International Journal of Primatology

, Volume 33, Issue 2, pp 428–439 | Cite as

Seasonal Effects on Sleeping Site Ecology in a Nocturnal Pair-Living Lemur (Avahi occidentalis)

  • Rindrahatsarana Ramanankirahina
  • Marine Joly
  • Elke Zimmermann


Seasonal changes may have a strong effect on the safety of sleeping sites in arboreal primates. For example, changes in vegetation thickness may impact predation risk and energy expenditure related to thermoregulation. We investigated how seasonality influenced sleeping site characteristics and usage pattern in an arboreal primate living in a highly seasonal environment. The western woolly lemur (Avahi occidentalis) lives in the dry deciduous forest of northwestern Madagascar, where leaf coverage greatly varies across the year. We examined the hypothesis that these lemurs change their sleeping site behavior dependent on season. We collected data on sleeping site height and location, and characterized usage patterns in six radiotagged pairs between May and December 2008. During the late dry season, pairs preferentially slept in the middle part of a tree. In contrast, there was no height preference during the early rainy season. The lemurs used more sleeping sites during the early rainy than during the late dry season and stayed more days at the same sleeping tree in the late dry season. Our findings support the hypothesis that season affects sleeping site selection in an arboreal primate species living in a highly seasonal environment. During the late dry season, western woolly lemurs are particularly conspicuous to hunters and we therefore suggest a better monitoring of the forest in this season to guarantee their future survival.


Season Sleeping site Socioecology Woolly lemur 



We thank the Malagasy Authorities, in particular the Ministère de l’Environnement et des Forêts and the Madagascar National Parks, for their permission to conduct this study in the National Park of Ankarafantsika. For the help we received in Ankarafantsika, we thank Nicole Andriaholinirina and Mananjara. Further, we thank Robin Crompton for advising us in the design of the backpacks. R. Ramanankirahina is indebted to DAAD (Deutscher Akademischer Austausch Dienst) for financial support. We thank Ute Radespiel for her valuable comments on a previous version of the manuscript and Frances Sherwood-Brock for proofreading the English. We also thank Oliver Schülke, Joanna Setchell, and two anonymous reviewers for their comments that greatly improved the manuscript.


