Advertisement

Chimpanzee (Pan troglodytes schweinfurthii) Group Sleep and Pathogen-Vector Avoidance: Experimental Support for the Encounter-Dilution Effect

Abstract

Sleep is essential for survival, yet it represents a time of extreme vulnerability, including through exposure to parasites and pathogens transmitted by biting insects. To reduce the risks of exposure to vector-borne disease, the encounter-dilution hypothesis proposes that the formation of groups at sleep sites is influenced by a “selfish herd” behavior, where individuals dilute risk by sleeping with other group members. To investigate this hypothesis in the context of chimpanzee (Pan troglodytes schweinfurthii) sleep site selection, we employed four light traps that we also baited with nontoxic chemical attractants to capture insects throughout the night. Across 74 nights with 294 traps set, we collected 66,545 individual insects. Consistent with the encounter-dilution hypothesis, we found that insect exposure, inferred by absolute numbers of insects caught in nighttime traps, was strongly influenced by the grouping of traps. Specifically, single traps caught more insects—including vector transmitting female mosquitoes—than grouped traps, and the number of insects caught increased with increasing distance between grouped traps. Moreover, ground sleep sites caught fewer insects than arboreal sleep sites. In addition, traps associated with Cynometra alexandri trees resulted in significantly lower catch rates than Pseudospondias microcarpa–associated traps. Our results suggest wild chimpanzees use group sleep as a strategy to avoid biting insects that serve as hosts for vector-borne diseases.

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

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

Change history

  • 10 January 2020

    The original version of this article unfortunately contained a mistake in the authorgroup section.

References

  1. Allan, C., Sivell, D., & Lee, T. (1996). Semuliki (Toro) Game Reserve, Uganda: Results of the Frontier-Uganda Biological Assessment. Society for Environmental Exploration, Report No. 7.

  2. Altizer, S., Nunn, C. L., Thrall, P. H., Gittleman, J. L., Antonovics, J., et al (2003). Social organization and parasite risk in mammals: Integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics, 34, 517–547.

  3. Anderson, J. R. (1998). Sleep, sleeping sites, and sleep-related activities: Awakening to their significance. American Journal of Primatology, 46(1), 63–75.

  4. Baldwin, P. J., Sabater Pi, J., McGrew, W. C., & Tutin, C. E. G. (1981). Comparisons of nests made by different populations of chimpanzees (Pan troglodytes). Primates, 22, 474–486.

  5. Bartoń, K. (2015). version 1.15.6.

  6. Bates, D., Maecher, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1–48.

  7. Brownlow, A. R., Plumptre, A. J., Reynolds, V., & Ward, R. (2001). Sources of variation in the nesting behavior of chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda. American Journal of Primatology, 55(1), 49–55.

  8. Capellini, I., Barton, R. A., McNamara, P., Preston, B., & Nunn, C. L. (2008). Ecology and evolution of mammalian sleep. Evolution, 62, 1764–1776.

  9. Coolidge, F. L., & Wynn, T. (2006). The effects of the tree-to-ground sleep transition in the evolution of cognition in early Homo. Before Farming, 4(11), 1–18.

  10. Davies, C. R., Ayres, J. M., Dye, C., & Deane, L. M. (1991). Malaria infection rate of Amazonian primates increases with body weight and group size. Functional Ecology, 5(5), 655–662.

  11. Dunbar, R. I. (1991). Functional significance of social grooming in primates. Folia Primatologica, 57(3), 121–131.

  12. Fauchald, P., Rødven, R., Bårdsen, B. J., Langeland, K., Tveraa, T., Yoccoz, N. G., & Ims, R. A. (2007). Escaping parasitism in the selfish herd: Age, size and density-dependent warble fly infestation in reindeer. Oikos, 116(3), 491–499.

  13. Fruth, B. (1995). Nests and nest groups in wild bonobos (Pan Paniscus): Ecological and behavioural correlates. Aachen: Verlag Shaker.

  14. Fruth, B., & Hohmann, G. (1996). Nest building behavior in the great apes: The great leap forward? In L. F. Marchant & T. Nishida (Eds.), Great ape societies (pp. 225–240). Cambridge: Cambridge University Press.

  15. Fruth, B., Tagg, N., & Stewart, S. (2018). Sleep and nesting behavior in primates: A review. American Journal of Physical Anthropology, 166(3), 499–509.

  16. Furuichi, T., & Hashimoto, C. (2000). Ground beds of chimpanzees in the Kalinzu Forest. Uganda Pan Africa News, 7, 26–28.

  17. Humle, T., & Matsuzawa, T. (2001). Behavioural diversity among the wild chimpanzee populations of Bossou and neighbouring areas, Guinea and Cote d'Ivoire, West Africa: A preliminary report. Folia Primatologica, 72, 57–68.

  18. Hunt, K. D., & McGrew, W. C. (Eds.) (2002). Chimpanzees in the dry habitats of Assirik, Senegal and at the Semliki Wildlife Reserve, Uganda. Cambridge: Cambridge University Press.

