Skip to main content

Advertisement

SpringerLink
Log in

Spatiotemporal Variation in Bonobo (Pan paniscus) Habitat Use in a Forest–Savanna Mosaic

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

Understanding the ecological and behavioral variation of primates is central to improving conservation strategies. Studies of chimpanzees (Pan troglodytes) have shown marked behavioral variability across a wide range of habitats. By comparison, bonobos (Pan paniscus) occur mainly in continuous forest sites, and socioecological models explaining behavioral differences between the two species are based on the assumption that bonobo habitat is richer and more stable than chimpanzee habitats. The objective of this study was to assess bonobo ecology in a forest–savanna mosaic. We specifically explored 1) bonobo home range size, habitat use, and dietary composition; 2) forest fragmentation in a bonobo community’s home range; and 3) seasonality of dietary diversity, habitat use, and spatial distribution. Using 2 years of observational data on location, habitat type, and dietary composition, we found that the bonobo community's home range size, density, and dietary diversity were similar to those observed in continuous forest sites. Bonobos used areas with lower forest fragmentation than the surrounding areas and preferentially spent time in forested habitats. During the dry season, bonobos consumed a lower diversity of fruit species, spent more time in sparse forest with Marantaceae understory, and were closer to the seasonal center of their home range than during the rainy season. Our results contribute to our understanding of behavioral variation in bonobos and suggest that forest–savanna mosaic is valuable to bonobo conservation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Albert, A., Huynen, M.-C., Savini, T., & Hambuckers, A. (2013). Influence of food resources on the ranging pattern of northern pig-tailed macaques (Macaca leonina). International Journal of Primatology, 34(4), 696–713. https://doi.org/10.1007/s10764-013-9690-z.

    Article  Google Scholar 

  • Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49(3–4), 227–266.

    Article  CAS  Google Scholar 

  • Badrian, A., & Badrian, N. (1984). Social organization of Pan paniscus in the Lomako Forest, Zaire. In R. L. Susman (Ed.), The pygmy chimpanzee (pp. 325–346). New York: Springer-Verlag http://link.springer.com/chapter/10.1007/978-1-4757-0082-4_13.

    Chapter  Google Scholar 

  • Badrian, N., & Malenky, R. K. (1984). Feeding ecology of Pan paniscus in the Lomako Forest, Zaire. In R. L. Susman (Ed.), The pygmy chimpanzee (pp. 275–299). New York: Springer-Verlag http://link.springer.com/chapter/10.1007/978-1-4757-0082-4_11.

    Chapter  Google Scholar 

  • Baldwin, P. J., McGrew, W. C., & Tutin, C. E. (1982). Wide-ranging chimpanzees at Mt. Assirik, Senegal. International Journal of Primatology, 3(4), 367–385.

    Article  Google Scholar 

  • Barton, R. A., Whiten, A., Strum, S. C., Byrne, R. W., & Simpson, A. J. (1992). Habitat use and resource availability in baboons. Animal Behaviour, 43(5), 831–844. https://doi.org/10.1016/S0003-3472(05)80206-4.

    Article  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(1), 33. https://doi.org/10.1007/s10764-005-0722-1.

    Article  Google Scholar 

  • Beaune, D., Bretagnolle, F., Bollache, L., Bourson, C., Hohmann, G., & Fruth, B. (2013). Ecological services performed by the bonobo (Pan paniscus): Seed dispersal effectiveness in tropical forest. Journal of Tropical Ecology, 29(5), 367–380. https://doi.org/10.1017/S0266467413000515.

    Article  Google Scholar 

  • Bicca-Marques, J. C. (2003). How do howler monkeys cope with habitat fragmentation? In L. K. Marsh (Ed.), Primates in fragments: Ecology and Conservation (pp. 283–303). New York: Springer Science+Business Media. https://doi.org/10.1007/978-1-4757-3770-7_18.

    Chapter  Google Scholar 

  • Boesch, C., Hohmann, G., & Marchant, L. F. (2002). Behavioural diversity in chimpanzees and bonobos. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Boyle, S. A., Lenz, B. B., Gilbert, K. A., Sprionello, W. R., Gómez, M. S., et al. (2013). Primates of the Biological Dynamics of Forest Fragments Project: A history. In L. K. Marsh & C. A. Chapman (Eds.), Primates in fragments: Complexity and resilience (pp. 57–74). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media. https://doi.org/10.1007/978-1-4614-8839-2_5

  • Boyle, S. A., Lourenço, W. C., da Silva, L. R., & Smith, A. T. (2009). Home range estimates vary with sample size and methods. Folia Primatologica, 80(1), 33–42. https://doi.org/10.1159/000201092.

