Skip to main content

Advertisement

SpringerLink
Log in

Water Availability Impacts Habitat Use by Red-Fronted Lemurs (Eulemur rufifrons): An Experimental and Observational Study

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

Abstract

With the predicted increase in extreme weather events as a result of global climate change, animals living in dry or seasonally dry habitats are likely to experience dramatic fluctuations in water availability from season to season and year to year. Understanding how animals respond to short-term changes in water availability is paramount for future conservation and management of water-dependent wild populations. We investigated how short-term changes to the availability of water influenced habitat use of four groups of red-fronted lemurs (Eulemur rufifrons) in a dry deciduous forest in western Madagascar using detailed spatial data collected from GPS collars over 15 weeks. We experimentally manipulated water availability in the habitat and compared ranging patterns of the lemurs during the experiments to those before and after the experiments. Lemur groups shifted the intensity of their habitat use relative to changes in natural and experimental water availability. Specifically, lemurs were more likely to spend time in areas near experimental water sources during the experiment than in the same areas without water. Lemurs were less likely to spend time near previous habitual water sources when experimental water sources were available. We observed shifts in ranging intensity in response to natural changes to water availability when waterholes disappeared across the dry season. Our findings support the importance of water for shaping wild animal ranging patterns. We propose that water should be a primary consideration in future studies of habitat use, especially given the potential for climate change and human land use to further alter water availability for wild animals.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alba-Mejia, L., Caillaud, D., Montenegro, O. L., Sánchez-Palomino, P., & Crofoot, M. C. (2013). Spatiotemporal interactions among three neighboring groups of free-ranging white-footed tamarins (Saguinus leucopus) in Colombia. International Journal of Primatology, 34(6), 1281–1297.

    Google Scholar 

  • Alberts, S. C. (2018). Social influences on survival and reproduction: Insights from a long-term study of wild baboons. Journal of Animal Ecology, 88, 1–20.

    Google Scholar 

  • Altmann, J., Hausfater, G., & Altmann, S. A. (1985). Demography of Amboseli baboons, 1963–1983. American Journal of Primatology, 8(2), 113–125.

    PubMed  Google Scholar 

  • Amorim, F., Jorge, I., Beja, P., & Rebelo, H. (2018). Following the water? Landscape-scale temporal changes in bat spatial distribution in relation to Mediterranean summer drought. Ecology and Evolution, 8, 5801–5814.

    PubMed  PubMed Central  Google Scholar 

  • Amoroso, C. R., Frink, A. G., & Nunn, C. L. (2017). Water choice as a counterstrategy to faecally transmitted disease: An experimental study in captive lemurs. Behaviour, 154, 1239–1258.

    Google Scholar 

  • Amoroso, C. R., Kappeler, P. M., Fichtel, C., & Nunn, C. L. (2019). Fecal contamination, parasite risk, and waterhole use by wild animals in a dry deciduous forest. Behavioral Ecology and Sociobiology, 73, 153.

    Google Scholar 

  • Baker, A. (2003). Land use and water quality. Hydrological Processes, 17(12), 2499–2501.

    Google Scholar 

  • Barton, R. A., Whiten, A., Strum, S. C., Byrne, R. W., & Simpson, A. J. (1992). Habitat use and resource availability in baboons. Animal Behaviour, 43(5), 831–844.

    Google Scholar 

  • Bleich, V. C., Marshal, J. P., & Andrew, N. G. (2010). Habitat use by a desert ungulate: Predicting effects of water availability on mountain sheep. Journal of Arid Environments, 74(6), 638–645.

    Google Scholar 

  • Boroski, B. B., & Mossman, A. S. (1996). Distribution of mule deer in relation to water sources in northern California. The Journal of Wildlife Management, 60(4), 770–776.

    Google Scholar 

  • Campos, F. A., & Fedigan, L. M. (2009). Behavioral 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(1), 101–111.

    PubMed  Google Scholar 

  • Clapp, J. G., & Beck, J. L. (2016). Short-term impacts of fire-mediated habitat alterations on an isolated bighorn sheep population. Fire Ecology, 12(3), 80–98.

