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Chimpanzee (Pan troglodytes verus) Diet Composition and Food Availability in a Human-Modified Landscape at Lagoas de Cufada Natural Park, Guinea-Bissau

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Abstract

Nonhuman primate populations are facing widespread conversion of their habitat to human-modified landscapes dominated by agriculture, in which cultivated species may constitute alternative food resources, particularly during periods of wild food scarcity. We assessed intraseasonal variation in dietary composition and diversity of the western chimpanzee (Pan troglodytes verus) at Lagoas de Cufada Natural Park, Guinea-Bissau, a forest–savannah mosaic disturbed by humans, in relation to food availability. We also investigated spatial variation in dietary composition. We collected phenological data from March 2011 to February 2012 by sampling focal plant taxa and conducted macroscopic analyses of fecal samples and feeding remains during the dry season (February–May and October–December) of 2011. More fruits were available in the dry than in the wet season, and ripe fruit availability peaked in the late dry season. Chimpanzees showed a fruit-based diet composed of 31 identified plant species. Fecal samples (N = 210) were dominated by wild species (82 % volume), while cultivated species were rare (0.9 % volume; 17 % volume of unidentified species). The consumption of fruit species increased with ripe fruit availability, but a few wild fruit species were selected disproportionately to their overall availability. There was no association between dietary composition and distances among fecal samples, suggesting that chimpanzees have access to and largely use the same set of plant species over the entire study area. Moreover, the proximity to agricultural areas did not influence dietary composition. Our findings highlight that chimpanzees in this human-modified landscape still rely mostly on the consumption of wild fruit species and rarely include cultivated foods in their diet. Overall, our study underscores the importance of knowledge of feeding ecology to understand better the effects of anthropogenic habitat modification on primate diet and distribution as well as the limits to their persistence in the expanding human-dominated agricultural landscapes across their range.

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References

  • Amaro, A. P. (2011). Constituição da baseline para projectos de carbono no parque da Cufada no âmbito do mecanismo REDD+. Master's thesis, Universidade Nova de Lisboa, Lisbon.

  • Anderson, D. P., Nordheim, E. V., Moermond, T. C., Gone Bi, Z. B., & Boesch, C. (2005). Factors influencing tree phenology in Taï National Park, Côte d'Ivoire. Biotropica, 37, 631–640.

    Article  Google Scholar 

  • Anderson, J., Williamson, E., & Carter, J. (1983). Chimpanzees of Sapo Forest, Liberia: Density, nests, tools and meat-eating. Primates, 24, 594–601.

    Article  Google Scholar 

  • Atsalis, S. (1999). Diet of the brown mouse lemur (Microcebus rufus) in Ranomafana National Park, Madagascar. International Journal of Primatology, 20, 193–229.

    Article  Google Scholar 

  • Baldwin, P. J., McGrew, W. C., & Tutin, C. E. G. (1982). Wide-ranging chimpanzees at Mt. Assirik, Senegal. International Journal of Primatology, 3, 367–385.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Basabose, A. K. (2005). Ranging patterns of chimpanzees in a Montane Forest of Kahuzi, Democratic Republic of Congo. International Journal of Primatology, 26, 33–54.

    Article  Google Scholar 

  • Bertolani, P., & Pruetz, J. D. (2011). Seed reingestion in savannah chimpanzees (Pan troglodytes verus) at Fongoli, Senegal. International Journal of Primatology, 32, 1123–1132.

    Article  Google Scholar 

  • Boesch, C., & Boesch, H. (1983). Optimisation of nut-cracking with natural hammers by wild chimpanzees. Behaviour, 83, 265–286.

    Article  Google Scholar 

  • Campbell, G., Kuehl, H., N'Goran Kouamé, P., & Boesch, C. (2008). Alarming decline of West African chimpanzees in Côte d'Ivoire. Current Biology, 18, R903–R904.

