Water choice as a counterstrategy to faecally transmitted disease: an experimental study in captive lemurs

in Behaviour
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?

Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.


Have Institutional Access?

Access content through your institution. Any other coaching guidance?



Many parasites and pathogens are transmitted via water, including through faecal contamination of water sources. Yet water is essential for survival, and some species gain nutritional and other benefits from coprophagy. We investigated how primates balance the risks of faecal pathogen transmission with potential benefits of faeces ingestion in their selection of water sources by conducting behavioural experiments with five species of lemurs (Family Lemuridae) in captivity. Subjects were given a choice between clean water and water ‘contaminated’ with disinfected faecal material, which contained cues associated with faecally transmitted parasites, but minimal risk. We found that lemurs exhibited strong preferences for the clean water. This pattern was supported even at low levels of faecal contamination and in species adapted to water-limited habitats, for which choosiness about water quality could present a dehydration risk. Our results strongly support the hypothesis that avoiding faecal contamination is important in water selection.



Behringer, D.C., Butler, M.J. & Shields, J.D. (2006). Avoidance of disease by social lobsters. — Nature 441: 421.

Bertolani, P. & Pruetz, J.D. (2011). Seed reingestion in savannah chimpanzees (Pan troglodytes verus) at Fongoli, Senegal. — Int. J. Primatol. 32: 1123-1132.

Bouwman, K.M. & Hawley, D.M. (2010). Sickness behaviour acting as an evolutionary trap? Male house finches preferentially feed near diseased conspecifics. — Biol. Lett. 6: 462-465.

Combes, C. (2001). Parasitism: the ecology and evolution of intimate interactions. — University of Chicago Press, Chicago, IL.

Cooper, J., Gordon, I.J. & Pike, A.W. (2000). Strategies for the avoidance of faeces by grazing sheep. — Appl. Anim. Behav. Sci. 69: 15-33.

Crowell-Davis, S.L. & Caudle, A.B. (1989). Coprophagy by foals: recognition of maternal feces. — Appl. Anim. Behav. Sci. 24: 267-272.

Curtis, V.A. (2014). Infection avoidance behaviour in humans and other animals. — Trends Immunol. 35: 457-464.

Fish, K.D., Sauther, M.L., Loudon, J.E. & Cuozzo, F.P. (2007). Coprophagy by wild ring-tailed lemurs (Lemur catta) in human-disturbed locations adjacent to the Beza Mahafaly Special Reserve, Madagascar. — Am. J. Primatol. 69: 713-718.

Garner, C.E., Smith, S., de Lacy Costello, B., White, P., Spencer, R., Probert, C.S.J. & Ratcliffe, N.M. (2007). Volatile organic compounds from feces and their potential for diagnosis of gastrointestinal disease. — FASEB J. 21: 1675-1688.

Gemmill, A. & Gould, L. (2008). Microhabitat variation and its effects on dietary composition and intragroup feeding interactions between adult female Lemur catta during the dry season at Beza Mahafaly Special Reserve, southwestern Madagascar. — Int. J. Primatol. 29: 1511-1533.

Goodman, S.M. & Bensted, J.P. (eds) (2007). The natural history of Madagascar. — University of Chicago Press, Chicago, IL.

Harcourt, A.H. & Stewart, K.J. (1978). Coprophagy by wild mountain gorilla. — Afr. J. Ecol. 16: 223-225.

Hart, B.L. (1990). Behavioral adaptatons to pathogens and parasites: five strategies. — Neurosci. Biobehav. Rev. 14: 273-294.

Hart, B.L. (1992). Behavioral adaptations to parasites: an ethological approach. — J. Parasitol. 78: 256-265.

Hart, B.L. (1994). Behavioural defense against parasites: interaction with parasite invasiveness. — Parasitology 109: S139-S151.

Hart, B.L. (2011). Behavioural defences in animals against pathogens and parasites: parallels with the pillars of medicine in humans. — Philos. Trans. Roy. Soc. B: Biol. Sci. 366: 3406-3417.

Hausfater, G. & Meade, B.J. (1982). Alternation of sleeping groves by yellow baboons (Papio cynocephalus) as a strategy for parasite avoidance. — Primates 23: 287-297.

Hirakawa, H.I.R. (2001). Coprophagy in leporids and other mammalian herbivores. — Mammal Rev. 31: 61-80.

Hladik, C.M., Charles-Dominique, P., Valdebouze, P., Delort-Laval, J. & Flanzy, J. (1971). Caecotrophy in a phyllophagous primate of the genus Lepilemur and correlations with the peculiarities of its digestive system. — C. R. Acad. Sci. Hebd. Seances. Acad. Sci. D 272: 3191-3194.

Hook, M.A., Lambeth, S.P., Perlman, J.E., Stavisky, R., Bloomsmith, M.A. & Schapiro, S.J. (2002). Inter-group variation in abnormal behavior in chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). — Appl. Anim. Behav. Sci. 76: 165-176.

Hopper, L.M., Freeman, H.D. & Ross, S.R. (2016). Reconsidering coprophagy as an indicator of negative welfare for captive chimpanzees. — Appl. Anim. Behav. Sci. 176: 112-119.

Hutchings, M.R., Athanasiadou, S., Kyriazakis, I. & Gordon, I.J. (2003). Can animals use foraging behaviour to combat parasites?P. Nutr. Soc. 62: 361-370.

