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Chimpanzee (Pan troglodytes verus) Density and Environmental Gradients at Their Biogeographical Range Edge

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Abstract

Identifying ecological gradients at the range edge of a species is an essential step in revealing the underlying mechanisms and constraints that limit the species’ geographic range. We aimed to describe the patterns of variation in chimpanzee (Pan troglodytes verus) density and habitat characteristics perpendicular to the northern edge of their range and to investigate potential environmental mechanisms underlying chimpanzee distribution in a savanna–mosaic habitat. We estimated chimpanzee densities at six sites forming a 126-km latitudinal gradient at the biogeographical range edge of the western chimpanzee in the savanna–mosaic habitats of southeastern Senegal. To accompany these data, we used systematically placed vegetation plots to characterize the habitats at each site for habitat heterogeneity, tree density and size, and floral assemblages, among other variables. We found that both biotic and abiotic factors are potential determinants of the chimpanzee range limit in this ecoregion. Specifically, chimpanzee-occupied landscapes at the limit had smaller available floral assemblages less habitat heterogeneity, and contained fewer closed canopy habitats in which chimpanzees could seek refuge from high temperatures than in landscapes farther from the range limit. This pattern was accompanied by a decline in chimpanzee density with increasing proximity to the range limit. Our results provide several indications of the potential limits of food species diversity, thermal refuge, and water availability to the chimpanzee niche and the implications of these limits for chimpanzee biogeography, especially in the face of climate change predictions, as well as for species distributional modeling more generally.

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References

  • Abwe, E. E., Morgan, B. J., Tchiengue, B., Kentatchime, F., Doudja, R., et al (2019). Habitat differentiation among three Nigeria–Cameroon chimpanzee (Pan troglodytes ellioti) populations. Ecology and Evolution, 9(3), 1489–1500.

    PubMed  PubMed Central  Google Scholar 

  • Adams, D. C., & Anthony, C. D. (1996). Using randomization techniques to analyse behavioural data. Animal Behaviour, 51(4), 733–738.

    Google Scholar 

  • Altmann, S. A. (1974). Baboons, space, time and energy. American Zoologist, 14, 221–248.

    Google Scholar 

  • Baayen, R. H. (2008). Analyzing linguistic data: A practical introduction to statistics using R. Cambridge: Cambridge University Press.

    Google Scholar 

  • Balcomb, S. R., Chapman, C. A., & Wrangham, R. W. (2000). Relationship between chimpanzee (Pan troglodytes) density and large, fleshy-fruit tree density: Conservation implications. American Journal of Primatology, 51(3), 197–203.

    CAS  PubMed  Google Scholar 

  • Barnes, M. E. (2001). Seed predation, germination and seedling establishment of Acacia erioloba in northern Botswana. Journal of Arid Environments, 49, 541–554.

    Google Scholar 

  • Barratt, C. D., Lester, J. D., Gratton, P., Onstein, R. E., Kalan, A. K., et al. (2020). Late Quaternary habitat suitability models for chimpanzees (Pan troglodytes) since the Last Interglacial (120,000 BP). BioRxiv, doi: https://www.biorxiv.org/content/10.1101/2020.05.15.066662v1

  • Barton, K. (2019). MuMIn: Multi-model inference. R package version, 1(43), 15 https://CRAN.R-project.org/package=MuMIn.

    Google Scholar 

  • 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 

  • Battin, J. (2004). When good animals love bad habitats: Ecological traps and the conservation of animal populations. Conservation Biology, 18(6), 1482–1491.

    Google Scholar 

  • Boesch, C. (1996). Social grouping in Tai chimpanzees. In L. Marchant & T. Nishida (Eds.), Great ape societies (pp. 101–113). Cambridge: Cambridge University Press.

    Google Scholar 

  • Bogart, S. L., & Pruetz, J. D. (2008). Ecological context of savanna chimpanzee (Pan troglodytes verus) termite fishing at Fongoli, Senegal. American Journal of Primatology, 70(6), 605–612.

