of Cheirogaleus major. International Journal of Primatology, 27, 1569–1588.

    Article  Google Scholar 

  • Lehman, S. M., Rajaonson, A., & Day, S. (2006b). Lemur responses to edge effects in the Vohibola III classified forest, Madagascar. American Journal of Primatology, 68, 293–299.

    Article  PubMed  Google Scholar 

  • Lehman, S. M., Ratsimbazafy, J., Rajaonson, A., & Day, S. (2006c). Decline of Propithecus diadema edwardsi and Varecia variegata variegata (Primates: Lemuridae) in south-east Madagascar. Oryx, 40, 108–111.

    Article  Google Scholar 

  • Lehtonen, J., Mustonen, O., Ramiarinjanahary, H., Niemelä, J., & Rita, H. (2001). Habitat use by endemic and introduced rodents along a gradient of forest disturbance in Madagascar. Biodiversity and Conservation, 10, 1185–1202.

    Article  Google Scholar 

  • Lowry, P. P., Schatz, G. E., & Phillipson, P. B. (1997). The classification of natural and anthropogenic vegetation in Madagascar. In S. M. Goodman & B. D. Patterson (Eds.), Natural change and human impact in Madagascar (pp. 93–123). Washington, DC: Smithsonian Institution Press.

    Google Scholar 

  • Mittermeier, R. A., Wallis, J., Rylands, A. B., Ganzhorn, J. U., Oates, J. F., Williamson, E. A., et al. (2009). Primates in peril: the world’s 25 most endangered primates 2008–2010. Primate Conservation, 24, 1–57.

    Article  Google Scholar 

  • Mittermeier, R. A., Louis, E. E., Richardson, M., Schwitzer, C., Langrand, O., Rylands, A. B., et al. (2010). Lemurs of Madagascar (3rd ed.). Arlington, VA: Conservation International.

    Google Scholar 

  • Morriss, D. H., Arrigo-Nelson, S. J., Karpanty, S. M., Gerber, B. D., & Wright, P. C. (2009). Ranging behavior flexibility in response to habitat disturbance by Milne-Edwards’ sifakas (Propithecus edwardsi) in Ranomafana National Park. American Journal of Physical Anthropology, 138, 194.

    Google Scholar 

  • Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403, 853–858.

    Article  PubMed  CAS  Google Scholar 

  • Overdorff, D. J. (1991). Ecological correlates to social structure in two prosimian primates: Eulemur fulvus rufus and Eulemur rubriventer in Madagascar. Ph.D. dissertation, Duke University, Durham, NC.

  • Overdorff, D. J. (1996). Ecological correlates to activity and habitat use of two prosimian primates: Eulemur rubriventer and Eulemur fulvus rufus in Madagascar. American Journal of Primatology, 40, 327–342.

    Article  Google Scholar 

  • Plumptre, A., & Cox, D. (2006). Counting primates for conservation: primate surveys in Uganda. Primates, 47, 65–73.

    Article  PubMed  Google Scholar 

  • Pochron, S. T., Tucker, W. T., & Wright, P. C. (2004). Demography, life history, and social structure in Propithecus diadema edwardsi from 1986–2000 in Ranomafana National Park, Madagascar. American Journal of Physical Anthropology, 125, 61–72.

    Article  PubMed  Google Scholar 

  • Siegel, S., & Castellan, N. J. (1988). Nonparametric statistics for the behavioral sciences. New York: McGraw-Hill.

    Google Scholar 

  • Skorupa, J. (1988). The effects of selective timber harvesting on rainforest primates in Kibale Forest, Uganda. Ph.D. dissertation, University of California at Davis, Davis.

  • Struhsaker, T. T. (1997). Ecology of an African rainforest: Logging in Kibale and the conflict between conservation and exploitation. Gainesville: University Press of Florida.

    Google Scholar 

  • Tabachnick, B. G., & Fidell, L. S. (2007). Using multivariate statistics (5th ed.). New York: Allyn and Bacon.

    Google Scholar 

  • Tan, C. L. (1999). Group composition, home range size, and diet of three sympatric bamboo lemur species (Genus Hapalemur) in Ranomafana National Park, Madagascar. International Journal of Primatology, 20, 547–566.

    Article  Google Scholar 

  • Tecot, S. R. (2008). Seasonality and predictability: The hormonal and behavioral responses of the red-bellied lemur (Eulemur rubriventer) in Ranomafana National Park, southeastern Madagascar. Ph.D. dissertation, University of Texas, Austin.

  • White, F. J., Overdorff, D. J., Balko, E. A., & Wright, P. C. (1995). Distribution of ruffed lemurs (Varecia variegata) in Ranomafana National Park, Madagascar. Folia Primatologica, 64, 124–131.

    Article  Google Scholar 

  • Whitesides, G. H., Oates, J. F., Green, S. M., & Kluberdanz, R. P. (1988). Estimating primate densities from transects in a west African rain forest: a comparison of techniques. The Journal of Animal Ecology, 57, 345–367.

