Tolerant food sharing and reciprocity is precluded by despotism among bonobos but not chimpanzees
Open accessAbstract
Tolerant food sharing among human foragers can largely be explained by reciprocity. In contrast, food sharing among chimpanzees and bonobos may not always reflect reciprocity, which could be explained by different dominance styles: in egalitarian societies reciprocity is expressed freely, while in more despotic groups dominants may hinder reciprocity. We tested the degree of reciprocity and the influence of dominance on food sharing among chimpanzees and bonobos in two captive groups. First, we found that chimpanzees shared more frequently, more tolerantly, and more actively than bonobos. Second, among chimpanzees, food received was the best predictor of food shared, indicating reciprocal exchange, whereas among bonobos transfers were mostly unidirectional. Third, chimpanzees had a shallower and less linear dominance hierarchy, indicating that they were less despotic than bonobos. This suggests that the tolerant and reciprocal sharing found in chimpanzees, but not bonobos, was made possible by the absence of despotism. To investigate this further, we tested the relationship between despotism and reciprocity in grooming using data from an additional five groups and five different study periods on the main groups. The results showed that i) all chimpanzee groups were less despotic and groomed more reciprocally than bonobo groups, and ii) there was a general negative correlation between despotism and grooming reciprocity across species. This indicates that an egalitarian hierarchy may be more common in chimpanzees, at least in captivity, thus fostering reciprocal exchange. We conclude that a shallow dominance hierarchy was a necessary precondition for the evolution of human‐like reciprocal food sharing. Am J Phys Anthropol 143:41–51, 2010. © 2010 Wiley‐Liss, Inc.
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Food sharing between unrelated individuals outside the mating context is rare but has been reported for humans, vampire bats, chimpanzees and bonobos.
“Food sharing between unrelated individuals outside the mating context is rare but has been reported for humans, vampire bats, chimpanzees and bonobos [13,46,48,49,52].”
From Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees (2014) · cites this paper as [48]
Cites
R: A Language and Environment for Statistical Computing
R Core Team (2000) · doi:10.32614/r.manuals · Cited by 355,706 · see citing works
Observational study of behavior: sampling methods
Altmann, J. (1974) · Behaviour · doi:10.1163/156853974x00534 · Cited by 13,891 · see citing works
Mixed-Effects Models in Sand S-PLUS
Pinheiro, J. C., & Bates, D. M. (2000) · Statistics and Computing · doi:10.1007/978-1-4419-0318-1 · Cited by 11,187 · see citing works
The Evolution of Reciprocal Altruism
Trivers, R. L. (1971) · The Quarterly Review of Biology · doi:10.1086/406755 · Cited by 11,010 · see citing works
nlme : Linear and nonlinear mixed effects models
DebRoy, S. (2006) · Medical Entomology and Zoology · Cited by 10,009 · see citing works
Mixed-Effects Models in S and S-PLUS
(2001) · Technometrics · doi:10.1198/tech.2001.s574 · Cited by 9,278 · see citing works
Generalized linear mixed models: a practical guide for ecology and evolution
Bolker, B. M., Brooks, M. E., Clark, C. J., Geange, S. W., Poulsen, J. R., Stevens, M. H. H., & White, J.-S. S. (2009) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2008.10.008 · Cited by 8,910 · see citing works
Regression and time series model selection in small samples
HURVICH, C. M., & TSAI, C.-L. (1989) · Biometrika · doi:10.1093/biomet/76.2.297 · Cited by 6,586 · see citing works
Model selection in ecology and evolution
