Skip to main content
SpringerLink
Log in

Multiple Ecological Factors Influence the Location of Proboscis Monkey (Nasalis larvatus) Sleeping Sites in West Kalimantan, Indonesia

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

Abstract

Multiple ecological factors have been hypothesized to influence primate sleeping site selection. Testing multiple hypotheses about sleeping site selection permits examination of the relative strength of distinct ecological factors and expands our ability to understand how selection pressures influence primate sleeping behavior. Here we examine how avoidance of biting insects, thermoregulation, foraging efficiency, tree stability, and interspecific competition influence selection of sleeping sites by proboscis monkeys (Nasalis larvatus) in Indonesian Borneo. We collected data on relative insect abundance, temperature, rainfall, food availability, group size, sleeping site location, and presence of other primates for 12 mo. Using formal model comparison and information criteria, we analyzed the relative importance of these ecological factors in determining one aspect of sleeping site location: distance from the river. Our models supported the avoidance of biting insects and the foraging efficiency hypotheses. Proboscis monkeys slept further inland on nights when the abundance of sandflies was high along the river, and when less food was available along the river. Many studies suggest that primates select sleeping trees and locations to reduce predation risk; our study indicates that additional factors may also be important in determining sleeping site selection.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Albert, A., Savini, T., & Huynen, M. C. (2011). Sleeping site selection and presleep behavior in wild pigtailed macaques. American Journal of Primatology, 73(12), 1222–1230.

    Article  PubMed  Google Scholar 

  • Anderson, J. R. (2000). Sleep-related behavioural adaptations in free-ranging anthropoid primates. Sleep Medicine Reviews, 4(4), 355–373.

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Barnett, A. A., Shaw, P., Spironello, W. R., MacLarnon, A., & Ross, C. (2012). Sleeping site selection by golden-backed uacaris, Cacajao melanocephalus ouakary (Pitheciidae), in Amazonian flooded forests. Primates, 53(3), 273–285.

    Article  PubMed  Google Scholar 

  • Bennett, E. L., & Sebastian, A. C. (1988). Social organization and ecology of proboscis monkeys (Nasalis larvatus) in mixed coastal forest in Sarawak. International Journal of Primatology, 9(3), 233–255.

    Article  Google Scholar 

  • Bernard, H., Matsuda, I., Hanya, G., & Ahmad, A. H. (2011). Characteristics of night sleeping trees of proboscis monkeys (Nasalis larvatus) in Sabah, Malaysia. International Journal of Primatology, 32(1), 259–367.

    Article  Google Scholar 

  • Brotcorne, F., Maslarov, C., Wandia, I. N., Fuentes, A., Beudels-Jamar, R. C., & Huynen, M.-C. (2014). The role of anthropic, ecological, and social factors in sleeping site choice by long-tailed macaques (Macaca fascicularis). American Journal of Primatology, 76, 1140–1150.

    Article  PubMed  Google Scholar 

  • Burnham, K. P., & Anderson, D. R. (2002). Model selection and multi-model inference: A practical information-theoretic approach. New York: Springer Science+Business Media.

    Google Scholar 

  • Chapman, C. A., Chapman, L. J., & Mclaughlin, R. L. (1989). Multiple central place foraging by spider monkeys: travel consequences of using many sleeping sites. Oecologia, 79(4), 506–511.

    Article  CAS  PubMed  Google Scholar 

  • Cheyne, S. M., Hoing, A., Rinear, J., & Sheeran, L. K. (2012). Sleeping site selection by agile gibbons: the influence of tree stability, fruit availability and predation risk. Folia Primatologica, 83(3–6), 299–311.

    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 (London), 270(1), 192–198.

    Google Scholar 

  • Dudley, R., & Milton, K. (1990). Parasite deterrence and the energetic costs of slapping in howler monkeys, Aloatta palliata. Journal of Mammalogy, 71(3), 463–465.

    Article  Google Scholar 

  • Feilen, K. L. (2014). Feeding ecology and sleeping site selection of proboscis monkeys (Nasalis larvatus) in West Kalimantan, Indonesia. University of California–Davis.

  • Feilen, K. L., & Marshall, A. J. (2014). Sleeping site selection by proboscis monkeys (Nasalis larvatus) in West Kalimantan, Indonesia. American Journal of Primatology. doi:10.1002/ajp.22298.

    PubMed  Google Scholar 

  • Freeland, W. J. (1977). Blood-sucking flies and primate polyspecific associations. Nature, 269(5631), 801–802.

    Article  CAS  PubMed  Google Scholar 

  • Hamilton, W. (1982). Baboon sleeping site preferences and relationships to primate grouping patterns. American Journal of Primatology, 3, 41–53.

    Article  Google Scholar 

  • Hausfater, G., & Meade, B. J. (1982). Alteration of sleeping groves by yellow baboons Papio cynocephalus as a strategy for parasite avoidance. Primates, 23(2), 287–297.