  1. Albignac, R. (1972). The carnivores of Madagascar. In R. Battistini, G. Richard-Vindard, & W. Junk (Eds.), Biogeography and ecology in Madagascar (pp. 667–682). The Hague: W. Junk B. B.Google Scholar
  2. Albignac, R. (1981). Lemurine social and territorial organization in a northwestern Malagasy forest (restricted area of Ampijoroa). In A. B. Chiarelli & R. S. Corrucini (Eds.), Primate behavior and sociobiology (pp. 25–29). Berlin: Springer-Verlag.CrossRefGoogle Scholar
  3. Anderson, J. R., & McGrew, W. C. (1984). Guinea baboons (Papio papio) at a sleeping site. American Journal of Primatology, 6, 1–14.CrossRefGoogle Scholar
  4. Aquino, R., & Encarnación, F. (1986). Characteristics and use of sleeping sites in Aotus (Cebidae: Primates) in the Amazon lowlands of Peru. American Journal of Primatology, 11, 319–331.CrossRefGoogle Scholar
  5. Biebouw, K., Bearder, S. K., & Nekaris, K. A. I. (2009). Tree hole utilisation by the hairy-eared dwarf lemur (Allocebus trichotis) in Analamazaotra Special Reserve. Folia Primatologica, 80, 89–103.CrossRefGoogle Scholar
  6. Boinski, S., Treves, A., & Chapman, C. A. (2000). A critical evaluation of the influence of predators on primates: Effects on group travel. In S. Boinski & P. A. Garber (Eds.), On the move: How and why animals travel in groups (pp. 43–72). Chicago: University of Chicago Press.Google Scholar
  7. Charles-Dominique, P. (1977). Ecology and behavior of nocturnal primates. New York: Columbia University Press.Google Scholar
  8. Cowlishaw, G. (1994). Vulnerability to predation in baboon populations. Behaviour, 131, 293–304.CrossRefGoogle Scholar
  9. Cui, L.-W., Quan, R.-C., & Xiao, W. (2006). Sleeping sites of black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Baima Snow Mountain, China. Journal of Zoology, 270, 192–198.Google Scholar
  10. Di Bitetti, M. A., Vidal, E. M. L., Baldovino, M. C., & Benesovsky, V. (2000). Sleeping site preferences in tufted capuchin monkeys (Cebus apella nigritus). American Journal of Primatology, 50, 257–274.PubMedCrossRefGoogle Scholar
  11. Fan, P.-F., & Jiang, X.-L. (2008). Sleeping sites, sleeping trees and sleep related behaviors of black crested gibbons (Nomascus concolor jingdongensis) at Mt Wuliang, Central Yunnan, China. American Journal of Primatology, 70, 153–160.PubMedCrossRefGoogle Scholar
  12. Field, A. (2009). Discovering statistics using SPSS (3rd ed.). London: SAGE.Google Scholar
  13. Franklin, S. P. (2004). Predator influence on golden lion tamarin nest choice and presleep behavior. M.Sc. thesis, University of Maryland.Google Scholar
  14. Ganzhorn, J. U., Abraham, J. P., & Razanahoera-Rakotomalala, M. (1985). Some aspects of the natural history and food selection of Avahi laniger. Primates, 26, 452–463.CrossRefGoogle Scholar
  15. Garcia, G., & Goodman, S. M. (2003). Hunting of protected animals in the Parc National d’Ankarafantsika, north-western Madagascar. Oryx, 37, 115–118.CrossRefGoogle Scholar
  16. Harcourt, C., & Thornback, J. (1990). Lemurs of Madagascar and the Comoros. The IUCN red data book. Gland: IUCN.Google Scholar
  17. Heymann, E. W. (1995). Sleeping habits of tamarins: Saguinus mystax and Saguinus fuscicollis (Mammalia, Primates, Callitrichidae) in north-eastern Peru. Journal of Zoology, 237, 211–226.CrossRefGoogle Scholar
  18. Janson, C. H. (1998). Testing the predation hypothesis for vertebrate sociality: prospects and pitfalls. Behaviour, 135, 389–410.CrossRefGoogle Scholar
  19. Joly, M. (2010). Tsidy, repahaka sy Fotsife: 15 years research on nocturnal lemurs in the Ankafarantsika National Park, Madagascar. Revue de Primatologie, 3, 1–18.Google Scholar
  20. Kenward, R. E. (1987). Wildlife radio tagging. London: Academic.Google Scholar
  21. Li, D., Grueter, C. C., Ren, G. P., Zhou, Q., Li, M., Peng, Z., & Wei, F. (2006). Characteristics of night-time sleeping places selected by golden monkeys (Rhinopithecus bieti) in the Samage forest, Baima snow mountain nature reserve, China. Integrative Zoology, 1, 141–152.PubMedCrossRefGoogle Scholar
  22. Martin, R. D. (1972). A preliminary field-study of the lesser mouse lemur (Microcebus murinus). Advances in Ethology, 9, 43–89.Google Scholar
  23. Meddis, R. (1983). The evolution of sleep. In A. Mayes (Ed.), Sleep mechanisms and functions in humans and animal (pp. 57–95). Wokingham: Van Nostrand.Google Scholar
  24. Mittermeier, R. A., Louis, E. E., Jr., Richardson, M., Schwitzer, C., Langrand, O., Rylandy, et al. (2010). Lemurs of Madagascar (3rd ed.). Arlington, USA: Conservation International.Google Scholar
  25. Nicoll, M. E., & Langrand, O. (1989). Madagascar: Revue de la conservation et des aires protégés. Gland: World Wide Fund for Nature.Google Scholar
  26. Petter, J. J., Albignac, R., & Rumpler, Y. (1977). Mammifères lémuriens. Faune de Madagascar. Paris: ORSTOM CNRS.Google Scholar
  27. Phoonjampa, R., Koenig, A., Borries, C., Gale, G. A., & Savini, T. (2010). Selection of sleeping trees in pileated gibbons (Hylobates pileatus). American Journal of Primatology, 72, 617–625.PubMedGoogle Scholar
  28. Pruetz, J. D., Fulton, S. J., Marchant, L. F., McGrew, W. C., Schiel, M., & Walter, M. (2008). Arboreal nesting as anti-predator adaptation by Savanna Chimpanzees (Pan troglodytes verus) in southeastern Senegal. American Journal of Primatology, 70, 1–9.CrossRefGoogle Scholar
  29. Radespiel, U., Cepok, S., Zietemann, V., & Zimmermann, E. (1998). Sex specific usage patterns of sleeping sites in grey mouse lemurs (Microcebus murinus) in northwestern Madagascar. American Journal of Primatology, 51, 21–40.CrossRefGoogle Scholar
