Skip to main content

Advertisement

Log in

Diet and Use of Fallback Foods by Rwenzori Black-and-White Colobus (Colobus angolensis ruwenzorii) in Rwanda: Implications for Supergroup Formation

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

Abstract

When preferred foods are scarce, one strategy employed by primates is to switch to an alternative food item of lower quality or preferability, i.e., a fallback food. In the montane rainforest of Nyungwe National Park in southwestern Rwanda, Rwenzori black-and-white colobus (Colobus angolensis ruwenzorii) (hereafter Rwenzori colobus) form a supergroup comprising hundreds of individuals. Over 13 mo we investigated how this supergroup uses resources in periods of resource abundance vs. periods of resource scarcity. Based on 5603 feeding records we first identified preferred foods and then identified fallback foods as those food categories or species whose consumption increases when preferred foods, or preferred food categories, are less available. When the availability of 19 preferred food items was low, fruticose lichens (Usnea sp.) contributed >50% of the monthly diet for the Rwenzori colobus. Moreover, consumption of lichens was significantly negatively related to the availability of preferred foods. Fruticose lichens can therefore be considered a fallback food for Rwenzori colobus that sustains the supergroup during periods of reduced food availability. This result, in combination with previous findings that mature foliage in Nyungwe is of high quality and does not elicit feeding competition, points to the importance of resources in facilitating supergroup formation. However, several other montane forests in Eastern Africa also harbor fruticose lichens and yet support only small groups of Angolan colobus, suggesting that additional factors such as sufficient forest size and limited fragmentation and hunting pressure by humans are required for supergroups to form.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Altmann, S. A. (1974). Baboons, space, time, and energy. American Zoologist, 14(1), 221–248. https://doi.org/10.1093/icb/14.1.221.

    Article  Google Scholar 

  • Altmann, S. A. (1998). Foraging for survival: Yearling baboons in Africa. Chicago: University of Chicago Press.

    Google Scholar 

  • Anderson, J., Rowcliffe, J., & Cowlishaw, G. (2007). The Angola black-and-white colobus (Colobus angolensis palliatus) in Kenya: Historical range contraction and current conservation status. American Journal of Primatology, 69, 664–680. https://doi.org/10.1002/ajp.20377.

    Article  CAS  PubMed  Google Scholar 

  • Arseneau-Robar, T. J. M., Joyce, M. M., Stead, S. M., & Teichroeb, J. A. (2018). Proximity and grooming patterns reveal opposite-sex bonding in Rwenzori Angolan colobus monkeys (Colobus angolensis ruwenzorii). Primates, 59, 267–279. https://doi.org/10.1007/s10329-017-0643-6.

    Article  PubMed  Google Scholar 

  • Asensio, N., Korstjens, A. H., & Aureli, F. (2009). Fissioning minimizes ranging costs in spider monkeys: A multiple-level approach. Behavioral Ecology and Sociobiology, 63(5), 649–659. https://doi.org/10.1007/s00265-008-0699-9.

    Article  Google Scholar 

  • Aureli, F., Schaffner, C. M., Boesch, C., Bearder, S. K., Call, J., et al (2008). Fission-fusion dynamics: new research frameworks. Current Anthropology, 49(4), 627–654. https://doi.org/10.1086/586708.

    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), 1–21. https://doi.org/10.1002/ajp.10049.

    Article  PubMed  Google Scholar 

  • Bates, D., Maechler, M., Bolker, B., Walker, S., Christensen, R. H. B., et al. (2015). Package ‘lme4’. Convergence, 12(1), 2.

  • Bissell, H. (2014a). The nutritional ecology of the black-and-white snub-nosed monkey. Doctoral dissertation, University of Wisconsin–Madison.

  • Bissell, H. (2014b). Nutritional implications of the high-elevation lifestyle of Rhinopithecus bieti. In N. B. Grow, S. Gursky-Doyen, & A. Krzton (Eds.), High altitude primates (pp. 199–210). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media.

  • Bocian, C. M. (1997). Niche separation of black-and-white colobus monkeys (Colobus angolensis and C. guereza) in the Ituri Forest. Doctoral dissertation, the City University of New York,

  • 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 

  • Chapman, C. A., Twinomugisha, D., Teichroeb, J. A., Valenta, K., Sengupta, R., et al. (2016). How do primates survive among humans? Mechanisms employed by vervet monkeys at Lake Nabugabo, Uganda. In M. Waller (Ed.), Ethnoprimatology (pp. 77–94). Developments in Primatology: Progress and Prospects. Cham, Switzerland: Springer.

  • Clarke, G. P. (2000). Defining the eastern African coastal forests. In N. D. Burgess & G. P. Clarke (Eds.), Coastal forests of Eastern Africa (pp. 9–27). Gland, Switzerland and Cambridge: IUCN.

