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Mothers Frequent Caves: Lactation Affects Chimpanzee (Pan troglodytes verus) Cave Use in Southeastern Senegal

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Abstract

Caves play an important ecological role for nonhuman primates in Africa and Asia. Savanna chimpanzees (Pan troglodytes verus) living in the Mandingue plateau of Senegal and Mali use caves for thermoregulation, where these refugia provide a cool microclimate during the hot, dry season. In this study, we examined cave use frequency for a chimpanzee community in southeastern Senegal. We used images from a camera trap placed at the mouth of a large laterite cave to investigate the hypotheses that sex, reproductive state, and seasonality influence the frequency of cave use. The camera collected 14,053 still images of chimpanzees between 2011 and 2013 over 325 camera trap days. Our results indicate no difference in cave use frequency between males and females overall. However, female reproductive state did significantly influence cave use, with lactating mothers using the cave more frequently than both males and nonlactating females. Chimpanzees used the cave during the hottest times of the day and were more likely to visit the cave during periods of low water availability and high maximum temperatures associated with the dry season. These results suggest the importance of thermoregulation in extreme heat for all individuals, and specifically for lactating females with nursing infants that likely experience higher metabolic and hydration stress. This study provides insight into the dynamics of primate cave use by contributing evidence that chimpanzee cave use may be influenced by reproductive states in addition to thermoregulatory needs.

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References

  • Aggarwal, A., & Upadhyay, R. (2013). Heat stress and animal productivity. New Delhi, India: Springer.

    Google Scholar 

  • Bá, A.T., Sambou B., Ervik F., Goudiaby A., Camara C., & Diallo, D. (1997). Végétation et flore. Parc Trans-frontalier du Niokolo Badiar. Union Européenne-Niokolo Badier, Niokolo Badier.

  • Badji, L., Ndiaye, P. I., Lindshield, S. M., Ba, C. T., & Pruetz, J. (2018). Savanna chimpanzee (Pan troglodytes verus) nesting ecology at Bagnomba (Kedougou, Senegal). Primates, 59, 235–241.

    CAS  PubMed  Google Scholar 

  • Baldwin, P. J. (1979). The natural history of the chimpanzee (Pan troglodytes verus) at Mt. Assirik, Senegal. PhD thesis, University of Stirling, Scotland.

  • Barrett, L., Gaynor, D., Rendall, D., Mitchell, D., & Henzi, S. P. (2004). Habitual cave use and thermoregulation in chacma baboons (Papio hamadryas ursinus). Journal of Human Evolution, 46, 215–222.

    CAS  PubMed  Google Scholar 

  • Barton, K. (2019). Package ‘MuMIn’: Multi-Model Inference

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

    Google Scholar 

  • Berger, L. R., Hawks, J., de Ruiter, D. J., Churchill, S. E., Schmid, P., et al (2015). Homo naledi, a new species of the genus Homo from the Dinaledi Chamber, South Africa. Elife, 4, e09560.

    PubMed Central  Google Scholar 

  • Boesch, C. (1991). The effects of leopard predation on grouping patterns in forest chimpanzees. Behavior, 117, 220–241.

    Google Scholar 

  • Boesch, C. (1996). Social grouping in Tai chimpanzees. Great Ape Societies, 101–113.

  • Bouchama, A., Al Mohanna, F., El-Sayed, R., Eldali, A., Saussereau, E., et al (2005). Experimental heatstroke in baboon: Analysis of the systemic inflammatory response. Shock, 24(4), 332–335.

    CAS  PubMed  Google Scholar 

  • Boyer, K. M. (2011). Chimpanzee conservation in light of impending iron ore mining project in SE Senegal. (Unpublished master's thesis). Iowa State University. Ames, IA.

  • Boyer Ontl, K. M., & Pruetz, J. D. (2014). Giving the forest eyes: The benefits of using camera traps to study unhabituated chimpanzees (Pan troglodytes verus) in southeastern Senegal. International Journal of Primatology, 35, 881–894.

    Google Scholar 

  • Brain, C. K. (1981). The hunters or the hunted? An introduction to African cave taphonomy. Chicago: University of Chicago Press.

    Google Scholar 

  • Butte, N. F., Hopkinson, J. M., Mehta, N., Moon, J. K., & Smith, E. O. B. (1999). Adjustments in energy expenditure and substrate utilization during late pregnancy and lactation. The American Journal of Clinical Nutrition, 69(2), 299–307.