    Article  Google Scholar 

  • Chancellor, R. L., Rundus, A. S., & 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(1), 115–133. https://doi.org/10.1007/s10764-011-9561-4.

    Article  Google Scholar 

  • Conklin-Brittain, N. L., Knott, C. D., & Wrangham, R. W. (2001). The feeding ecology of apes. In The apes: Challenges for the 21st century (pp. 167–174). http://www.researchgate.net/publication/230823364_The_Feeding_Ecology_of_Apes/file/79e415053546b78615.pdf. Accessed 25 July 2014.

  • Curtis, J. T. (1959). The vegetation of Wisconsin: An ordination of plant communities. Madison: University of Wisconsin Press.

    Google Scholar 

  • Demichelis, C., Oszwald, J., Gasquet-Blanchard, C., Narat, V., Bokika, J.-C., et al (2020). Multidimensional analysis of landscape dynamics in a Central African forest-savannah mosaic. African Journal of Ecology. https://doi.org/10.1111/aje.12750.

  • Dupain, J., Van Elsacker, L., Nell, C., Garcia, P., Ponce, F., & Huffman, M. A. (2002). New evidence for leaf swallowing and Oesophagostomum infection in bonobos (Pan paniscus). International Journal of Primatology, 23(5), 1053–1062.

    Article  Google Scholar 

  • Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fernandez-Duque, E., et al (2017). Impending extinction crisis of the world’s primates: Why primates matter. Science Advances, 3(1), e1600946. https://doi.org/10.1126/sciadv.1600946.

    Article  PubMed  PubMed Central  Google Scholar 

  • Estrada, A., Saenz, J., Harvey, C., Naranjo, E., Muñoz, D., & Rosales-Meda, M. (2006). Primates in agroecosystems: Conservation value of some agricultural practices in Mesoamerican landscapes. In A. Estrada, P. A. Garber, M. M. Pavelka, & L. Luecke (Eds.), New perspectives in the study of Mesoamerican primates (pp. 437–470). Developments of Primatology: Progress and Prospects. New York: Springer Science+Business Media. http://link.springer.com/chapter/10.1007/0-387-25872-8_22.

  • 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. https://doi.org/10.1002/ajp.20577.

    Article  PubMed  Google Scholar 

  • Ferreguetti, Á. C., Pereira-Ribeiro, J., Prevedello, J. A., Tomás, W. M., Rocha, C. F. D., & Bergallo, H. G. (2018). One step ahead to predict potential poaching hotspots: Modeling occupancy and detectability of poachers in a neotropical rainforest. Biological Conservation, 227, 133–140. https://doi.org/10.1016/j.biocon.2018.09.009.

    Article  Google Scholar 

  • Fiore, A. D. (2003). Ranging behavior and foraging ecology of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in Yasuní National Park, Ecuador: Lagothrix range use and foraging ecology. American Journal of Primatology, 59(2), 47–66. https://doi.org/10.1002/ajp.10065.

    Article  PubMed  Google Scholar 

  • Fruth, B., Hickey, J. R., André, C., Furuichi, T., Hart, J., et al. (2016). Pan paniscus: The IUCN Red List of Threatened Species 2016: e.T15932A102331567. International Union for Conservation of Nature. https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T15932A17964305.en

  • Furuichi, T. (2009). Factors underlying party size differences between chimpanzees and bonobos: A review and hypotheses for future study. Primates, 50(3), 197–209. https://doi.org/10.1007/s10329-009-0141-6.

    Article  PubMed  Google Scholar 

  • Furuichi, T., Mulavwa, M., Yangozene, K., Yamba-Yamba, M., Motema-Salo, B., et al. (2008). Relationships among fruit abundance, ranging rate, and party size and composition of bonobos at Wamba. In T. Furuichi & J. Thompson (Eds.), The bonobos: Behavior, ecology, and conservation (pp. 135–149). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media. https://doi.org/10.1007/978-0-387-74787-3_8

  • Galan-Acedo, C., Arroyo-Rodriguez, V., Andresen, E., & Arasa-Gisbert, R. (2019). Ecological traits of the world’s primates. Scientific Data, 6, 55. https://doi.org/10.1038/s41597-019-0059-9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Garmendia, A., Arroyo-Rodríguez, V., Estrada, A., Naranjo, E. J., & Stoner, K. E. (2013). Landscape and patch attributes impacting medium- and large-sized terrestrial mammals in a fragmented rain forest. Journal of Tropical Ecology, 29(4), 331–344. https://doi.org/10.1017/S0266467413000370.