    Google Scholar 

  • Clink, D. J., Dillis, C., Feilen, K. L., Beaudrot, L., & Marshall, A. J. (2017). Dietary diversity, feeding selectivity, and responses to fruit scarcity of two sympatric Bornean primates (Hylobates albibarbis and Presbytis rubicunda rubida). PLoS One, 12(3). https://doi.org/10.1371/journal.pone.0173369.

  • Coles, R. C., Lee, P. C., & Talebi, M. (2012). Fission-fusion dynamics in southern muriquis (Brachyteles arachnoides) in continuous Brazilian Atlantic Forest. International Journal of Primatology, 33(1), 93–114. https://doi.org/10.1007/s10764-011-9555-2.

    Article  Google Scholar 

  • Crawford, A. (2012). Conflict-sensitive conservation in Nyungwe National Park: Conflict analysis. Winnipeg, Manitoba, Canada: International Institute for Sustainable Development.

    Google Scholar 

  • Dasilva, G. L. (1994). Diet of Colobus polykomos on Tiwai Island: Selection of food in relation to its seasonal abundance and nutritional quality. International Journal of Primatology, 15(5), 655–680. https://doi.org/10.1007/Bf02737426.

    Article  Google Scholar 

  • Davenport, T. R., De Luca, D. W., Bracebridge, C. E., Machaga, S. J., Mpunga, N. E., et al (2010). Diet and feeding patterns in the kipunji (Rungwecebus kipunji) in Tanzania’s Southern Highlands: A first analysis. Primates, 51(3), 213–220. https://doi.org/10.1007/s10329-010-0190-x.

    Article  PubMed  Google Scholar 

  • Devkota, S., Chaudhary, R. P., Werth, S., & Scheidegger, C. (2017). Indigenous knowledge and use of lichens by the lichenophilic communities of the Nepal Himalaya. Journal of Ethnobiology and Ethnomedicine, 13(15). https://doi.org/10.1186/s13002-017-0142-2.

  • Dolado, R., Cooke, C., & Beltran, F. S. (2016). How many for lunch today? Seasonal fission-fusion dynamics as a feeding strategy in wild red-capped mangabeys (Cercocebus torquatus). Folia Primatologica, 87(3), 197–212. https://doi.org/10.1159/000449220.

    Article  Google Scholar 

  • Doran, D. (1997). Influence of seasonality on activity patterns, feeding behavior, ranging, and grouping patterns in Tai chimpanzees. International Journal of Primatology, 18(2), 183–206. https://doi.org/10.1023/A:1026368518431.

    Article  Google Scholar 

  • Doran-Sheehy, D., Mongo, P., Lodwick, J., & Conklin-Brittain, N. L. (2009). Male and female western gorilla diet: Preferred foods, use of fallback resources, and implications for ape versus old world monkey foraging strategies. American Journal of Physical Anthropology, 140(4), 727–738. https://doi.org/10.1002/ajpa.21118.

    Article  CAS  PubMed  Google Scholar 

  • Dunham, N. T. (2017). Feeding ecology and dietary flexibility of Colobus angolensis palliatus in relation to habitat disturbance. International Journal of Primatology, 38(3), 553–571. https://doi.org/10.1007/s10764-017-9965-x.

    Article  Google Scholar 

  • Erb, W. M., Borries, C., Lestari, N. S., & Ziegler, T. (2012). Demography of simakobu (Simias concolor) and the impact of human disturbance. American Journal of Primatology, 74(6), 580–590.

    Article  Google Scholar 

  • Fashing, P. J. (2001). Feeding ecology of guerezas in the Kakamega Forest, Kenya: The importance of Moraceae fruit in their diet. International Journal of Primatology, 22(4), 579–609. https://doi.org/10.1023/A:1010737601922.

    Article  Google Scholar 

  • Fashing, P. J., Mulindahabi, F., Gakima, J. B., Masozera, M., Mununura, I., et al (2007). Activity and ranging patterns of Colobus angolensis ruwenzorii in Nyungwe Forest, Rwanda: Possible costs of large group size. International Journal of Primatology, 28(3), 529–550. https://doi.org/10.1007/s10764-006-9095-3.

    Article  Google Scholar 

  • Fashing, P. J., Nguyen, N., Venkataraman, V. V., & Kerby, J. T. (2014). Gelada feeding ecology in an intact ecosystem at Guassa, Ethiopia: Variability over time and implications for theropith and hominin dietary evolution. American Journal of Physical Anthropology, 155(1), 1–16. https://doi.org/10.1002/ajpa.22559.