    CAS  PubMed  Google Scholar 

  • Butte, F. E., Wong, W. W., & Hopkinson, J. M. (2001). Energy requirements of lactating women derived from doubly labeled water and milk energy output. The Journal of Nutrition, 131(1), 53–58.

  • Canale, C. I., Perret, M., & Henry, P. Y. (2012). Torpor use during gestation and lactation in a primate. Naturwissenschaften, 99, 159–163.

    CAS  PubMed  Google Scholar 

  • Clutton-Brock, T. H., Albon, S. D., & Guinness, F. E. (1989). Fitness costs of gestation and lactation in wild mammals. Nature, 337, 260–262.

    CAS  PubMed  Google Scholar 

  • Culver, D. C. (1982). Cave life: Evolution and ecology. Cambridge, MA: Harvard University Press.

    Google Scholar 

  • Das, R., Sailo, L., Verma, N., Bharti, P., & Saikia, J. (2016). Impact of heat stress on health and performance of dairy animals: A review. Veterinary World, 9(3), 260.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Di Silvestre, I., Novell, O., & Bogliani, G. (2000). Feeding habits of the spotted hyaena in the Niokolo Koba National Park, Senegal. African Journal of Ecology, 38, 102–107.

    Google Scholar 

  • Dufour, D. L., & Sauther, M. L. (2002). Comparative and evolutionary dimensions of the energetics of human pregnancy and lactation. American Journal of Human Biology, 14, 584–602.

    CAS  PubMed  Google Scholar 

  • Fauci, A. S., Braunwald, E., Kasper, D., Hauser, S., Longo, D., Jameson, J. L., & Loscalso, J. (Eds.) (2008). Harrison's principles of internal medicine (17th ed.). New York: McGraw-Hill Education.

    Google Scholar 

  • Field, A. (2005). Discovering statistics using SPSS. London: SAGE.

    Google Scholar 

  • Fox, J., & Weisberg, S. (2011). An R companion to applied regression. Thousand Oaks, CA: SAGE.

    Google Scholar 

  • Fuller, A., Mitchell, D., Maloney, S. K., & Hetem, R. S. (2016). Towards a mechanistic understanding of the responses of large terrestrial mammals to heat and aridity associated with climate change. Climate Change Responses, 3(1), 10.

    Google Scholar 

  • Gauer, R., & Meyers, B. K. (2019). Heat-related illnesses. American Family Physician, 99(8), 482–489.

  • Gittleman, J. L., & Thompson, S. D. (1988). Energy allocation in mammalian reproduction. American Zoologist, 28, 863–875.

    Google Scholar 

  • Glazer, J. L. (2005). Management of heatstroke and heat exhaustion. American Family Physician, 71(11), 2133–2140.

    PubMed  Google Scholar 

  • Grueter, C. C., & Ding, W. (2007). An observation of François’ langurs using caves at Mayanghe National Nature Reserve, Guizhou, China. Zoological Research, 27, 558–560.

    Google Scholar 

  • Halperin, S. (1979). Temporary association patterns in free ranging chimpanzees: An assessment of individual grouping preferences. In D. Hamburg & E. McCown (Eds.), The great apes (pp. 491–499). Menlo Park, CA: Benjamin-Cummings.

    Google Scholar 

  • Harrison, M. J. S., & Hladik, C. M. (1986). Un primate granivore: le Colobe noir dans la forêt du Gabon: potentialité d'évolution du comportement alimentaire. Revue d'écologie—la Terre et la Vie, 41, 281–298.

    Google Scholar 

  • Henshilwood, C. S., d’Errico, F., van Niekerk, K. L., Coquinot, Y., Jacobs, Z., et al (2011). A 100,000–year-old ochre-processing workshop at Blombos Cave, South Africa. Science, 334, 219–222.

    CAS  PubMed  Google Scholar 

  • Herman, C. P. (1993). Effects of heat on appetite. In Institute of Medicine Committee on Military Nutrition Research & B. M. Marriott (Eds.), Nutritional needs in hot environments: Applications for military personnel in field operations (pp. 187–214). Washington, DC: National Academies Press.

  • Huang, C., Wei, F., Li, M., Li, Y., & Sun, R. (2003). Sleeping cave selection, activity pattern and time budget of white-headed langurs. International Journal of Primatology, 24, 813–824.