    Article  Google Scholar 

  • Gazagne, E., José-Domínguez, J. M., Huynen, M.-C., Hambuckers, A., Poncin, P., et al (2020). Northern pigtailed macaques rely on old growth plantations to offset low fruit availability in a degraded forest fragment. American Journal of Primatology, 82(5), e23117. https://doi.org/10.1002/ajp.23117.

    Article  PubMed  Google Scholar 

  • Georgiev, A. V., Thompson, M. E., Lokasola, A. L., & Wrangham, R. W. (2011). Seed predation by bonobos (Pan paniscus) at Kokolopori, Democratic Republic of the Congo. Primates, 52, 309–314. https://doi.org/10.1007/s10329-011-0256-4.

    Article  PubMed  Google Scholar 

  • Grant, J. W. A., Chapman, C. A., & Richardson, K. S. (1992). Defended versus undefended home range size of carnivores, ungulates and primates. Behavioral Ecology and Sociobiology, 31(3), 149–161. https://doi.org/10.1007/BF00168642.

    Article  Google Scholar 

  • Gruber, T., & Clay, Z. (2016). A comparison between bonobos and chimpanzees: A review and update. Evolutionary Anthropology: Issues, News, and Reviews, 25(5), 239–252. https://doi.org/10.1002/evan.21501.

    Article  Google Scholar 

  • Grueter, C. C., Li, D., Ren, B., & Wei, F. (2009). Choice of analytical method can have dramatic effects on primate home range estimates. Primates, 50(1), 81–84. https://doi.org/10.1007/s10329-008-0113-2.

    Article  PubMed  Google Scholar 

  • Hanya, G., Kiyono, M., Yamada, A., Suzuki, K., Furukawa, M., et al (2006). Not only annual food abundance but also fallback food quality determines the Japanese macaque density: Evidence from seasonal variations in home range size. Primates, 47(3), 275–278. https://doi.org/10.1007/s10329-005-0176-2.

    Article  PubMed  Google Scholar 

  • Harris, T. R., & Chapman, C. A. (2007). Variation in diet and ranging of black and white colobus monkeys in Kibale National Park, Uganda. Primates, 48(3), 208–221. https://doi.org/10.1007/s10329-006-0036-8.

    Article  PubMed  Google Scholar 

  • Hashimoto, C., & Furuichi, T. (2015). Sex differences in ranging and association patterns in chimpanzees in comparison with bonobos. In T. Furuichi, J. Yamagiwa, & F. Aureli (Eds.), Dispersing primate females (pp. 105–126). Tokyo: Springer Japan. https://doi.org/10.1007/978-4-431-55480-6_5.

    Chapter  Google Scholar 

  • Hashimoto, C., Tashiro, Y., Kimura, D., Enomoto, T., Ingmanson, E. J., et al (1998). Habitat use and ranging of wild bonobos (Pan paniscus) at Wamba. International Journal of Primatology, 19(6), 1045–1060.

    Article  Google Scholar 

  • Hendershott, R., Rawson, B., & Behie, A. (2018). Home range size and habitat use by Cat Ba langurs (Trachypithecus poliocephalus) in a disturbed and fragmented habitat. International Journal of Primatology, 39(4), 547–566. https://doi.org/10.1007/s10764-018-0051-9.

    Article  Google Scholar 

  • Hernandez-Aguilar, R. A., Moore, J., & Stanford, C. B. (2013). Chimpanzee nesting patterns in savanna habitat: Environmental influences and preferences. American Journal of Primatology, 75(10), 979–994. https://doi.org/10.1002/ajp.22163.

    Article  PubMed  Google Scholar 

  • Hickey, J. R., Carroll, J. P., & Nibbelink, N. P. (2012). Applying landscape metrics to characterize potential habitat of bonobos (Pan paniscus) in the Maringa-Lopori-Wamba landscape, Democratic Republic of Congo. International Journal of Primatology, 33(2), 381–400. https://doi.org/10.1007/s10764-012-9581-8.

    Article  Google Scholar 

  • Hickey, J. R., Nackoney, J., Nibbelink, N. P., Blake, S., Bonyenge, A., et al (2013). Human proximity and habitat fragmentation are key drivers of the rangewide bonobo distribution. Biodiversity and Conservation, 22(13–14), 3085–3104. https://doi.org/10.1007/s10531-013-0572-7.