  19. Koops, K., McGrew, W., Matsuzawa, T., & Leslie, K. A. (2012b). Terrestrial nest-building by wild chimpanzees (Pan troglodytes): Implications for the tree-to-ground sleep transition in early hominins. American Journal of Physical Anthropology, 148, 351–361.

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

  21. Kortlandt, A. (1992). On chimpanzee dormitories and early hominid home sites. Current Anthropology, 33(4), 399–401.

  22. Krebs, B. L., Anderson, T. K., Goldberg, T. L., Hamer, G. L., Kitron, U. D., et al (2014). Host group formation decreases exposure to vector-borne disease: A field experiment in a ‘hotspot’of West Nile virus transmission. Proceedings of the Royal Society of London B: Biological Sciences, 281(1796), 20141586.

  23. Landsoud-Soukate, J., Tutin, C. E. G., & Fernandez, M. (1995). Intestinal parasites of sympatric gorillas and chimpanzees in the Lopé Reserve, Gabon. Annals of Tropical Medicine and Parasitology, 89(1), 73.

  24. Largo, C. J., Bastian, M. L., & van Schaik, C. P. (2009). Mosquito avoidance drives selection of nest tree species in Bornean orang-Utans. Folia Primatologica, 80(2), 163–163.

  25. Lesku, J. A., Roth, T. C., Amlaner, C. J., & Lima, S. L. (2006). A phylogenetic analysis of sleep architecture in mammals: The integration of anatomy, physiology, and ecology. American Naturalist, 168(4), 441–453.

  26. Lima, S. L., & Rattenborg, N. C. (2007). A behavioural shutdown can make sleeping safer: A strategic perspective on the function of sleep. Animal Behavior, 74(2), 189–197.

  27. Lima, S. L., Rattenborg, N. C., Lesku, J. A., & Amlaner, C. J. (2005). Sleeping under the risk of predation. Animal Behaviour, 70(4), 723–736.

  28. Lourenço-de-Oliveira, R., & Luz, S. L. (1996). Simian malaria at two sites in the Brazilian Amazon-II: Vertical distribution and frequency of anopheline species inside and outside the forest. Memórias do Instituto Oswaldo Cruz, 91(6), 687–694.

  29. MacKinnon, J. (1974). The behaviour and ecology of wild orang-utans (Pongo pygmaeus). Animal Behaviour, 22, 3–74.

  30. Matsuzawa, T., & Yamakoshi, G. (Eds.) (1996). Comparison of chimpanzee material culture between Bossou and Nimba, West Africa. Cambridge: Cambridge University Press.

  31. Maughan, J. E., & Stanford, C. B. (2001). Terrestrial nesting by chimpanzees in Bwindi Impenetrable National Forest, Uganda. American Journal of Physical Anthropology, 32, 204.

  32. McGrew, W., Marchant, L., & Nishida, T. (1996). Great ape societies. Cambridge: Cambridge University Press.

  33. McGrew, W. C. (2004). The cultured chimpanzee: Reflections on cultural primatology. New York: Cambridge University Press.

  34. Moore, S. L., & Wilson, K. (2002). Parasites as a viability cost of sexual selection in natural populations of mammals. Science, 297(5589), 2015–2018.

  35. Mooring, M. S., & Hart, B. L. (1992). Animal grouping for protection from parasites: Selfish herd and encounter-dilution effects. Behaviour, 123, 173–193.

  36. Morey, R. D., Rouder, J. N., & Jamil, T. (2015). BayesFactor: Computation of Bayes factors for common designs. R package version 0.9 9, 2014.

  37. Nunn, C. L. (2012). Primate disease ecology in comparative and theoretical perspective. American Journal of Primatology, 74(6), 497–509.

  38. Nunn, C. L., & Altizer, S. (2006). Infectious diseases in primates. New York: Oxford University Press.

  39. Nunn, C. L., & Heymann, E. W. (2005). Malaria infection and host behavior: A comparative study of Neotropical primates. Behavioral Ecology and Sociobiology, 59(1), 30–37.

  40. Nunn, C. L., McNamara, P., Capellini, I., Preston, B. T., & Barton, R. A. (2010). Primate sleep in phylogenetic perspective. In P. McNamara, R. A. Barton, & C. L. Nunn (Eds.), Evolution and sleep: Phylogenetic and functional perspectives (pp. 123–145). New York: Cambridge University Press.

  41. Nunn, C. L., & Samson, D. R. (2018). Sleep in a comparative context: Investigating how human sleep differs from sleep in other primates. American Journal of Physical Anthropology, 166(3), 601–612.

  42. Nunn, C. L., Thrall, P. H., Stewart, K., & Harcourt, A. H. (2008). Emerging infectious diseases and animal social systems. Evolutionary Ecology, 22, 519–543.

  43. Pruetz, J. D., Fulton, S. J., Marchant, L. F., McGrew, W. C., & Waller, M. S. M. (2008). Arboreal nesting as anti-predator adaptation by savanna chimpanzees (Pan troglodytes verus) in southeastern Senegal. American Journal of Primatology, 70(4), 393–401.