    Google Scholar 

  • Crofoot, M. C. (2013). The cost of defeat: Capuchin groups travel further, faster and later after losing conflicts with neighbors. American Journal of Physical Anthropology, 152(1), 79–85.

    PubMed  Google Scholar 

  • Curtis, V. a. (2014). Infection-avoidance behaviour in humans and other animals. Trends in Immunology, 35(10), 457–464.

    CAS  PubMed  Google Scholar 

  • Davies, N., Gramotnev, G., Seabrook, L., Bradley, A., Baxter, G., et al (2013). Movement patterns of an arboreal marsupial at the edge of its range: A case study of the koala. Movement Ecology, 1(1), 1–15.

    Google Scholar 

  • DeFries, R., & Eshleman, K. N. (2004). Land-use change and hydrologic processes: A major focus for the future. Hydrological Processes, 18(11), 2183–2186.

    Google Scholar 

  • Desbureaux, S., & Damania, R. (2018). Rain, forests and farmers: Evidence of drought induced deforestation in Madagascar and its consequences for biodiversity conservation. Biological Conservation, 221(October), 357–364.

    Google Scholar 

  • Dias, P. A. D., Rangel-Negrín, A., Coyohua-Fuentes, A., & Canales-Espinosa, D. (2014). Factors affecting the drinking behavior of black howler monkeys (Alouatta pigra). Primates, 55(1), 1–5.

    PubMed  Google Scholar 

  • Foley, C., Pettorelli, N., & Foley, L. (2008). Severe drought and calf survival in elephants. Biology Letters, 4(5), 541–544.

    PubMed  PubMed Central  Google Scholar 

  • Gordon, G., Brown, A. S., & Pulsford, T. (1988). A koala (Phascolarctos cinereus Goldfuss) population crash during drought and heatwave conditions in south-western Queensland. Australian Journal of Ecology, 13(4), 451–461.

    Google Scholar 

  • Hamilton, W. J. (1985). Demographic consequences of a food and water shortage to desert chacma baboons, Papio ursinus. International Journal of Primatology, 6(5), 451–462.

    Google Scholar 

  • Herrera, J. P., Borgerson, C., Tongasoa, L., Andriamahazoarivosoa, P., Rasolofoniaina, B. J. R., et al (2018). Estimating the population size of lemurs based on their mutualistic food trees. Journal of Biogeography, 45, 2546–2563.

    Google Scholar 

  • Horne, J. S., Garton, E. O., Krone, S. M., & Lewis, J. S. (2007). Analyzing animal movements using Brownian Bridges. Ecology, 88(9), 2354–2363.

    PubMed  Google Scholar 

  • Jackson, R. B., Carpenter, S. R., Dahm, C. N., McKnight, D. M., Naiman, R. J., et al (2001). Water in a changing world. Ecological Applications, 11(4), 1027–1045.

    Google Scholar 

  • Janson, C. (2014). Death of the (traveling) salesman: Primates do not show clear evidence of multi-step route planning. American Journal of Primatology, 76(5), 410–420.

    PubMed  Google Scholar 

  • Janson, C. H., & Di Bitetti, M. S. (1997). Experimental analysis of food detection in capuchin monkeys: Effects of distance, travel speed, and resource size. Behavioral Ecology and Sociobiology, 41(1), 17–24.

    Google Scholar 

  • Jolly, A. (2013). Berenty Reserve, Madagascar: A long time in a small space. In P. M. Kappeler & D. P. Watts (Eds.), Long-term field studies of primates (pp. 21–44). Berlin and Heidelberg: Springer-Verlag.

    Google Scholar 

  • Kappeler, P. M., & Fichtel, C. (2012). A 15-year perspective on the social organization and life history of the sifaka in Kirindy Forest. In P. M. Kappeler & D. P. Watts (Eds.), Long-term field studies of primates (pp. 101–121). Berlin and Heidelberg: Springer-Verlag.