Johnson, J. B., & Omland, K. S. (2004) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2003.10.013 · Cited by 3,838 · see citing works
The Chimpanzees of Gombe: Patterns of Behavior
Goodall, J. R. (1986) · DigitalGeorgetown (Georgetown University Library) · Cited by 3,384 · see citing works
Alexander, R. D. (2017) · Routledge eBooks · doi:10.4324/9780203700976 · Cited by 1,695 · see citing works
The Behaviour of Free-living Chimpanzees in the Gombe Stream Reserve
Van Lawick-Goodall, J. (1968) · Animal Behaviour Monographs · doi:10.1016/s0066-1856(68)80003-2 · Cited by 1,571 · see citing works
Hunting behavior of wild chimpanzees in the Taï National Park
Boesch, C., & Boesch, H. (1989) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330780410 · Cited by 976 · see citing works
Noë, R., & Hammerstein, P. (1994) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00167053 · Cited by 922 · see citing works
Woodburn, J. (1982) · Man · doi:10.2307/2801707 · Cited by 918 · see citing works
Boehm, C. (2009) · Harvard University Press eBooks · doi:10.2307/j.ctvjf9xr4 · Cited by 877 · see citing works
Extending the Linear Model with R
Faraway, J. J. (2016) · Chapman & Hall/CRC eBooks · doi:10.1201/9781315382722 · Cited by 832 · see citing works
The ecology of social relationships amongst female primates
van Schaik, A. (1989) · Medical Entomology and Zoology · Cited by 722 · see citing works
Cooperative hunting in wild chimpanzees
Boesch, C. (1994) · Animal Behaviour · doi:10.1006/anbe.1994.1285 · Cited by 650 · see citing works
An improved test of linearity in dominance hierarchies containing unknown or tied relationships
VRIES, H. D. (1995) · Animal Behaviour · doi:10.1016/0003-3472(95)80053-0 · Cited by 590 · see citing works
Measuring and testing the steepness of dominance hierarchies
VRIES, H. D., Stevens, J. M. G., & Vervaecke, H. (2006) · Animal Behaviour · doi:10.1016/j.anbehav.2005.05.015 · Cited by 583 · see citing works
Self-citationTo give and to give not: the behavioral ecology of human food transfers
Gurven, M. (2004) · Behavioral and Brain Sciences · doi:10.1017/s0140525x04000123 · Cited by 582 · see citing works
Tolerance Allows Bonobos to Outperform Chimpanzees on a Cooperative Task
Hare, B. A., Melis, A. P., Woods, V. E., Hastings, S., & Wrangham, R. W. (2007) · Current Biology · doi:10.1016/j.cub.2007.02.040 · Cited by 526 · see citing works
The Chimpanzee's service economy: Food for grooming
de Waal, F. Β. Μ. (1997) · Evolution and Human Behavior · doi:10.1016/s1090-5138(97)00085-8 · Cited by 479 · see citing works
Food sharing and reciprocal obligations among chimpanzees
de Waal, F. Β. Μ. (1989) · Journal of Human Evolution · doi:10.1016/0047-2484(89)90074-2 · Cited by 465 · see citing works
Why do chimpanzees hunt and share meat?
Mitani, J. C., & Watts, D. P. (2001) · Animal Behaviour · doi:10.1006/anbe.2000.1681 · Cited by 451 · see citing works
Tutin, C. E. G. (1979) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00293242 · Cited by 446 · see citing works
Stepwise Model Fitting and Statistical Inference: Turning Noise into Signal Pollution
Mundry, R., & Nunn, C. L. (2008) · The American Naturalist · doi:10.1086/593303 · Cited by 440 · see citing works
Extending the Linear Model with R
Faraway, J. J. (2005) · Chapman & Hall/CRC eBooks · doi:10.1201/b15416 · Cited by 434 · see citing works
The Predatory Behavior of Wild Chimpanzees
Teleki, G. (1973) · Medical Entomology and Zoology · Cited by 392 · see citing works
A proximate perspective on reciprocal altruism
Brosnan, S. F., & de Waal, F. Β. Μ. (2002) · Human Nature · doi:10.1007/s12110-002-1017-2 · Cited by 375 · see citing works
Behavioural Diversity in Chimpanzees and Bonobos
