Dietary Ecology of the Nigeria–Cameroon Chimpanzee (Pan troglodytes ellioti)

Abstract

Examining the diets of primate populations inhabiting different habitat types could be useful in understanding local adaptation and divergence between these populations. In Cameroon, the Nigeria–Cameroon chimpanzee (Pan troglodytes ellioti) is subdivided into two genetically distinct populations that occupy different habitat types; one occurs in forests to the west and the other in a forest–woodland–savanna mosaic (ecotone) in the center of the country. We used macroscopic fecal sample assessment to investigate dietary differences in relation to monthly fruit availability among P. t. ellioti communities in both habitat types: at Ebo Forest (rainforest) and Mbam and Djerem National Park (ecotone). We collected data simultaneously across three sites: Bekob and Njuma (rainforest) and Ganga (ecotone) from January 2016 to December 2017. In the dry season, fruits were the most important dietary component at Bekob and Njuma, while nonfruit plant material (leaves, pith, and bark) were most important at Ganga. In the wet season, the proportion of fruits in the diet was greatest at Ganga, while nonfruit plant material dominated chimpanzee diets at Bekob and Njuma. Chimpanzees at Bekob ate more fruits from introduced and secondary forest plant species than those at Njuma and Ganga, especially during periods of fruit scarcity. Animal consumption was higher at Ganga and was inversely associated with fruit consumption. These observations link habitat diversity to differences in feeding ecology among genetically distinct populations of P. t. ellioti. We speculate that dietary differences reflect broader socioecological variation between these populations, and collectively, that these factors promote intraspecific divergence.

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References

  1. Abernethy, K. A., Maisels, F., & White, L. J. T. (2016). Environmental issues in Central Africa. Annual Review of Environment and Resources, 41, 1–33.

    Google Scholar 

  2. Abwe, E. E. (2018). Linking behavioral diversity with genetic and ecological variation in the Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti). Drexel University.

  3. Abwe, E. E., & Morgan, B. J. (2008). The Ebo forest: Four years of preliminary research and conservation of the Nigeria-Cameroon chimpanzee (Pan troglodytes). PanAfrica News, 15, 26.

    Google Scholar 

  4. 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 

  5. Astaras, C., Muhlenberg, M., & Waltert, M. (2008). Note in drill (Mandrillus leucophaeus) ecology and conservation status in Korup National Park, Southwest Cameroon. American Journal of Primatology, 70, 306–310.

    PubMed  Google Scholar 

  6. Basabose, A. K. (2002). Diet composition of chimpanzees inhabiting the Montane forest of Kahuzi, Democratic Republic of Congo. American Journal of Primatology, 58, 1–21.

    PubMed  Google Scholar 

  7. Basabose, A. K. (2004). Fruit availability and chimpanzee party size at Kahuzi montane forest, Democratic Republic of Congo. Primates, 45, 211–219.

    PubMed  Google Scholar 

  8. Berenbaum, M. R. (1996). Bugs in the system: Insects and their impact on human affairs. New York: Basic Books.

    Google Scholar 

  9. Bessa, J., Sousa, C., & Hockings, K. J. (2015). Feeding ecology of chimpanzees (Pan troglodytes verus) inhabiting a forest-mangrove-savanna-agricultural matrix at Caiquene-Cadique, Cantanhez National Park, Guinea-Bissau. American Journal of Primatology, 77, 651–665.

    PubMed  Google Scholar 

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

    Google Scholar 

  11. 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, 605–612.

    PubMed  Google Scholar 

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

    Google Scholar 

  13. Caldecott, J. O., & Miles, L. (2005). World atlas of great apes and their conservation. Berkeley: University of California Press.

    Google Scholar 

  14. Carvalho, J., Vicente, L., & Marques, T. (2015). Chimpanzee (Pan troglodytes verus) diet composition and food availability in a human-modified landscape at Lagoas de Cufada Natural Park, Guinea-Bissau. International Journal of Primatology, 36, 802–822.

    Google Scholar 

  15. Chancellor, R., Rundus, A., & Nyandwi, S. (2012). The influence of seasonal variation on chimpanzee (Pan troglodytes schweinfurthii) fallback food consumption, nest group size, and habitat use in Gishwati, a Montane rain forest fragment in Rwanda. International Journal of Primatology, 33, 115–133.