  44. Rätti, O., Ojanen, U., & Helle, P. (2006). Brief report Increasing group size dilutes black fly attack rate in black grouse. Ornis Fennica, 83, 86–90.

  45. Rifkin, J. L., Nunn, C. L., & Garamszegi, L. Z. (2012). Do animals living in larger groups experience greater parasitism? A meta-analysis. The American Naturalist, 180(1), 70–82.

  46. Roiz, D., Roussel, M., Muñoz, J., Ruiz, S., Soriguer, R., & Figuerola, J. (2012). Efficacy of mosquito traps for collecting potential West Nile mosquito vectors in a natural Mediterranean wetland. The American Journal of Tropical Medicine and Hygiene, 86(4), 642–648.

  47. Samson, D. R., Crittenden, A. N., Mabulla, I. A., Mabulla, A. Z. P., & Nunn, C. L. (2017). Chronotype variation drives night-time sentinel-like behaviour in hunter–gatherers. Proceedings of the Royal Society of London B: Biological Sciences, 284(1858), 20170967.

  48. Samson, D. R., & Hunt, K. D. (2012). A thermodynamic comparison of arboreal and terrestrial sleeping sites for dry-habitat chimpanzees (Pan troglodytes schweinfurthii) at the Toro-Semliki Wildlife Reserve, Uganda. American Journal of Primatology, 74(9), 811–818.

  49. Samson, D. R., & Hunt, K. D. (2014). Chimpanzees preferentially select sleeping platform construction tree species with biomechanical properties that yield stable, firm, but compliant nests. PLoS ONE, 9(4), e95361.

  50. 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.

  51. Samson, D. R., & Nunn, C. L. (2015). Sleep intensity and the evolution of human cognition. Evolutionary Anthropology, 24(6), 225–237.

  52. Schülke, O., & Ostner, J. (2012). Ecological and social influences on sociality. In J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombit, & J. B. Silk (Eds.), The evolution of primate societies (pp. 195–219). Chicago: University of Chicago Press.

  53. Sept, J. M. (1992). Was there no place like home? A new perspective on early hominid archaeological sites from the mapping of chimpanzee nests. Current Anthropology, 33(2), 187–207.

  54. Stewart, F. A. (2011). Why sleep in a nest? Empirical testing of the function of simple shelters made by wild chimpanzees. American Journal of Physical Anthropology, 146, 313–318.

  55. Stewart, F. A., & Pruetz, J. D. (2013). Do chimpanzee nests serve an anti-predatory function? American Journal of Primatology, 75(6), 593–604.

  56. Tagg, N., McCarthy, M., Dieguez, P., Bocksberger, G., Willie, J., et al (2018). Nocturnal activity in wild chimpanzees (Pan troglodytes): Evidence for flexible sleeping patterns and insights into human evolution. American Journal of Physical Anthropology, 166(3), 510–529.

  57. Tagg, N., Willie, J., Petre, C.-A., & Haggis, O. (2013). Ground night nesting in chimpanzees: New insights from central chimpanzees (Pan troglodytes troglodytes) in South-East Cameroon. Folia Primatologica, 84(6), 362–383.

  58. R Development Core Team (2016). R: A language and environment for statistical computing. Vienna, Austria.

  59. Worthman, C. M., & Melby, M. K. (2002). Toward a comparative developmental ecology of human sleep. In M. A. Carskadon (Ed.), Adolescent sleep patterns: Biological, social, and psychological influences (pp. 69–117). Cambridge: Cambridge University Press.

  60. Wrangham, R., & Carmody, R. (2010). Human adaptation to the control of fire. Evolutionary Anthropology, 19(5), 187–199.

Download references

Acknowledgments

We are grateful to the Government of Uganda, the Uganda Wildlife Authority, and the National Research Council. We would like to thank the two anonymous reviewers and the editor for their commentary and suggestions that significantly improved the quality of the original manuscript. We are thankful to the staff at the Semliki Chimpanzee Project, particularly Moses Comeboy, and Duke University for funding.

Author information

DRS, KDH, and CLN conceived and designed the experiments. DRS, LAL, KG, SW, BL performed the experiments. DRS, BJW analyzed the data. DRS wrote the manuscript; other authors provided editorial advice.

Correspondence to David R. Samson.

Additional information

The original version of this article was revised: Author Samantha Wylie’s family name was incorrectly presented as “Wiley”.

Handling Editor: Joanna M. Setchell

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Samson, D.R., Louden, L.A., Gerstner, K. et al. Chimpanzee (Pan troglodytes schweinfurthii) Group Sleep and Pathogen-Vector Avoidance: Experimental Support for the Encounter-Dilution Effect. Int J Primatol 40, 647–659 (2019) doi:10.1007/s10764-019-00111-z

Download citation

Keywords

  • Chimpanzee
  • Disease vector
  • Encounter-dilution
  • Sleep
  • Sociality