    Article  Google Scholar 

  • Hohmann, G., Fowler, A., Sommer, V., & Ortmann, S. (2006). Frugivory and gregariousness of Salonga bonobos and Gashaka chimpanzees: The influence of abundance and nutritional quality of fruit. In G. Hohmann, M. M. Robins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 123–159). Cambridge: Cambridge University Press.

    Google Scholar 

  • Humle, T., Maisels, F., Oates, J. F., Plumptre, A., & Williamson, E. A. (2016). Pan troglodytes: The IUCN Red List of Threatened Species 2016: e.T159 33A129038584. International Union for Conservation of Nature. https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T15933A17964454.en

  • Hunt, K. D., & McGrew, W. C. (2002). Chimpanzees in the dry habitats at Assirik, Senegal, and at Semliki Wildlife Reserve, Uganda. In C. Boesch, G. Hohmann, & L. F. Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos. Cambridge: Cambridge University Press http://public.eblib.com/choice/publicfullrecord.aspx?p=217791. Accessed July 2020.

  • Idani, G., Kuroda, S., Kano, T., & Asato, R. (1994). Flora and vegetation of Wamba Forest, Central Zaire with reference to Bonobo (Pan paniscus) foods. Tropics, 3(3/4), 309–332.

    Article  Google Scholar 

  • Inogwabini, B.-I., Bewa, M., Longwango, M., Abokome, M., & Vuvu, M. (2008). The bonobos of the Lake Tumba – Lake Maindombe Hinterland: Threats and opportunities for population conservation. In T. Furuichi & J. Thompson (Eds.), The bonobos: Behavior, ecology and conservation (pp. 273–290). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media. http://www.springerlink.com.gate1.inist.fr/content/l5731j1w944043t3/. Accessed 6 December 2011

  • Irwin, M. T. (2008). Diademed sifaka (Propithecus diadema) ranging and habitat use in continuous and fragmented forest: Higher density but lower viability in fragments? Biotropica, 40(2), 231–240. https://doi.org/10.1111/j.1744-7429.2007.00368.x.

    Article  Google Scholar 

  • IUCN, & ICCN. (2012). Bonobo (Pan paniscus) conservation strategy 2012–2022 (IUCN/SSC Primate.). Gland, Switzerland.

  • Kano, T. (1992). The last ape: Pygmy chimpanzee behavior and ecology. Stanford, CA: Stanford University Press.

    Google Scholar 

  • Kano, T., & Mulavwa, M. (1984). Feeding ecology of the pygmy chimpanzees (Pan paniscus) of Wamba. In R. L. Susman (Ed.), The pygmy chimpanzee: Evolutionary biology and behavior (pp. 233–274). New York: Springer-Verlag.

    Chapter  Google Scholar 

  • Katsis, L., Cunneyworth, P. M. K., Turner, K. M. E., & Presotto, A. (2018). Spatial patterns of primate electrocutions in Diani, Kenya. International Journal of Primatology, 39(4), 493–510. https://doi.org/10.1007/s10764-018-0046-6.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kawamoto, Y., Takemoto, H., Higuchi, S., Sakamaki, T., Hart, J. A., Hart, T. B., et al (2013). Genetic structure of wild bonobo populations: Diversity of mitochondrial DNA and geographical distribution. PLoS ONE, 8(3), e59660. https://doi.org/10.1371/journal.pone.0059660.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kshettry, A., Vaidyanathan, S., & Athreya, V. (2017). Leopard in a tea-cup: A study of leopard habitat-use and human-leopard interactions in north-eastern India. PLoS ONE, 12(5), e0177013. https://doi.org/10.1371/journal.pone.0177013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindshield S. R., Hernandez-Aguilar A., Korstjens A. H., Marchant L.F., Narat V., Ndiaye P. I., Ogawa H., Piel A. K., Pruetz J. D., Stewart F. A., van Leeuwen K. L., Wessling E. G., Yoshikawa M. (in prep). Chimpanzee (Pan troglodytes) in Savanna landscapes

  • Lucchesi, S., Cheng, L., Janmaat, K., Mundry, R., Pisor, A., & Surbeck, M. (2020). Beyond the group: How food, mates, and group size influence intergroup encounters in wild bonobos. Behavioral Ecology, 31(2), 519–532. https://doi.org/10.1093/beheco/arz214.

    Article  Google Scholar 

  • Malenky, R. K., & Stiles, E. W. (1991). Distribution of terrestrial herbaceous vegetation and its consumption by Pan paniscus in the Lomako Forest, Zaire. American Journal of Primatology, 23(3), 153–169.