    Google Scholar 

  16. Chapman, C. A., Balcomb, S. R., Gillespie, T. R., Skorupa, J. P., & Struhsaker, T. T. (2000). Long-term effects of logging on African primate communities: A 28-year comparison from Kibale National Park, Uganda. Conservation Biology, 14, 207–217.

    Google Scholar 

  17. Chapman, C. A., Chapman, L. J., Wrangham, R., Isabirye-Basuta, G., & Ben-David, K. (1997). Spatial and temporal variability in the structure of a tropical forest. African Journal of Ecology, 35, 287–302.

    Google Scholar 

  18. Chapman, C. A., Chapman, L. J., Zanne, A. E., Poulsen, J. R., & Clark, C. J. (2005). A 12-year phenological record of fruiting: Implications for frugivore populations and indicators of climate change. In J. L. Dew & J. P. Boubli (Eds.), Tropical fruits and frugivores (pp. 75–92). New York: Springer Science+Business Media.

    Google Scholar 

  19. Chapman, C. A., & Fedigan, L. M. (1990). Dietary differences between neighboring Cebus capucinus groups: Local traditions, food availability or responses to food profitability? Folia Primatologica, 54(3–4), 177–186.

    CAS  Google Scholar 

  20. Chapman, C. A., Wrangham, R., & Chapman, L. J. (1994). Indices of habitat-wide fruit abundance in tropical forests. Biotropica, 26, 160–171.

    Google Scholar 

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

    Google Scholar 

  22. Chaves, Ó. M., Stoner, K. E., & Arroyo-Rodríguez, V. (2011). Seasonal differences in activity patterns of Geoffroyi's spider monkeys (Ateles geoffroyi) living in continuous and fragmented forests in Southern Mexico. International Journal of Primatology, 32(4), 960–973.

    Google Scholar 

  23. Chaves, O. M., Stoner, K. E., & Arroyo-Rodríguez, V. (2012). Differences in diet between spider monkey groups living in forest fragments and continuous forest in Mexico. Biotropica, 44(1), 105–113.

    Google Scholar 

  24. Cristóbal-Azkarate, J., & Arroyo-Rodríguez, V. (2007). Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: Effects of habitat fragmentation and implications for conservation. American Journal of Primatology, 69(9), 1013–1029.

    PubMed  Google Scholar 

  25. Deblauwe, I. (2009). Temporal variation in insect-eating by chimpanzees and gorillas in southeast Cameroon: Extension of niche differentiation. International Journal of Primatology, 30, 229.

    Google Scholar 

  26. Deblauwe, I., Dupain, J., Nguenang, G., Werdenich, D., & Van Elsacker, L. (2003). Insectivory by Gorilla gorilla gorilla in Southeast Cameroon. International Journal of Primatology, 24(3), 493–502.

    Google Scholar 

  27. Deblauwe, I., & Janssens, G. P. (2008). New insights in insect prey choice by chimpanzees and gorillas in southeast Cameroon: The role of nutritional value. American Journal Physical Anthropology, 135, 42–55.

    Google Scholar 

  28. Dillis, C., Beaudrot, L., Feilen, K. L., Clink, D. J., Wittmer, H. U., & Marshall, A. J. (2015). Modeling the ecological and phenological predictors of fruit consumption by gibbons (Hylobates albibarbis). Biotropica, 47(1), 85–93.

    Google Scholar 

  29. Doran, D. (1997). Influence of seasonality on activity patterns, feeding behavior, ranging, and grouping patterns in Tai chimpanzees. International Journal of Primatology, 18, 183–206.

    Google Scholar 

  30. Dowsett-Lemaire, F., & Dowsett, R. (2001). First survey of the birds and mammals of the Yabassi area, South-western Cameroon. Unpublished report for WWF Cameroon.

  31. Dutton, P., & Chapman, H. (2015). Dietary preferences of a submontane population of the rare Nigerian-Cameroon chimpanzee (Pan troglodytes ellioti) in Ngel Nyaki Forest Reserve, Nigeria. American Journal of Primatology, 77, 86–97.

