Skip to main content

Advertisement

SpringerLink
Log in

The Effect of Climatic Factors on the Activity Budgets of Barbary Macaques (Macaca sylvanus)

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

Abstract

Climatic conditions can significantly affect the behavior of animals and constrain their activity or geographic distribution. Barbary macaques (Macaca sylvanus) are one of the few primates that live outside the tropics. Here we analyze if and how the activity budgets of Barbary macaques are affected by climatic variables, i.e., air temperature, relative humidity, rainfall, and snow coverage. We collected scan sampling data on the activity budgets of four groups of macaques living in the Middle Atlas Mountains of Morocco from June 2008 to January 2011. This habitat is characterized by extreme seasonal changes, from cold and snowy winters to hot and dry summers. The activity budgets of the macaques differed across months but not across the time of day (with the exception of time spent feeding). The monkeys spent significantly more time feeding or foraging when there was no snow than when snow coverage was moderate or major. Daily rainfall was positively related to resting time and negatively to time spent moving or in social behavior. Air temperature was negatively related to time spent feeding or foraging. Finally, time spent on social behavior was significantly lower when relative humidity was high. These data indicate that environmental factors significantly affect the time budgets of endangered Barbary macaques, a species that has been little studied in the wild. Our findings support previous studies on temperate primates in showing that snow coverage can have negative consequences on the feeding ecology and survival of these species.

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

  • Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49, 227–267.

    Article  PubMed  CAS  Google Scholar 

  • Barrett, L., Gaynor, D., Rendall, D., Mitchell, D., & Henzi, S. P. (2004). Habitual cave use and thermoregulation in chacma baboons (Papio hamadryas ursinus). Journal of Human Evolution, 46, 215–222.

    Article  PubMed  CAS  Google Scholar 

  • Bernstein, I. S. (1972). Daily activity cycles and weather influences on a pigtail monkey group. Folia Primatologica, 18, 390–415.

    Article  Google Scholar 

  • Bettridge, C., Lehmann, J., & Dunbar, R. I. M. (2010). Trade-offs between time, predation risk and life history, and their implications for biogeography: a systems modelling approach with a primate case study. Ecological Modelling, 221, 777–790.

    Article  Google Scholar 

  • Camperio Ciani, A., Palentini, L., Arahou, M., Martinoli, L., Capiluppi, C., & Mouna, M. (2005). Population decline of Macaca sylvanus in the Middle Atlas of Morocco. Biological Conservation, 121, 635–641.

    Article  Google Scholar 

  • Campos, F. A., & Fedigan, L. M. (2009). Behavioural adaptations to heat stress and water scarcity in white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica. American Journal of Physical Anthropology, 138, 101–111.

    Article  PubMed  Google Scholar 

  • Chapman, C. A., & Chapman, L. J. (1991). The foraging itinerary of spider monkeys: when to eat leaves? Folia Primatologica, 56, 162–166.

    Article  Google Scholar 

  • Clutton-Brock, T. H., & Harvey, P. H. (1977). Primate ecology and social organisation. Journal of Zoology, 183, 1–39.

    Article  Google Scholar 

  • Deag, J. M. (1980). Interactions between males and unweaned Barbary macaques: testing the agonistic buffering hypothesis. Behaviour, 75, 54–81.

    Article  Google Scholar 

  • Deag, J. M. (1985). The diurnal patterns of behaviour of the wild Barbary macaque (Macaca sylvanus). Journal of Zoology, 206, 403–413.

    Article  Google Scholar 

  • Dunbar, R. I. M. (1992). Time: a hidden constraint on the behavioural ecology of baboons. Behavioral Ecology and Sociobiology, 31, 35–49.

    Article  Google Scholar 

  • Dunbar, R. I. M., Korstjens, A. H., & Lehmann, J. (2009). Time as an ecological constraint. Biological Reviews, 84, 413–429.

    Article  PubMed  CAS  Google Scholar 

  • El Alami, A., van Lavieren, E., Rachida, A., & Chait, A. (2012). Differences in activity budgets and diet between semiprovisioned and wild-feeding groups of the endangered Barbary macaque (Macaca sylvanus) in the Central High Atlas Mountains, Morocco. American Journal of Primatology, 74, 210–216.

    Article  Google Scholar 

  • Fa, J. E. (1984). Habitat distribution and habitat preference in Barbary macaques (Macaca sylvanus). International Journal of Primatology, 5, 273–286.

    Article  Google Scholar 

  • Fa, J. E. (1986). Use of time and resources by provisioned troops of monkeys: Social behaviour, time and energy in the Barbary macaque (Macaca sylvanus L.) at Gibraltar. Contributions to Primatology, 23, 1–377.