    Google Scholar 

  • Kappeler, P. M., & Fichtel, C. (2015). Eco-evo-devo of the lemur syndrome: Did adaptive behavioral plasticity get canalized in a large primate radiation?, 12, 1–16.

    Google Scholar 

  • Kelley, E. (2011). Lemur catta in the Region of Cap Sainte-Marie, Madagascar: Introduced cacti, xerophytic Didiereaceae-Euphorbia bush, and tombs. Washington University in St. Louis. Retrieved from http://openscholarship.wustl.edu/etd%0A, http://openscholarship.wustl.edu/etd/176

  • Kelley, E. A. (2013). The ranging behavior of Lemur catta in the region of Cap Sainte-Marie, Madagascar. American Journal of Physical Anthropology, 150(1), 122–132.

    PubMed  Google Scholar 

  • Kittle, A. M., Bukombe, J. K., Sinclair, A. R. E., Mduma, S. A. R., & Fryxell, J. M. (2015). Landscape-level movement patterns by lions in western Serengeti: Comparing the influence of inter-specific competitors, habitat attributes and prey availability. Movement Ecology, 4(1), 1–18.

    Google Scholar 

  • Knight, M. H. (1995). Drought-related mortality of wildlife in the southern Kalahari and the role of man. African Journal of Ecology, 33(4), 377–394.

    Google Scholar 

  • Koch, F., Signer, J., Kappeler, P. M., & Fichtel, C. (2016). The role of the residence-effect on the outcome of intergroup encounters in Verreaux’s sifakas. Scientific Reports, 6(June), 1–7.

    Google Scholar 

  • Korine, C., Adams, R., Russo, D., Fisher-Phelps, M., & Jacobs, D. (2015). Bats and water: anthropogenic alterations threaten global bat populations. In C. C. Voigt & T. Kingston (Eds.), Bats in the Anthropocene: Conservation of bats in a changing world (pp. 215–240). Cham, Switzerland: Springer International.h.

    Google Scholar 

  • Kranstauber, B., Kayss, R., Lapoint, S. D., Wikelski, M., & Safi, K. (2012). A dynamic Brownian bridge movement model to estimate utilization distributions for heterogeneous animal movement. Journal of Animal Ecology, 81(4), 738–746.

    Google Scholar 

  • Marshal, J. P., Bleich, V. C., Krausman, P. R., Reed, M. L., & Andrew, N. G. (2006). Factors affecting habitat use and distribution of desert mule deer in an arid environment. Wildlife Society Bulletin, 34(3), 609–619.

    Google Scholar 

  • Mercado Malabet, F. M., & Colquhoun, I. C. (2018). Realized habitat choices of crowned lemurs (Eulemur coronatus) in a heavily disturbed forest fragment: A case study of flexible distribution patterns. In Program of the 87th meeting of the American Association of Physical Anthropologists (p. 175).

    Google Scholar 

  • Ndlovu, M., Pérez-Rodríguez, A., Devereux, E., Thomas, M., Colina, A., & Molaba, L. (2018). Water for African elephants (Loxodonta africana): Faecal microbial loads affect use of artificial waterholes. Biology Letters, 14(8), 20180360.

    PubMed  PubMed Central  Google Scholar 

  • Noser, R., & Byrne, R. W. (2007). Travel routes and planning of visits to out-of-sight resources in wild chacma baboons, Papio ursinus. Animal Behaviour, 73(2), 257–266.

    Google Scholar 

  • Noser, R., & Byrne, R. W. (2014). Change point analysis of travel routes reveals novel insights into foraging strategies and cognitive maps of wild baboons. American Journal of Primatology, 76(5), 399–409.

    PubMed  Google Scholar 

  • Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & Team, R. C. (2018). nlme: Linear and Nonlinear Mixed Effects Models. R package version. https://cran.r-project.org/package=nlme.

