Skip to main content
Log in

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

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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 

  • 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.

    Chapter  Google Scholar 

  • Anderson, J. R., & McGrew, W. C. (1984). Guinea baboons (Papio papio) at a sleeping site. American Journal of Primatology, 6, 1–14.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Charles-Dominique, P. (1977). Ecology and behavior of nocturnal primates. New York: Columbia University Press.

    Google Scholar 

  • Cowlishaw, G. (1994). Vulnerability to predation in baboon populations. Behaviour, 131, 293–304.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Field, A. (2009). Discovering statistics using SPSS (3rd ed.). London: SAGE.

    Google Scholar 

  • Franklin, S. P. (2004). Predator influence on golden lion tamarin nest choice and presleep behavior. M.Sc. thesis, University of Maryland.

  • 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.

    Article  Google Scholar 

  • Garcia, G., & Goodman, S. M. (2003). Hunting of protected animals in the Parc National d’Ankarafantsika, north-western Madagascar. Oryx, 37, 115–118.

    Article  Google Scholar 

  • Harcourt, C., & Thornback, J. (1990). Lemurs of Madagascar and the Comoros. The IUCN red data book. Gland: IUCN.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Janson, C. H. (1998). Testing the predation hypothesis for vertebrate sociality: prospects and pitfalls. Behaviour, 135, 389–410.

    Article  Google Scholar 

  • 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 

  • Kenward, R. E. (1987). Wildlife radio tagging. London: Academic.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Martin, R. D. (1972). A preliminary field-study of the lesser mouse lemur (Microcebus murinus). Advances in Ethology, 9, 43–89.

    Google Scholar 

  • 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 

  • 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.

  • Nicoll, M. E., & Langrand, O. (1989). Madagascar: Revue de la conservation et des aires protégés. Gland: World Wide Fund for Nature.

    Google Scholar 

  • Petter, J. J., Albignac, R., & Rumpler, Y. (1977). Mammifères lémuriens. Faune de Madagascar. Paris: ORSTOM CNRS.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Reichard, U. (1998). Sleeping site, sleeping places, and presleep behavior of gibbons (Hylobates lar). American Journal of Primatology, 46, 35–62.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • Struhsaker, T. T. (1967). Social structure among vervet monkeys (Cercopithecus aethiops). Behaviour, 29, 83–121.

    Article  Google Scholar 

  • Sussman, R. W., & Rakotozafy, A. (1994). Plant diversity and structural analysis of a tropical dry forest in southwestern Madagascar. Biotropica, 26, 241–254.

    Article  Google Scholar 

  • Tattersall, I. (1982). The primates of Madagascar. New York: Columbia University Press.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • Warren, R. D., & Crompton, R. H. (1997). Locomotor ecology of Lepilemur edwardsi and Avahi occidentalis. American Journal of Physical Anthropology, 104, 471–486.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rindrahatsarana Ramanankirahina.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ramanankirahina, R., Joly, M. & Zimmermann, E. Seasonal Effects on Sleeping Site Ecology in a Nocturnal Pair-Living Lemur (Avahi occidentalis). Int J Primatol 33, 428–439 (2012). https://doi.org/10.1007/s10764-012-9587-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-012-9587-2

Keywords

Navigation