    Article  PubMed  Google Scholar 

  • Fimbel, C., Vedder, A., Dierenfeld, E., & Mulindahabi, F. (2001). An ecological basis for large group size in Colobus angolensis in the Nyungwe Forest, Rwanda. African Journal of Ecology, 39, 83–92. https://doi.org/10.1111/j.1365-2028.2001.00276.x.

    Article  Google Scholar 

  • Fischer, E., & Killmann, D. (2008). Illustrated field guide to the plants of Nyungwe National Park Rwanda. University of Koblenz-Landau, Campus Koblenz: Department of Geography of the Institute for Integrated Natural Sciences.

  • Frahm, J. P. (1990). The ecology of epiphytic bryophytes on Mt. Kinabalu, Sabah (Malaysia). Nova Hedwigia, 51, 121–132.

    Google Scholar 

  • Ganas, J., Ortmann, S., & Robbins, M. M. (2008). Food preferences of wild mountain gorillas. American Journal of Primatology, 70(10), 927–938. https://doi.org/10.1002/ajp.20584.

    Article  PubMed  Google Scholar 

  • Grueter, C. C. (2017). Environmental seasonality. In A. Fuentes (Ed.), The international encyclopedia of primatology (pp. 342–344). Hoboken: John Wiley & Sons.

    Google Scholar 

  • Grueter, C. C., Li, D., Ren, B., Wei, F., Xiang, Z., & van Schaik, C. P. (2009). Fallback foods of temperate-living primates: A case study on snub-nosed monkeys. American Journal of Physical Anthropology, 140(4), 700–715. https://doi.org/10.1002/ajpa.21024.

    Article  PubMed  Google Scholar 

  • Grueter, C. C., Deschner, T., Behringer, V., Fawcett, K., & Robbins, M. M. (2014). Socioecological correlates of energy balance using urinary C-peptide measurements in wild female mountain gorillas. Physiology & Behavior, 127, 13–19. https://doi.org/10.1016/j.physbeh.2014.01.009.

    Article  CAS  Google Scholar 

  • Hakizimana, D. (2014). Densité et écologie des chimpanzés (Pan troglodytes schweinfurthii) dans le Parc National de la Kibira, Burundi. Doctoral dissertation, Université de Liège, Liège, Belgique.

  • Hakizimana, D., & Huynen, M. C. (2013). Chimpanzee (Pan troglodytes schweinfurthii) population density and abundance in Kibira National Park, Burundi. Pan Africa News, 20(2), 16–19.

  • Hakizimana, D., Hambuckers, A., Brotcorne, F., & Huynen, M. C. (2015). Characterization of nest sites of chimpanzees (Pan troglodytes schweinfurthii) in Kibira National Park, Burundi. African Primates, 10, 1–12.

    Google Scholar 

  • Hanya, G., Yoshihiro, S., Zamma, K., Matsubara, H., Ohtake, M., et al (2004). Environmental determinants of the altitudinal variations in relative group densities of Japanese macaques on Yakushima. Ecological Research, 19, 485–493. https://doi.org/10.1111/j.1440-1703.2004.00662.x.

    Article  Google Scholar 

  • Hanya, G., Menard, N., Qarro, M., Tattou, M. I., Fuse, M., et al (2011). Dietary adaptations of temperate primates: Comparisons of Japanese and Barbary macaques. Primates, 52(2), 187–198. https://doi.org/10.1007/s10329-011-0239-5.

    Article  PubMed  Google Scholar 

  • Harrell, F. E., Jr. (2014). rms: Regression modeling strategies. (R package version 5.1–1 ed.).

  • Hawthorne, W. D. (1993). East African coastal forest botany. In J. C. Lovett & S. K. Wasser (Eds.), Biogeography and ecology of the rain forests of Eastern Africa (pp. 57–99). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Hegerl, C., Burgess, N. D., Nielsen, M. R., Martin, E., Ciolli, M., & Rovero, F. (2017). Using camera trap data to assess the impact of bushmeat hunting on forest mammals in Tanzania. Oryx, 51, 87–97. https://doi.org/10.1017/S0030605315000836.

    Article  Google Scholar 

  • Hemingway, C. A., & Bynum, N. (2005). The influence of seasonality on primate diet and ranging. In D. K. Brockman & C. P. van Schaik (Eds.), Seasonality in primates: Studies of living and extinct human and non-Human primates (Vol. 44, pp. 57–104). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Holmes, S. M., Gordon, A. D., Louis, E. E., & Johnson, S. E. (2016). Fission-fusion dynamics in black-and-white ruffed lemurs may facilitate both feeding strategies and communal care of infants in a spatially and temporally variable environment. Behavioral Ecology and Sociobiology, 70(11), 1949–1960. https://doi.org/10.1007/s00265-016-2201-4.