    Article  Google Scholar 

  • Malenky, R. K., & Wrangham, R. (1994). A quantitative comparison of terrestrial herbaceous food consumption by Pan paniscus in the Lomako Forest, Zaire, and Pan troglodytes in the Kibale Forest, Uganda. American Journal of Primatology, 32(1), 1.

    Article  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(3), 213–226. https://doi.org/10.1002/ajp.1350160304.

    Article  CAS  PubMed  Google Scholar 

  • Mitani, J. C., & Rodman, P. S. (1979). Territoriality: The relation of ranging pattern and home range size to defendability, with an analysis of territoriality among primate species. Behavioral Ecology and Sociobiology, 5(3), 241–251. https://doi.org/10.1007/BF00293673.

    Article  Google Scholar 

  • Mohneke, M., & Fruth, B. (2008). Bonobo (Pan paniscus) density estimation in the SW-Salonga National Park, Democratic Republic of Congo: Common methodology revisited. In T. Furuichi & J. Thompson (Eds.), The bonobos: Behavior, ecology and conservation (pp. 151–166). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media. http://link.springer.com/chapter/10.1007/978-0-387-74787-3_9.

  • Mohr, C. O. (1947). Table of equivalent populations of North American small mammals. American Midland Naturalist, 37(1), 223. https://doi.org/10.2307/2421652.

    Article  Google Scholar 

  • Moore, J. (1996). Savanna chimpanzees, referential models and the last common ancestor. In L. F. Marchant, T. Nishida, & W. C. McGrew (Eds.), Great ape societies (pp. 275–292). Cambridge: Cambridge University Press. https://doi.org/10.1017/CBO9780511752414.022.

    Chapter  Google Scholar 

  • Myneni, R. B., Hall, F. G., Sellers, P. J., & Marshak, A. L. (1995). The interpretation of spectral vegetation indexes. IEEE Transactions on Geoscience and Remote Sensing, 33(2), 481–486.

    Article  Google Scholar 

  • Namur, C. de. (1990). Aperçu sur la végétation de l’Afrique centrale atlantique. In R. Lanfranchi & D. Schwartz (Eds.), Paysages quaternaires de l’Afrique Centrale atlantique (ORSTOM., pp. 60–67). Paris.

  • Narat, V. (2014). Interactions bonobos-habitats-humains: Habituation, écologie, santé et conservation. Thèse de Doctorat en Sciences de la Nature et de l’Homme, Spécialité Eco-éthologie. Muséum national d’Histoire naturelle, Paris. https://hal.archives-ouvertes.fr/tel-02159268/. Accessed July 2020

  • Narat, V., Pennec, F., Ledo-Bisson, L., Bokika Ngawolo, J. C., Dumez, R., & Krief, S. (2015a). Bonobo conservation as a means for local development: An innovative local initiative of community-based conservation in Democratic Republic of Congo. Journal of Primatology, 4(2). https://doi.org/10.4172/2167-6801.1000127.

  • Narat, V., Pennec, F., Simmen, B., Ngawolo, J. C. B., & Krief, S. (2015b). Bonobo habituation in a forest–savanna mosaic habitat: Influence of ape species, habitat type, and sociocultural context. Primates, 56(4), 339–349. https://doi.org/10.1007/s10329-015-0476-0.

    Article  PubMed  Google Scholar 

  • Ndiaye, P. I., Badji, L., Lindshield, S. M., & Pruetz, J. D. (2018). Nest-building behaviour by chimpanzees (Pan troglodytes verus) in the non-protected area of Diaguiri (Kedougou, Senegal): Implications for conservation. Folia Primatologica, 89(5), 316–326. https://doi.org/10.1159/000490945.

    Article  Google Scholar 

  • Oelze, V. M., Douglas, P. H., Stephens, C. R., Surbeck, M., Behringer, V., et al (2016). The steady state great ape? Long term isotopic records reveal the effects of season, social rank and reproductive status on bonobo feeding behavior. PLoS ONE, 11(9), e0162091. https://doi.org/10.1371/journal.pone.0162091.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(6), 1397–1412. https://doi.org/10.1007/s10764-007-9210-0.

    Article  Google Scholar 

  • Onderdonk, D. A., & Chapman, C. A. (2000). Coping with forest fragmentation: The primates of Kibale National Park, Uganda. International Journal of Primatology, 21(4), 587–611.