Marchant, L. (2002) · Cambridge University Press eBooks · doi:10.1017/cbo9780511606397 · Cited by 369 · see citing works
Matman: a Program for the Analysis of Sociometric Matrices and Behavioural Transition Matrices
VRIES, H. D., Netto, W. J., & Hanegraaf, P. L. H. (1993) · Behaviour · doi:10.1163/156853993x00218 · Cited by 342 · see citing works
Attitudinal reciprocity in food sharing among brown capuchin monkeys
de Waal, F. B. M. (2000) · Animal Behaviour · doi:10.1006/anbe.2000.1471 · Cited by 302 · see citing works
de Waal, F. Β. Μ., & Lanting, F. (1997) · Medical Entomology and Zoology · Cited by 294 · see citing works
The Chimpanzees of the Budongo Forest
Reynolds, V. (2005) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198515463.001.0001 · Cited by 294 · see citing works
Meat sharing among the Gombe chimpanzees: harassment and reciprocal exchange
Gilby, I. C. (2006) · Animal Behaviour · doi:10.1016/j.anbehav.2005.09.009 · Cited by 287 · see citing works
The Biology of Moral SystemsRichard D. Alexander New York: Aldine De Gruyter, 1987
Barner-Barry, C. (1988) · Politics and the Life Sciences · doi:10.1017/s0730938400003816 · Cited by 265 · see citing works
The chimpanzees of the Budongo Forest : ecology, behaviour, and conservation
Reynolds, V. (2005) · Cited by 260 · see citing works
Wild Chimpanzees Exchange Meat for Sex on a Long-Term Basis
Gomes, C. M., & Boesch, C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005116 · Cited by 249 · see citing works
Behavioural ecology of chimpanzees in Gombe National Park, Tanzania
Wrangham, R. W. (1975) · Apollo (University of Cambridge) · doi:10.17863/cam.16415 · Cited by 248 · see citing works
A selfish origin for human food sharing: Tolerated theft
Jones, N. G. B. (1984) · Ethology and Sociobiology · doi:10.1016/0162-3095(84)90030-x · Cited by 236 · see citing works
Predatory behavior among wild chimpanzees of the mahale mountains
Nishida, T., Uehara, S., & Nyundo, R. (1979) · Primates · doi:10.1007/bf02373826 · Cited by 230 · see citing works
Bonobos Exhibit Delayed Development of Social Behavior and Cognition Relative to Chimpanzees
Wobber, V., Wrangham, R. W., & Hare, B. A. (2010) · Current Biology · doi:10.1016/j.cub.2009.11.070 · Cited by 213 · see citing works
The Social Behavior of Chimpanzees and Bonobos: Empirical Evidence and Shifting Assumptions
Stanford, C. B. (1998) · Current Anthropology · doi:10.1086/204757 · Cited by 203 · see citing works
Social behavior of wild pygmy chimpanzees (Pan paniscus) of Wamba: A preliminary report
Kano, T. (1980) · Journal of Human Evolution · doi:10.1016/0047-2484(80)90053-6 · Cited by 189 · see citing works
Primate hunting by bonobos at LuiKotale, Salonga National Park
Surbeck, M., & Hohmann, G. (2008) · Current Biology · doi:10.1016/j.cub.2008.08.040 · Cited by 178 · see citing works
Food Transfers Among Hiwi Foragers of Venezuela: Tests of Reciprocity
Gurven, M., Hill, K. R., Kaplan, H. S., Hurtado, A., & Lyles, R. (2000) · Human Ecology · doi:10.1023/a:1007067919982 · Cited by 176 · see citing works
A conceptual framework for nonkin food sharing: timing and currency of benefits
Stevens, J. R., & Gilby, I. C. (2004) · Animal Behaviour · doi:10.1016/j.anbehav.2003.04.012 · Cited by 176 · see citing works
Self-citationHierarchy in the Forest: The Evolution of Egalitarian Behavior
BOEHM, C. (1999) · doi:10.4159/9780674028449 · Cited by 167 · see citing works
Dynamics in social organization of bonobos ( Pan paniscus )
Hohmann, G., & Fruth, B. (2002) · Cambridge University Press eBooks · doi:10.1017/cbo9780511606397.014 · Cited by 166 · see citing works
Reciprocal altruism: 30 years later
Trivers, R. L. (2006) · Springer eBooks · doi:10.1007/3-540-28277-7_4 · Cited by 161 · see citing works