Hutchings, M.R., Kyriazakis, I., Papachristou, T.G., Gordon, I.J. & Jackson, F. (2000). The herbivores’ dilemma: trade-offs between nutrition and parasitism in foraging decisions. — Oecologia 124: 242-251.

Jacobs, G.H. (2008). Primate color vision: a comparative perspective. — Visual Neurosci. 25: 619-633.

Kavaliers, M., Choleris, E. & Pfaff, D.W. (2005). Recognition and avoidance of the odors of parasitized conspecifics and predators: differential genomic correlates. — Neurosci. Biobehav. Rep. 29: 1347-1359.

Kiesecker, J.M., Skelly, D.K., Beard, K.H. & Preisser, E. (1999). Behavioral reduction of infection risk. — Proc. Natl Acad. Sci. USA 96: 9165-9168.

Kilpatrick, S.J., Lee, T.M. & Moltz, H. (1983). The maternal pheromone of the rat: testing some assumptions underlying a hypothesis. — Physiol. Behav. 30: 539-543.

Koch, H. & Schmid-Hempel, P. (2011). Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. — Proc. Natl Acad. Sci. USA 108: 19288-19292.

Krause, J. & Godin, J.G.J. (1996). Influence of parasitism on shoal choice in the banded killifish (Fundulus diaphanus, Teleostei, Cyprinodontidae). — Ethology 102: 40-49.

Krief, S., Jamart, A. & Hladik, C.M. (2004). On the possible adaptive value of coprophagy in free-ranging chimpanzees. — Primates 45: 141-145.

Leonhardt, S.D., Tung, J., Camden, J.B., Leal, M. & Drea, C.M. (2009). Seeing red: behavioral evidence of trichromatic color vision in strepsirrhine primates. — Behav. Ecol. 20: 1-12.

Markham, A.C., Alberts, S.C. & Altmann, J. (2016). Haven for the night: sleeping site selection in a wild primate. — Behav. Ecol. 27: 29-35.

Mittermeier, R.A., Louis, E.E., Richardson, M., Schwitzer, C., Langrand, O., Rylands, A.B., Hawkins, F., Rajaobelina, S., Ratsimbazafy, J., Rasoloarison, R., Roos, C., Kappeler, P.M. & MacKinnon, J.M. (2010). Lemurs of Madagascar, 3rd edn.Conservation International, Washington, DC.

Moore, J. (2002). Parasites and the behavior of animals. — Oxford University Press, New York, NY.

Müller-Graf, C.D., Collins, D.A., Packer, C. & Woolhouse, M.E. (1997). Schistosoma mansoni infection in a natural population of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. — Parasitol. 115: 621-627.

Nunn, C.L. & Altizer, S. (2006). Infectious diseases in primates: behavior, ecology, and evolution. — Oxford University Press, New York, NY.

Nunn, C.L., Thrall, P.H. & Kappeler, P.M. (2014). Shared resources and disease dynamics in spatially structured populations. — Ecol. Model. 272: 198-207.

Patz, J.A., Graczyk, T.K., Geller, N. & Vittor, A.Y. (2000). Effects of environmental change on emerging parasitic diseases. — Int. J. Parasitol. 30: 1395-1405.

Perry, R. (1999). Desiccation survival of parasitic nematodes. — Parasitology 119: S19-S30.

Poirotte, C., Massol, F., Herbert, A., Willaume, E., Bomo, P.M., Kappeler, P.M. & Charpentier, M.J.E. (2017). Mandrills use olfaction to socially avoid parasitized conspecifics. — Sci. Adv. 3: e1601721.

Sakamaki, T. (2010). Coprophagy in wild bonobos (Pan paniscus) at Wamba in the Democratic Republic of the Congo: a possibly adaptive strategy?Primates 51: 87-90.

Sarabian, C. & MacIntosh, A.J.J. (2015). Hygienic tendencies correlate with low geohelminth infection in free-ranging macaques. — Biol. Lett. 11: 20150757.

Slifko, T.R., Smith, H.V. & Rose, J.B. (2000). Emerging parasite zoonoses associated with water and food. — Int. J. Parasitol. 30: 1379-1393.

Soave, O. & Brand, C.D. (1991). Coprophagy in animals: a review. — Cornell Vet. 81: 357-364.

Troyer, K. (1984). Behavioral acquisition of the hindgut fermentation system by hatchling Iguana iguana. — Behav. Ecol. Sociobiol. 14: 189-193.

Willms, W.D., Kenzie, O.R., McAllister, T.A., Colwell, D., Veira, D., Wilmshurst, J.F., Entz, T. & Olson, M.E. (2002). Effects of water quality on cattle performance. — J. Range Manage. 55: 452-460.


  • Experimental setup. (a) Experiment 1, choice test between clean tap water and water ‘contaminated’ with disinfected faeces; (b) Experiment 2, choice test between clean tap water and water ‘contaminated’ with disinfected faeces, but filtered and diluted; (c) Experiment 3, habituation test, same as Experiment 1, but with blue colour dye added to both choices.

    View in gallery
  • All drinking events recorded in the three experiments. Asterisks denote significant difference from chance (0.5) in a binomial test: p<0.0001, ∗∗p<0.0005.

    View in gallery
  • Results of Experiments 1, 2 and 3.

    View in gallery
  • All drinking events recorded in Experiment 2. Results of the choice test with dilute stimulus, separated by species.

    View in gallery


Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 13 13 10
Full Text Views 6 6 6
PDF Downloads 3 3 3
EPUB Downloads 0 0 0