    Article  Google Scholar 

  • Onishi, E., Brooks, J., Leti, I., Monghiemo, C., Bokika, J. C., Shintaku, Y., Idani, G., Yamamoto, S. (2020). Nkala Forest: Introduction of a forest-savanna mosaic field site of wild bonobos and its future prospects. Pan Africa News, 27(1), 2–5.

  • Pearce, F., Carbone, C., Cowlishaw, G., & Isaac, N. J. B. (2013). Space-use scaling and home range overlap in primates. Proceedings of the Royal Society B: Biological Sciences, 280(1751). https://doi.org/10.1098/rspb.2012.2122.

  • 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, D.R.Congo). Plant Ecology and Evolution, 149(2), 199–215. https://doi.org/10.5091/plecevo.2016.1157.

    Article  Google Scholar 

  • 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. https://doi.org/10.1016/j.jhevol.2017.08.016.

    Article  PubMed  Google Scholar 

  • Porter, L. M., Sterr, S. M., & Garber, P. A. (2007). Habitat use and ranging behavior of Callimico goeldii. International Journal of Primatology, 28(5), 1035–1058. https://doi.org/10.1007/s10764-007-9205-x.

    Article  Google Scholar 

  • 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. https://doi.org/10.1007/s10764-011-9494-y.

    Article  Google Scholar 

  • Pruetz, J. D. (2006). Feeding ecology of savanna chimpanzees 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., & 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.

    Article  Google Scholar 

  • QGIS Development Team. (2018). QGIS Geographic Information System. Open Source Geospatial Foundation. http://qgis.org. Accessed July 2018

  • R Core Team. (2018). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org

  • Reinartz, G. E., Isia, I. B., Ngamankosi, M., & Wema, L. W. (2006). Effects of forest type and human presence on bonobo (Pan paniscus) density in the Salonga National Park1. International Journal of Primatology, 27, 603–634. https://doi.org/10.1007/s10764-006-9020-9.

    Article  Google Scholar 

  • Riley, E. P., & Fuentes, A. (2011). Conserving social–ecological systems in Indonesia: Human–nonhuman primate interconnections in Bali and Sulawesi. American Journal of Primatology, 73(1), 62–74. https://doi.org/10.1002/ajp.20834.

    Article  PubMed  Google Scholar 

  • 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. https://doi.org/10.1023/A:1023741328338.

    Article  Google Scholar 

  • Sabater Pi, J., & Vea, J. (1990). Nest-building and population estimates of the bonobo from the Lokoe-Lilungu-Ikomaloki region of Zaire. Primate Conservation, 11, 43–48.

    Google Scholar 

  • Sabater Pi, J., & Vea, J. J. (1994). Comparative inventory of foods consumed by the wild pygmy chimpanzee (Pan paniscus; Mammalia) in the Lilungu-Lokofe region of the Republic of Zaire. Journal of African Zoology, 108(4), 381–396.

    Google Scholar 

  • Samuni, L., Wegdell, F., & Surbeck, M. (n.d. preprint). Behavioural diversity of bonobo prey preference as a potential cultural trait. bioRxiv, 2020.06.02.130245. https://doi.org/10.1101/2020.06.02.130245

  • Schoener, T. W. (1971). Theory of feeding strategies. Annual Review of Ecology and Systematics, 2(1), 369–404. https://doi.org/10.1146/annurev.es.02.110171.002101.

    Article  Google Scholar 

  • Serckx, A., Huynen, M.-C., Bastin, J.-F., Hambuckers, A., Beudels-Jamar, R. C., et al (2014). Nest grouping patterns of bonobos (Pan paniscus) in relation to fruit availability in a forest-savannah mosaic. PLoS ONE, 9(4), e93742. https://doi.org/10.1371/journal.pone.0093742.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Serckx, A., Kühl, H. S., Beudels-Jamar, R. C., Poncin, P., Bastin, J.-F., & Huynen, M.-C. (2015). Feeding ecology of bonobos living in forest-savannah mosaics: Diet seasonal variation and importance of fallback foods: Bonobo diet in forest-savannah mosaics. American Journal of Primatology, 77(9), 948–962. https://doi.org/10.1002/ajp.22425.

    Article  PubMed  PubMed Central  Google Scholar 

  • Setchell, J. M., Fairet, E., Shutt, K., Waters, S., & Bell, S. (2017). Biosocial conservation: Integrating biological and ethnographic methods to study human–primate interactions. International Journal of Primatology, 38(2), 401–426. https://doi.org/10.1007/s10764-016-9938-5.