  • Pinkus, S., Smith, J. N. M., & Jolly, A. (2005). Feeding competition between introduced Eulemur fulvus and native Lemur catta during the birth season at Berenty Reserve, southern Madagascar. In A. Jolly, R. W. Sussman, N. Koyama, & H. Rasamimanana (Eds.), Ringtailed lemur biology: Lemur catta in Madagascar (pp. 119–140). Developments in Primatology: Progress and Prospects). New York: Springer Science+Business Media.

    Google Scholar 

  • Poirotte, C., Benhamou, S., Mandjembe, A., Willaume, E., Kappeler, P. M., & Charpentier, M. J. E. (2017). Gastrointestinal parasitism and recursive movements in free-ranging mandrills. Animal Behaviour, 134, 87–98.

    Google Scholar 

  • Purdon, A., & van Aarde, R. J. (2017). Water provisioning in Kruger National Park alters elephant spatial utilisation patterns. Journal of Arid Environments, 141, 45–51.

    Google Scholar 

  • Pyritz, L. W., Fichtel, C., Huchard, E., & Kappeler, P. M. (2013). Determinants and outcomes of decision-making, group coordination and social interactions during a foraging experiment in a wild primate. PLoS ONE, 8(1), e53144.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pyritz, L. W., Kappeler, P. M., & Fichtel, C. (2011). Coordination of group movements in wild red-fronted lemurs (Eulemur rufifrons): Processes and influence of ecological and reproductive seasonality. International Journal of Primatology, 32(6), 1325–1347.

    PubMed  PubMed Central  Google Scholar 

  • R Development Core Team, R (2011). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  • Rehnus, M., Marconi, L., Hacklànder, K., & Filli, F. (2013). Seasonal changes in habitat use and feeding strategy of the mountain hare (Lepus timidus) in the Central Alps. Hystrix, 24(2), 161–165.

    Google Scholar 

  • Rosinger, A., & Tanner, S. (2015). Water from fruit or the river? Examining hydration strategies and gastrointestinal illness among Tsimane’ adults in the Bolivian Amazon. Public Health Nutrition, 18(6), 1098–1108.

    PubMed  Google Scholar 

  • Sapir, N., Abramsky, Z., Shochat, E., & Izhaki, I. (2004). Scale-dependent habitat selection in migratory frugivorous passerines. Naturwissenschaften, 91(11), 544–547.

    CAS  PubMed  Google Scholar 

  • Sapolsky, R. M. (1986). Endocrine and behavioral correlates of drought in wild olive baboons (Papio anubis). American Journal of Primatology, 11(3), 217–227.

    CAS  PubMed  Google Scholar 

  • Sawyer, H., Kauffman, M. J., Nielson, R. M., & Horne, J. S. (2009). Identifying and prioritizing ungulate migration routes for landscape-level conservation. Ecological Applications, 19(8), 2016–2025.

    PubMed  Google Scholar 

  • Schlaepfer, D. R., Bradford, J. B., Lauenroth, W. K., Munson, S. M., Tietjen, B., et al (2017). Climate change reduces extent of temperate drylands and intensifies drought in deep soils. Nature Communications, 8, 1–9.

    Google Scholar 

  • Schnoell, A. V., & Fichtel, C. (2012). Wild redfronted lemurs (Eulemur rufifrons) use social information to learn new foraging techniques. Animal Cognition, 15(4), 505–516.

    PubMed  PubMed Central  Google Scholar 

  • Scholz, F., & Kappeler, P. M. (2004). Effects of seasonal water scarcity on the ranging behavior of Eulemur fulvus rufus. International Journal of Primatology, 25(3), 599–613.

    Google Scholar 

  • Seidel, D. P., & Boyce, M. S. (2015). Patch-use dynamics by a large herbivore. Movement Ecology, 3(1), 1–10.

    Google Scholar 

  • Simpson, N. O., Stewart, K. M., & Bleich, V. C. (2011). What have we learned about water developments for wildlife? Not enough! California Fish and Game, 97(4), 109–209.

    Google Scholar 

  • Springer, A., Razafimanantsoa, L., Fichtel, C., & Kappeler, P. M. (2015). Comparison of three short-term immobilization regimes in wild verreaux’s sifakas (Propithecus verreauxi): ketamine–xylazine, ketamine–xylazine–atropine, and tiletamine–zolazepam. Journal of Zoo and Wildlife Medicine, 46(3), 482–490.

