International Journal of Primatology

, Volume 37, Issue 3, pp 371–389 | Cite as

Estimating Encounter Rates and Densities of Three Lemur Species in Northeastern Madagascar

  • Asia J. MurphyEmail author
  • Zach J. Farris
  • Sarah Karpanty
  • Felix Ratelolahy
  • Marcella J. Kelly


Primate populations, including Madagascar’s lemurs, are threatened worldwide and conservationists need accurate population estimates to develop targeted conservation plans. We sought to fill knowledge gaps for three lemur taxa —white-fronted brown lemur (Eulemur albifrons); eastern woolly lemur (Avahi laniger); and Allocebus/Microcebus, a category combining observations of hairy-eared dwarf lemurs (Allocebus trichotis) and mouse lemurs (Microcebus spp.)— in northeastern Madagascar by estimating their density, examining how their encounter rates and densities vary across three different forest types, and monitoring trends in encounter rates and densities at resurveyed sites, using data from surveys at six forest sites over a 4-year period (2010–2013). Landscape density for white-fronted brown lemur, eastern woolly lemur, and Allocebus/Microcebus was 21.5 (SE 3.67), 57.7 (SE 9.17), and 39.1 (SE 9.55) individuals/km2, respectively. There was no difference in density estimates at intact and intermediately degraded forest sites; however, we encountered white-fronted brown lemurs more often in intact forest (1.64 ± SE 0.40 individuals/km) than in intermediately degraded and degraded forest (0.15 ± SE 0.06 and 0.16 ± SE 0.06 individuals/km). In addition, we encountered white-fronted brown lemurs at lower rates in 2013 (0.15 ± SE 0.06 individuals/km) compared to 2010 (0.82 ± SE 0.12 individuals/km) at a resurveyed site. Our findings emphasize that primate researchers must account for variation in how lemur encounter rates and densities differ between intact and degraded forests, and although we observed a decline in white-fronted brown lemur encounter rate at our resurveyed site, we caution that changes in lemur encounter rates may simply reflect lower detection rates rather than lower density. Future research should focus on using conventional distance sampling techniques, which are infrequently used in primate studies, to provide more robust density estimates as a way to accurately assess trends and the effects of anthropogenic pressures on lemur populations.


Distance sampling Habitat degradation Primate Rainforest 



This research was funded by the National Science Foundation (grant no. DGE 0822220), Sigma Xi, Cleveland Metroparks Zoo, European Association for Zoos and Aquaria, Idea Wild, National Geographic Society-Waitts grant #W96-10, People’s Trust for Endangered Species, Virginia Tech Chapter of Sigma Xi, Virginia Tech, and Wildlife Conservation Society Madagascar Program (WCS-MP). We thank Dean Stauffer and Steig Johnson for all the advice they provided. We thank our Malagasy field assistants B. L. Donah, Marka’Helin, R. Wilson, B. J. R. Rasolofoniaina, E. J. G. Anjaraniaina, Didice, and Augustain; numerous Malagasy collaborators; and our many field volunteers and data entry volunteers. We thank WCS-MP, especially Christopher Holmes, and Antongil Conservation for logistical aid and the Madagascar Government and Madagascar National Parks (MNP) for permitting this project. We appreciate the comments of two anonymous reviewers and the editor-in-chief, which greatly improved this contribution.

This material is based on work supported by the National Science Foundation Graduate Research Fellowship. Any opinion, findings, and conclusions or recommendations expressed in this material are those of the authors(s) and do not necessarily reflect the views of the National Science Foundation.

