Optimal diet and functional response models are used to understand the evolution of primate foraging strategies. The predictions of these models can be tested by examining the geographic and seasonal variation in dietary diversity. Dietary diversity is a useful tool that allows dietary comparisons across differing sampling locations and time periods. Bonobos (Pan paniscus) are considered primarily frugivorous and consume fruits, leaves, insects, vertebrates, terrestrial herbaceous vegetation, and flowers. Frugivores, like bonobos, are valuable for examining dietary diversity and testing foraging models because they eat a variety of species and are subject to seasonal shifts in fruit availability. Frugivorous primate species thus allow for tests of how variation in dietary diversity is correlated with variation in ecological factors. We investigated measures of dietary diversity in bonobos at two research camps across field seasons within the same protected area (N’dele and Iyema) in Lomako Forest, Democratic Republic of the Congo. We compared the results of behavioral observation (1984/1985, 1991, 1995, 2014, and 2017) and fecal washing analysis (2007 and 2009) between seasons and study period using three diversity indices (Shannon’s, Simpson’s, and SW evenness). The average yearly dietary diversity indices at N’dele were Shannon’s = 2.04, Simpson’s D = 0.82, and SW evenness = 0.88 while at Iyema, the indices were Shannon’s = 2.02, Simpson’s D = 0.82, and SW evenness = 0.88. Behavioral observation data sets yielded significantly higher dietary diversity indices than fecal washing data sets. We found that food item (fruit, leaf, and flower) consumption was not associated with seasonal food availability for the 2017 behavioral observation data set. Shannon’s index was lower during periods when fewer bonobo dietary items were available to consume and higher when fruit was abundant. Finally, we found that optimal diet models best-explained patterns of seasonal food availability and dietary diversity. Dietary diversity is an essential factor to consider when understanding primate diets and can be a tool in understanding variation in primate diets, particularly among frugivores. Dietary diversity varies across populations of the same species and across time, and it is critical in establishing a complete understanding of how primate diets change over time.

1.
Albrechtsen L, Macdonald DW, Johnson PJ, Castelo R, Fa JE (2007). Faunal loss from bushmeat hunting: empirical evidence and policy implications in Bioko Island. Environmental Science and Policy 10: 654–667.
2.
Altmann J (1974). Observational study of behavior: sampling methods. Behaviour 49: 227–266.
3.
Altmann SA (1991). Diets of yearling female primates (Papio cynocephalus) predict lifetime fitness. Proceedings of the National Academy of Sciences 88: 420–423.
4.
Altmann SA, Wagner SS (1978). A general model of optimal diet. Recent Advances in Primatology 1: 407–414.
5.
Basabose AK (2002). Diet composition of chimpanzees inhabiting the montane forest of Kahuzi, Democratic Republic of Congo. American Journal of Primatology 58: 1–21.
6.
Boubli JP, Dew JL (2005). Tropical Fruits and Frugivores: The Search for Strong Interactors. Berlin, Springer.
7.
Brand CM, White FJ, Wakefield ML, Waller MT, Ruiz-López MJ, Ting N (2016). Initiation of genetic demographic monitoring of bonobos (Pan paniscus) at Iyema, Lomako Forest, DRC. Primate Conservation 30: 103–111.
8.
Bray J, Emery Thompson M, Muller MN, Wrangham RW, Machanda ZP (2018). The development of feeding behavior in wild chimpanzees (Pan troglodytes schweinfurthii). American Journal of Physical Anthropology 165: 34–46.
9.
Chapman CA, Chapman LJ (1999). Implications of small scale variation in ecological conditions for the diet and density of red colobus monkeys. Primates 40: 215.
10.
Chapman CA, Chapman LJ, Cords M, Gathua JM, Gautier-Hion A, Lambert JE, Rode K, Tutin CE, White LJ (2004b). Variation in the diets of Cercopithecus species: differences within forests, among forests, and across species. In The Guenons: Diversity and Adaptation in African Monkeys(Glenn ME, Cords M, eds.), pp 325–350. Boston, Springer.
11.
Chapman CA, Chapman LJ, Naughton-Treves L, Lawes MJ, Mcdowell LR (2004a). Predicting folivorous primate abundance: validation of a nutritional model. American Journal of Primatology62: 55–69.
12.
Chapman CA, Chapman LJ, Wrangham R, Hunt K, Gebo D, Gardner L (1992). Estimators of fruit abundance of tropical trees. Biotropica 24: 527–531.
13.
Chapman CA, Wrangham R, Chapman LJ (1994). Indices of habitat-wide fruit abundance in tropical forest. Biotropica 26: 160–171.
14.