    PubMed  Google Scholar 

  • Bogart, S. L., & Pruetz, J. D. (2011). Insectivory of savanna chimpanzees (Pan troglodytes verus) at Fongoli, Senegal. American Journal of Physical Anthropology, 145(1), 11–20.

    PubMed  Google Scholar 

  • Bongers, F., Poorter, L., Van Rompaey, R. S. A. R., & Parren, M. (1999). Distribution of twelve moist forest canopy tree species in Liberia and Cote d'Ivoire: Response curves to a climatic gradient. Journal of Vegetation Science, 10(3), 371–382.

    Google Scholar 

  • Bortolamiol, S., Cohen, M., Potts, K., Pennec, F., Rwaburindore, P., et al (2014). Suitable habitats for endangered frugivorous mammals: Small-scale comparison, regeneration forest and chimpanzee density in Kibale National Park, Uganda. PloS ONE, 9(7), e102177.

    PubMed  PubMed Central  Google Scholar 

  • Brown, J. H. (1984). On the relationship between abundance and distribution of species. American Naturalist, 124(2), 255–279.

    Google Scholar 

  • Brown, J. H., Mehlman, D. W., & Stevens, G. C. (1995). Spatial variation in abundance. Ecology, 76(7), 2028–2043.

    Google Scholar 

  • Buckland, S. T., Anderson, D. R., Burnham, K. P., Laake, J. L., Borchers, D. L., & Thomas, L. (2001). Introduction to distance sampling: Estimating abundance of biological populations. Oxford: Oxford University Press.

    Google Scholar 

  • Cahill, A. E., Aiello-Lammens, M. E., Caitlin Fisher-Reid, M., Hua, X., Karanewsky, C. J., et al (2014). Causes of warm-edge range limits: Systematic review, proximate factors and implications for climate change. Journal of Biogeography, 41(3), 429–442.

    Google Scholar 

  • Chapman, C. A., Chapman, L. J., & Wrangham, R. (1995). Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology, 36(1), 59–70.

    Google Scholar 

  • Chown, S. L., & Gaston, K. J. (1999). Exploring links between physiology and ecology at macro-scales: The role of respiratory metabolism in insects. Biological Reviews, 74(1), 87–120.

    Google Scholar 

  • Conklin-Brittain, N. L., Wrangham, R. W., & Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. II. Macronutrients. International Journal of Primatology, 19(6), 971–998.

    Google Scholar 

  • Core Team, R. (2019). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing https://www.R-project.org/.

    Google Scholar 

  • Crowther, T. W., Glick, H., Covey, K., Bettigole, C., Maynard, D., et al (2015). Mapping tree density at a global scale. Nature, 525(7568), 201.

    CAS  PubMed  Google Scholar 

  • Emery Thompson, M., Kahlenberg, S. M., Gilby, I. C., & Wrangham, R. W. (2007). Core area quality is associated with variance in reproductive success among female chimpanzees at Kibale National Park. Animal Behaviour, 73(3), 501–512.

    Google Scholar 

  • Emery Thompson, M., Muller, M. N., Wrangham, R. W., Lwanga, J. S., & Potts, K. B. (2009). Urinary C-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees. Hormones and Behavior, 55(2), 299–305.

    PubMed  Google Scholar 

  • Emery Thompson, M., Muller, M. N., Kahlenberg, S. M., & Wrangham, R. W. (2010). Dynamics of social and energetic stress in wild female chimpanzees. Hormones and Behavior, 58(3), 440–449.

    PubMed  Google Scholar 

  • Engelbrecht, B. M., Comita, L. S., Condit, R., Kursar, T. A., Tyree, M. T., et al (2007). Drought sensitivity shapes species distribution patterns in tropical forests. Nature, 447(7140), 80.

    CAS  PubMed  Google Scholar 

  • Fall, S. (2006). Analysis of mean climate conditions in Senegal (1971–98). Earth Interactions, 10(5), 1–40.