Supplementary material

10764_2016_9906_MOESM1_ESM.docx (322 kb)
ESM 1 (DOCX 322 kb)


  1. Akaike, H. (1973). Information theory and an extension of the maximum likelihood principle. In B. N. Petran & F. Csaki (Eds.), Second International Symposium on Information Theory (pp. 267–281). Budapest: Akadémiai Kiadó.Google Scholar
  2. Araldi, A., Barelli, C., Hodges, K., & Rovero, F. (2014). Density estimation of the endangered Udzungwa red colobus (Procolobus gordonorum) and other arboreal primates in the Udzungwa Mountains using systematic distance sampling. International Journal of Primatology, 35(5), 941–956.CrossRefGoogle Scholar
  3. Atsalis, S. (1999). Seasonal fluctuations in body fat and activity levels in a rain-forest species of mouse lemur, Microcebus rufus. International Journal of Primatology, 20(6), 884–910.CrossRefGoogle Scholar
  4. Borgerson, C. (2015). The effects of illegal hunting and habitat on two sympatric endangered primates. International Journal of Primatology, 36, 74–93.CrossRefGoogle Scholar
  5. Brooks, T. M., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A., Rylands, A. B., Konstant, W. R., et al. (2002). Habitat loss and extinction in the hotspots of biodiversity. Conservation Biology, 16(4), 909–923.CrossRefGoogle Scholar
  6. Buckland, S. T. (1985). Perpendicular distance models for line transect sampling. Biometrics, 41(1), 177–195.CrossRefPubMedGoogle Scholar
  7. 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
  8. Campera, M., Serra, V., Balestri, M., Barresi, M., Ravaolahy, M., Randriatafika, F., et al. (2014). Effects of habitat quality and seasonality on ranging patterns of collared brown lemur (Eulemur collaris) in littoral forest fragments. International Journal of Primatology, 35, 957–975.CrossRefGoogle Scholar
  9. Charnov, E. L., & Berrigan, D. (1993). Why do female primates have such long lifespans and so few babies? Or life in the slow lane. Evolutionary Anthropology, 1, 191–194.CrossRefGoogle Scholar
  10. Cusack, J. J., Dickman, A. J., Rowcliffe, J. M., Carbone, C., Macdonald, D. W., & Coulson, T. (2015). Random versus game trail-based camera trap placement strategy for monitoring terrestrial mammal communities. PLoS ONE, 10(5), e0126373.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Dolins, F. L., Jolly, A., Rasamimanana, H., Ratsimbazafy, J., Feistner, A. T., & Ravoavy, F. (2010). Conservation education in Madagascar: Three case studies in the biologically diverse island-continent. American Journal of Primatology, 72(5), 391–406.CrossRefPubMedGoogle Scholar
  12. 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(2), 183–193.CrossRefPubMedGoogle Scholar
  13. Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics, 34, 487–515.CrossRefGoogle Scholar
  14. Farris, Z. J. (2014). Response of Madagascar's endemic carnivores to fragmentation, hunting, and exotic carnivores across the Masoala-Makira landscape. PhD dissertation, Virginia Polytechnic Institute and State University.Google Scholar
  15. Farris, Z. J., Karpanty, S. M., Ratelolahy, F., & Kelly, M. J. (2014). Predator–primate distribution, activity, and co-occurrence in relation to habitat and human activity across fragmented and contiguous forests in northeastern Madagascar. International Journal of Primatology, 35(5), 859–880.CrossRefGoogle Scholar
  16. Farris, Z. J., Golden, C. D., Karpanty, S., Murphy, A., Stauffer, D., Ratelolahy, F., et al. (2015). Hunting, exotic carnivores, and habitat loss: anthropogenic effects on a native carnivore community, Madagascar. PLoS ONE, 10(9), e0136456.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Ganzhorn, J. U. (1988). Food partitioning among Malagasy primates. Oecologia, 75, 436–450.CrossRefGoogle Scholar
  18. Ganzhorn, J. U. (1995). Low-level disturbance effects on primary production, leaf chemistry, and lemur populations. Ecology, 76(7), 2084–2096.CrossRefGoogle Scholar