    Article  CAS  PubMed  Google Scholar 

  • Carvalho, J. S., Marques, T. A., & Vicente, L. (2013). Population status of Pan troglodytes verus in Lagoas de Cufada Natural Park, Guinea-Bissau. PLoS One, 8, e71527.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carvalho, J. S., Meyer, C. F. J., Vicente, L., & Marques, T. A. (2015). Where to nest? Ecological determinants of chimpanzee nest abundance and distribution at the habitat and tree species scale. American Journal of Primatology, 77, 186–199.

    Article  PubMed  Google Scholar 

  • Catarino, L., Martins, E. S., & Diniz, M. A. (2002). Vegetation structure and ecology of the Cufada Lagoon (Guinea-Bissau). African Journal of Ecology, 40, 252–299.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Chapman, C. A., Chapman, L. J., Struhsaker, T. T., Zanne, A. E., Clark, C. J., & Poulsen, J. R. (2005). A long-term evaluation of fruiting phenology: Importance of climate change. Journal of Tropical Ecology, 21, 31–45.

    Article  Google Scholar 

  • Chapman, C. A., Chapman, L. J., Wrangham, R., Hunt, K., Gebo, G., & Gardner, L. (1992). Estimators of fruit abundance of tropical trees. Biotropica, 24, 527–531.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Chapman, C. A., Wrangham, R. W., Chapman, L. J., Kennard, D. K., & Zanne, A. E. (1999). Fruit and flower phenology at two sites in Kibale National Park, Uganda. Journal of Tropical Ecology, 15, 189–211.

    Article  Google Scholar 

  • Colwell, R. K. (2013). EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. User's Guide and application. Retrieved from http://purl.oclc.org/estimates

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

    Article  Google Scholar 

  • Duvall, C. S. (2008). Chimpanzee diet in the Bafing area, Mali. African Journal of Ecology, 46, 679–683.

    Article  Google Scholar 

  • Frankie, G. W., Baker, H. G., & Opler, P. A. (1974). Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. Journal of Ecology, 62, 881–919.

    Article  Google Scholar 

  • Gelman, A. (2013). P values and statistical practice. Epidemiology, 24, 69–72.

    Article  PubMed  Google Scholar 

  • Gotelli, N. J., & Colwell, R. K. (2010). Estimating species richness. In A. E. Magurran & B. J. McGill (Eds.), Biological diversity: Frontiers in measurement and assessment (pp. 39–54). Oxford: Oxford University Press.

    Google Scholar 

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

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Hernandez-Aguilar, R. A., Moore, J. I. M., & Stanford, C. B. (2013). Chimpanzee nesting patterns in savanna habitat: Environmental influences and preferences. American Journal of Primatology, 75, 979–994.

    Article  PubMed  Google Scholar 

  • Hladik, C. M. (1977). Chimpanzees of Gabon and chimpanzees of Gombe: Some comparative data on the diet. In T. H. Clutton-Brock (Ed.), Primate ecology: Studies of feeding and ranging behavior in lemurs, monkey and apes (pp. 481–501). London: Academic Press.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Hockings, K. J., & McLennan, M. R. (2012). From forest to farm: Systematic review of cultivar feeding by chimpanzees – management implications for wildlife in anthropogenic landscapes. PLoS One, 7, e33391.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hockings, K. J., & Sousa, C. (2012). Differential utilization of cashew – a low-conflict crop – by sympatric humans and chimpanzees. Oryx, 46, 375–381.

  • Humle, T., & Matsuzawa, T. (2004). Oil palm use by adjacent communities of chimpanzees at Bossou and Nimba Mountains, West Africa. International Journal of Primatology, 25, 551–581.

    Article  Google Scholar 

  • IBAP. (2008). Plano de gestão Parque Natural das Lagoas de Cufada, Guiné-Bissau, 2008–2018.

  • IUCN. (2015). IUCN Red List of threatened species. Version 2014.3. Retrieved from http://www.iucnredlist.org (Accessed June 2015).

  • Jost, L. (2006). Entropy and diversity. Oikos, 113, 363–375.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Kormos, R., Boesch, C., Bakarr, M. I., & Butynski, T. (2003). West African chimpanzees: Status survey and conservation action plan. Gland, Switzerland and Cambridge: IUCN.