    Google Scholar 

  • Fick, S. E., & Hijmans, R. J. (2017). WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37(12), 4302–4315.

    Google Scholar 

  • Foerster, S., Zhong, Y., Pintea, L., Murray, C. M., Wilson, M. L., et al (2016). Feeding habitat quality and behavioral trade-offs in chimpanzees: A case for species distribution models. Behavioral Ecology, 27(4), 1004–1016.

    PubMed  PubMed Central  Google Scholar 

  • Forstmeier, W., & Schielzeth, H. (2011). Cryptic multiple hypotheses testing in linear models: Overestimated effect sizes and the winner's curse. Behavioral Ecology and Sociobiology, 65(1), 47–55.

    PubMed  Google Scholar 

  • Furuichi, T., Hashimoto, C., & Tashiro, Y. (2001). Fruit availability and habitat use by chimpanzees in the Kalinzu Forest, Uganda: Examination of fallback foods. International Journal of Primatology, 22, 929–945.

    Google Scholar 

  • Gelman, A., & Hill, J. (2007). Data analysis using regression and multilevel/hierarchical models. Cambridge: Cambridge University Press.

    Google Scholar 

  • Haccou, P., & Meelis, E. (1994). Statistical analyses of behavioural data. Oxford: Oxford University Press.

    Google Scholar 

  • Hamilton, W. J., Buskirk, R. E., & Buskirk, W. H. (1976). Defense of space and resources by chacma (Papio ursinus) baboon troops in an African desert and swamp. Ecology, 57, 1264–1272.

    Google Scholar 

  • Hargreaves, A. L., Samis, K. E., & Eckert, C. G. (2014). Are species’ range limits simply niche limits writ large? A review of transplant experiments beyond the range. American Naturalist, 183(2), 157–173.

    Google Scholar 

  • Heinicke, S., Mundry, R., Boesch, C., Amarasekaran, B., Barrie, A., et al (2019). Characteristics of positive deviants in western chimpanzee populations. Frontiers in Ecology and Evolution, 7, 16.

  • Holt, R. D. (2009). Bringing the Hutchinsonian niche into the 21st century: Ecological and evolutionary perspectives. Proceedings of the National Academy of Sciences of the USA, 106, 19659–19665.

    CAS  PubMed  Google Scholar 

  • Humle, T., Boesch, C., Duvall, C., Ellis, C.M., Farmer, K.H., et al.(2008). Pan troglodytes ssp. verus. The IUCN Red List of Threatened Species 2008: eT15935A5323101.

  • Humle, T., Boesch, C., Campbell, G., Junker, J., Koops, K., et al.(2016). Pan troglodytes ssp. verus. The IUCN Red List of Threatened Species 2016: eT15935A102327574.

  • Hutchinson, G. E. (1961). The paradox of the plankton. American Naturalist, 95(882), 137–145.

    Google Scholar 

  • Isbell, L. A., Rothman, J. M., Young, P. J., & Rudolph, K. (2013). Nutritional benefits of Crematogaster mimosa ants and Acacia drepanolobium gum for patas monkeys and vervets in Laikipia, Kenya. American Journal of Physical Anthropology, 150, 286–300.

    PubMed  Google Scholar 

  • Janmaat, K. R., Boesch, C., Byrne, R., Chapman, C. A., Goné Bi, Z. B., et al (2016). Spatio-temporal complexity of chimpanzee food: How cognitive adaptations can counteract the ephemeral nature of ripe fruit. American Journal of Primatology, 78(6), 626–645.

    PubMed  Google Scholar 

  • Jantz, S., Pintea, L., Nackoney, J., & Hansen, M. (2016). Landsat ETM+ and SRTM data provide near real-time monitoring of chimpanzee (Pan troglodytes) habitats in Africa. Remote Sensing, 8(5), 427.