Charnov EL (1976). Optimal foraging, the marginal value theorem. Theoretical Population Biology 9: 129–136.
15.
Clutton-Brock TH (1974). Primate social organisation and ecology. Nature 250(5467): 539–542.
16.
Cobden AK (2014). Party Animals: Food, Sociality and Stress in Wild Bonobos ( Pan paniscus) of Iyema, Lomako Forest, Democratic Republic of Congo. PhD thesis, Emory University.
17.
Constantino PJ, Wright BW (2009). The importance of fallback foods in primate ecology and evolution. American Journal of Physical Anthropology 140: 599–602.
18.
Cui Z, Shao Q, Grueter CC, Wang Z, Lu J, Raubenheimer D (2019). Dietary diversity of an ecological and macronutritional generalist primate in a harsh high-altitude habitat, the Taihangshan macaque (Macaca mulatta tcheliensis). American Journal of Primatology 81: e22965.
19.
Doran DM, McNeilage A, Greer D, Bocian C, Mehlman P, Shah N (2002). Western lowland gorilla diet and resource availability: new evidence, cross-site comparisons, and reflections on indirect sampling methods. American Journal of Primatology 58: 91–116.
20.
Edwards MS, Ullrey DE (1999). Effect of dietary fiber concentration on apparent digestibility and digesta passage in non-human primates. II. Hindgut- and foregut-fermenting folivores. Zoo Biology: Published in Affiliation with the American Zoo and Aquarium Association 18: 537–549.
21.
Erhart EM, Tecot SR, Grassi C (2018). Interannual variation in diet, dietary diversity, and dietary overlap in three sympatric strepsirrhine species in southeastern Madagascar. International Journal of Primatology 39: 289–311.
22.
Fruth B, Hohmann G (2018). Food sharing across borders: first observation of intercommunity meat sharing by bonobos at LuiKotale, DRC. Human Nature 29: 91–103.
23.
Furuichi T (1989). Social interactions and the life history of female Pan paniscus in Wamba, Zaire. International Journal of Primatology 10: 173–197.
24.
Furuichi T, Hashimoto C, Tashiro Y (2001). Fruit availability and habitat use by chimpanzees in the Kalinzu Forest, Uganda: examination of fallback foods. International Journal of Primatology 22: 929–945.
25.
Grassi C (2006). Variability in habitat, diet, and social structure of Hapalemur griseus in Ranomafana National Park, Madagascar. American Journal of Physical Anthropology 131: 50–63.
26.
Gruber T, Clay Z (2016). A comparison between bonobos and chimpanzees: a review and update. Evolutionary Anthropology: Issues, News, and Reviews 25: 239–252.
27.
Hanya G, Chapman CA (2013). Linking feeding ecology and population abundance: a review of food resource limitation on primates. Ecological Research 28: 183–190.
28.
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.
29.
Harrison MJ (1984). Optimal foraging strategies in the diet of the green monkey, Cercopithecus sabaeus, at Mt. Assirik, Senegal. International Journal of Primatology 5: 435.
30.
Heiduck S (1997). Food choice in masked titi monkeys (Callicebus personatus melanochir): selectivity or opportunism? International Journal of Primatology 18: 487–502.
31.
Hohmann G, Fruth B (2003). Lui Kotal – a new site for field research on bonobos in the Salonga National Park. Pan Africa News 10: 25–27.
32.
Holling CS (1959). Some characteristics of simple types of predation and parasitism. Canadian Entomologist 91: 385–398.
33.
Holling CS (1965). The functional response of predators to prey density and its role in mimicry and population regulation. The Memoirs of the Entomological Society of Canada 97(suppl 45): 5–60.
34.
Kano T (1989). The sexual behavior of pygmy chimpanzees. In Understanding Chimpanzees(Heltne PG, Marquardt LA, eds.), pp 176–183. Cambridge, Harvard University Press.
35.
Kano T, Mulavwa M (1984). Feeding ecology of the pygmy chimpanzees (Pan paniscus) of Wamba. In The Pygmy Chimpanzee(Susman RL, ed.), pp 233–274. New York, Springer US.
36.
Kappeler PM, Cuozzo FP, Fichtel C, Ganzhorn JU, Gursky-Doyen S, Irwin MT, Ichino S, Lawler R, Nekaris KA-I, Ramanamanjato J-B, Radespiel U, Sauther ML, Wright PC, Zimmermann E (2017). Long-term field studies of lemurs, lorises, and tarsiers. Journal of Mammalogy 98: 661–669.
37.
Kim S, Lappan S, Choe JC (2012). Responses of Javan gibbon (Hylobates moloch) groups in submontane forest to monthly variation in food availability: evidence for variation on a fine spatial scale. American Journal of Primatology74: 1154–1167.
