Advertisement

International Journal of Primatology

, Volume 40, Issue 6, pp 647–659 | Cite as

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

  • David R. SamsonEmail author
  • Luke A. Louden
  • Katie Gerstner
  • Samantha Wylie
  • Ben Lake
  • Bradley J. White
  • Charles L. Nunn
  • Kevin D. Hunt
Article

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.

Keywords

Chimpanzee Disease vector Encounter-dilution Sleep Sociality 

Notes

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 Contributions

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.

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.Google Scholar
  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.CrossRefGoogle Scholar
  3. Anderson, J. R. (1998). Sleep, sleeping sites, and sleep-related activities: Awakening to their significance. American Journal of Primatology, 46(1), 63–75.PubMedCrossRefPubMedCentralGoogle Scholar
  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.CrossRefGoogle Scholar
  5. Bartoń, K. (2015). version 1.15.6.Google Scholar
  6. Bates, D., Maecher, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67, 1–48.CrossRefGoogle Scholar
  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.PubMedCrossRefPubMedCentralGoogle Scholar
  8. Capellini, I., Barton, R. A., McNamara, P., Preston, B., & Nunn, C. L. (2008). Ecology and evolution of mammalian sleep. Evolution, 62, 1764–1776.PubMedPubMedCentralCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  11. Dunbar, R. I. (1991). Functional significance of social grooming in primates. Folia Primatologica, 57(3), 121–131.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  13. Fruth, B. (1995). Nests and nest groups in wild bonobos (Pan Paniscus): Ecological and behavioural correlates. Aachen: Verlag Shaker.Google Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefPubMedCentralGoogle Scholar
  16. Furuichi, T., & Hashimoto, C. (2000). Ground beds of chimpanzees in the Kalinzu Forest. Uganda Pan Africa News, 7, 26–28.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefPubMedCentralGoogle Scholar
  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.CrossRefGoogle Scholar
  21. Kortlandt, A. (1992). On chimpanzee dormitories and early hominid home sites. Current Anthropology, 33(4), 399–401.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefPubMedCentralGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefPubMedCentralGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefPubMedCentralGoogle Scholar
  29. MacKinnon, J. (1974). The behaviour and ecology of wild orang-utans (Pongo pygmaeus). Animal Behaviour, 22, 3–74.CrossRefGoogle Scholar
  30. Matsuzawa, T., & Yamakoshi, G. (Eds.) (1996). Comparison of chimpanzee material culture between Bossou and Nimba, West Africa. Cambridge: Cambridge University Press.Google Scholar
  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.Google Scholar
  32. McGrew, W., Marchant, L., & Nishida, T. (1996). Great ape societies. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  33. McGrew, W. C. (2004). The cultured chimpanzee: Reflections on cultural primatology. New York: Cambridge University Press.CrossRefGoogle Scholar
  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.PubMedCrossRefPubMedCentralGoogle Scholar
  35. Mooring, M. S., & Hart, B. L. (1992). Animal grouping for protection from parasites: Selfish herd and encounter-dilution effects. Behaviour, 123, 173–193.CrossRefGoogle Scholar
  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.Google Scholar
  37. Nunn, C. L. (2012). Primate disease ecology in comparative and theoretical perspective. American Journal of Primatology, 74(6), 497–509.PubMedCrossRefPubMedCentralGoogle Scholar
  38. Nunn, C. L., & Altizer, S. (2006). Infectious diseases in primates. New York: Oxford University Press.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefPubMedCentralGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefPubMedCentralGoogle Scholar
  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.Google Scholar
  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.PubMedCrossRefPubMedCentralGoogle Scholar
  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.PubMedPubMedCentralCrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefPubMedCentralGoogle Scholar
  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.PubMedPubMedCentralCrossRefGoogle Scholar
  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.PubMedCrossRefPubMedCentralGoogle Scholar
  51. Samson, D. R., & Nunn, C. L. (2015). Sleep intensity and the evolution of human cognition. Evolutionary Anthropology, 24(6), 225–237.PubMedCrossRefPubMedCentralGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  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.PubMedCrossRefPubMedCentralGoogle Scholar
  55. Stewart, F. A., & Pruetz, J. D. (2013). Do chimpanzee nests serve an anti-predatory function? American Journal of Primatology, 75(6), 593–604.PubMedCrossRefPubMedCentralGoogle Scholar
  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.PubMedCrossRefPubMedCentralGoogle Scholar
  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.CrossRefGoogle Scholar
  58. R Development Core Team (2016). R: A language and environment for statistical computing. Vienna, Austria.Google Scholar
  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.Google Scholar
  60. Wrangham, R., & Carmody, R. (2010). Human adaptation to the control of fire. Evolutionary Anthropology, 19(5), 187–199.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019
corrected publication 2020

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of Toronto, MississaugaMississaugaCanada
  2. 2.Department of Evolutionary AnthropologyDuke UniversityDurhamUSA
  3. 3.Department of Biological SciencesPurdue UniversityWest LafayetteUSA
  4. 4.Department of AnthropologyWayne State UniversityDetroitUSA
  5. 5.Department of AnthropologyUniversity of NevadaLas VegasUSA
  6. 6.Lester E. Fisher Center for the Study and Conservation of ApesLincoln Park ZooChicagoUSA
  7. 7.Department of Entomology at the Center for Disease Vector ResearchUniversity of California, RiversideRiversideUSA
  8. 8.Duke Global Health InstituteDuke UniversityDurhamUSA
  9. 9.Department of AnthropologyIndiana UniversityBloomingtonUSA

Personalised recommendations