    Google Scholar 

  • Junker, J., Blake, S., Boesch, C., Campbell, G., du Toit, L., et al (2012). Recent decline in suitable environmental conditions for African great apes. Diversity and Distributions, 18(11), 1077–1091.

    Google Scholar 

  • Kawecki, T. J. (2008). Adaptation to marginal habitats. Annual Review of Ecology, Evolution, and Systematics, 39, 321–342.

    Google Scholar 

  • Kinnaird, M. F., & O’Brien, T. G. (2005). Fast foods of the forest: The influence of figs on primates and hornbills across Wallace’s line. In J. L. Dew & J. P. Boubli (Eds.), Tropical fruits and frugivores: The search for strong interactors (pp. 155–184). New York: Springer Science+Business Media.

    Google Scholar 

  • Korstjens, A. H., Lehmann, J., & Dunbar, R. I. M. (2010). Resting time as an ecological constraint on primate biogeography. Animal Behaviour, 79(2), 361–374.

    Google Scholar 

  • Kortlandt, A. (1983). Marginal habitats of chimpanzees. Journal of Human Evolution, 12(3), 231–278.

    Google Scholar 

  • Kouakou, C. Y., Boesch, C., & Kühl, H. (2009). Estimating chimpanzee population size with nest counts: Validating methods in Taï National Park. American Journal of Primatology, 71(6), 447–457.

    PubMed  Google Scholar 

  • Kühl, H. (2008). Best practice guidelines for the surveys and monitoring of great ape populations. Gland, Switzerland: IUCN.

    Google Scholar 

  • Kühl, H. S., Sop, T., Williamson, E. A., Mundry, R., Brugière, D., et al (2017). The Critically Endangered western chimpanzee declines by 80%. American Journal of Primatology, 79(9), e22681.

    Google Scholar 

  • Lindshield, S. M. (2014). Multilevel analysis of the foraging decisions of western chimpanzees (Pan troglodytes verus) and resource scarcity in a savanna environment at Fongoli, Senegal. PhD thesis, Iowa State University, Ames, IA.

  • Lindshield, S., Bogart, S. L., Gueye, M., Ndiaye, P. I., & Pruetz, J. D. (2019). Informing protection efforts for critically endangered chimpanzees (Pan troglodytes verus) and sympatric mammals amidst rapid growth of extractive industries in Senegal. Folia Primatologica, 90(2), 124–136.

    Google Scholar 

  • Marshall, A. J. (2009). Are montane forests demographic sinks for Bornean white-bearded gibbons Hylobates albibarbis? Biotropica, 41(2), 257–267.

    Google Scholar 

  • Marshall, A. J., & Leighton, M. (2006). How does food availability limit the population density of white-bearded gibbons? In G. Hohmann, M. Robbins, & C. Boesch (Eds.), Feeding ecology of the apes and other primates (pp. 311–333). Cambridge: Cambridge University Press.

    Google Scholar 

  • Marshall, A. J., Boyko, C. M., Feilen, K. L., Boyko, R. H., & Leighton, M. (2009a). Defining fallback foods and assessing their importance in primate ecology and evolution. American Journal of Physical Anthropology, 140(4), 603–614.

    PubMed  Google Scholar 

  • Marshall, A. J., Ancrenaz, M., Brearley, F. Q., Fredriksson, G., Ghaffar, N., et al (2009b). The effects of habitat quality, phenology, and floristics on populations of Bornean and Sumatran orangutans: Are Sumatran forests more productive than Bornean forests? In C. van Schaik, S. A. Wich, T. M. Setia, & S. S. U. Atmoko (Eds.), Orangutans: Geographic variation in behavioral ecology and conservation (pp. 97–117). Oxford: Oxford University Press.

    Google Scholar 

  • Marshall, A. J., Beaudrot, L., & Wittmer, H. U. (2014). Responses of primates and other frugivorous vertebrates to plant resource variability over space and time at Gunung Palung National Park. International Journal of Primatology, 35(6), 1178–1201.