    Google Scholar 

  • Huppatz, D. J. (2012). The first interior? Reconsidering the cave. Journal of Interior Design, 37, 1–8.

    Google Scholar 

  • Jensen, S. A., Mundry, R., Nunn, C. L., Boesch, C., & Leendertz, F. H. (2009). Non-invasive body temperature measurement of wild chimpanzees using fecal temperature decline. Journal of Wildlife Diseases, 45(2), 542–546.

    PubMed  Google Scholar 

  • Johnson, M. S., & Speakman, J. R. (2001). Limits to sustained energy intake. V. Effect of cold-exposure during lactation in Mus musculus. Journal of Experimental Biology, 204, 1967–1977.

    CAS  Google Scholar 

  • Kashiwagi, K., Abe, Y., & Takai, M. (2012). Cave use by Japanese macaques (Macaca fuscata) in heavy snowfall area, central Japan. Primate Research, 141–153.

  • Kashiwagi, K., Tsuji, Y., Yamamura, T., Takai, M., & Shimizu, M. (2018). Presence of feces in the abandoned Nokado Mine, Tochigi Prefecture of Central Japan, Provides further evidence of cave use by Japanese macaques. Primate Research, 34(1), 79–85.

  • Król, E., & Speakman, J. (2003a). Limits to sustained energy intake VI. Energetics of lactation in laboratory mice at thermoneutrality. Journal of Experimental Biology, 206, 4255–4266.

    Google Scholar 

  • Król, E., & Speakman, J. (2003b). Limits to sustained energy intake VII. Milk energy output in laboratory mice at thermoneutrality. Journal of Experimental Biology, 206, 4267–4281.

    Google Scholar 

  • Kummer, H. (1968). Social organization of hamadryas baboons. Chicago: University of Chicago Press.

    Google Scholar 

  • Lehmann, J., & Boesch, C. (2003). Sex differences in chimpanzee sociality. International Journal of Primatology, 29(1), 65–81.

    Google Scholar 

  • Lindshield, S., Danielson, B. J., Rothman, J. M., & Pruetz, J. D. (2017). Feeding in fear? How adult male western chimpanzees (Pan troglodytes verus) adjust to predation and savanna habitat pressures. American Journal of Physical Anthropology, 163, 480–496.

    PubMed  Google Scholar 

  • Lindshield, S., Ndiaye, P. I., Walters, A., Gueye, M., & Bogart, S. L. (2020). Facultative nocturnality in savanna chimpanzees at risk of carnivore depredation in Niokolo-Koba National Park, Senegal. International Journal of Primatology.

  • McGrew, W. C., Baldwin, P. J., & Tutin, C. E. G. (1981). Chimpanzees in a hot, dry, and open habitat: Mt. Assirik, Senegal, West Africa. Journal of Human Evolution, 10, 227–244.

    Google Scholar 

  • McGrew, W. C., McKee, J. K., & Tutin, C. E. G. (2003). Primates in caves: Two new reports of Papio spp. Journal of Human Evolution, 44, 521–526.

    PubMed  Google Scholar 

  • Minamisawa, H., Smith, M. L., & Siesjö, B. K. (1990). The effect of mild hyperthermia and hypothermia on brain damage following 5, 10, and 15 minutes of forebrain ischemia. Annals of Neurology, 28(1), 26–33.

    CAS  PubMed  Google Scholar 

  • Mitchell, D., Fuller, A., & Maloney, S. K. (2009). Homeothermy and primate bipedalism: Is water shortage or solar radiation the main threat to baboon (Papio hamadryas) homeothermy? Journal of Human Evolution, 56(5), 439–446.

    PubMed  Google Scholar 

  • Morrison, P. (1962). An analysis of body temperature in the chimpanzee. Journal of Mammalogy, 43(2), 166–171.

    Google Scholar 

  • Nakagawa, S., & Schielzeth, H. (2013). A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods in Ecology and Evolution, 4(2), 133–142.

    Google Scholar 

  • Neal Webb, S., & Pruetz J. (2020). Reproductive patterns of West-African chimpanzees (Pan troglodytes verus) living in a savanna mosaic environment. International Journal of Primatology.

  • Neville, M. C., Keller, R., Seacat, J., Lutes, V., Neifert, M., et al (1988). Studies in human lactation: Milk volumes in lactating women during the onset of lactation and full lactation. The American Journal of Clinical Nutrition, 48(6), 1375–1386.