    Article  Google Scholar 

  • Inogwabini, B. I., Hall, J. S., Vedder, A., Curran, B., Yamagiwa, J., & Basabose, K. (2000). Status of large mammals in the mountain sector of Kahuzi-Biega National Park, Democratic Republic of Congo, in 1996. African Journal of Ecology, 38(4), 269–276. https://doi.org/10.1046/j.1365-2028.2000.00223.x.

    Article  Google Scholar 

  • Iversen, M., Aars, J., Haug, T., Alsos, I. G., Lydersen, C., et al (2013). The diet of polar bears (Ursus maritimus) from Svalbard, Norway, inferred from scat analysis. Polar Biology, 36(4), 561–571. https://doi.org/10.1007/s00300-012-1284-2.

    Article  Google Scholar 

  • Janzen, D. H. (1970). Herbivores and the number of tree species in tropical forests. The American Naturalist, 104(940), 501–528. https://doi.org/10.1086/282687.

    Article  Google Scholar 

  • Jones, T., Hawes, J. E., Norton, G. W., & Hawkins, D. M. (2019). Effect of protection status on mammal richness and abundance in Afromontane forests of the Udzungwa Mountains, Tanzania. Biological Conservation, 229, 78–84. https://doi.org/10.1016/j.biocon.2018.11.015.

    Article  Google Scholar 

  • Jordano, P. (2000). Fruits and frugivory. In M. Fenner (Ed.), Seeds: The ecology of regeneration in plant communities, 2nd ed. (pp. 125–166). Wallingford: CABI Publishing.

    Chapter  Google Scholar 

  • Kasereka, B., Muhigwa, J. B. B., Shalukoma, C., & Kahekwa, J. M. (2006). Vulnerability of habituated Grauer's gorilla to poaching in the Kahuzi-Biega National Park, DRC. African Study Monographs, 27(1), 15–26. https://doi.org/10.14989/68246.

    Article  Google Scholar 

  • Kirkpatrick, R. C. (1996). Ecology and behavior of the Yunnan snub nosed langur Rhinopithecus bieti (Colobinae). Doctoral dissertation, University of California, Davis.

  • Knott, C. D. (1998). Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating food availability. International Journal of Primatology, 19, 1061–1079. https://doi.org/10.1023/A:1020330404983.

    Article  Google Scholar 

  • Knott, C. D. (2005). Energetic responses of food availability in the great apes: Implications for hominin evolution. In D. K. Brockman & C. P. van Schaik (Eds.), Seasonality in primates: Studies of living and extinct human and non-human primates (pp. 351–378). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Kümpel, N. F., Rowcliffe, J. M., Cowlishaw, G., & Milner-Gulland, E. J. (2009). Trapper profiles and strategies: Insights into sustainability from hunter behaviour. Animal Conservation, 12(6), 531–539. https://doi.org/10.1111/j.1469-1795.2009.00279.x.

    Article  Google Scholar 

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

  • Lambert, J. E., Chapman, C. A., Wrangham, R. W., & Conklin-Brittain, N. L. (2004). Hardness of cercopithecine foods: Implications for the critical function of enamel thickness in exploiting fallback foods. American Journal of Physical Anthropology, 125, 363–368. https://doi.org/10.1002/ajpa.10403.

    Article  PubMed  Google Scholar 

  • le Gros Clark, W. E. (1966). History of the primates: An introduction to the study of fossil man. Chicago: University of Chicago Press.

    Google Scholar 

  • Lehmann, J., Korstjens, A. H., & Dunbar, R. I. M. (2007). Fission–fusion social systems as a strategy for coping with ecological constraints: A primate case. Evolutionary Ecology, 21(5), 613–663. https://doi.org/10.1007/s10682-006-9141-9.

    Article  Google Scholar 

  • Leighton, M. (1993). Modeling dietary selectivity by Bornean orangutans: Evidence for integration of multiple criteria in fruit selection. International Journal of Primatology, 14(2), 257–313. https://doi.org/10.1007/BF02192635.

    Article  Google Scholar 

  • Liu, X., Stanford, C. B., Yang, J., Yao, H., & Li, Y. (2013). Foods eaten by the Sichuan snub-nosed monkey (Rhinopithecus roxellana) in Shennongjia National Nature Reserve, China, in relation to nutritional chemistry. American Journal of Primatology, 75(8), 860–871. https://doi.org/10.1002/ajp.22149.

    Article  CAS  PubMed  Google Scholar 

  • Luo, T., Pan, Y., Ouyang, H., Shi, P., Luo, J., et al (2004). Leaf area index and net primary productivity along subtropical to alpine gradients in the Tibetan Plateau. Global Ecology and Biogeography, 13(4), 345–358. https://doi.org/10.1111/j.1466-822X.2004.00094.x.