    Google Scholar 

  • Martinez-Meyer, E. (2005). Climate change and biodiversity: Some considerations in forecasting shifts in species' potential distributions. Biodiversity Informatics, 2, 42–55.

    Google Scholar 

  • Massa, B. E. (2011). Predicting conflict over scarce resources: Chimpanzees (Pan troglodytes verus) and Fulbe pastoralists. Master’s thesis: Duke University, Durham, NC.

    Google Scholar 

  • Mbow, C., Nielsen, T. T., & Rasmussen, K. (2000). Savanna fires in east-central Senegal: Distribution patterns, resource management and perceptions. Human Ecology, 28, 561–583.

    Google Scholar 

  • McGrew, W. C., Baldwin, P. J., & Tutin, C. E. (1981). Chimpanzees in a hot, dry and open habitat: Mt. Assirik, Senegal. West Africa. Journal of Human Evolution, 10(3), 227–244.

    Google Scholar 

  • McGrew, W., Baldwin, P., & Tutin, C. (1988). Diet of wild chimpanzees (Pan troglodytes verus) at Mt. Assirik, Senegal: I. Composition. American Journal of Primatology, 16(3), 213–226.

    CAS  PubMed  Google Scholar 

  • Miller, D. L. (2017). Distance: Distance sampling detection function and abundance estimation. R package version 0.9.7. https://CRAN.R-project.org/package=Distance

  • Milton, K., Giacalone, J., Wright, S. J., & Stockmayer, G. (2005). Do frugivore population fluctuations reflect fruit production? Evidence from Panama. In L. Dew & J. P. Boubli (Eds.), Tropical fruits and frugivores: The search for strong interactors (pp. 5–35). New York: Springer Science+Business Media.

    Google Scholar 

  • Moegenburg, S. M., & Levey, D. J. (2003). Do frugivores respond to fruit harvest? An experimental study of short-term responses. Ecology, 84(10), 2600–2612.

    Google Scholar 

  • Mundry, R., & Fischer, J. (1998). Use of statistical programs for nonparametric tests of small samples often leads to incorrect P-values: Examples from animal behaviour. Animal Behaviour, 56, 256–259.

  • Murray, C. M., Eberly, L. E., & Pusey, A. E. (2006). Foraging strategies as a function of season and rank among wild female chimpanzees (Pan troglodytes). Behavioral Ecology, 17(6), 1020–1028.

    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 

  • Nguelet, F. L. M., Koumba, C. R. Z., Mavoungou, J. F., Nzengue, E., Akomo-Okoue, E. F., et al (2016). Etude de la relation entre l’abondance des grands mammifères frugivores et celle des fruits dans le Parc National de Moukalaba-Doudou, Gabon. International Journal of Biological and Chemical Sciences, 10(5), 1969–1982.

    Google Scholar 

  • Pearson, R. G., & Dawson, T. P. (2003). Predicting the impacts of climate change on the distribution of species: Are bioclimate envelope models useful? Global Ecology and Biogeography, 12(5), 361–371.

    Google Scholar 

  • Pennec, F., Krief, S., Hladik, A., Lubini Ayingweu, C., Bortolamiol, S., et al (2016). Floristic and structural vegetation typology of bonobo habitats in a forest-savanna mosaic (Bolobo Territory, DR Congo). Plant Ecology and Evolution, 149(2), 199–215.

    Google Scholar 

  • Plumptre, A. J., & Cox, D. (2006). Counting primates for conservation: Primate surveys in Uganda. Primates, 47(1), 65–73.

    PubMed  Google Scholar 

  • Potter, D. M., & Griffiths, D. J. (2006). Omnibus permutation tests of the overall null hypothesis in datasets with many covariates. Journal of Biopharmaceutical Statistics, 16, 327–341.