    Google Scholar 

  • Fleagle, J. G. (1999). Primate adaptation and evolution. San Diego: Academic Press.

    Google Scholar 

  • Fooden, J. (2007). Systematic review of the Barbary macaque, Macaca sylvanus (Linnaeus, 1758). Fieldiana Zoology, 113, 1–60.

    Article  Google Scholar 

  • Hanya, G., Ménard, N., Qarro, M., Ibn Tattou, M., Fuse, M., Vallet, et al. (2011). Dietary adaptations of temperate primates: comparisons of Japanese and Barbary macaques. Primates, 52, 187–198.

    Article  PubMed  Google Scholar 

  • Hetem, R. S., Strauss, W. M., Fick, L. G., Maloney, S. K., Meyer, L. C. R., Shobrak, M., et al. (2012). Does size matter? Comparison of body temperature and activity of free-living Arabian oryx (Oryx leucoryx) and the smaller Arabian sand gazelle (Gazella subgutturosa marica) in the Saudi desert. Journal of Comparative Physiology. B, 182, 437–449.

    Article  Google Scholar 

  • Hill, R. A. (2006). Thermal constraints on activity scheduling and habitat choice in baboons. American Journal of Physical Anthropology, 129, 242–249.

    Article  PubMed  Google Scholar 

  • Hill, R. A., Barrett, L., Gaynor, D., Weingrill, T., Dixon, P., Payne, H., et al. (2003). Day length, latitude and behavioural (in)flexibility in baboons (Papio cynocephalus ursinus). Behavioral Ecology and Sociobiology, 53, 278–286.

    Google Scholar 

  • Hill, R. A., Barrett, L., Gaynor, D., Weingrill, T., Dixon, P., Payne, H., et al. (2004). Day length variation and seasonal analyses of behaviour. South African Journal of Wildlife Research, 34, 39–44.

    Google Scholar 

  • Isbell, L. A., & Young, C. P. (1993). Social and ecological influences on activity budgets of vervet monkeys, and their implications for group living. Behavioral Ecology and Sociobiology, 32, 377–385.

    Article  Google Scholar 

  • IUCN (2012). IUCN Red List of Threatened Species. Version 2012.2. Retrieved from: www.iucnredlist.org. Accessed 24 Nov 2012.

  • Iwamoto, T., & Dunbar, R. I. M. (1983). Thermoregulation, habitat quality, and the behavioural ecology of gelada baboons. Journal of Animal Ecology, 52, 357–366.

    Article  Google Scholar 

  • Korstjens, A. H., Lehmann, J., & Dunbar, R. I. M. (2010). Resting time as an ecological constraint on primate biogeography. Animal Behaviour, 79, 361–374.

    Article  Google Scholar 

  • Li, Y., Liu, X., Liao, M., Yang, J., & Stanford, C. B. (2009). Characteristics of a group of Hubei golden snub-nosed monkeys (Rhinopithecus roxellana hubeiensis) before and after major snow storms. American Journal of Primatology, 71, 523–526.

    Article  PubMed  Google Scholar 

  • Mehlman, P. T. (1989). Comparative density, demography, and ranging behavior of Barbary macaques (Macaca sylvanus) in marginal and prime conifer habitats. International Journal of Primatology, 10, 269–292.

    Article  Google Scholar 

  • Ménard, N. (2002). Ecological plasticity of Barbary macaques (Macaca sylvanus). Evolutionary Anthropology, 11, 95–100.

    Article  Google Scholar 

  • Ménard, N., & Qarro, M. (1999). Bark stripping and water availability: a comparative study between Moroccan and Algerian Barbary macaques (Macaca sylvanus). Revue d’Ecologie, 54, 123–132.

    Google Scholar 

  • Ménard, N., & Vallet, D. (1997). Behavioral responses of Barbary macaque (Macaca sylvanus) to variations in environmental conditions in Algeria. American Journal of Primatology, 43, 285–304.

    Article  PubMed  Google Scholar 

  • Nakayama, Y., Matsuoka, S., & Watanuki, Y. (1999). Feeding rates and energy deficits of juvenile and adult Japanese monkeys in a cool temperate area with snow coverage. Ecological Research, 14, 291–301.

    Article  Google Scholar 

  • Ostner, J. (2002). Social thermoregulation in redfronted lemurs (Eulemur fulvus fulvus). Folia Primatologica, 73, 175–180.

    Article  Google Scholar 

  • Pinheiro, J. C., & Bates, D. M. (2000). Mixed effects models in S and S-PLUS. New York: Springer.