    PubMed  Google Scholar 

  • Switalski, A. B., & Bateman, H. L. (2017). Anthropogenic water sources and the effects on Sonoran Desert small mammal communities. PeerJ, 5, e4003.

    PubMed  PubMed Central  Google Scholar 

  • Trenberth, K. E., Dai, A., van der Schrier, G., Jones, P. D., Barichivich, J., et al (2014). Global warming and changes in drought. Nature Climate Change, 4(1), 17–22.

    Google Scholar 

  • Tsurim, I., Sapir, N., Belmaker, J., Shanni, I., Izhaki, I., et al (2008). Drinking water boosts food intake rate, bnody mass increase, and fat accumulation in migratory blackcaps (Sylvia stricapilla). Oecologia, 156, 21–30.

    PubMed  Google Scholar 

  • van Gils, J. A., van der Geest, M., De Meulenaer, B., Gillis, H., Piersma, T., & Folmer, E. O. (2015). Moving on with foraging theory: Incorporating movement decisions into the functional response of a gregarious shorebird. Journal of Animal Ecology, 84(2), 554–564.

    Google Scholar 

  • Viana, D. S., Granados, J. E., Fandos, P., Pérez, J. M., Cano-Manuel, F. J., et al (2018). Linking seasonal home range size with habitat selection and movement in a mountain ungulate. Movement Ecology, 6(1), 1–11.

    PubMed  PubMed Central  Google Scholar 

  • Wanders, N., & Wada, Y. (2015). Human and climate impacts on the 21st century hydrological drought. Journal of Hydrology, 526(August), 208–220.

    Google Scholar 

Download references

Acknowledgments

We would like to thank Léonard Razafimanantsoa and the field assistants and staff of the German Primate Center (DPZ) Research Station at Kirindy Forest and the CNFEREF Morondava for supporting our study. We appreciate Mael Jaonasy Frangico’s valuable assistance with the data collection for this project. We thank James Herrera for feedback on the analytical methods and three anonymous reviewers, Dr. Onja Razafindratsima, and Prof. Joanna Setchell for feedback on the manuscript. We also would like to thank MICET (Madagascar Institute for the Conservation of Tropical Environments) for their support and facilitation of permits. This study was funded by NSF-1613482, the Margot Marsh Biodiversity Foundation, Primate Conservation, Inc., and Duke Graduate School International Dissertation Travel Grant.

Author information

Authors and Affiliations

  1. Department of Evolutionary Anthropology, Duke University, Durham, NC, 27708, USA

    Caroline R. Amoroso & Charles L. Nunn

  2. Behavioral Ecology and Sociobiology Unit, German Primate Center – Leibniz Institute for Primate Research, Göttingen, Germany

    Peter M. Kappeler & Claudia Fichtel

  3. Department of Sociobiology/Anthropology, University of Göttingen, Göttingen, Germany

    Peter M. Kappeler

  4. Duke Global Health Institute, Duke University, Durham, NC, USA

    Charles L. Nunn

Authors
  1. Caroline R. Amoroso
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter M. Kappeler
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claudia Fichtel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Charles L. Nunn
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CRA conceived and designed the study with input from CLN, PMK, and CF. CRA carried out the study and analyzed the data. PMK and CF provided logistical support. CRA wrote the manuscript; other authors provided editorial advice.

Corresponding author

Correspondence to Caroline R. Amoroso.

Additional information

Handling Editor: Onja H. Razafindratsima

Electronic supplementary material

ESM 1

(DOCX 25 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Amoroso, C.R., Kappeler, P.M., Fichtel, C. et al. Water Availability Impacts Habitat Use by Red-Fronted Lemurs (Eulemur rufifrons): An Experimental and Observational Study. Int J Primatol 41, 61–80 (2020). https://doi.org/10.1007/s10764-020-00136-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-020-00136-9

Keywords

Search

Navigation