Stanford, C. B. (1999) · Princeton University Press eBooks · doi:10.1515/9780691222080 · Cited by 160 · see citing works
Social behavior and relationship among wild chimpanzees of the Mahali mountains
Nishida, T. (1970) · Primates · doi:10.1007/bf01730675 · Cited by 158 · see citing works
Cooperation and competition in chimpanzees: Current understanding and future challenges
Mitani, J. C. (2009) · Evolutionary Anthropology: Issues, News, and Reviews · doi:10.1002/evan.20229 · Cited by 156 · see citing works
Interaction over Food among Pygmy Chimpanzees
Kuroda, S. (1984) · Springer eBooks · doi:10.1007/978-1-4757-0082-4_12 · Cited by 151 · see citing works
Types of Dominance in a Chimpanzee Colony
Noë, R., de Waal, F. Β. Μ., & van Hooff, J. A. R. A. M. (1980) · Folia Primatologica · doi:10.1159/000155949 · Cited by 148 · see citing works
The Hunting Apes: Meat Eating and the Origins of Human Behavior
Stanford, C. B. (1999) · Project Muse (Johns Hopkins University) · Cited by 147 · see citing works
Hohmann, G., & Fruth, B. (2007) · Folia Primatologica · doi:10.1159/000110679 · Cited by 142 · see citing works
Chimpanzees Share Forbidden Fruit
Hockings, K. J., Humle, T., Anderson, J. R., Biro, D., Sousa, C., Ohashi, G., & Matsuzawa, T. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000886 · Cited by 138 · see citing works
Carnivority and Cannibalism Observed among Forest-living Chimpanzees
Suzuki, A. K. (1971) · The Journal of Anthropological Society of Nippon · doi:10.1537/ase1911.79.30 · Cited by 134 · see citing works
Dominance and its Behavioral Measures in a Captive Group of Bonobos (Pan paniscus)
Vervaecke, H., de Vries, H. D., & Elsacker, L. V. (2000) · International Journal of Primatology · doi:10.1023/a:1005471512788 · Cited by 131 · see citing works
Reciprocal exchange in chimpanzees and other primates
Mitani, J. C. (2006) · Springer eBooks · doi:10.1007/3-540-28277-7_6 · Cited by 127 · see citing works
Cues of ownership in long-tailed macaques, Macaca fascicularis
Kummer, H., & Cords, M. (1991) · Animal Behaviour · doi:10.1016/s0003-3472(05)80238-6 · Cited by 125 · see citing works
Sex Differences in the Steepness of Dominance Hierarchies in Captive Bonobo Groups
Stevens, J. M. G., Vervaecke, H., VRIES, H. D., et al. (2007) · International Journal of Primatology · doi:10.1007/s10764-007-9186-9 · Cited by 120 · see citing works
Self-citationThe evolution of reciprocal sharing
Moore, J. (1984) · Ethology and Sociobiology · doi:10.1016/0162-3095(84)90031-1 · Cited by 114 · see citing works
The Rowwise Correlation between Two Proximity Matrices and the Partial Rowwise Correlation
VRIES, H. D. (1993) · Psychometrika · doi:10.1007/bf02294470 · Cited by 113 · see citing works
No evidence of short-term exchange of meat for sex among chimpanzees
Gilby, I. C., Thompson, M. E., Ruane, J. D., & Wrangham, R. W. (2010) · Journal of Human Evolution · doi:10.1016/j.jhevol.2010.02.006 · Cited by 105 · see citing works
Components of Relationship Quality in Chimpanzees
Fraser, O. N., Schino, G., & Aureli, F. (2008) · Ethology · doi:10.1111/j.1439-0310.2008.01527.x · Cited by 104 · see citing works
Hunting and meat sharing by chimpanzees at Ngogo, Kibale National Park, Uganda
Watts, D. P., & Mitani, J. C. (2002) · Cambridge University Press eBooks · doi:10.1017/cbo9780511606397.024 · Cited by 99 · see citing works
Chimpanzee predation in the Mahale mountains from August 1979 to May 1982
Takahata, Y., Hasegawa, T., & Nishida, T. (1984) · International Journal of Primatology · doi:10.1007/bf02735758 · Cited by 95 · see citing works
Food sharing: a model of manipulation by harassment
Stevens, J. R. (2002) · Behavioral Ecology · doi:10.1093/beheco/13.3.393 · Cited by 90 · see citing works
Self-citationHow bonobos handle hunts and harvests: why share food?