    Article  PubMed  Google Scholar 

  • Sha, J. C. M., & Hanya, G. (2013). Diet, activity, habitat use, and ranging of two neighboring groups of food-enhanced long-tailed macaques (Macaca fascicularis). American Journal of Primatology, 75(6), 581–592. https://doi.org/10.1002/ajp.22137.

    Article  PubMed  Google Scholar 

  • Skinner, M. F., & Pruetz, J. D. (2012). Reconstruction of periodicity of repetitive linear enamel hypoplasia from perikymata counts on imbricational enamel among dry-adapted chimpanzees (Pan troglodytes verus) from Fongoli, Senegal. American Journal of Physical Anthropology, 149(3), 468–482. https://doi.org/10.1002/ajpa.22145.

    Article  PubMed  Google Scholar 

  • Southwood, T. R. (1978). Ecological methods: With particular reference to the study of insect populations, 2nd ed. Dordrecht: Springer. https://doi.org/10.1007/978-94-009-1225-0

  • Strier, K. B. (2017). What does variation in primate behavior mean? American Journal of Physical Anthropology, 162(S63), 4–14. https://doi.org/10.1002/ajpa.23143.

    Article  PubMed  Google Scholar 

  • 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(4), eaar2964. https://doi.org/10.1126/sciadv.aar2964.

    Article  PubMed  PubMed Central  Google Scholar 

  • Terada, S., Nackoney, J., Sakamaki, T., Mulavwa, M. N., Yumoto, T., & Furuichi, T. (2015). Habitat use of bonobos (Pan paniscus) at Wamba: Selection of vegetation types for ranging, feeding, and night-sleeping: Habitat use of bonobos at Wamba. American Journal of Primatology, 77(6), 701–713. https://doi.org/10.1002/ajp.22392.

    Article  PubMed  Google Scholar 

  • Tesfaye, D., Fashing, P. J., Bekele, A., Mekonnen, A., & Atickem, A. (2013). Ecological flexibility in Boutourlini’s blue monkeys (Cercopithecus mitis boutourlinii) in Jibat Forest, Ethiopia: A comparison of habitat use, ranging behavior, and diet in intact and fragmented forest. International Journal of Primatology, 34(3), 615–640. https://doi.org/10.1007/s10764-013-9684-x.

    Article  Google Scholar 

  • Thompson, J. A. M. (1997). The history, taxonomy and ecology of the bonobo (Pan paniscus Schwarz, 1929) with a first description of a wild population living in a forest/savanna mosaic habitat. Dissertation, Univeristy of Oxford.

  • Thompson, J. A. M. (2002). Bonobos of the Lukuru Wildlife Research Project. In Behavioural diversity in chimpanzees and bonobos. Cambridge: Cambridge University Press. https://doi.org/10.1017/CBO9780511606397.007.

    Book  Google Scholar 

  • Thompson, J. A. M., Nestor, L. M., & Kabanda, R. B. (2008). Traditional land-use practices for bonobo conservation. In T. Furuichi & J. Thompson (Eds.), The bonobos: Behavior, ecology, and conservation, Developments in Primatology: Progress and Prospects (pp. 227–244). New York: Springer Science+Business Media.

    Chapter  Google Scholar 

  • Tutin, C. E. (1999). Fragmented living: Behavioural ecology of primates in a forest fragment in the Lopé Reserve, Gabon. Primates, 40(1), 249–265.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Twinomugisha, D., & Chapman, C. A. (2008). Golden monkey ranging in relation to spatial and temporal variation in food availability. African Journal of Ecology, 46(4), 585–593. https://doi.org/10.1111/j.1365-2028.2007.00905.x.

    Article  Google Scholar 

  • Uehara, S. (1988). Grouping patterns of wild pygmy chimpanzees (Pan paniscus) observed at a marsh grassland amidst the tropical rain forest of Yalosidi, Republic of Zaire. Primates, 29(1), 41–52.

    Article  Google Scholar 

  • Van Krunkelsven, E. (2001). Density estimation of bonobos (Pan paniscus) in Salonga National Park, Congo. Biological Conservation, 99(3), 387–391.

    Article  Google Scholar 

  • van Leeuwen, K. L., Hill, R. A., & Korstjens, A. H. (2020). 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.

  • van Schaik, C. P., & Brockman, D. K. (2005). Seasonality in primate ecology, reproduction, and life history: An overview. In D. K. Brockman & C. P. van Schaik (Eds.), Seasonality in primates (pp. 3–20). Cambridge: Cambridge University Press. https://doi.org/10.1017/CBO9780511542343.002.