    Article  Google Scholar 

  • Ma, C., Fan, P. F., Zhang, Z. Y., Li, J. H., Shi, X. C., & Xiao, W. (2017). Diet and feeding behavior of a group of 42 Phayre's langurs in a seasonal habitat in Mt. Gaoligong, Yunnan, China. American Journal of Primatology, 79(10), e22695. https://doi.org/10.1002/ajp.22695.

    Article  Google Scholar 

  • Maisels, F., Gautier-Hion, A., & Gautier, J.-P. (1994). Diets of two sympatric colobines in Zaire: More evidence on seed-eating in forests on poor soils. International Journal of Primatology, 15(5). https://doi.org/10.1007/BF02737427.

  • Marks, D. L., Swain, T., Goldstein, S., Richard, A., & Leighton, M. (1988). Chemical correlates of rhesus monkey food choice: The influence of hydrolyzable tannins. Journal of Chemical Ecology, 14(1), 213–235. https://doi.org/10.1007/BF01022543.

    Article  CAS  PubMed  Google Scholar 

  • Marlowe, F. W., & Berbesque, J. C. (2009). Tubers as fallback foods and their impact on Hadza hunter-gatherers. American Journal of Physical Anthropology, 140(4), 751–758. https://doi.org/10.1002/ajpa.21040.

    Article  PubMed  Google Scholar 

  • Marshall, A. R. (2007). Disturbance in the Udzungwas: Responses of monkeys and trees to forest degradation. Doctoral dissertation, University of York,

  • Marshall, A. J., & Wrangham, R. W. (2007). Evolutionary consequences of fallback foods. International Journal of Primatology, 28(6), 1219. https://doi.org/10.1007/s10764-007-9218-5.

    Article  Google Scholar 

  • McKeever, S. (1960). Food of the northern flying squirrel in northeastern California. Journal of Mammalogy, 41, 270–271. https://doi.org/10.2307/1376371.

    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. https://doi.org/10.1007/s10764-013-9683-y.

    Article  Google Scholar 

  • Ménard, N., Vallet, D., & Gautier-Hion, A. (1985). Démographie et reproduction de Macaca sylvanus dans différents habitats en Algérie. Folia Primatologica, 44(2), 65–81. https://doi.org/10.1159/000156198.

    Article  Google Scholar 

  • Mendel, F. (1976). Postural and locomotor behavior of Alouatta palliata on various substrates. Folia Primatologica, 26(1), 36–53. https://doi.org/10.1159/000155728.

    Article  CAS  Google Scholar 

  • Miller, A., Uwingeneye, G., Ndayishimiye, D., Kaplin, B., Judge, D., & Grueter, C. C. (2018). The 'anatomy' of a supergroup of Colobus angolensis ruwenzorii in Nyungwe National Park. Paper presented at the 27th International Primatological Society Congress, Nairobi.

  • Moore, J. F., Mulindahabi, F., Masozera, M. K., Nichols, J. D., Hines, J. E., et al (2018). Are ranger patrols effective in reducing poaching-related threats within protected areas? Journal of Applied Ecology, 55(1), 99–107. https://doi.org/10.1111/1365-2664.12965.

    Article  Google Scholar 

  • Moreno-Black, G. (1974). Differential habitat utilization of four African Cercopithecidae. Doctoral dissertation, University of Florida, Gainesville.

  • 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. https://doi.org/10.1002/ajp.20350.

    Article  CAS  PubMed  Google Scholar 

  • Mosdossy, K. N., Melin, A. D., & Fedigan, L. M. (2015). Quantifying seasonal fallback on invertebrates, pith, and bromeliad leaves by white-faced capuchin monkeys (Cebus capucinus) in a tropical dry forest. American Journal of Physical Anthropology, 158(1), 67–77. https://doi.org/10.1002/ajpa.22767.

    Article  PubMed  Google Scholar 

  • Nagelkerke, N. J. D. (1991). A note on a general definition of the coefficient of determination. Biometrika, 78, 691–692. https://doi.org/10.1093/biomet/78.3.691.

    Article  Google Scholar 

  • Nakagawa, N. (1989). Bioenergetics of Japanese monkeys (Macaca fuscata) on Kinkazan Island during winter. Primates, 30, 441–460. https://doi.org/10.1007/BF02380873.

    Article  Google Scholar 

  • Nakagawa, N. (1997). Determinants of the dramatic seasonal changes in the intake of energy and protein by Japanese monkeys in a cool temperate forest. American Journal of Primatology, 41, 267–288. https://doi.org/10.1002/(SICI)1098-2345(1997)41:4<267::AID-AJP1>3.0.CO;2-V.