    PubMed  Google Scholar 

  32. Eppley, T. M., Verjans, E., & Donati, G. (2011). Coping with low-quality diets: A first account of the feeding ecology of the southern gentle lemur, Hapalemur meridionalis, in the Mandena littoral forest, southeast Madagascar. Primates, 52(1), 7–13.

    PubMed  Google Scholar 

  33. Fan, P. F., & Jiang, X. L. (2008). Effects of food and topography on ranging behavior of black crested gibbon (Nomascus concolor jingdongensis) in Wuliang Mountain, Yunnan, China. American Journal of Primatology, 70(9), 871–878.

    PubMed  Google Scholar 

  34. Fowler, A., & Sommer, V. (2007). Subsistence technology of Nigerian chimpanzees. International Journal of Primatology, 28, 997–1023.

    Google Scholar 

  35. Fox, E. A., van Schaik, C. P., Sitompul, A., & Wright, D. N. (2004). Intra-and interpopulational differences in orangutan (Pongo pygmaeus) activity and diet: Implications for the invention of tool use. American Journal of Physical Anthropology, 125(2), 162–174.

    PubMed  Google Scholar 

  36. Freitas, C. H. D., Setz, E. Z., Araújo, A. R., & Gobbi, N. (2008). Agricultural crops in the diet of bearded capuchin monkeys, Cebus libidinosus Spix (Primates: Cebidae), in forest fragments in southeast Brazil. Revista Brasileira de Zoologia, 25(1), 32–39.

    Google Scholar 

  37. 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 

  38. Gonder, M. K., Disotell, T. R., & Oates, J. F. (2006). New genetic evidence on the evolution of chimpanzee populations, and implications for taxonomy. International Journal of Primatology, 27, 1103–1127.

  39. Gonder, M. K., Locatelli, S., Ghobrial, L., Mitchell, M. W., Kujawski, J. T., et al. (2011). Evidence from Cameroon reveals differences in the genetic structure and history of chimpanzee populations. Proceedings of the National Academy of Sciences of the USA, 108, 4766–4771.

  40. Hanya, G., Noma, N., & Agetsuma, N. (2003). Altitudinal and seasonal variations in the diet of Japanese macaques in Yakushima. Primates, 44(1), 51–59.

    PubMed  Google Scholar 

  41. Head, J. S., Boesch, C., Makaga, L., & Robbins, M. M. (2011). Sympatric chimpanzees (Pan troglodytes troglodytes) and gorillas (Gorilla gorilla gorilla) in Loango National Park, Gabon: Dietary composition, seasonality, and intersite comparisons. International Journal of Primatology, 32, 755–775.

    Google Scholar 

  42. Hemingway, C. A., & Bynum, N. (2005). The influence of seasonailty on primate diet and ranging. In D. K. Brockman & C. V. Schaik (Eds.), Seasonality in primates: Studies of living and extinct human and non-human primates. Cambridge:: Cambridge Univeristy Press.

  43. Herbinger, I., Boesch, C., & Rothe, H. (2001). Territory characteristics among three neighboring chimpanzee communities in the Tai National Park, Cote d'Ivoire. International Journal of Primatology, 22, 143–167.

    Google Scholar 

  44. Hernandez-Aguilar, R. A. (2009). Chimpanzee nest distribution and site reuse in a dry habitat: Implications for early hominin ranging. Journal of Human Evolution, 57, 350–364.

    PubMed  Google Scholar 

  45. Hockings, K. J., Anderson, J. R., & Matsuzawa, T. (2009). Use of wild and cultivated foods by chimpanzees at Bossou, Republic of Guinea: Feeding dynamics in a human-influenced environment. American Journal of Primatology, 71, 636–646.

    PubMed  Google Scholar 

  46. Hockings, K. J., Anderson, J. R., & Matsuzawa, T. (2012). Socioecological adaptations by chimpanzees, Pan troglodytes verus, inhabiting an anthropogenically impacted habitat. Animal Behaviour, 83, 801–810.