    Google Scholar 

  • Lambert, J. (2002). Digestive retention times in forest guenons (Cercopithecus spp.) with reference to chimpanzees (Pan troglodytes). International Journal of Primatology, 23, 1169–1185.

    Article  Google Scholar 

  • Lambert, J. E. (2007). Seasonality, fallback strategies, and natural selection: A chimpanzee and Cercopithecoid model for interpreting the evolution of the hominin diet. In P. S. Ungar (Ed.), Evolution of the human diet: The known, the unknown, and the unknowable (pp. 324–343). Oxford and New York: Oxford University Press.

    Google Scholar 

  • Lambert, J. E., & Garber, P. A. (1998). Evolutionary and ecological implications of primate seed dispersal. American Journal of Primatology, 45, 9–28.

    Article  CAS  PubMed  Google Scholar 

  • Legendre, P., & Legendre, L. (1998). Numerical ecology: Developments in environmental modelling, 20 (2nd ed.). Amsterdam: Elsevier.

    Google Scholar 

  • Levi, T., & Peres, C. A. (2013). Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree. Biological Conservation, 163, 99–106.

    Article  Google Scholar 

  • Marshall, A. J., & Wich, S. (2013). Characterization of primate environments through assessment of plant phenology. In E. J. Sterling, N. Bynum, & M. E. Blair (Eds.), Primate ecology and conservation: A handbook of techniques (pp. 103–127). Oxford: Oxford University Press.

    Chapter  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nishida, T., & Shigeo, U. (1983). Natural diet of chimpanzees (Pan troglodytes schweinfurthii): Long-term record from the Mahale Mountains, Tanzania. African Study Monographs, 3, 109–130.

    Google Scholar 

  • Oates, J. F., Tutin, C. E. G., Humle, T., Wilson, M. L., Baillie, J. E. M., Balmforth, Z., et al. (2008). Pan troglodytes. The IUCN Red List of threatened species. Version 2014.3. www.iucnredlist.org (Accessed June 4, 2015).

  • Oksanen, J., Blanchet, F. G., Kindt, R., P., L., Minchin, P. R., O'Hara, R. B., et al. (2012). Community ecology package. R package version 2.0-3. http://CRAN.R-project.org/package=vegan

  • Panda, S. S., Hoogenboom, G., & Paz, J. O. (2010). Remote sensing and geospatial technological applications for site-specific management of fruit and nut crops: A review. Remote Sensing, 2, 1973–1997.

    Article  Google Scholar 

  • Phillips, C., & Lancelotti, C. (2014). Chimpanzee diet: Phytolithic analysis of feces. American Journal of Primatolog, 76, 757–773.

    Article  Google Scholar 

  • Phillips, C., & McGrew, W. (2013). Identifying species in chimpanzee (Pan troglodytes) feces: A methodological lost cause? International Journal of Primatology, 34, 792–807.

    Article  Google Scholar 

  • Phillips, C. A., & McGrew, W. C. (2014). Macroscopic inspection of ape feces: What's in a quantification method? American Journal of Primatology, 76, 539–550.

    Article  PubMed  Google Scholar 

  • Quéméré, E., Hibert, F., Miquel, C., Lhuillier, E., Rasolondraibe, E., Champeau, J., et al. (2013). A DNA metabarcoding study of a primate dietary diversity and plasticity across its entire fragmented range. PLoS One, 8, e58971.

    Article  PubMed Central  PubMed  Google Scholar 

  • R Development Core Team. (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/ (Version 3.0.2).

  • Reynolds, V., Plumptre, A. J., Greenham, J., & Harborne, J. (1998). Condensed tannins and sugars in the diet of chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda. Oecologia, 115, 331–336.

    Article  Google Scholar 

  • Sabater-Pí, J. (1979). Feeding behaviour and diet of chimpanzees (Pan troglodytes troglodytes) in the Okorobikó Mountains of Rio Muni (West Africa). Zeitschrift für Tierpsychologie, 50, 265–281.

    Article  PubMed  Google Scholar 

  • Sousa, J., Vicente, L., Gippoliti, S., Casanova, C., & Sousa, C. (2013). Local knowledge and perceptions of chimpanzees in Cantanhez National Park, Guinea-Bissau. American Journal of Primatology, 76, 122–134.