  19. Ganzhorn, J. U., Malcomber, S., Andrianantoanina, O., & Goodman, S. M. (1997). Habitat characteristics and lemur species richness in Madagascar. Biotropica, 29(3), 331–343.CrossRefGoogle Scholar
  20. Golden, C. D. (2009). Bushmeat hunting and use in the Makira Forest, north-eastern Madagascar: a conservation and livelihoods issue. Oryx, 43(3), 386.CrossRefGoogle Scholar
  21. Goodman, S. M. (2004). Predation on lemurs. In S. M. Goodman & J. P. Benstead (Eds.), The natural history of Madagascar (pp. 1221–1228). Chicago: The University of Chicago Press.Google Scholar
  22. Herrera, J. P., Wright, P. C., Lauterbur, E., Ratovonjanahary, L., & Taylor, L. L. (2011). The effects of habitat disturbance on lemurs at Ranomafana National Park, Madagascar. International Journal of Primatology, 32, 1091–1108.CrossRefGoogle Scholar
  23. Irwin, M. T., & Raharison, J. L. (2009). Ecosystem in decay: factors influencing primate species extinctions in forest fragments of Tsinjoarivo, Madagascar. American Journal of Physical Anthropology, 155–155.Google Scholar
  24. 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(10), 2351–2362.CrossRefGoogle Scholar
  25. IUCN. (2015). The IUCN red list of threatened species version 2015.4. Version 2015.4. Retrieved March 24, 2016 from
  26. Karpanty, S. M. (2006). Direct and indirect impacts of raptor predation on lemurs in southeastern Madagascar. International Journal of Primatology, 27(1), 239–261.CrossRefGoogle Scholar
  27. Kress, W. J., Schatz, G. E., Andrianifahanana, M., & Morland, H. S. (1994). Pollination of Ravenala madagascariensis (Strelitziaceae) by lemurs in Madagascar: evidence for an archaic coevolutionary system? American Journal of Botany, 81(5), 542–551.CrossRefGoogle Scholar
  28. Kun-Rodrigues, C., Salmona, J., Besolo, A., Rasolondraibe, E., Rabarivola, C., Marques, T. A., et al. (2014). New density estimates of a threatened sifaka species (Propithecus coquereli) in Ankarafantsika National Park. American Journal of Primatology, 76(6), 515–528.CrossRefPubMedGoogle Scholar
  29. Laurance, W. F., & Useche, D. C. (2009). Environmental synergisms and extinctions of tropical species. Conservation Biology, 23(6), 1427–1437.CrossRefPubMedGoogle Scholar
  30. Lehman, S. M. (2006). Effects of transect selection and seasonality on lemur density estimates in southeastern Madagascar. International Journal of Primatology, 27(4), 1041–1057.CrossRefGoogle Scholar
  31. Lehman, S. M., Rajaonson, A., & Day, S. (2006a). Edge effects and their influence on lemur density and distribution in southeast Madagascar. American Journal of Physical Anthropology, 129, 232–241.CrossRefPubMedGoogle Scholar
  32. 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(3), 293–299.CrossRefPubMedGoogle Scholar
  33. Meyler, S. V., Salmona, J., Ibouroi, M. T., Besolo, A., Rasolondraibe, E., Radespiel, U., et al. (2012). Density estimates of two endangered nocturnal lemur species from northern Madagascar: new results and a comparison of commonly used methods. American Journal of Primatology, 74(5), 414–422.CrossRefPubMedGoogle Scholar
  34. Mittermeier, R. A., Louis, E. E., Richardson, M., Schwitzer, C., Langrand, O., Rylands, A. B., et al. (2010). Lemurs of Madagascar, 3rd ed. Conservation International.Google Scholar
  35. Muldoon, K. M., & Goodman, S. M. (2015). Primates as predictors of mammal community diversity in the forest ecosystems of Madagascar. PLoS ONE, 10(9), e0136787.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403, 853–858.CrossRefPubMedGoogle Scholar
  37. Peres, C. A. (2001). Synergistic effects of subsistence hunting and habitat fragmentation on Amazonian forest vertebrates. Conservation Biology, 15(6), 1490–1505.CrossRefGoogle Scholar