    Google Scholar 

  47. Hohmann, G., Fowler, A., Sommer, V., & Ortmann, S. (2012). Frugivory and gregariousness of Salonga bonobos and Gashaka chimpanzees: The influence of abundance and nutritional quality of fruit. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 123–159). Cambridge: Cambridge University Press.

    Google Scholar 

  48. Humle, T., & Matsuzawa, T. (2001). Behavioural diversity among the wild chimpanzee populations of Bossou and neighbouring areas, Guinea and Cote d’Ivoire, West Africa. Folia Primatologica, 72(2), 57–68.

    CAS  Google Scholar 

  49. Hunt, K. D., & McGrew, W. C. (2002). Chimpanzees in the dry habitats of Assirik, Senegal and Semliki wildlife reserve, Uganda. In C. Boesch, G. Hohmann, & L. F. Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos (pp. 35–51). Cambridge: Cambridge University Press.

    Google Scholar 

  50. Itoh, N., & Nishida, T. (2007). Chimpanzee grouping patterns and food availability in Mahale Mountains National Park, Tanzania. Primates, 48, 87–96.

    PubMed  Google Scholar 

  51. Kamgang, S. A., Bobo, K. S., Maisels, F., Ambahe, R. D., Ongono, D. E., et al (2018). The relationship between the abundance of the Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti) and its habitat: A conservation concern in the Mbam-Djerem National Park, Cameroon. BMC Ecology, 18, 40.

    PubMed  PubMed Central  Google Scholar 

  52. Kühl, H. S., Boesch, C., Kulik, L., Haas, F., Arandjelovic, M., et al (2019). Human impact erodes chimpanzee behavioral diversity. Science, 363(6434), 1453–1455.

    PubMed  Google Scholar 

  53. Kulp, J., & Heymann, E. W. (2015). Ranging, activity budget, and diet composition of red titi monkeys (Callicebus cupreus) in primary forest and forest edge. Primates, 56(3), 273–278.

    PubMed  PubMed Central  Google Scholar 

  54. Lahm, S. A. (1986). Diet and habitat preference of Mandrillus sphinx in Gabon: Implications of foraging strategy. American Journal of Primatology, 11(1), 9–26.

    PubMed  Google Scholar 

  55. Lambert, J. E., & Rothman, J. M. (2015). Fallback foods, optimal diets, and nutritional targets: Primate responses to varying food availability and quality. Annual Review of Anthropology, 44, 493–512.

    Google Scholar 

  56. Letouzey, R. (1985). Notice de la carte phytogeographique du Cameroun au 1: 500,000 (1985).

  57. Mahmoud, M. I., Campbell, M. J., Sloan, S., Alamgir, M., & Laurance, W. F. (2019). Land-cover change threatens tropical forests and biodiversity in the Littoral Region. Cameroon. Oryx, 1–10.

  58. Maisels, F. (2005). Mbam Djerem National Park, Cameroon: At the forest's edge. Canopee, 27, 2–6.

    Google Scholar 

  59. Maisels, F., Ambahe, R., Ambassa, E., & Fotso, R. (2007). New northwestern range limit of the Northern Talapoin, Mbam et Djerem National Park. Cameroon. Primate Conservation, 89–91.

  60. Marshall, A., & Wrangham, R. (2007). Evolutionary consequences of fallback foods. International Journal of Primatology, 28, 1219–1235.

    Google Scholar 

  61. Marshall, A. J., Ancrenaz, M., Brearley, F. Q., Fredriksson, G. M., Ghaffar, N., et al (2009). The effects of forest phenology and floristics on populations of Bornean and Sumatran orangutans. In S. A. Wich, S. U. Atmoko, T. M. Setia, & C. P. van Schaik (Eds.), Orangutans: Geographical variation in behavioral ecology (pp. 97–118). Oxford: Oxford University Press.

    Google Scholar 

  62. McConkey, K. R., Aldy, F., Ario, A., & Chivers, D. J. (2002). Selection of fruit by gibbons (Hylobates muelleri × agilis) in the rain forests of Central Borneo. International Journal of Primatology, 23(1), 123–145.