    CAS  PubMed  Google Scholar 

  • Oftedal, O. T. (1984). Milk composition, milk yield and energy output at peak lactation: A comparative review. Symposia of the Zoological Society of London, 51, 33–85.

    Google Scholar 

  • Patou-Mathis, M. (2000). Neanderthal subsistence behaviors in Europe. International Journal of Osteoarchaeology, 10, 379–395.

    Google Scholar 

  • Pepper, J. W., Mitani, J. C., & Watts, D. P. (1999). General gregariousness and specific social preferences among wild chimpanzees. International Journal of Primatology, 20, 613–632.

    Google Scholar 

  • Pragna, P., Archana, P. R., Aleena, J., Sejian, V., Krishnan, G., et al (2017). Heat stress and dairy cow: Impact on both milk yield and composition. International Journal of Dairy Science, 12(1), 1–11.

    CAS  Google Scholar 

  • Prentice, A. M., & Prentice, A. (1988). Energy costs of lactation. Annual Review of Nutrition, 8, 63–79.

    CAS  PubMed  Google Scholar 

  • Pruetz, J. D. (2007). Evidence of cave use by savanna chimpanzees (Pan troglodytes verus) at Fongoli, Senegal: Implications for thermoregulatory behavior. Primates, 48, 316–319.

    CAS  PubMed  Google Scholar 

  • Pruetz, J. D. (2018). Nocturnal behavior by a diurnal ape, the West African chimpanzee (Pan troglodytes verus), in a savanna environment at Fongoli, Senegal. American Journal of Physical Anthropology, 166, 541–548.

    PubMed  Google Scholar 

  • Pruetz, J. D., & Bertolani, P. (2009). Chimpanzee (Pan troglodytes verus) behavioral responses to stresses associated with living in a savannah-mosaic environment: Implications for hominin adaptations to open habitats. PaleoAnthropology, 2009, 252–262.

    Google Scholar 

  • Pruetz, J. D., Marchant, L. F., Arno, J., & McGrew, W. C. (2002). Survey of savanna chimpanzees (Pan troglodytes verus) in southeastern Sénégal. American Journal of Primatology, 58, 35–43.

    CAS  PubMed  Google Scholar 

  • Pruetz, J. D., Ontl, K. B., Cleaveland, E., Lindshield, S., Marshack, J., Wessling, E. G. (2017). Intragroup lethal aggression in West African chimpanzees (Pan troglodytes verus): Inferred killing of a former alpha male at fongoli, Senegal. International Journal of Primatology, 38(1), 31–57.

  • Pusey, A. E. (1983). Mother-offspring relationships in chimpanzees after weaning. Animal Behaviour, 31(2), 363–377.

    Google Scholar 

  • R Core Team (2019). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

    Google Scholar 

  • Reconyx (2017) PC800 HyperFireTM 3828 Creekside Ln, Ste 2, Holmen, WI.

  • Redmond, I. M., & Shoshani, J. (1987). Mount Elgon elephants. Elephant Interest Group Newsletter, 2, 46–66.

    Google Scholar 

  • Republic of Senegal. (2011). Kedougou: Situation economique et Sociale Regionale 2010. Dakar, Senegal: Service Régional de la Statistique et de la Démographie de Kédougou (SRSD) et Agence Nationale de la Statistique et de la Demographie (ANSD). Retrieved from http://www.ansd.sn/ (accessed January 7, 2014).

  • Reynolds, S. C., & Kibii, J. M. (2011). Sterkfontein at 75: Review of paleoenvironments, fauna, dating and archaeology from the hominin site of Sterkfontein (Gauteng Province, South Africa). Palaeontologia africana, 46, 59–88.

    Google Scholar 

  • Roffman, I., Nevo, E., Panchevre, M., & Ronen, A. (2016). Cultural and physical characteristics of near-arid savanna chimpanzees in Mali. Human Evolution, 31(4), 191–214.

    Google Scholar 

  • Sauther, M. L., Cuozzo, F. P., Jacky, I. Y., Fish, K. D., LaFleur, M., et al (2013). Limestone cliff-face and cave use by wild ring-tailed lemurs (Lemur catta) in southwestern Madagascar. Madagascar Conservation & Development, 8(2), 73–80.