38.
Koenig A, Beise J, Chalise MK, Ganzhorn JU (1998). When females should contest for food – testing hypotheses about resource density, distribution, size, and quality with hanuman langurs (Presbytis entellus). Behavioral Ecology and Sociobiology 42: 225–237.
39.
Krebs J (1984). Optimization in behavioural ecology. In Behavioural Ecology: An Evolutionary Approach (Krebs JR, Davies NB, eds.), pp 91–121. Oxford, Blackwell.
40.
Lambert J (2007). Seasonality, fallback strategies, and natural selection: a chimpanzee and cercopithecoid model for interpreting the evolution of hominin diet. In Evolution of the Human Diet: The Known, the Unknown, and the Unknowable (Ungar PS, ed.), pp 324–343. Oxford, Oxford University Press.
41.
Lambert JE (1998). Primate digestion: interactions among anatomy, physiology, and feeding ecology. Evolutionary Anthropology: Issues, News, and Reviews 7: 8–20.
42.
Lambert JE, Rothman JM (2015). Fallback foods, optimal diets, and nutritional targets: primate responses to varying food availability and quality. Annual Review of Anthropology 44: 493–512.
43.
Lehman CL, Tilman D (2000). Biodiversity, stability, and productivity in competitive communities. The American Naturalist 156: 534–552.
44.
Leighton M (1993). Modeling dietary selectivity by Bornean orangutans: evidence for integration of multiple criteria in fruit selection. International Journal of Primatology 14: 257–313.
45.
Loudon JE, Kimel HM, Waller MT, Wakefield ML, Hickmott A, White FJ, Sponheimer M (2017). Pairing feeding observations with stable isotope data from bonobo (Pan paniscus) fecal samples from the Lomako Nature Reserve, Democratic Republic of the Congo. American Journal of Physical Anthropology 162: 267.
46.
Loudon JE, Wakefield ML, Kimel HM, Waller MT, Hickmott AJ, White FJ, Sponheimer M (2019). Stable isotope data from bonobo (Pan paniscus) faecal samples from the Lomako Forest Reserve, Democratic Republic of the Congo. African Journal of Ecology 57: 437–442.
47.
Lozano J, Moleón M, Virgós E (2006). Biogeographical patterns in the diet of the wildcat, Felis silvestris Schreber, in Eurasia: factors affecting the trophic diversity. Journal of Biogeography 33: 1076–1085.
48.
MacArthur RH, Pianka ER (1966). On optimal use of a patchy environment. The American Naturalist 100: 603–609.
49.
Magurran AE (1988). Ecological Diversity and Its Measurement. Princeton, Princeton University Press.
50.
Marshall AJ, Boyko CM, Feilen KL, Boyko RH, Leighton M (2009). Defining fallback foods and assessing their importance in primate ecology and evolution. American Journal of Physical Anthropology 140: 603–614.
51.
Marshall AJ, Wrangham RW (2007). Evolutionary consequences of fallback foods. International Journal of Primatology 28: 1219–1235.
52.
McConkey KR, Ario A, Aldy F, Chivers DJ (2003). Influence of forest seasonality on gibbon food choice in the rain forests of Barito Ulu, Central Kalimantan. International Journal of Primatology 24: 19–32.
53.
McGrew WC, Baldwin PJ, Tutin CEG (1988). Diet of wild chimpanzees (Pan troglodytes verus) at Mt. Assirik, Senegal. I. Composition. American Journal of Primatology 16: 213–226.
54.
McGrew WC, Marchant LF, Phillips CA (2009). Standardised protocol for primate faecal analysis. Primates 50: 363–366.
55.
Mitani JC, Watts DP, Lwanga JS (2002). Ecological and social correlates of chimpanzee party size and composition. In Behavioural Diversity in Chimpanzees and Bonobos(Boesch C, Hohmann G, Marchant LF, eds.), pp 102–111. Cambridge, Cambridge University Press.
56.
Mittelbach GG, McGill BJ (2019). Community Ecology. Oxford, Oxford University Press.
57.
Newton-Fisher N (1999). The diet of chimpanzees in the Budongo Forest Reserve, Uganda. African Journal of Ecology 37: 344–354.
58.
Oelze VM, Fuller BT, Richards MP, Fruth B, Surbeck M, Hublin J-J, Hohmann G (2011). Exploring the contribution and significance of animal protein in the diet of bonobos by stable isotope ratio analysis of hair. Proceedings of the National Academy of Sciences 108: 9792–9797.
59.