    Google Scholar 

  63. McConkey, K. R., Ario, A., Aldy, F., & Chivers, D. J. (2003). Influence of forest seasonality on gibbon food choice in the rain forests of Barito Ulu, Central Kalimantan. International Journal of Primatology, 24(1), 19–32.

    Google Scholar 

  64. McGrew, W. C., Ensminger, A. L., Marchant, L. F., Pruetz, J. D., & Vigilant, L. (2004). Genotyping aids field study of unhabituated wild chimpanzees. American Journal of Primatology, 63, 87–93.

    CAS  PubMed  Google Scholar 

  65. McGrew, W. C., Marchant, L. F., & Nishida, T. (Eds.) (1996). Great ape societies. Cambridge: Cambridge University Press.

    Google Scholar 

  66. McGrew, W. C., Marchant, L. F., & Phillips, C. A. (2009). Standardised protocol for primate faecal analysis. Primates, 50, 363–366.

    PubMed  Google Scholar 

  67. McLennan, M. R. (2010). Chimpanzee ecology and interactions with people in an unprotected human-dominated landscape at Bulindi, western Uganda. Oxford Brookes University.

  68. McLennan, M. R. (2013). Diet and feeding ecology of chimpanzees (Pan troglodytes) in Bulindi, Uganda: Foraging strategies at the forest–farm interface. International Journal of Primatology, 34, 585–614.

    Google Scholar 

  69. Mitchell, M. W., Locatelli, S., Abwe, E. E., Ghobrial, L., & Gonder, M. K. (2018). Male-driven differences in chimpanzee (Pan troglodytes) population genetic structure across three habitats in Cameroon and Nigeria. International Journal of Primatology, 39, 581–601.

    Google Scholar 

  70. Mitchell, M. W., Locatelli, S., Ghobrial, L., Pokempner, A. A., Sesink Clee, P. R., et al (2015a). The population genetics of wild chimpanzees in Cameroon and Nigeria suggests a positive role for selection in the evolution of chimpanzee subspecies. BMC Evolutionary Biology, 15, 3.

    PubMed  PubMed Central  Google Scholar 

  71. Mitchell, M. W., Locatelli, S., Sesink Clee, P. R., Thomassen, H. A., & Gonder, M. K. (2015b). Environmental variation and rivers govern the structure of chimpanzee genetic diversity in a biodiversity hotspot. BMC Evolutionary Biology, 15, 1.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Mittermeier, R. A., Wilson, D. E., & Rylands, A. B. (2013). Handbook of the mammals of the world: Primates. Barcelona: Lynx Edicions.

    Google Scholar 

  73. Moore, J. (1996). Savanna chimpanzees, referential models and the last common ancestor. In W. C. McGrew, L. F. Marchant, & T. Nishida (Eds.), Great ape societies (pp. 275–292). Cambridge: Cambridge University Press.

    Google Scholar 

  74. Morgan, B. J. (2001). Ecology of mammalian frugivores in the Réserve de Faune du Petit Loango. Gabon: University of Cambridge.

    Google Scholar 

  75. Morgan, B. J., & Abwe, E. E. (2006). Chimpanzees use stone hammers in Cameroon. Current Biology, 16, R632–R633.

    CAS  PubMed  Google Scholar 

  76. Morgan, B. J., Adeleke, A., Bassey, T., Bergl, R., Dunn, A., et al. (2011). Regional action plan for the conservation of the Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti). Gland, Switzerland and San Diego, CA: IUCN/SSC Primate Specialist Group and Zoological Society of San Diego, CA.

  77. Morgan, B. J., Wild, C., & Ekobo, A. (2003). Newly discovered gorilla population in the Ebo Forest, Littoral Province, Cameroon. International Journal of Primatology, 24, 1129–1137.

    Google Scholar 

  78. Morgan, D., & Sanz, C. (2006). Chimpanzee feeding ecology and comparisons with sympatric gorillas in the Goualougo Triangle, Republic of Congo. In G. Hohmann, M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 97–122). Cambridge: Cambridge University Press.

    Google Scholar 

  79. Moscovice, L., Issa, M., Petrzelkova, K., Keuler, N., Snowdon, C., & Huffman, M. (2007). Fruit availability, chimpanzee diet, and grouping patterns on Rubondo Island, Tanzania. American Journal of Primatology, 69, 487–502.