    Article  CAS  PubMed  Google Scholar 

  • Nash, T. H. (2008). Lichen biology, 2nd ed. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Nasi, R., Taber, A., & Van Vliet, N. (2011). Empty forests, empty stomachs? Bushmeat and livelihoods in the Congo and Amazon Basins. International Forestry Review, 13(3), 355–368. https://doi.org/10.1505/146554811798293872.

    Article  Google Scholar 

  • Nielsen, M. R. (2006). Importance, cause and effect of bushmeat hunting in the Udzungwa Mountains, Tanzania: Implications for community based wildlife management. Biological Conservation, 128(4), 509–516. https://doi.org/10.1016/j.biocon.2005.10.017.

    Article  Google Scholar 

  • Nishida, T., Itani, J., Hiraiwa, M., & Hasegawa, T. (1981). A newly-discovered population of Colobus angolensis in East Africa. Primates, 22(4), 557–563. https://doi.org/10.1007/BF02381247.

    Article  Google Scholar 

  • Nyirambangutse, B., Zibera, E., Uwizeye, F. K., Nsabimana, D., Bizuru, E., et al (2017). Carbon stocks and dynamics at different successional stages in an Afromontane tropical forest. Biogeosciences, 14, 1285–1303. https://doi.org/10.5194/bg-14-1285-2017.

    Article  Google Scholar 

  • Oates, J. F. (1996). Habitat alteration, hunting and the conservation of folivorous primates in African forests. Australian Journal of Ecology, 21, 1–9. https://doi.org/10.1111/j.1442-9993.1996.tb00580.x.

    Article  Google Scholar 

  • OBPE (2014). Plan d’Aménagement et de Gestion du Parc National de la Kibira. In L. Ntahuga (Ed.), Bujumbura, Burundi: Office Burundais pour la Protection de l'Environnement.

  • Owens, J. R., Honarvar, S., Nessel, M., & Hearn, G. W. (2015). From frugivore to folivore: altitudinal variations in the diet and feeding ecology of the Bioko Island drill (Mandrillus leucophaeus poensis). American Journal of Primatology, 77(12), 1263–1275. https://doi.org/10.1002/ajp.22479.

    Article  PubMed  Google Scholar 

  • Pegau, R. E. (1968). Growth rates of important reindeer forage lichens on the Seward Peninsula, Alaska. Arctic, 21(4), 255–259.

    Article  Google Scholar 

  • Peres, C. A. (1994). Primate responses to phenological change in an Amazonian terra firme forest. Biotropica, 26, 98–112. https://doi.org/10.2307/2389114.

    Article  Google Scholar 

  • Plumptre, A. J., Masozera, M., Fashing, P. J., McNeilage, A., Ewango, C., et al (2002). Biodiversity surveys of the Nyungwe forest Reserve in SW Rwanda. Wildlife Conservation Society Working Papers, 19, 1–95.

    Google Scholar 

  • Porter, L. M., Garber, P. A., & Nacimento, E. (2009). Exudates as a fallback food for Callimico goeldii. American Journal of Primatology, 71(2), 120–129. https://doi.org/10.1002/ajp.20630.

    Article  CAS  PubMed  Google Scholar 

  • Preston, M. A. (2011). Anthropogenic disturbance of forests, its effects on primates, and conservation in West Usambara, Tanzania. Doctoral dissertation, University of California.

  • Quantum GIS Development Team (2012). Quantum GIS geographic information system 2.0. 0 ed., Vol. 2.

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

  • Rahbek, C. (1995). The elevational gradient of species richness: A uniform pattern? Ecography, 18(2), 200–205. https://doi.org/10.1111/j.1600-0587.1995.tb00341.x.

  • Remis, M. J. (1997). Western lowland gorillas (Gorilla gorilla gorilla) as seasonal frugivores: use of variable resources. American Journal of Primatology, 43, 87–109. https://doi.org/10.1002/(SICI)1098-2345(1997)43:2<87::AID-AJP1>3.0.CO;2-T.

  • Remis, M. J., & Kpanou, J. B. (2011). Primate and ungulate abundance in response to multi-use zoning and human extractive activities in a Central African Reserve. African Journal of Ecology, 49(1), 70–80. https://doi.org/10.1111/j.1365-2028.2010.01229.x.

    Article  Google Scholar 

  • Ren, B., Li, D., Garber, P. A., & Li, M. (2012). Fission–fusion behavior in Yunnan snub-nosed monkeys (Rhinopithecus bieti) in Yunnan, China. International Journal of Primatology, 33(5), 1096–1109. https://doi.org/10.1007/s10764-012-9586-3.

