Abstract
One of the goals for primate feeding ecology is to understand the factors that affect inter- and intra-specific variations. Therefore, a detailed description of basic feeding ecology in as many populations as possible is necessary and warrants further understanding. The black-and-white colobus (Colobus guereza) or guereza is widely distributed in Africa and is one of the well-studied colobines in terms of their feeding; they demonstrate considerable variation in their diets in response to local conditions. We studied the diet of a group of guerezas in the Kalinzu Forest, Uganda, for over 30 consecutive months using behavioral observation (4308 h in total), phenology, and vegetation surveys. A total of 31 plant species were consumed by the study group. This study group was predominantly folivorous; the majority of their feeding time was involved in feeding on young leaves (87%). However, during certain times of the year, fruits and seeds accounted for 45% of monthly feeding time. Young leaves of Celtis durandii were by far the most important food, which constituted 58% of the total feeding records. There was a significant increase in the consumption of fruits and flowers once young leaf availability was low, but their consumption of fruits did not significantly increase even when fruit availability was high. Their monthly dietary diversity increased as the number of available plants with young leaves declined, suggesting that much of the dietary diversity in the study group may be attributable to the young leaf portion of their diet. Our findings may help contribute to a better understanding of the dietary adaptations and feeding ecology of guerezas in response to local environmental conditions.
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References
Bocian CM (1997) Niche separation of black-and-white colobus monkeys (Colobus angolensis and C. guereza) in the Ituri Forest. Ph. D. Ph. D. thesis, City University of New York, New York.
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, Verlag
Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM (2011) Primates in perspective. Oxford University Press, New York
Chapman CA, Chapman LJ (2002) Foraging challenges of red colobus monkeys: influence of nutrients and secondary compounds. Comp Biochem Physiol A 133:861–875. https://doi.org/10.1016/s1095-6433(02)00209-x
Chapman CA, Chapman LJ, Rode KD, Hauck EM, McDowell LR (2003) Variation in the nutritional value of primate foods: among trees, time periods, and areas. Int J Primatol 24:317–333. https://doi.org/10.1023/a:1023049200150
Chivers D (1994) Functional anatomy of the gastrointestinal tract. In: Davies A, Oates J (eds) Colobine monkeys: their ecology, behaviour and evolution. Cambridge University Press, Cambridge, pp 205–227
Clutton-Brock TH (1975) Feeding behaviour of red colobus and black and white colobus in East Africa. Folia Primatol 23:165–207. https://doi.org/10.1159/000155671
Colwell RK (2013) EstimateS: Statistical estimation of species richness and shared species from samples, version 8.0. http://purl.oclc.org/estimates
Davies G (1991) Seed-eating by red leaf monkeys (Presbytis rubicunda) in dipterocarp forest of northern Borneo. Int J Primatol 12:119–144. https://doi.org/10.1007/bf02547577
Fashing PJ (2001) Feeding ecology of guerezas in the Kakamega Forest, Kenya: the importance of Moraceae fruit in their diet. Int J Primatol 22:579–609. https://doi.org/10.1023/a:1010737601922
Fashing PJ (2011) African colobine monkeys: their behavior, ecology, and conservation. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM (eds) Primates in perspective, 2nd edn. Oxford University Press, Oxford, pp 203–229
Gordon IJ, Prins HH, Mallon J, Puk LD, Miranda EB, Starling-Manne C, van der Wal R, Moore B, Foley W, Lush L, Maestri R, Matsuda I, Clauss M (2019) The ecology of browsing and grazing in other vertebrate taxa. In: Gordon IJ, Prins HH (eds) The ecology of browsing and grazing II. Springer, Cham, pp 339–404
Hanya G, Tsuji Y, Grueter CC (2013) Fruiting and flushing phenology in Asian tropical and temperate forests: implications for primate ecology. Primates 54:101–110. https://doi.org/10.1007/s10329-012-0341-3
Harris TR, Chapman CA (2007) Variation in diet and ranging of black and white colobus monkeys in Kibale National Park, Uganda. Primates 48:208–221. https://doi.org/10.1007/s10329-006-0036-8
Hashimoto C, Furuichi T, Tashiro Y, Kimura D (1999) Vegetation of the Kalinzu Forest, Uganda: ordination of forest types using principal component analysis. Afr Study Monogr 20:229–239
Hemingway CA, Bynum N (2005) The influence of seasonality on primate diet and ranging. In: Brockman DK, van Schaik CP (eds) Seasonality in primates. Cambridge University Press, Cambridge.
Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70. https://doi.org/10.2307/4615733
Hussein I, Afework B, Dereje Y (2017) Population structure and feeding ecology of Guereza (Colobus guereza) in Borena-Sayint National Park, northern Ethiopia. Int J Biodiver Conserv 9:323–333. https://doi.org/10.5897/ijbc2017.1114
Kirkpatrick RC (2011) The Asian colobines: diversity among leaf-eating monkeys. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM (eds) Primates in perspective, 2nd edn. Oxford University Press, Oxford, pp 189–202
Lambert JE, Rothman JM (2015) Fallback foods, optimal diets, and nutritional targets: primate responses to varying food availability and quality. Ann Rev Anthropol 44:493–512. https://doi.org/10.1146/annurev-anthro-102313-025928
Marshall AJ, Wrangham RW (2007) Evolutionary consequences of fallback foods. Int J Primatol 28:1219–1235. https://doi.org/10.1007/s10764-007-9218-5
Matsuda I, Tuuga A, Higashi S (2009) The feeding ecology and activity budget of proboscis monkeys. Am J Primatol 71:478–492. https://doi.org/10.1002/ajp.20677
Matsuda I, Clauss M, Tuuga A, Sugau J, Hanya G, Yumoto T, Bernard H, Hummel J (2017) Factors affecting leaf selection by foregut-fermenting proboscis monkeys: new insight from in vitro digestibility and toughness of leaves. Sci Rep 7:42774. https://doi.org/10.1038/srep42774
Matsuda I, Chapman CA, Clauss M (2019) Colobine forestomach anatomy and diet. J Morphol 280:1608–1616. https://doi.org/10.1002/jmor.21052
Mittermeier RA, Rylands AB, Wilson DE (2013) Handbook of the mammals of the world. Primates. Lynx Edicions, Barcelona
Newton P (1992) Feeding and ranging patterns of forest hanuman langurs (Presbytis entellus). Int J Primatol 13:245–285. https://doi.org/10.1007/bf02547816
Oates JF (1977) The Guereza and Its Food. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. Academic Press, New York, pp 276–319
Pielou EC (1966) Shannon's formula as a measure of specific diversity: its use and misuses. Am Nat 104:463–465
Poulsen JR, Clark CJ, Connor EF, Smith TB (2002) Differential resource use by primates and hornbills: implications for seed dispersal. Ecology 83:228–240. https://doi.org/10.1890/0012-9658(2002)083[0228:drubpa]2.0.co;2
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
R Core Development Team (2019) R: a language and environment for statistical computing. Foundation for Statistical Computing, Vienna
Wasserman MD, Chapman CA (2003) Determinants of colobine monkey abundance: the importance of food energy, protein and fibre content. J Anim Ecol 72:650–659. https://doi.org/10.1046/j.1365-2656.2003.00736.x
Yeager CP (1989) Feeding ecology of the proboscis monkey (Nasalis larvatus). Int J Primatol 10:497–530. https://doi.org/10.1007/bf02739363
Zhou Q, Wei F, Li M, Huang C, Luo B (2006) Diet and food choice of Trachypithecus francoisi in the Nonggang Nature Reserve, China. Int J Primatol 27:1441–1460. https://doi.org/10.1007/s10764-006-9082-8
Zinner D, Tesfaye D, Stenseth NC, Bekele A, Mekonnen A, Doeschner S, Atickem A, Roos C (2019) Is Colobus guereza gallarum a valid endemic Ethiopian taxon? Primate Biol 6:7–16. https://doi.org/10.5194/pb-6-7-2019
Acknowledgements
We are grateful to the Uganda National Council for Science and Technology, the Uganda Forestry Department, and Uganda Wildlife Authority for permission to work in the Kalinzu Forest. Our appreciation goes to the research assistants and managers from this project, particularly, Mina Isaji, Hodaka Matsuo, Natsumi Aruga, Reiko Okano, and Charles Lakwo because, without their a lot of assistances for accommodating and facilitating data collection for this project, it would not have been possible to conduct this study. We also thank Olivia Wanyana Maganyi of the Herbarium of Makerere University for her help in identification of plants and Yuri Oi, Nao Oi, Masayo Nomoto, and Misa Kurachi for their help in data entry work. Finally, we are grateful to anonymous reviewers for their fruitful comments. This study was partly financed by the HOPE and Human Evolution Project of the Primate Research Institute, Kyoto University; JSPS KAKENHI (#19H03308 to IM, #25304019 to CH, #16H02753 to TY, #21255006 and #25257409 to HI, #24570257 to YT) and Strategic Young Researcher Overseas Visits Program for Accelerating Brain Circulation from JSPS (to H. Hirai). All research was conducted in compliance with animal care regulations and applicable Uganda laws.
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Matsuda, I., Ihobe, H., Tashiro, Y. et al. The diet and feeding behavior of the black-and-white colobus (Colobus guereza) in the Kalinzu Forest, Uganda. Primates 61, 473–484 (2020). https://doi.org/10.1007/s10329-020-00794-6
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DOI: https://doi.org/10.1007/s10329-020-00794-6