    CAS  PubMed  Google Scholar 

  80. Moynihan, K. J., Caldwell, E. R., Sellier, U. L., Kaul, C. F., Daetwyler, N. A., et al. (2004). Chad Export Project: Environmental protection measures. In SPE International Conference on Health, Safety, and Environment in Oil and Gas Exploration and Production. Society of Petroleum Engineers.

  81. Ndimbe, M. S., Morgan, B. J., Marino, J., & Abwe, E. E. (2016). Population density estimate of the Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti) in the Ebo forest, Cameroon. Unpublished report.

  82. Newton-Fisher, N. E. (1999). The diet of chimpanzees in the Budongo Forest Reserve, Uganda. African Journal of Ecology, 37, 344–354.

    Google Scholar 

  83. Newton-Fisher, N. E. (2003). The home range of the Sonso community of chimpanzees from the Budongo Forest, Uganda. African Journal of Ecology, 41, 150–156.

    Google Scholar 

  84. Nkurunungi, J. B., Ganas, J., Robbins, M. M., & Stanford, C. B. (2004). A comparison of two mountain gorilla habitats in Bwindi Impenetrable National Park, Uganda. African Journal of Ecology, 42, 289–297.

    Google Scholar 

  85. Oates, J. F., Bergl, R., & Linder, J. (2004). Africa's Gulf of Guinea forests: Biodiversity patterns and conservation priorities. Advances in Applied Biodiversity Science, 6, 1–95.

    Google Scholar 

  86. Ogawa, H., Idani, G., Moore, J., Pintea, L., & Hernandez-Aguilar, A. (2007). Sleeping parties and nest distribution of chimpanzees in the savanna woodland, Ugalla, Tanzania. International Journal of Primatology, 28, 1397–1412.

    Google Scholar 

  87. Pavelka, M. S., & Knopff, K. H. (2004). Diet and activity in black howler monkeys (Alouatta pigra) in southern Belize: Does degree of frugivory influence activity level? Primates, 45(2), 105–111.

    PubMed  Google Scholar 

  88. Piel, A. K., Strampelli, P., Greathead, E., Hernandez-Aguilar, R. A., Moore, J., & Stewart, F. A. (2017). The diet of open-habitat chimpanzees (Pan troglodytes schweinfurthii) in the Issa valley, western Tanzania. Journal of Human Evolution, 112, 57–69.

    PubMed  Google Scholar 

  89. 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, 1269–1277.

    Google Scholar 

  90. Potts, K. B., Watts, D. P., & Wrangham, R. W. (2011). Comparative feeding ecology of two communities of chimpanzees (Pan troglodytes) in Kibale National Park, Uganda. International Journal of Primatology, 32, 669–690.

    Google Scholar 

  91. Prado-Martinez, J., Sudmant, P. H., Kid, J. M., Li, H., Kelley, J. L., et al (2013). Great ape genome diversity. Nature, 499, 471–475.

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Pruetz, J. D. (2006). Feeding ecology of savanna chimpanzees (Pan troglodytes verus) at Fongoli, Senegal. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates. Ecological, physical and behavioral aspects (pp. 326–364). Cambridge: Cambridge University Press.

    Google Scholar 

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

    Google Scholar 

  94. Core Team, R. (2017). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  95. Robbins, M. M., & McNeilage, A. (2003). Home range and frugivory patterns of mountain gorillas in Bwindi Impenetrable National Park, Uganda. International Journal of Primatology, 24(3), 467–491.

    Google Scholar 

  96. Rothman, J. M., Nkurunungi, J. B., Shannon, B. F., & Bryer, M. A. (2014). High altitude diets: Implications for the feeding and nutritional ecology of mountain gorillas. In High Altitude Primates (pp. 247–264). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media.

  97. Russo, S. E., Campbell, C. J., Dew, J. L., Stevenson, P. R., & Suarez, S. A. (2005). A multi-forest comparison of dietary preferences and seed dispersal by Ateles spp. International Journal of Primatology, 26(5), 1017–1037.