Fruth, B., & Hohmann, G. (2002) · Cambridge University Press eBooks · doi:10.1017/cbo9780511606397.023 · Cited by 84 · see citing works
Schino, G., & Aureli, F. (2008) · Biological Journal of the Linnean Society · doi:10.1111/j.1095-8312.2008.01067.x · Cited by 68 · see citing works
The Bonobo’s Adaptive Potential: Social Relations under Captive Conditions
Stevens, J. M. G., Vervaecke, H., & Elsacker, L. V. (2007) · Springer eBooks · doi:10.1007/978-0-387-74787-3_2 · Cited by 63 · see citing works
Self-citationField Observations on Meat Sharing among Bonobos (Pan paniscus)
Hohmann, G., & Fruth, B. (1993) · Folia Primatologica · doi:10.1159/000156695 · Cited by 60 · see citing works
Intersexual food transfer among orangutans: do females test males for coercive tendency?
van Noordwijk, M. A., & van Schaik, C. P. (2009) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-009-0728-3 · Cited by 51 · see citing works
VRIES, H. D., Stevens, J. M. G., Elsacker, L. V., & Vervaecke, H. (2005) · Behaviour · doi:10.1163/1568539055010075 · Cited by 49 · see citing works
Self-citationFurther studies on predation by chimpanzees of the Mahale Mountains
Kawanaka, K. (1982) · Primates · doi:10.1007/bf02381320 · Cited by 42 · see citing works
Rate of metabolism in the smallest simian primate, the pygmy marmoset (Cebuella pygmaea)
Genoud, M., Martin, R. D., & Gläser, D. (1997) · American Journal of Primatology · doi:10.1002/(sici)1098-2345(1997)41:3 · Cited by 41 · see citing works
Play behavioural tactics under space reduction: social challenges in bonobos, Pan paniscus
Tacconi, G., & Palagi, E. (2009) · Animal Behaviour · doi:10.1016/j.anbehav.2009.06.004 · Cited by 36 · see citing works
Gore, M. A. (1993) · Animal Behaviour · doi:10.1006/anbe.1993.1091 · Cited by 35 · see citing works
Effect of spatial crowding on aggressive behavior in a bonobo colony
Sannen, A., Elsacker, L. V., & Eens, M. (2004) · Zoo Biology · doi:10.1002/zoo.20024 · Cited by 30 · see citing works
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- Authors
- Jaeggi, A. V., Stevens, J. M. G., & Van Schaik, C. P.
- Affiliations
- University of Zurich (CH)
- Royal Zoological Society of Antwerp (BE)
- Corresponding author
- Jaeggi, Adrian V.
- Venue
- American Journal of Physical Anthropology
- Publisher
- Wiley
- Published
- 2010-08-16
- Volume
- 143
- Issue
- 1
- Pages
- 41-51
- ISSN
- 0002-9483 (ISSN-L)
- 1096-8644
- OpenAlex
- W2082643407
- Cited by
- 205
- References
- 83
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 5 · 2023: 44 · 2022: 9 · 2021: 19 · 2020: 4 · 2019: 10 · 2018: 7 · 2017: 17 · 2016: 20 · 2015: 20 · 2014: 8 · 2013: 9 · 2012: 11
- FWCI
- 13.44
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Locations
- American Journal of Physical Anthropology (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Cogito Foundation
- Vlaamse regering
- Topics
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Evolutionary Psychology and Human Behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- food sharing, reciprocity, despotism, dominance hierarchy, bonobos, chimpanzees, grooming, egalitarianism, primate social behavior, evolution of cooperation
- MeSH terms
- Animals, Pan troglodytes, Cooperative Behavior, Feeding Behavior, Female, Male, Monte Carlo Method, Social Behavior, Social Dominance, Pan paniscus
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