    Article  PubMed  Google Scholar 

  • Stevenson, P. R. (2001). The relationship between fruit production and primate abundance in Neotropical communities. Biological Journal of the Linnean Society, 72, 161–178.

    Article  Google Scholar 

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

    Google Scholar 

  • Suzuki, A. (1969). An ecological study of chimpanzees in a savanna woodland. Primates, 10, 103–148.

    Article  Google Scholar 

  • ter Braak, C. F., & Verdonschot, P. M. (1995). Canonical correspondence analysis and related multivariate methods in aquatic ecology. Aquatic Sciences, 57, 255–289.

    Article  Google Scholar 

  • Tutin, C. E. G., & Fernandez, M. (1985). Foods consumed by sympatric populations of Gorilla g. gorilla and Pan t. troglodytes in Gabon: Some preliminary data. International Journal of Primatology, 6, 27–43.

    Article  Google Scholar 

  • Tutin, C. E. G., & Fernandez, M. (1993a). Faecal analysis as a method of describing diets of apes: Examples from sympatric gorillas and chimpanzees at Lope, Gabon. Tropics, 2, 189–197.

    Article  Google Scholar 

  • Tutin, C. E. G., & Fernandez, M. (1993b). Relationships between minimum temperature and fruit production in some tropical forest trees in Gabon. Journal of Tropical Ecology, 9, 241–248.

    Article  Google Scholar 

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

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • van Schaik, C., Terborgh, J., & Wright, S. J. (1993). The phenology of tropical forests: Adaptive significance and consequences for primary consumers. Annual Review of Ecology and Systematics, 24, 353–377.

    Article  Google Scholar 

  • Watts, D. P., Potts, K. B., Lwanga, J. S., & Mitani, J. C. (2012a). Diet of chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda, 2. temporal variation and fallback foods. American Journal of Primatology, 74, 130–144.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Wrangham, R. (1977). Feeding behaviour of chimpanzees in Gombe National Park, Tanzania. In T. H. Clutton-Brock (Ed.), Primate ecology (pp. 503–538). London: Academic Press.

    Google Scholar 

  • Wrangham, R. W., Chapman, C. A., & Chapman, L. J. (1994). Seed dispersal by forest chimpanzees in Uganda. Journal of Tropical Ecology, 10, 355–368.

    Article  Google Scholar 

  • Wrangham, R. W., Conklin-Brittain, N. L., & Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance: I. Antifeedants. International Journal of Primatology, 19, 949–970.

    Article  Google Scholar 

  • Zuur, A. F., Ieno, E. N., & Smith, G. M. (2007). Analysing ecological data. New York: Springer.

    Book  Google Scholar 

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Acknowledgments

We thank the Instituto da Biodiversidade e das Áreas Protegidas (Guinea-Bissau) for permits and logistical support. We are grateful to LCNP staff (Honório Pereira, Benjamim Indec, Justo Nadum, Idrissa Camará, Abu Dabô, Agostinho N’fanda, Bacari Sanhá, Bafode Mané, Musa Mané, and Umaru Candê) and the villagers (especially Sadjo Camará) for their great assistance during data collection. Thanks to project Dari, especially Catarina Casanova and Celine Madeira. We also thank Christoph Meyer, Ainara Cortés-Avizanda, the reviewers, and the editors for helpful comments. Land cover data were generously provided by Luís Catarino, Joana Melo, and André Pinto from Instituto de Investigação Científica e Tropical (Portugal). This work was funded by a doctoral scholarship (SFRH/BD/60702/2009) to J. S. Carvalho from Fundação para a Ciência e a Tecnologia (Portugal). J. S. Carvalho further thanks Conservation International for financial support.

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Carvalho, J.S., Vicente, L. & Marques, T.A. Chimpanzee (Pan troglodytes verus) Diet Composition and Food Availability in a Human-Modified Landscape at Lagoas de Cufada Natural Park, Guinea-Bissau. Int J Primatol 36, 802–822 (2015). https://doi.org/10.1007/s10764-015-9856-y

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