    Article  Google Scholar 

  • Koops, K., McGrew, W. C., de Vries, H., & Matsuzawa, T. (2012). Nest-building by chimpanzees (Pan troglodytes verus) at Seringbara, Nimba Mountains: Antipredation, thermoregulation, and antivector hypotheses. International Journal of Primatology, 33(2), 356–380.

    Article  Google Scholar 

  • Krief, S., Levrero, F., Krief, J. M., Thanapongpichat, S., Imwong, M., et al. (2012). Investigations on anopheline mosquitoes close to the nest sites of chimpanzees subject to malaria infection in Ugandan Highlands. Malaria Journal, 11(116), doi:10.1186/1475-2875-11-116.

  • Lassen, S. B., Nielsen, S. A., & Kristensen, M. (2012). Identity and diversity of blood meal hosts of biting midges (Diptera: Ceratopogonidae: Culicoides Latreille) in Denmark. Parasites & Vectors, 5(1), 143.

  • Lutermann, H., Verburgt, L., & Rendigs, A. (2010). Resting and nesting in a small mammal: sleeping sites as a limiting resource for female grey mouse lemurs. Animal Behaviour, 79(6), 1211–1219.

    Article  Google Scholar 

  • Matsuda, I., Tuuga, A., Akiyama, Y., & Higashi, S. (2008). Selection of river crossing location and sleeping site by proboscis monkeys (Nasalis larvatus) in Sabah, Malaysia. American Journal of Primatology, 70(11), 1097–1101.

    Article  PubMed  Google Scholar 

  • Matsuda, I., Tuuga, A., & Higashi, S. (2009). Ranging behavior of proboscis monkeys in a riverine forest with special reference to ranging in inland forest. International Journal of Primatology, 30(2), 313–325.

    Article  Google Scholar 

  • Matsuda, I., Tuuga, A., & Higashi, S. (2010). Effects of water level on sleeping-site selection and inter-group association in proboscis monkeys: why do they sleep alone inland on flooded days? Ecological Research, 25, 475–482.

    Article  Google Scholar 

  • Matsuda, I., Tuuga, A., & Bernard, H. (2011). Riverine refuging by proboscis monkeys (Nasalis larvatus) and sympatric primates: implications for adaptive benefits of the riverine habitat. Mammalian Biology, 76(2), 165–171.

    Article  Google Scholar 

  • Nakagawa, S., & Freckleton, R. P. (2011). Model averaging, missing data and multiple imputation: a case study for behavioural ecology. Behavioral Ecology and Sociobiology, 65(1), 103–116.

    Article  Google Scholar 

  • Nunn, C. L., & Heymann, E. W. (2005). Malaria infection and host behavior: a comparative study of neotropical primates. Behavioral Ecology and Sociobiology, 59, 30–37.

    Article  Google Scholar 

  • Ozbel, Y., Sanjoba, C., Alten, B., Asada, M., Depaquit, J., et al. (2011). Distribution and ecological aspects of sand fly (Diptera: Psychodidae) species in Sri Lanka. Journal of Vector Ecology, 36, S77–S86.

    Article  PubMed  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(7), 617.

    PubMed  Google Scholar 

  • Prasetyo, D., Ancrenaz, M., Morrogh-Bernard, H. C., Utami Atmoko, S., Wich, S. A., & van Schaik, C. P. (2009). Nest building in orangutans. In Orangutans: Geographical variation in behavioral ecology (pp. 269–277). Oxford: Oxford University Press.

    Google Scholar 

  • Ramakrishnan, U., & Coss, R. G. (2001). Strategies used by bonnet macaques (Macaca radiata) to reduce predation risk while sleeping. Primates, 42(3), 193–206.

    Article  Google Scholar 

  • R Development Core Team (2013). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.

  • Salter, R. E., MacKenzie, N. A., Nightingale, N., Aken, K. M., & Chai, P. (1985). Habitat use, ranging behavior, and food habitat of the proboscis monkey, Nasalis larvatus (van Wurmb), in Sarawak. Primates, 26(4), 436–451.

    Article  Google Scholar 

  • Samson, D. R., Muehlenbein, M. P., & Hunt, K. D. (2013). Do chimpanzees (Pan troglodytes schweinfurthii) exhibit sleep related behaviors that minimize exposure to parasitic arthropods? A preliminary report on the possible anti-vector function of chimpanzee sleeping platforms. Primates, 54(1), 73–80.

    Article  PubMed  Google Scholar 

  • Sebastian, A. C. (2000). Proboscis monkeys in Danau Sentarum National Park. Borneo Research Bulletin, 31, 359–371.

  • Smith, A. C., Knogge, C., Huck, M., Loettker, P., Buchanan-Smith, H. M., & Heyman, 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(3), 340–353.

    Article  PubMed  Google Scholar 

  • Teichroeb, J. A., Holmes, T. D., & Sicotte, P. (2012). Use of sleeping trees by ursine colobus monkeys (Colobus vellerosus) demonstrates the importance of nearby food. Primates, 53(3), 287–296.