Oelze VM, Fahy G, Hohmann G, Robbins MM, Leinert V, Lee K, Eshuis H, Seiler N, Wessling EG, Head J, Boesch C, Kühl HS (2016). Comparative isotope ecology of African great apes. Journal of Human Evolution 101: 1–16.
60.
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013). Package “vegan.” Community Ecology Package, Version 2(9): 1–295.
61.
Phillips CA, McGrew WC (2014). Macroscopic inspection of ape feces: what’s in a quantification method? American Journal of Primatology 76: 539–550.
62.
Pielou EC (1974). Population and Community Ecology: Principles and Methods. Boca Raton, CRC Press.
63.
Potts KB, Watts DP, Wrangham RW (2011). Comparative feeding ecology of two communities of chimpanzees (Pan troglodytes) in Kibale National Park, Uganda. International Journal of Primatology 32: 669–690.
64.
Pyke GH, Pulliam HR, Charnov EL (1977). Optimal foraging: a selective review of theory and tests. The Quarterly Review of Biology 52: 137–154.
65.
Raubenheimer D, Simpson SJ, Mayntz D (2009). Nutrition, ecology and nutritional ecology: toward an integrated framework. Functional Ecology23: 4–16.
66.
R Core Team (2017). R: a language and environment for statistical computing.
67.
Richard AF (1985). Primates in Nature. Vol 4. New York, Freeman.
68.
Rothman JM, Chapman CA, Van Soest PJ (2012). Methods in primate nutritional ecology: a user’s guide. International Journal of Primatology 33: 542–566.
69.
Sayers K, Norconk MA, Conklin-Brittain NL (2009). Optimal foraging on the roof of the world: Himalayan langurs and the classical prey model. American Journal of Physical Anthropology 141: 337–357.
70.
Serckx A, Kühl HS, Beudels-Jamar RC, 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: 948–962.
71.
Shannon CE, Weaver W (1949). A Mathematical Model of Communication. Vol 11. Urbana, University of Illinois Press.
72.
Simpson EH (1949). Measurement of diversity. Nature163: 688.
73.
Strier KB (2015). Primate Behavioral Ecology. Abingdon, Routledge.
74.
Surbeck M, Hohmann G (2008). Primate hunting by bonobos at LuiKotale, Salonga National Park. Current Biology 18: R906–R907.
75.
Tutin CEG, Fernandez M (1993). Composition of the diet of chimpanzees and comparisons with that of sympatric lowland gorillas in the Lopé Reserve, Gabon. American Journal of Primatology 30: 195–211.
76.
Tutin CEG, Fernandez M, Rogers ME, Williamson EA, McGrew WC (1991). Foraging profiles of sympatric lowland gorillas and chimpanzees in the Lopé Reserve, Gabon. Philosophical Transactions of the Royal Society of London Series B 334: 179–186.
77.
Wakefield ML, Hickmott AJ, Brand CM, Takaoka IY, Meador LM, Waller MT, White FJ (2019). New observations of meat eating and sharing in wild bonobos (Pan paniscus) at Iyema, Lomako Forest Reserve, Democratic Republic of the Congo. Folia Primatologica 90: 179–189.
78.
Watts D (1984). Composition and variability of mountain gorilla diets in the Central Virungas. American Journal of Primatology 7: 323–356.
79.
White F (1986). Census and preliminary observations on the ecology of the black-faced black spider monkey (Ateles paniscus chamek) in Manu National Park, Peru. American Journal of Primatology 11: 125–132.
80.
White FJ (1992). Pygmy chimpanzee social organization: variation with party size and between study sites. American Journal of Primatology 26: 203–214.
81.
White FJ (1996). Comparative socio-ecology of Pan paniscus. In Great Ape Societies (McGrew WC, Marchant LF, Nishida T, eds.), pp 29–41. Cambridge, Cambridge University Press.
82.
White FJ (1998). Seasonality and socioecology: the importance of variation in fruit abundance to bonobo sociality. International Journal of Primatology 19: 1013–1027.
83.
White FJ, Wood KD (2007). Female feeding priority in bonobos, Pan paniscus, and the question of female dominance. American Journal of Primatology 69: 837–850.
84.
White FJ, Wrangham RW (1988). Feeding competition and patch size in the chimpanzee species Pan paniscus and Pan troglodytes. Behaviour 105: 148–164.
85.
Wickham H (2009). Ggplot: using the grammar of graphics with R.
86.
Zhou Y-B, Newman C, Xu W-T, Buesching CD, Zalewski A, Kaneko Y, Macdonald DW, Xie Z-Q (2011). Biogeographical variation in the diet of Holarctic martens (genus Martes, Mammalia: Carnivora: Mustelidae): adaptive foraging in generalists. Journal of Biogeography 38: 137–147.
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.