    Google Scholar 

  98. Russon, A. E., Wich, S. A., Ancrenaz, M., Kanamori, T., Knott, C. D., et al (2009). Geographic variation in orangutan diets. In S. A. Wich, S. S. Utami Atmoko, T. Mitra Setia, & C. P. van Schaik (Eds.), Orangutans: Geographic variation in behavioral ecology (pp. 135–156). Oxford: Oxford University Press.

    Google Scholar 

  99. Sanz, C. M., & Morgan, D. B. (2007). Chimpanzee tool technology in the Goualougo Triangle, Republic of Congo. Journal of Human Evolution, 52, 420–433.

    PubMed  Google Scholar 

  100. 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, 2.

    PubMed  PubMed Central  Google Scholar 

  101. Smith, T. B., Wayne, R. K., Girman, D. J., & Bruford, M. W. (1997). A role for ecotones in generating rainforest biodiversity. Science, 276, 1855–1857.

    CAS  Google Scholar 

  102. Sommer, V., Buba, U., Jesus, G., & Pascual-Garrido, A. (2017). Sustained myrmecophagy in Nigerian chimpanzees: Preferred or fallback food? American Journal of Physical Anthropology, 162, 328–336.

    PubMed  Google Scholar 

  103. Stanford, C. B. (1998). The social behavior of chimpanzees and bonobos: Empirical evidence and shifting assumptions. Current Anthropology, 39, 399–420.

    Google Scholar 

  104. Stanford, C. B., & Nkurunungi, J. B. (2003). Behavioral ecology of sympatric chimpanzees and gorillas in Bwindi Impenetrable National Park, Uganda: Diet. International Journal of Primatology, 24, 901–918.

    Google Scholar 

  105. Strindberg, S., Maisels, F., Williamson, E. A., Blake, S., Stokes, E. J., et al (2018). Guns, germs, and trees determine density and distribution of gorillas and chimpanzees in Western Equatorial Africa. Science Advances, 4, eaar2964.

    PubMed  PubMed Central  Google Scholar 

  106. Stumpf, R. (2011). Chimpanzees and bonobos: Inter-and intraspecies diversity. In C. J. Campbell, A. Fuentes, K. C. Mackinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 340–356). Oxford: Oxford University Press.

    Google Scholar 

  107. Suarez, S. A. (2006). Diet and travel costs for spider monkeys in a nonseasonal, hyperdiverse environment. International Journal of Primatology, 27(2), 411–436.

    Google Scholar 

  108. Sugiyama, Y., & Koman, J. (1992). The flora of Bossou: Its utilization by chimpanzees and humans. African Study Monographs, 13, 127–169.

    Google Scholar 

  109. Tsuji, Y., Ito, T. Y., Wada, K., & Watanabe, K. (2015). Spatial patterns in the diet of the Japanese macaque Macaca fuscata and their environmental determinants. Mammal Review, 45(4), 227–238.

    Google Scholar 

  110. Tutin, C., McGrew, W., & Baldwin, P. (1983). Social organization of savanna-dwelling chimpanzees, Pan troglodytes verus, at Mt. Assirik, Senegal. Primates, 24, 154–173.

    Google Scholar 

  111. Tutin, C. E., Ham, R. M., White, L. J., & Harrison, M. J. (1997). The primate community of the Lope Reserve, Gabon: Diets, responses to fruit scarcity, and effects on biomass. American Journal of Primatology, 42, 1–24.

    CAS  PubMed  Google Scholar 

  112. Tutin, C. E. G., Fernandez, M., Rogers, M. E., Williamson, E. A., McGrew, W. C., et al (1991). Foraging profiles of sympatric lowland gorillas and chimpanzees in the Lope Reserve, Gabon [and Discussion]. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 334, 179–186.

    CAS  PubMed  Google Scholar 

  113. 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, 306–316.

    Google Scholar 

  114. van Schaik, C. P., Marshall, A. J., & Wich, S. A. (2009). Geographic variation in orangutan behavior and biology. In S. A. Wich, S. S. Utami Atmoko, T. Mitra Setia, & C. P. van Schaik (Eds.), Orangutans: Geographic variation in behavioral ecology and conservation (pp. 351–361). Oxford: Oxford University Press.