    Article  PubMed  Google Scholar 

  • Thiry, V., Stark, D. J., Goossens, B., Slachmuylder, J. L., Vercauteren Drubbel, R., & Vercauteren, M. (2016). Use and selection of sleeping sites by proboscis monkeys, Nasalis larvatus, along the Kinabatangan River, Sabah, Malaysia. Folia Primatologica, 87(3), 180–196.

    Article  Google Scholar 

  • Tiwananthagorn, S., Bhutto, A. M., Baloch, J. H., Soomro, F. R., Kawamura, Y., et al. (2012). Zoophilic feeding behaviour of phlebotomine sand flies in the endemic areas of cutaneous leishmaniasis of Sindh Province, Pakistan. Parasitology Research, 111(1), 125–133.

    Article  PubMed  Google Scholar 

  • van Buuren, S., & Groothuis-Oudshoorn, K. (2011). mice: Multivariate imputation by chained equations in R. Journal of Statistical Software, 45(3), 1–67.

    Article  Google Scholar 

  • van Schaik, C. P., van Amerongen, A., & van Noordwijk, M. A. (1996). Riverine refuging by wild Sumatran long-tailed macaques (Macaca fasicularis). In J. E. Fa & D. G. Lindburg (Eds.), Evolution and ecology of macaque societies (pp. 160–181). New York: Cambridge University Press.

    Google Scholar 

  • Vasilakis, N., Hanley, K. A., Holmes, E. C., Weaver, S. C., & Cardosa, J. (2011). Fever from the forest: prospects for the continued emergence of sylvatic dengue virus and its impact on public health. Nature Reviews Microbiology, 9(7), 532–541.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vythilingam, I., Tan, C., Asmad, M., Chan, S., Lee, K., & Singh, B. (2006). Natural transmission of Plasmodium knowlesi to humans by Anopheles latens in Sarawak, Malaysia. Transactions of the Royal Society of Tropical Medicine and Hygiene, 100(11), 1087–1088.

  • Whitten, A. J. (1982). The role of ants in selection of night trees by gibbons. Biotropica, 14(3), 237–238.

    Article  Google Scholar 

  • Xiang, Z., Xiao, W., & Huo, S. (2011). Selection of sleeping sites and sleeping trees by black-and-white snub-nosed monkeys (Rhinopithecus bieti) in Honglaxueshan National Nature Reserve, Tibet. Acta Theriologica Sinica, 31(4), 330–337.

    Google Scholar 

  • Yeager, C. P. (1989). Feeding ecology of the proboscis monkey (Nasalis larvatus). International Journal of Primatology, 10(6), 497–530.

    Article  Google Scholar 

  • Yeager, C. P. (1991). Proboscis monkey (Nasalis larvatus) social organization: intergroup patterns of association. American Journal of Primatology, 23, 73–86.

    Article  Google Scholar 

  • Yeager, C. P. (1993). Ecological constrains on intergroup associations in the proboscis monkey (Nasalis larvatus). Tropical Biodiversity, 1(2), 89–100.

    Google Scholar 

Download references

Acknowledgments

We thank the Indonesian government, the State Ministry of Research and Technology (RISTEK), and the mayor of Sungai Tolak for giving us permission to conduct this research. All work conformed to research regulations at the University of California, Davis and the laws of the Republic of Indonesia. We acknowledge the support and efforts of the Indonesian field assistants that worked on this project: Ferman, Iskandar and M. Ali. We thank Universitas Tanjungpura (UNTAN) and Flora and Fauna International–Indonesia for serving as our Indonesian counterparts for this project. This manuscript was greatly improved by thoughtful comments from Lynne Isbell, Ikki Matsuda, Vincent Nijman, Joanna Setchell, and an anonymous reviewer. Mark Grote provided invaluable assistance with statistical analysis. This research was funded by a U.S. Fulbright Student Fellowship, a Boren Fellowship, the University of California, Davis Department of Anthropology, and Primate Conservation, Inc.

Author information

Authors and Affiliations

  1. Department of Anthropology, University of California, Davis, CA, 95616, USA

    Katie L. Feilen

  2. Disney’s Animal Programs, Lake Buena Vista, FL, 32830, USA

    Katie L. Feilen

  3. Department of Anthropology, University of Michigan, Ann Arbor, MI, 48109, USA

    Andrew J. Marshall

  4. Program in the Environment, University of Michigan, Ann Arbor, MI, 48109, USA

    Andrew J. Marshall

  5. School for Natural Resources and Environment, University of Michigan, Ann Arbor, MI, 48109, USA

    Andrew J. Marshall

Authors
  1. Katie L. Feilen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrew J. Marshall
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Katie L. Feilen.

Ethics declarations

Conflict of Interest

The authors have no conflict of interest or competing financial interests to declare.

Additional information

Handling Editor: Joanna M. Setchell

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Feilen, K.L., Marshall, A.J. Multiple Ecological Factors Influence the Location of Proboscis Monkey (Nasalis larvatus) Sleeping Sites in West Kalimantan, Indonesia. Int J Primatol 38, 448–465 (2017). https://doi.org/10.1007/s10764-017-9953-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-017-9953-1

Keywords

Search

Navigation