  30. Radespiel, U., Ehresmann, P., & Zimmermann, E. (2003). Species-specific usage of sleeping sites in two sympatric mouse lemur species (Microcebus murinus, M. ravelobensis) in northwestern Madagascar. American Journal of Primatology, 59, 139–151.PubMedCrossRefGoogle Scholar
  31. Ramanankirahina, R., Joly, M., & Zimmermann, E. (2011). Peaceful primates: affiliation, aggression, and the question of female dominance in a nocturnal pair-living lemur (Avahi occidentalis). American Journal of Primatology, 73, 1261–1268.PubMedCrossRefGoogle Scholar
  32. Ramangason, G. S. (1988). Flore et végétation de la Forêt d’Ampijoroa. In L. Rakotovao, V. Barre, & J. Sayer (Eds.), L’équilibre des écosystèmes forestiers à Madagascar (pp. 130–137). Gland: IUCN.Google Scholar
  33. Rasoloharijaona, S. (2001). Contribution à l’étude comparative de la communication vocale et de la vie sociale de deux formes de Lepilemur (Geoffroy 1858) (Lepilemuridae, Petter et al. 1977) provenant de la forêt humide de l’Est de Madagascar. Ph.D. Dissertation, Université d’Antananarivo, Madagascar.Google Scholar
  34. Rasoloharijaona, S., Rakotosamimanana, B., Randrianambinina, B., & Zimmermann, E. (2003). Pair-specific usage of sleeping sites and their implications for social organization in a nocturnal malagasy primate, the Milne Edwards' sportive lemur (Lepilemur edwardsi). American Journal of Physical Anthropology, 122, 251–258.PubMedCrossRefGoogle Scholar
  35. Rasoloharijaona, S., Randrianambinina, B., & Zimmermann, E. (2008). Sleeping site ecology in a rain-forest dwelling nocturnal lemur (Lepilemur mustelinus): implications for sociality and conservation. American Journal of Primatology, 70, 247–253.PubMedCrossRefGoogle Scholar
  36. Rayadin, Y., & Saitoh, T. (2008). Individual variation in nest size and nest site features of the Bornean orangutans (Pongo pygmaeus). American Journal of Primatology, 71, 393–399.CrossRefGoogle Scholar
  37. Reichard, U. (1998). Sleeping site, sleeping places, and presleep behavior of gibbons (Hylobates lar). American Journal of Primatology, 46, 35–62.PubMedCrossRefGoogle Scholar
  38. Scheumann, M., Rabesandratana, A., & Zimmermanna, E. (2007). Predation, communication and cognition in lemurs. In S. Gursky & K. A. I. Nekaris (Eds.), Primate anti-predator strategies (pp. 100–126). New York: Springer.CrossRefGoogle Scholar
  39. Schmelting, B. (2000). Saisonale Aktivität und Reproduktionsbiologie von grauen Mausmaki- Männchen (Microcebus murinus, Miller JF 1777) in Nordwest Madagaskar. Hannover: School of Veterinary Medicine Hannover.Google Scholar
  40. Schülke, O., & Kappeler, P. M. (2003). So near and yet so far: Territorial pairs, but low cohesion between pair partners in a nocturnal lemur, Phaner furcifer. Animal Behaviour, 65, 331–343.CrossRefGoogle Scholar
  41. Sehen, L., Goetze, D., Rajeriarison, C., Roger, E., Thorén, S., & Radespiel, U. (2010). Structural and floristic traits of habitats with differing relative abundance of the lemurs Microcebus murinus and M. ravelobensis in northwestern Madagascar. Ecotropica, 16, 15–20.Google Scholar
  42. Smith, A. C., Knogge, C., Huck, M., Löttker, P., Buchanan-Smith, H. M., & Heymann, E. W. (2007). Long-term patterns of sleeping site use in wild Saddleback (Saguinus fuscicollis) and Mustached tamarins (S. mystax): Effects of foraging, thermoregulation, predation, and resource defense constraints. American Journal of Physical Anthropology, 134, 340–353.PubMedCrossRefGoogle Scholar
  43. Struhsaker, T. T. (1967). Social structure among vervet monkeys (Cercopithecus aethiops). Behaviour, 29, 83–121.CrossRefGoogle Scholar
  44. Sussman, R. W., & Rakotozafy, A. (1994). Plant diversity and structural analysis of a tropical dry forest in southwestern Madagascar. Biotropica, 26, 241–254.CrossRefGoogle Scholar
  45. Tattersall, I. (1982). The primates of Madagascar. New York: Columbia University Press.Google Scholar
  46. Thalmann, U. (2001). Food resource characteristics in two nocturnal lemurs with different social behaviour: Avahi occidentalis and Lepilemur edwardsi. International Journal of Primatology, 22, 287–324.CrossRefGoogle Scholar
  47. Thalmann, U. (2003). Woolly lemur, woolly lemurs, avahy, fotsy-fe, ampongy, tsarafangitra, dadintsifaky. In S. M. Goodmann & J. P. Benstead (Eds.), The natural history of Madagascar (pp. 1340–1342). Chicago: University of Chicago Press.Google Scholar
  48. van Schaik, C. P., Terborgh, J. W., & Wright, S. J. (1993). The phenology of tropical forests: significance and consequences for primary comsumers. Annual Review of Ecological System, 24, 353–377.CrossRefGoogle Scholar
  49. Warren, R. D., & Crompton, R. H. (1997). Locomotor ecology of Lepilemur edwardsi and Avahi occidentalis. American Journal of Physical Anthropology, 104, 471–486.PubMedCrossRefGoogle Scholar
  50. Wright, S. J. (1996). Phenological responses to seasonality in tropical forest plants. In S. S. Mulkey, R. L. Chazdon, & A. P. Smith (Eds.), Tropical forest plant ecophysiology (pp. 440–460). New York: Chapman & Hall.CrossRefGoogle Scholar
  51. Xiang, Z.-F., Nie, S.-G., Chang, Z.-F., Wie, F.-W., & Li, M. (2010). Sleeping sites of Rhinopithecus brelichi at Yangaoping, Guizhou. International Journal of Primatology, 31, 59–71.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Rindrahatsarana Ramanankirahina
    • 1
  • Marine Joly
    • 1
  • Elke Zimmermann
    • 1
  1. 1.Institute of ZoologyUniversity of Veterinary Medicine HannoverHannoverGermany

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