    PubMed  Google Scholar 

  • Potts, K. B., & Lwanga, J. S. (2013). Floristic heterogeneity at Ngogo, Kibale National Park, Uganda and possible implications for habitat use by chimpanzees (Pan troglodytes). African Journal of Ecology, 52(4), 427–437.

    Google Scholar 

  • Potts, K. B., Chapman, C. A., & Lwanga, J. S. (2009). Floristic heterogeneity between forested sites in Kibale National Park, Uganda: Insights into the fine-scale determinants of density in a large-bodied frugivorous primate. Journal of Animal Ecology, 78(6), 1269–1277.

    Google Scholar 

  • Potts, K. B., Baken, E., Ortmann, S., Watts, D. P., & Wrangham, R. W. (2015). Variability in population density is paralleled by large differences in foraging efficiency in chimpanzees (Pan troglodytes). International Journal of Primatology, 36(6), 1101–1119.

    Google Scholar 

  • Pruetz, J. D. (2006). Feeding ecology of savanna chimpanzees (Pan troglodytes verus) at Fongoli, Senegal. In G. Hohmann, M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 161–182). Cambridge: Cambridge University Press.

    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(4), 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(3), 541–548.

    PubMed  Google Scholar 

  • Pruetz, J., & 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 

  • Pulliam, H. R. (1988). Sources, sinks, and population regulation. American Naturalist, 132(5), 652–661.

    Google Scholar 

  • Pusey, A., Williams, J., & Goodall, J. (1997). The influence of dominance rank on the reproductive success of female chimpanzees. Science, 277(5327), 828–831.

    CAS  PubMed  Google Scholar 

  • Quinn, G. P., & Keough, M. J. (2002). Experimental designs and data analysis for biologists. Cambridge: Cambridge University Press.

    Google Scholar 

  • Restrepo, C., Gomez, N., & Heredia, S. (1999). Anthropogenic edges, treefall gaps, and fruit–frugivore interactions in a neotropical montane forest. Ecology, 80(2), 668–685.

    Google Scholar 

  • Rey, P. J. (1995). Spatio-temporal variation in fruit and frugivorous bird abundance in olive orchards. Ecology, 76(5), 1625–1635.

    Google Scholar 

  • Rosenzweig, M. L. (1995). Species diversity in space and time. Cambridge: Cambridge University Press.

    Google Scholar 

  • Rovero, F., & Struhsaker, T. T. (2007). Vegetative predictors of primate abundance: Utility and limitations of a fine-scale analysis. American Journal of Primatology, 69(11), 1242–1256.

    PubMed  Google Scholar 

  • Samuni, L., Preis, A., Deschner, T., Crockford, C., & Wittig, R. M. (2018). Reward of labor coordination and hunting success in wild chimpanzees. Communications Biology, 1(1), 1–9.

  • Seoane, J., Justribo, J. H., García, F., Retamar, J., Rabadan, C., & Atienza, J. C. (2006). Habitat-suitability modelling to assess the effects of land-use changes on Dupont’s lark Chersophilus duponti: A case study in the Layna Important Bird Area. Biological Conservation, 128(2), 241–252.

  • Sesink Clee, P. R., Abwe, E. E., Ambahe, R. D., Anthony, N. M., Fotso, R., et al (2015). Chimpanzee population structure in Cameroon and Nigeria is associated with habitat variation that may be lost under climate change. BMC Evolutionary Biology, 15(1), 2.

    PubMed  PubMed Central  Google Scholar 

  • Sexton, J. P., McIntyre, P. J., Angert, A. L., & Rice, K. J. (2009). Evolution and ecology of species range limits. Annual Review of Ecology, Evolution, and Systematics, 40(1), 415–436.

    Google Scholar 

  • Siegel, S., & Castellan, N. J. (1988). Nonparametric statistics for the behavioral sciences (2nd ed.). New York: McGraw-Hill.

    Google Scholar 

  • Simpson, G. G. (1964). Species density of North American recent mammals. Systematic Zoology, 13, 57–73.