    Book  Google Scholar 

  • Robinson, J. G. (1984). Diurnal variation in foraging and diet in the wedge-capped capuchin Cebus olivaceus. Folia Primatologica, 43, 216–228.

    Article  Google Scholar 

  • Sato, H. (2012). Diurnal resting in brown lemurs in a dry deciduous forest, northwestern Madagascar: implications for seasonal thermoregulation. Primates, 53, 255–263.

    Article  PubMed  Google Scholar 

  • StataCorp. (2011). Stata statistical software: Release 12. Texas: Stata Press.

    Google Scholar 

  • Stelzner, J. K. (1988). Thermal effects on movement patterns of yellow baboons. Primates, 29, 91–105.

    Article  Google Scholar 

  • Stephens, D. W., & Krebs, J. R. (1986). Foraging theory. Princeton: Princeton University Press.

    Google Scholar 

  • Tabachnick, B. G., & Fidell, L. S. (2007). Using multivariate statistics. Boston: Pearson Education.

    Google Scholar 

  • Taub, D. M. (1984). A brief historical account of the recent decline in geographic distribution of the Barbary macaque in North Africa. In J. E. Fa (Ed.), The Barbary macaque: A case study in conservation (pp. 71–78). New York: Plenum Press.

    Chapter  Google Scholar 

  • van Doorn, A. C., O’Riain, M. J., & Swedell, L. (2010). The effects of extreme seasonality of climate and day length on the activity budget and diet of semi-commensal chacma baboons (Papio ursinus) in the Cape Peninsula of South Africa. American Journal of Primatology, 72, 104–112.

    PubMed  Google Scholar 

  • van Lavieren, E., & Wich, S. A. (2009). Decline of the Barbary macaques Macaca sylvanus in the cedar forest of the Middle Atlas Mountains, Morocco. Oryx, 44, 133–138.

    Article  Google Scholar 

  • Ventura, R., Majolo, B., Schino, G., & Hardie, S. (2005). Differential effects of ambient temperature and humidity on allogrooming, self-grooming, and scratching in wild Japanese macaques. American Journal of Physical Anthropology, 126, 453–457.

    Article  PubMed  Google Scholar 

  • Waters, S. S., Aksissou, M., El Harrad, A., Hobbelink, M. E., & Fa, J. E. (2007). Holding on in the Djebela: Barbary macaque Macaca sylvanus in northern Morocco. Oryx, 41, 106–108.

    Article  Google Scholar 

  • Xiang, Z. F., Huo, S., Xiao, W., Quan, R. C., & Grueter, C. C. (2007). Diet and feeding behavior of Rhinopithecus bieti at Xiaochangdu, Tibet: adaptations to a marginal environment. American Journal of Primatology, 69, 1141–1158.

    Article  PubMed  Google Scholar 

  • Zar, J. H. (1999). Biostatistical analysis. Upper Saddle River: Prentice Hall.

    Google Scholar 

Download references

Acknowledgments

We thank the Haut Commissariat aux Eaux et Forêts et à la Lutte Contre la Désertification of Morocco for research permission. We thank Marina Cords, Paul Garber, Joanna Setchell, and one anonymous reviewer for useful comments on an earlier draft of this manuscript. We also thank Laëtitia Maréchal, Pawel Fedurek, Paolo Piedimonte, Michael Madole, Dave Thomas, Sofia Santos, Maria Thunström, and Tom Smith for assistance in the field. We are grateful to Julia Ostner and Oliver Schülke for their valuable support to this study.

Author information

Authors and Affiliations

  1. School of Psychology, University of Lincoln, Lincoln, LN6 7TS, UK

    Bonaventura Majolo & Richard McFarland

  2. Brain Function Research Group, School of Physiology, University of the Witwatersrand, Parktown, Johannesburg, 2193, South Africa

    Richard McFarland

  3. Primate Social Evolution Group, Courant Research Centre Evolution of Social Behaviour, Georg-August University Göttingen, Göttingen, 37077, Germany

    Christopher Young

  4. École Nationale Forestière d’Ingénieurs, BP 511, Tabriquet, 1100, Salé, Morocco

    Mohamed Qarro

Authors
  1. Bonaventura Majolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard McFarland
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christopher Young
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohamed Qarro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bonaventura Majolo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Majolo, B., McFarland, R., Young, C. et al. The Effect of Climatic Factors on the Activity Budgets of Barbary Macaques (Macaca sylvanus). Int J Primatol 34, 500–514 (2013). https://doi.org/10.1007/s10764-013-9678-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-013-9678-8

Keywords

Search

Navigation