    Chapter  Google Scholar 

  • van Schaik, C. P., & Pfannes, K. R. (2005). Tropical climates and phenology: A primate perspective. In D. K. Brockman & C. P. Van Schaik (Eds.), Seasonality in primates: Studies of living and extinct human and non-human primates (pp. 23–54). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Vieira, W. F., Kerry, C., & Hockings, K. J. (2019). A comparison of methods to determine chimpanzee home-range size in a forest–farm mosaic at Madina in Cantanhez National Park, Guinea-Bissau. Primates, 1–11. https://doi.org/10.1007/s10329-019-00724-1

  • Wade, T. G., Riitters, K., Wickham, J. D., & Jones, K. B. (2003). Distribution and causes of global forest fragmentation. Conservation Ecology, 7(2), art7. https://doi.org/10.5751/ES-00530-070207.

    Article  Google Scholar 

  • Wallace, R. B. (2008). Factors influencing spider monkey habitat use and ranging patterns. In C. J. Campbell (Ed.), Spider monkeys (pp. 138–154). Cambridge: Cambridge University Press. https://doi.org/10.1017/CBO9780511721915.005.

    Chapter  Google Scholar 

  • Waller, M. T. (2011). The ranging behavior of bonobos in the Lomako Forest. Dissertation, University of Oregon. Retrieved from https://scholarsbank.uoregon.edu/xmlui/handle/1794/11648. Accessed Sept 2014

  • 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. https://doi.org/10.1016/j.jhevol.2018.03.001.

    Article  PubMed  Google Scholar 

  • White, F. (1998). Seasonality and socioecology: The importance of variation in fruit abundance to bonobo sociality. International Journal of Primatology, 19(6), 1013–1027.

    Article  Google Scholar 

  • White, F. J., & Wrangham, R. W. (1988). Feeding competition and patch size in the chimpanzee species Pan paniscus and Pan troglodytes. Behaviour, 148–164.

  • 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. C. McGrew, L. F. Marchant, & T. Nishida (Eds.), Great ape societies (pp. 45–57). Cambridge: Cambridge University Press. http://books.google.fr/books?hl=fr&lr=&id=iGfjJ4lKb1IC&oi=fnd&pg=PA45&dq=Socioecology+of+kanyawara+chimpanzee&ots=6KZ4RDpHG2&sig=t4fkXenueN-yZF_THI_lxOV5A44. Accessed Nov 2011

Download references

Acknowledgements

Our sincere thanks to local and national authorities in DRC. We are grateful to Mbou-Mon-Tour NGO (DRC) and to the unit of Eco-anthropology, the Pôle Image and Bonobo ECO (France) for their support in this research both monetary and in kind. We are most indebted to the two main local field assistants, Osa Otsiu Epany and Muzungu Ngofuna, for their great job in this long-term project and to trackers of the Embirima village. We are deeply grateful to anonymous reviewers; Erin Wessling, guest editor; and Johanna Setchell, editor-in-chief for their very important comments and suggestions to improve this manuscript. We thank Mallory Eckstut, PhD, from Edanz Group (https://en-author-services.edanzgroup.com/) for editing a draft of this manuscript.

Author information

Authors and Affiliations

  1. UMR 7206 Eco-anthropologie, CNRS/MNHN/Université de Paris, Musée de l’Homme, 17 place du Trocadéro, 75016, Paris, France

    Flora Pennec, Caroline Gérard, Laura Meterreau, Romain Laurent & Victor Narat

  2. Mbou-Mon-Tour NGO, 2 km from Nkala village, Bolobo Territory, Mai Ndombe Province, Democratic Republic of the Congo

    Claude Monghiemo & Jean-Christophe Bokika Ngawolo

Authors
  1. Flora Pennec
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Caroline Gérard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura Meterreau
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Claude Monghiemo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jean-Christophe Bokika Ngawolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Romain Laurent
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Victor Narat
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

FP and VN conceived and designed the study, encoded data, analyzed data, and wrote the manuscript. CG participated in the writing of the manuscript. LM encoded and analyzed data. CM and JCB supported data collection and protocol design. RL participated in data analyses.

Corresponding author

Correspondence to Victor Narat.

Additional information

Handling Editor: Erin G. Wessling

Supplementary Information

ESM 1

(PDF 255 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pennec, F., Gérard, C., Meterreau, L. et al. Spatiotemporal Variation in Bonobo (Pan paniscus) Habitat Use in a Forest–Savanna Mosaic. Int J Primatol 41, 775–799 (2020). https://doi.org/10.1007/s10764-020-00180-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-020-00180-5

Keywords

Search

Navigation