    Google Scholar 

  • Smith, T. M., Machanda, Z., Bernard, A. B., Donovan, R. M., Papakyrikos, A. M., et al (2013). First molar eruption, weaning, and life history in living wild chimpanzees. Proceedings of the National Academy of Sciences of the USA, 110(8), 2787–2791.

    CAS  PubMed  Google Scholar 

  • Speakman, J. R. (2008). The physiological costs of reproduction in small mammals. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 363, 375–398.

    PubMed  Google Scholar 

  • Speakman, J. R., & Król, E. (2010). Maximal heat dissipation capacity and hyperthermia risk: Neglected key factors in the ecology of endotherms. Journal of Animal Ecology, 79, 726–746.

    Google Scholar 

  • Terrien, J., Perret, M., & Aujard, F. (2011). Behavioral thermoregulation in mammals: A review. Frontiers in Bioscience, 16(4), 1428–1444.

    Google Scholar 

  • Thompson, M. E., Muller, M. N., & Wrangham, R. W. (2012). The energetics of lactation and the return to fecundity in wild chimpanzees. Behavioral Ecology, 23(6), 1234–1241.

  • Tooby, J., & DeVore, I. (1987). The reconstruction of hominid behavioral evolution through strategic modeling. In W. Kinzey (Ed.), The evolution of human behavior: Primate models (pp. 183–237). Albany: SUNY Press.

    Google Scholar 

  • Trinkaus, E. (1983). The Shanidar Neandertals. New York: Academic Press.

    Google Scholar 

  • Weather Underground. (2016). Weather history for Kedougou, Senegal and Kenieba, Mali. Retrieved from https://www.wunderground.com (Accessed July 6, 2016).

  • Wessling, E. G., Kühl, H. S., Mundry, R., Deschner, T., Pruetz, J. D. (2018). The costs of living at the edge: Seasonal stress in wild savanna-dwelling chimpanzees. Journal of Human Evolution, 121, 1–11.

  • Williams, A. M., Safranski, T. J., Spiers, D. E., Eichen, P. A., Coate, E. A., & Lucy, M. C. (2013). Effects of a controlled heat stress during late gestation, lactation, and after weaning on thermoregulation, metabolism, and reproduction of primiparous sows. Journal of Animal Science, 91, 2700–2714.

    CAS  PubMed  Google Scholar 

  • Yan, Y. E., Zhao, Y. Q., Wang, H., & Fan, M. (2006). Pathophysiological factors underlying heatstroke. Medical Hypotheses, 67, 609–617.

    CAS  PubMed  Google Scholar 

  • Zuberbühler, K., & Jenny, D. (2002). Leopard predation and primate evolution. Journal of Human Evolution, 43, 873–886.

    PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank the Republic of Senegal and the Direction des Eaux, Forêts, Chasse et de la Conservation des Sols du Sénégal for permission and assistance in working in the country. Many thanks to S. Keita for guidance and data collection in the field, and Todd Ontl and Jim Jones for their statistical support. We acknowledge the village of Kharakhena, Afrigold SUARL, Houston Zoo Wildlife Conservation Program, U.S. Fish and Wildlife Service Great Ape Conservation Fund (#96200-0-G096), Blank Park Zoo, Iowa State University, and Margot Marsh Biodiversity Fund for logistical, technical, and financial support. We would also like to thank the editors and reviewers at the International Journal of Primatology for their helpful comments, as well as Sarah Elton, Dietmar Zinner, David Watts, and anonymous reviewers for comments on previous versions of the manuscript. We thank Stacy Lindshield and Erin Wessling for the invitation to participate in this special volume on savanna chimpanzees.

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  1. Department of Anthropology, Iowa State University, Ames, IA, USA

    Kelly Boyer Ontl & Jill D. Pruetz

  2. Department of Anthropology, Ball State University, Muncie, IN, USA

    Kelly Boyer Ontl

  3. Department of Anthropology, Texas State University, San Marcos, TX, USA

    Jill D. Pruetz

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  1. Kelly Boyer Ontl
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KBO and JDP conceived and designed the study. KBO collected data, analyzed the data, and wrote the manuscript. JDP provided editorial advice and data collection.

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Correspondence to Kelly Boyer Ontl.

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Boyer Ontl, K., Pruetz, J.D. Mothers Frequent Caves: Lactation Affects Chimpanzee (Pan troglodytes verus) Cave Use in Southeastern Senegal. Int J Primatol 41, 916–935 (2020). https://doi.org/10.1007/s10764-020-00165-4

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