    Google Scholar 

  • Smith, W. P., Person, D. K., & Pyara, S. (2011). Source—sinks, metapopulations, and forest reserves: Conserving northern flying squirrels in the temperate rainforests of Southeast Alaska. In J. Liu, V. Hull, A. T. Morzillo, & J. A. Wiens (Eds.), Sources, sinks and sustainability (pp. 399–422). Cambridge: Cambridge University Press.

    Google Scholar 

  • Sousa, J., Barata, A. V., Sousa, C., Casanova, C. C., & Vicente, L. (2011). Chimpanzee oil-palm use in southern Cantanhez National Park, Guinea-Bissau. American Journal of Primatology, 73(5), 485–497.

    PubMed  Google Scholar 

  • Stoehr, A. M. (1999). Are significance thresholds appropriate for the study of animal behaviour? Animal Behaviour, 57(5), F22–F25.

    CAS  PubMed  Google Scholar 

  • Stone, O. M., Laffan, S. W., Curnoe, D., & Herries, A. I. (2013). The spatial distribution of chacma baboon (Papio ursinus) habitat based on an environmental envelope model. International Journal of Primatology, 34(2), 407–422.

    Google Scholar 

  • Tappan, G. G., Sall, M., Wood, E. C., & Cushing, M. (2004). Ecoregions and land cover trends in Senegal. Journal of Arid Environments, 59, 427–462.

    Google Scholar 

  • Thomas, L., Buckland, S. T., Rexstad, E. A., Laake, J. L., Strindberg, S., et al (2010). Distance software: Design and analysis of distance sampling surveys for estimating population size. Journal of Applied Ecology, 47(1), 5–14.

    Google Scholar 

  • Tweheyo, M., & Lye, K. A. (2003). Phenology of figs in Budongo Forest Uganda and its importance for the chimpanzee diet. African Journal of Ecology, 41(4), 306–316.

    Google Scholar 

  • van Leeuwen, K. L., Hill, R. A., & Korstjens, A. J. (2020a). Quantifying chimpanzee (Pan troglodytes) landscapes: An environmental approach to classifying forest and savanna chimpanzees. International Journal of Primatology.

  • van Leeuwen, K. L., Hill, R. A., & Korstjens, A. H. (2020b). Classifying chimpanzee (Pan troglodytes) landscapes across large-scale environmental gradients in Africa. International Journal of Primatology. https://doi.org/10.1007/s10764-020-00164-5

  • Vogel, E. R., Harrison, M. E., Zulfa, A., Bransford, T. D., Alavi, S. E., et al (2015). Nutritional differences between two orangutan habitats: Implications for population density. PloS ONE, 10(10), e0138612.

    PubMed  PubMed Central  Google Scholar 

  • Warnes, G. R., Bolker, B., & Lumley, T. (2018). gtools: Various R programming tools. R package version 3.8.1.

  • Watts, D. P., Potts, K. B., Lwanga, J. S., & Mitani, J. C. (2012). Diet of chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda, 1. Diet composition and diversity. American Journal of Primatology, 74(2), 114–129.

    PubMed  Google Scholar 

  • Webster, T. H., McGrew, W. C., Marchant, L. F., Payne, C. L., & Hunt, K. D. (2014). Selective insectivory at Toro-Semliki, Uganda: Comparative analyses suggest no ‘savanna’ chimpanzee pattern. Journal of Human Evolution, 71, 20–27.

    PubMed  Google Scholar 

  • Wessling, E. G., Deschner, T., Mundry, R., Pruetz, J. D., Wittig, R. M., & Kühl, H. S. (2018a). Seasonal variation in physiology challenges the notion of chimpanzees (Pan troglodytes verus) as a forest-adapted species. Frontiers in Ecology and Evolution, 6, 60.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Wessling, E. G., Oelze, V. M., Eshuis, H., Pruetz, J. D., & Kühl, H. S. (2019). Stable isotope variation in savanna chimpanzees (Pan troglodytes verus) indicate avoidance of energetic challenges through dietary compensation at the limits of the range. American Journal of Physical Anthropology, 168(4), 665–675.