    Article  Google Scholar 

  • Richards, P. W. (1952). The tropical rain forest. Cambridge: Cambridge University Press.

    Google Scholar 

  • Rimbach, R., Link, A., Montes-Rojas, A., Di Fiore, A., Heistermann, M., & Heymann, E. W. (2014). Behavioral and physiological responses to fruit availability of spider monkeys ranging in a small forest fragment. American Journal of Primatology, 76(11), 1049–1061. https://doi.org/10.1002/ajp.22292.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rothman, J. M., Pell, A. N., Nkurunungi, J. B., & Dierenfeld, E. S. (2006). Nutritional aspects of the diet of wild gorillas: How do Bwindi gorillas compare? In N. E. Newton-Fisher, H. Notman, J. D. Paterson, & V. Reynolds (Eds.), Primates of Western Uganda (pp. 153–169). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media.

  • RStudio (2017). RStudio: Integrated development environment for R. Boston: RStudio Inc..

    Google Scholar 

  • Rutagarama, E., & Martin, A. (2006). Partnerships for protected area conservation in Rwanda. Geographical Journal, 172(4), 291–305. https://doi.org/10.1111/j.1475-4959.2006.00217.x.

    Article  Google Scholar 

  • Sauther, M. L., & Cuozzo, F. P. (2009). The impact of fallback foods on wild ring-tailed lemur biology: A comparison of intact and anthropogenically disturbed habitats. American Journal of Physical Anthropology, 140(4), 671–686. https://doi.org/10.1002/ajpa.21128.

    Article  PubMed  Google Scholar 

  • Schreier, A. L., & Swedell, L. (2012). Ecology and sociality in a multilevel society: Ecological determinants of spatial cohesion in hamadryas baboons. American Journal of Physical Anthropology, 148(4), 580–588. https://doi.org/10.1002/ajpa.22076.

    Article  PubMed  Google Scholar 

  • Seifriz, W. (1924). The altitudinal distribution of lichens and mosses on Mt Gedeh, Java. Journal of Ecology, 12(2), 307–313. https://doi.org/10.2307/2255252.

    Article  Google Scholar 

  • Singh, L., & Singh, J. S. (1993). Importance of short-lived components of a dry tropical forest for biomass production and nutrient cycling. Journal of Vegetation Science, 4(5), 681–686. https://doi.org/10.2307/3236133.

    Article  Google Scholar 

  • 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(4), 901–918. https://doi.org/10.1023/A:1024689008159.

    Article  Google Scholar 

  • Switzer, W. M., Tang, S., Ahuka-Mundeke, S., Shankar, A., Hanson, D. L., et al (2012). Novel simian foamy virus infections from multiple monkey species in women from the Democratic Republic of Congo. Retrovirology, 9(1), 100. https://doi.org/10.1186/1742-4690-9-100.

    Article  PubMed  PubMed Central  Google Scholar 

  • Teichroeb, J. A., Bridgett, G. R., Corriveau, A., & Twinomugisha, D. (2019). The immediate impact of selective logging on Rwenzori Angolan colobus (Colobus angolensis ruwenzorii) at Lake Nabugabo, Uganda. In A. M. Behie, J. A. Teichroeb, & N. Malone (Eds.), Primate research and conservation in the Anthropocene (Vol. 82, pp. 120–140). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Topp-Jørgensen, E., Nielsen, M. R., Marshall, A. R., & Pedersen, U. (2009). Relative densities of mammals in response to different levels of bushmeat hunting in the Udzungwa Mountains, Tanzania. Tropical Conservation Science, 2(1), 70–87. https://doi.org/10.1177/194008290900200108.

    Article  Google Scholar 

  • Tsuji, Y., Hanya, G., & Grueter, C. C. (2013). Feeding strategies of primates in temperate and alpine forests: Comparison of Asian macaques and colobines. Primates, 54, 201–215. https://doi.org/10.1007/s10329-013-0359-1.

    Article  PubMed  Google Scholar 

  • Tutin, C. E. G., Ham, R. M., White, L. J. T., & Harrison, M. J. S. (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. https://doi.org/10.1002/(SICI)1098-2345(1997)42:1<1::AID-AJP1>3.0.CO;2-0.

    Article  CAS  PubMed  Google Scholar 

  • Ure, D. C., & Maser, C. (1982). Mycophagy of red-backed voles in Oregon and Washington. Canadian Journal of Zoology, 60(12), 3307–3315. https://doi.org/10.1139/z82-419.

    Article  Google Scholar 

  • van Schaik, C. P., & van Noordwijk, M. A. (1985). Interannual variability in fruit abundance and the reproductive seasonality in Sumatran long-tailed macaques (Macaca fascicularis). Journal of Zoology, 206(4), 533–549. https://doi.org/10.1111/j.1469-7998.1985.tb03557.x.