  38. Plumptre, A. J., & Cox, D. (2006). Counting primates for conservation: primate surveys in Uganda. Primates, 47(1), 65–73.CrossRefPubMedGoogle Scholar
  39. Radespiel, U., Olivieri, G., Rasolofoson, D. W., Rakotondratsimba, G., Rakotonirainy, O., Rasoloharijaona, S., et al. (2008). Exceptional diversity of mouse lemurs (Microcebus spp.) in the Makira region with the description of one new species. American Journal of Primatology, 70(11), 1033–1046.CrossRefPubMedGoogle Scholar
  40. Rakotondratsima, M., & Kremen, C. (2001). Suivi écologique de deux espèces de lémuriens diurnes Varecia variegata rubra et Eulemur fulvus albifrons dans la presqu’île de Masoala (1993 – 1998). Lemur News, 6, 31–35.Google Scholar
  41. Rakotondratsimba, G., Rasolofoson, D. W., Rakotonirainy, O., Ratsimbazafy, J., Rakotozafy, L., Rasolofoharivelo, T., et al. (2008). Les principaux facteurs menaçant les lémuriens de l’aire protégée de Makira. Lemur News, 13, 32–37.Google Scholar
  42. Rasolofoson, D. W., Rakotondratsimba, G., Rakotonirainy, O., Rasolofoharivelo, T., Rakotozafy, L., Ratsimbazafy, J., et al. (2007). Le bloc forestier de Makira charnière de lémuriens. Lemur News, 12, 49–53.Google Scholar
  43. Rasolofoson, D. W., Rakotonirainy, O., Rasolofoharivelo, T., Andrianandrasana, H., Rakotondratsimba, G., Ralisoamalala, R., et al. (2014). Prévision de la distribution des espèces de lémuriens du Parc Naturel Makira face aux changements climatiques, implication pour la conservation. Lemur News, 18, 48–52.Google Scholar
  44. Razafindratsima, O. H., Jones, T. A., & Dunham, A. E. (2014). Patterns of movement and seed dispersal by three lemur species. American Journal of Primatology, 76, 84–96.CrossRefPubMedGoogle Scholar
  45. Rivera-Milán, F. F., Bertuol, P., Simal, F., & Rusk, B. L. (2015). Distance sampling survey and abundance estimation of the critically endangered Grenada Dove (Leptotila wellsi). The Condor, 117(1), 87–93.CrossRefGoogle Scholar
  46. Schipper, J., Chanson, J. S., Chiozza, F., Cox, N. A., Hoffmann, M., Katariya, V., et al. (2008). The status of the world's land and marine mammals: diversity, threat, and knowledge. Science, 322(5899), 225–230.CrossRefPubMedGoogle Scholar
  47. Schütz, H., & Goodman, S. M. (1998). Photographic evidence of Allocebus trichotis in the Réserve Spéciale d’Anjanaharibe-Sud. Lemur News, 3, 22–23.Google Scholar
  48. Schwitzer, C., Mittermeier, R. A., Johnson, S. E., Donati, G., Irwin, M., Peacock, H., et al. (2014). Averting lemur extinctions amid Madagascar's political crisis. Science, 343, 842–843.CrossRefPubMedGoogle Scholar
  49. Tagg, N., & Willie, J. (2013). The influence of transect use by local people and reuse of transects for repeated surveys on nesting in western lowland gorillas (Gorilla gorilla gorilla) and central chimpanzees (Pan troglodytes troglodytes) in southeast Cameroon. International Journal of Primatology, 34(3), 554–570.CrossRefGoogle Scholar
  50. Thomas, L., Buckland, S. T., Rexstad, E. A., Laake, J. L., Strindberg, S., Hedley, S. L., et al. (2010). Distance software: design and analysis of distance sampling surveys for estimating population size. Journal of Applied Ecology, 47(1), 5–14.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Whitesides, G. H., Oates, J. F., Green, S. M., & Kluberdanz, R. P. (1988). Estimating primate densities from transects in a west African rainforest: a comparison of techniques. Journal of Animal Ecology, 57(2), 345–367.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Asia J. Murphy
    • 1
    Email author
  • Zach J. Farris
    • 1
  • Sarah Karpanty
    • 1
  • Felix Ratelolahy
    • 2
  • Marcella J. Kelly
    • 1
  1. 1.Department of Fish and Wildlife ConservationVirginia TechBlacksburgUSA
  2. 2.Wildlife Conservation Society Madagascar ProgramAntananarivoMadagascar

Personalised recommendations