    PubMed  Google Scholar 

  • White, T. C. R. (1978). The importance of a relative shortage of food in animal ecology. Oecologia, 33, 71–86.

    CAS  PubMed  Google Scholar 

  • Wild Chimpanzee Foundation (2016). Report: Inventaires Biologique pour la Création du Parc National du Moyen-Bafing: Wild Chimpanzee Foundation. Leipzig: Germany.

    Google Scholar 

  • Wittiger, L., & Boesch, C. (2013). Female gregariousness in Western Chimpanzees (Pan troglodytes verus) is influenced by resource aggregation and the number of females in estrus. Behavioral Ecology and Sociobiology, 67(7), 1097–1111.

    Google Scholar 

  • Wrangham, R. W. (1977). Feeding behaviour of chimpanzees in Gombe National Park, Tanzania. In T. H. Clutton-Brock (Ed.), Primate ecology: Studies of feeding and ranging behaviour in Lemurs, Monkeys and Apes (pp. 504–538). Philadelphia: Elsevier.

    Google Scholar 

  • Wrangham, R., Conklin, N., Chapman, C., Hunt, K., Milton, K., et al (1991). The significance of fibrous foods for Kibale Forest chimpanzees. Philosophical Transactions of the Royal Society London B: Biological Sciences, 334, 171–178.

    CAS  Google Scholar 

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Acknowledgements

We thank the Direction des Eaux, Forêts, Chasses et de la Conservation des Sols for their permission to conduct this work in Senegal. For their assistance in coordination of the Pan African Programme and subsequent data, we thank Henk Eshuis, Mimi Arandjelovic, Gaëlle Bocksburger, and Claudia Collette-Herf. We thank Ulises Villalobos-Flores, Modi Camara, Jacques Tamba Keita, Kaly Bindia, Madi Keita, Irene Gutiérrez, Nadia Mirghani, Salam Diallo, Samba Sylla, Amadou Diallo, Daouda Diallo, Samba Diallo, Amadou Foula Diallo, Yanina Mercado, and Claudia Gallego for their assistance with data collection. Sincere thanks to Isabel Ordaz Németh for assistance with the BIOCLIM dataset, Roger Mundry for assistance with model permutations, and to Liran Samuni, Erin Kane, Stacy Lindshield, Jo Setchell, and three anonymous reviewers for their comments on previous versions of this manuscript. This research was funded by the Max Planck Society; the National Geographic Society; Iowa State University; the Max Planck Society Innovation Fund; the Krekeler Foundation, and the Jane Goodall Institutes of UK, Germany, and Spain.

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Authors and Affiliations

  1. Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

    Erin G. Wessling, Paula Dieguez & Hjalmar S. Kühl

  2. Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, USA

    Erin G. Wessling

  3. Instituto Jane Goodall España, Station Biologique Fouta Djalon, Dindéfélo, Région de Kédougou, Senegal

    Manuel Llana & Liliana Pacheco

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

    Jill D. Pruetz

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  1. Erin G. Wessling
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  2. Paula Dieguez
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  3. Manuel Llana
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  4. Liliana Pacheco
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  5. Jill D. Pruetz
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  6. Hjalmar S. Kühl
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Contributions

EGW and HSK conceived and designed the study; EGW executed the study; and PD, ML, LP, and JDP contributed materials and/or data. EGW wrote the manuscript with input from all coauthors, who have approved of the final version of this manuscript.

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Correspondence to Erin G. Wessling.

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Wessling, E.G., Dieguez, P., Llana, M. et al. Chimpanzee (Pan troglodytes verus) Density and Environmental Gradients at Their Biogeographical Range Edge. Int J Primatol 41, 822–848 (2020). https://doi.org/10.1007/s10764-020-00182-3

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