    Google Scholar 

  115. 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 

  116. Wallace, R. B. (2005). Seasonal variations in diet and foraging behavior of Ateles chamek in a southern Amazonian tropical forest. International Journal of Primatology, 26(5), 1053–1075.

    Google Scholar 

  117. Watts, D. P., & Mitani, J. C. (2001). Boundary patrols and intergroup encounters in wild chimpanzees. Behaviour, 138, 299–327.

    Google Scholar 

  118. 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, 114–129.

    PubMed  Google Scholar 

  119. Wessling, E. G., Kuhl, 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.

    PubMed  Google Scholar 

  120. Whiten, A., Goodall, J., McGrew, W. C., Nishida, T., Reynolds, V., et al (1999). Cultures in chimpanzees. Nature, 399, 682–685.

    CAS  PubMed  Google Scholar 

  121. Whytock, R. C., & Morgan, B. J. (2010). The commercial trade in bushmeat potentially threatens raptor populations in the Ebo forest Cameroon. Gabar, 21, 1–7.

    Google Scholar 

  122. Wrangham, R., Conklin, N., Etot, G., Obua, J., Hunt, K., et al (1993). The value of figs to chimpanzees. International Journal of Primatology, 14, 243–256.

    Google Scholar 

  123. Wrangham, R. W., Chapman, C. A., Clark-Arcadi, A. P., & Isabirye-Basuta, G. (1996). Social ecology of Kanyawara chimpanzees: Implications for understanding the costs of great ape groups. In W. McGrew, L. Marchant, & T. Nishida (Eds.), Great ape societies (pp. 45–57). Cambridge: Cambridge University Press.

    Google Scholar 

  124. Wrangham, R. W., & Smuts, B. B. (1980). Sex differences in the behavioural ecology of chimpanzees in the Gombe National Park. Tanzania. Journal of Reproduction and Fertility Supplement, 13–31.

  125. Yamagiwa, J., & Basabose, A. (2006). Diet and seasonal changes in sympatric gorillas and chimpanzees at Kahuzi–Biega National Park. Primates, 47, 74–90.

    PubMed  Google Scholar 

  126. Yamagiwa, J., & Basabose, A. K. (2009). Fallback foods and dietary partitioning among Pan and Gorilla. American Journal of Physical Anthropology, 140, 739–750.

    PubMed  Google Scholar 

  127. Yamakoshi, G. (1998). Dietary responses to fruit scarcity of wild chimpanzees at Bossou, Guinea: Possible implications for ecological importance of tool use. American Journal of Physical Anthropology, 106, 283–295.

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank the Ministry of Scientific Research and Innovation and the Ministry of Forestry and Wildlife for authorization to carry out research in Ebo Forest and Mbam & Djerem National Park (MDNP). We are grateful for logistical support from Ebo Forest Research Project in Ebo, and Wildlife Conservation Society at MDNP. In the field, we had help from Daouda Betare, Thomas Elanga, Christian Mbella, Daniel Mfossa, Marcel Ketchen, Abwe Enang, Celestin Njukang, Julius Alobwede, Stanley Enongene, Solomon Ngongbia, Junior Kibong, Wilson Tuka, Elie Liboho, Lappe Blaise, Jonas Mam, Jean Melba, Daniel Batouan, and Felix Nkumbe. We are grateful to the reviewers, editors, and editor-in-chief for their invaluable comments and suggestions that improved the quality of this article.

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EEA, BF, AM, RCF, BJM and MKG conceived and designed the study. EEA, AD, FB, FK, and RD collected the data. EEA, DMV, MWM and MKG analyzed the data. EEA, BJM and MKG led the writing of the manuscript. All authors contributed to the drafts.

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Correspondence to Ekwoge E. Abwe.

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Abwe, E.E., Morgan, B.J., Doudja, R. et al. Dietary Ecology of the Nigeria–Cameroon Chimpanzee (Pan troglodytes ellioti). Int J Primatol 41, 81–104 (2020). https://doi.org/10.1007/s10764-020-00138-7

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Keywords

  • Chimpanzee
  • Diet
  • Ecotone
  • Rainforest
  • Seasonal variation