    Article  Google Scholar 

  • Worman, C., & Chapman, C. (2006). Densities of two frugivorous primates with respect to forest and fragment tree species composition and fruit availability. International Journal of Primatology, 27, 203–225.

    Article  Google Scholar 

  • Wright, P. C. (1995). Demography and life history of free-ranging Propithecus diadema edwardsi in Ranomafana National Park, Madagascar. International Journal of Primatology, 16, 835–854.

    Article  Google Scholar 

  • Wright, P. C. (1998). Impact of predation risk on the behaviour of Propithecus diadema edwardsi in the rainforest of Madagascar. Behaviour, 135, 483–512.

    Google Scholar 

  • Wright, P. C. (1999). Lemur traits and Madagascar ecology: coping with an island environment. Yearbook of Physical Anthropology, 110, 31–72.

    Article  Google Scholar 

  • Wright, P. C., & Andriamihaja, B. R. (2002). Making a rainforest national park work in Madagascar: Ranomafana National Park and its long-term research commitment. In J. Terborgh, C. van Schaik, L. Davenport, & M. Rao (Eds.), Making parks work: Strategies for preserving tropical nature (pp. 112–136). Washington, DC: Island Press.

    Google Scholar 

  • Wright, P. C., Heckscher, S. K., & Dunham, A. E. (1997). Predation on Milne-Edwards’ sifaka (Propithecus diadema edwardsi) by the fossa (Cryptoprocta ferox) in the rainforest of southeastern Madagascar. Folia Primatologica, 68, 34–43.

    Article  CAS  Google Scholar 

  • Wright, P. C., Razafindratsita, V. R., Pochron, S. T., & Jernvall, J. (2005). The key to Madagascar frugivores. In J. L. Dew & J. P. Boubli (Eds.), Tropical fruits and frugivores (pp. 121–138). Dordrecht: Springer.

    Chapter  Google Scholar 

  • Wright, P. C., Andriamihaja, B. R., & Raharimiandra, S. A. (2005). Tanala synecological relations with lemurs in southeastern Madagascar. In J. Paterson & J. Wallis (Eds.), Commensalism and conflict: The human-primate interface (pp. 118–145). Norman, OK: American Society of Primatologists.

    Google Scholar 

  • Wright, P. C., Johnson, S. E., Irwin, M. T., Jacobs, R. L., Schlitchting, P., Lehman, S. M., et al. (2008). The crisis of the critically endangered bamboo lemur (Prolemur simus). Primate Conservation, 23, 5–17.

    Article  Google Scholar 

  • Wright, P. C., Arrigo-Nelson, S. J., Hogg, K. L., Bannon, B., Morelli, T. L., Wyatt, J., et al. (2009). Habitat disturbance and seasonal fluctuations of lemur parasites in the rainforest of Ranomafana National Park, Madagascar. In M. Huffman & C. Chapman (Eds.), Primate parasite ecology: The dynamics and study of host-parasite relationships (pp. 311–330). Cambridge: Cambridge University Press.

    Google Scholar 

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Acknowledgments

We thank the Malagasy government and ANGAP for allowing us to conduct research in Madagascar. We thank ICTE, MICET, and the Centre ValBio for essential logistic and research support and our research technicians Rasendry Nirina Victor, Rajafindrakoto Georges, and Rakotonirina Andriamananatena Thierry Emile. We thank S. Green for his contribution and review of earlier versions of this manuscript and C. Borries, A. Koenig, 2 anonymous reviewers, and J. Setchell for their feedback and helpful comments that greatly improved the manuscript. Funds were provided by the University of Miami Beyond the Book Research Scholarship (J. P. Herrera), the National Science Foundation Research Experience for Undergraduates supplemental award to (NSF grant no. 0721233), Research Foundation award no. 1065277/43993 (P. C. Wright), and the NSF Graduate Research Fellowship, which supported J. P. Herrera during the writing of the manuscript.

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  1. Interdepartmental Doctoral Program in Anthropological Sciences, Stony Brook University, Stony Brook, NY, 11794, USA

    James P. Herrera

  2. Department of Anthropology, University of Miami, Coral Gables, FL, 33124, USA

    James P. Herrera & Linda L. Taylor

  3. Department of Anthropology, Stony Brook University, Stony Brook, NY, 11794, USA

    Patricia C. Wright

  4. Centre ValBio, BP33 Ranomafana, 312, Ifanadiana, Madagascar

    Patricia C. Wright

  5. Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY, 11794, USA

    Elise Lauterbur

  6. Department of Animal Behavior, University of Antananarivo, Antananarivo, 101, Madagascar

    Lantonirina Ratovonjanahary

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Herrera, J.P., Wright, P.C., Lauterbur, E. et al. The Effects of Habitat Disturbance on Lemurs at Ranomafana National Park, Madagascar. Int J Primatol 32, 1091–1108 (2011). https://doi.org/10.1007/s10764-011-9525-8

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