Fecal contamination, parasite risk, and waterhole use by wild animals in a dry deciduous forest
Waterholes are critically important to animal survival in dry habitats but are also a potential source of parasite exposure. Avoiding feces may effectively reduce parasite transmission risk, but may also impose costs, including greater travel distances to locate less contaminated resources. We studied factors influencing wild, water-dependent red-fronted lemurs’ (Eulemur rufifrons) selection of waterholes, including factors related to trade-offs between energy expenditure and parasite avoidance. Research took place in a dry deciduous forest in western Madagascar characterized by water scarcity during a pronounced local dry season. We tested whether fecal contamination influenced lemurs’ water selection with an experiment that gave lemurs a choice between clean and fecally contaminated water disinfected by boiling. We also monitored lemurs’ use of natural waterholes to determine how conspecific fecal contamination and travel distance influenced lemurs’ use of waterholes. Red-fronted lemurs displayed a strong preference for clean water in the experiment. At natural waterholes, we found a significant negative interaction between frequency of previous lemur visits and fecal contamination, and a longer return time to waterholes with increasing fecal contamination, revealing that lemurs returned to less contaminated waterholes more frequently and sooner. We also found that lemurs prioritized shorter travel distances over feces avoidance. Together, these results suggest that red-fronted lemurs exercised their preferences for avoiding parasite risk in their natural waterhole choices by avoiding highly contaminated waterholes, especially when waterholes were equidistant. Thus, fecal contamination and travel distance influence water selection in water-scarce habitats, with potential impacts on habitat use and ecological interactions.
Animals can take many measures to avoid becoming infected with parasites. One strategy involves avoiding reliable indicators of parasite presence, such as feces. Although avoiding feces may have many benefits, it may also have costs, such as when essential resources, like waterholes in a dry forest, inevitably become contaminated by the animals that use them. Using a choice experiment, we demonstrated that wild red-fronted lemurs preferred to avoid fecal contamination of water sources. From observations of lemurs’ waterhole choices, we determined that lemurs exercised this preference most when choosing among nearby waterholes, thus prioritizing energy conservation, and secondarily reducing the costs of parasite exposure risk. Avoidance of feces may thus have effects on lemurs’ patterns of habitat use and ecological interactions.
KeywordsDrinking Feces avoidance Field experiment Lemur Parasite avoidance Water
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 also would like to thank MICET (Madagascar Institute for the Conservation of Tropical Environments) for their support and facilitation of permits. We thank an anonymous reviewer for comments on the manuscript.
This work was financially supported by the National Science Foundation Doctoral Dissertation Research Improvement Grant (1613482), the Margot Marsh Biodiversity Foundation, Primate Conservation, Inc., and Duke Graduate School International Dissertation Travel Grant.
Compliance with ethical standards
The protocol for this research was approved by Duke University’s Institutional Animal Care and Use Committee (Protocol A008-17-01) and the Malagasy Ministry of the Environment, Water, and Forests. All applicable international, national, and/or institutional guidelines for the use of animals were followed.
Conflict of interest
The authors declare that they have no conflicts of interest.
- Hutchings MR, Kyriazakis I, Gordon IJ (2001) Herbivore physiological state affects foraging trade-off decisions between nutrient intake and parasite avoidance. Ecology 82:1138–1150. https://doi.org/10.1890/0012-9658(2001)082[1138:HPSAFT]2.0.CO;2 CrossRefGoogle Scholar
- Kokko H, Ranta E, Ruxton G, Lundberg P (2002) Sexually transmitted disease and the evolution of mating systems. Evolution 56:1091–1100. https://doi.org/10.1111/j.0014-3820.2002.tb01423.x CrossRefPubMedGoogle Scholar
- Moore J (2002) Parasites and the behavior of animals. Oxford University Press, New YorkGoogle Scholar
- Palumbo F, Ziglio G, Van der Beken A (2002) Detection methods of algae, protozoa, and helminths in fresh and drinking water. Wiley, New YorkGoogle Scholar
- Pyritz LW, Kappeler PM, Fichtel C (2011) Coordination of group movements in wild red-fronted lemurs (Eulemur rufifrons): processes and influence of ecological and reproductive seasonality. Int J Primatol 32:1325–1347. https://doi.org/10.1007/s10764-011-9549-0 CrossRefPubMedPubMedCentralGoogle Scholar
- Scholz F, Kappeler PM (2004) Effects of seasonal water scarcity on the ranging behavior of Eulemur fulvus rufus. Int J Primatol 25:599–613. https://doi.org/10.1023/B:IJOP.0000023577.32587.0b CrossRefGoogle Scholar
- Vicente J, Höfle U, Garrido JM, Fernandez-de-Mera IG, Acevedo P, Juste R, Barral M, Gortazar C (2007) Risk factors associated with the prevalence of tuberculosis-like lesions in fenced wild boar and red deer in south central Spain. Vet Res 38:451–464. https://doi.org/10.1051/vetres:2007002 CrossRefPubMedGoogle Scholar