    Article  Google Scholar 

  • van Schaik, C. P., Terborgh, J. W., & Wright, S. J. (1993). The phenology of tropical forests: adaptive significance and consequences for primary consumers. Annual Review of Ecology, Evolution, and Systematics, 24, 353–377. https://doi.org/10.1146/annurev.es.24.110193.002033.

    Article  Google Scholar 

  • Vedder, A., & Fashing, P. J. (2002). Diet of a 300-member Angolan colobus monkey (Colobus angolensis) supergroup in the Nyungwe forest, Rwanda. American Journal of Physical Anthropology Supplement, 34, 159–160.

    Google Scholar 

  • Ward, R. L., & Marcum, C. L. (2005). Lichen litterfall consumption by wintering deer and elk in western Montana. The Journal of Wildlife Management, 69(3), 1081–1089. https://doi.org/10.2193/0022-541X(2005)069[1081:LLCBWD]2.0.CO;2.

    Article  Google Scholar 

  • Watanabe, K. (1981). Variations in group composition and population density of the two sympatric Mentawaian leaf-monkeys. Primates, 22(2), 145–160. https://doi.org/10.1007/BF02382606.

    Article  Google Scholar 

  • Watts, D. P. (1984). Composition and variability of mountain gorilla diets in the central Virungas. American Journal of Primatology, 7(4), 323–356. https://doi.org/10.1002/ajp.1350070403.

    Article  PubMed  Google Scholar 

  • Weber, W. (1989). Conservation and development on Zaire-Nile divide: An analysis of value conflicts and convergence in the management of afromontane forests in Rwanda. Doctoral dissertation, University of Wisconsin–Madison.

  • Wittiger, L., & Boesch, C. (2013). Female gregariousness in western chimpanzees (Pan troglodytes verus) is influenced by resource aggregation and the number of females in estrus. Behavioral Ecology and Sociobiology, 67(7), 1097–1111. https://doi.org/10.1007/s00265-013-1534-5.

    Article  Google Scholar 

  • Wrangham, R., Cheney, D., Seyfarth, R., & Sarmiento, E. (2009). Shallow-water habitats as sources of fallback foods for hominins. American Journal of Physical Anthropology, 140(4), 630–642. https://doi.org/10.1002/ajpa.21122.

    Article  PubMed  Google Scholar 

  • Xiang, Z. F., Huo, S., Xiao, W., Quan, R. C., & Grueter, C. C. (2007). Diet and feeding behavior of Rhinopithecus bieti at Xiaochangdu, Tibet: Adaptations to a marginal environment. American Journal of Primatology, 69(10), 1141–1158. https://doi.org/10.1002/ajp.20412.

    Article  PubMed  Google Scholar 

  • Yamagiwa, J., & Basabose, A. K. (2006). Effects of fruit scarcity on foraging strategies of sympatric gorillas and chimpanzees. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 73–96). Cambridge: Cambridge University Press.

    Google Scholar 

Download references

Acknowledgments

We thank the government of Rwanda for allowing us to work in Nyungwe National Park and the Rwanda Development Board, specifically Antoine Mudakikwa, Innocent Ndikubwimana, and Ildephonse Kambogo for facilitating the research. We are thankful to the colobus trackers for assistance in the field. We gratefully acknowledge funding from Primate Conservation Inc. (grant #001337 & #001444), the University of Western Australia, and UWA Postgraduate Student Association. We thank our sponsors CooperVision, Southern Tarpaulins, SteriPen, Qatar Airways, and Osprey for their generous contribution of equipment. We thank those who contributed to the Chuffed Crowdfunding Project; the support was extremely valuable. For comments on an earlier version of this article, the authors thank Addisu Mekonnen, anonymous reviewers, and Joanna Setchell.

Author information

Authors and Affiliations

Authors

Contributions

AM and CCG originally formulated the idea; AM and CCG developed methodology; AM, GU, and DN conducted fieldwork; AM performed statistical analyses; AM wrote the manuscript and the other authors provided editorial advice.

Corresponding author

Correspondence to Alex Miller.

Additional information

Handling Editor: Addisu Mekonnen

Electronic supplementary material

ESM 1

(DOCX 43 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miller, A., Judge, D., Uwingeneye, G. et al. Diet and Use of Fallback Foods by Rwenzori Black-and-White Colobus (Colobus angolensis ruwenzorii) in Rwanda: Implications for Supergroup Formation. Int J Primatol 41, 434–457 (2020). https://doi.org/10.1007/s10764-020-00143-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-020-00143-w

Keywords

Navigation