Social tolerance in bonobos (Pan paniscus): what underlies individual and group variation?

Melissa Vanderheyden
Bonobo Black FridayWat gebeurt er als je een groep mensapen gelijktijdig laat grabbelen in een hoop pinda’s? Een recente studie neemt onder de loep hoe verdraagzaam bonobo’s zijn als er lekker eten in de buurt is. Daaruit blijkt dat de ene bonobo de andere niet is.Stel je voor: na een lange lezing ben je eindelijk op de receptie aanbeland. Iedereen heeft honger, maar tot in de verste hoeken van de zaal valt geen eten te bespeuren. Plots is hij daar. De reddende engel in zwart-wit, een zilveren plateau vol lekkers hoog boven het hoofd geheven.

Social tolerance in bonobos (Pan paniscus): what underlies individual and group variation?

Bonobo Black Friday

Wat gebeurt er als je een groep mensapen gelijktijdig laat grabbelen in een hoop pinda’s? Een recente studie neemt onder de loep hoe verdraagzaam bonobo’s zijn als er lekker eten in de buurt is. Daaruit blijkt dat de ene bonobo de andere niet is.Stel je voor: na een lange lezing ben je eindelijk op de receptie aanbeland. Iedereen heeft honger, maar tot in de verste hoeken van de zaal valt geen eten te bespeuren. Plots is hij daar. De reddende engel in zwart-wit, een zilveren plateau vol lekkers hoog boven het hoofd geheven. De kelner baant zich een weg door de massa en arriveert in jouw groep. Eindelijk oog in oog met die heerlijk geurende gefrituurde scampi’s. Iedereen kijkt. Je hoort je buurman krampachtig zijn overmatige speekselproductie onder controle houden. Wie slaat eerst toe?In dit soort situaties weten de meeste mensen doorgaans hun fatsoen te behouden. Bij apen ligt dat echter anders, zij kennen geen sociale regels. Toch?Een recente studie onderzoekt de verdraagzaamheid van bonobo’s in de nabijheid van voedsel. Op die manier wordt aan het licht gebracht of bepaalde apen elkaar beter tolereren, en wie liefst het verst uit elkaars buurt blijft. Door te kijken naar de koppels waarbij de tolerantie het hoogst is kan je afleiden welke relaties het belangrijkst zijn in de bonobomaatschappij.

Grabbelfestijn

Black Friday, de vrijdag na Thanksgiving waarop verkopers in de VS met mooie koopjes de klanten tot waanzin drijven. Wie kent de beelden niet? Ongeduldige wachtrijen voor winkeldeuren ’s ochtends. Mensen die trekken en duwen voor dat laatste, felbegeerde exemplaar. Voor het meten van de tolerantie bij bonobo’s wordt iets gelijkaardigs georganiseerd: een pindaversie van Black Friday. De geliefde pinda’s – ze heten niet voor niets apennootjes – worden verspreid over een afgebakend stukje grond. De bonobo’s worden losgelaten en … het grabbelen kan beginnen. De verdraagzaamheid per koppel wordt getest door de tijd die ze doorbrengen in elkaars buurt af te klokken.

Grumpy old bonobo

Wat blijkt? Niet alle apenkoppels zijn even (on)verdraagzaam. Bevriende koppels, bonobo’s die elkaar vaak vlooien, vertonen meer verdraagzaamheid. Hetzelfde geldt voor apen die dicht bij elkaar staan in de dominantierangorde.Ook blijkt dat oudere apen minder verdraagzaam zijn. Dat roept meteen associaties op met ongeduldige senioren in de supermarkt. Het grumpy old man syndroom, in Engelse bewoording. Er zou wel eens een grond van waarheid in kunnen zitten. Een andere bevinding was immers dat bonobovrouwtjes toleranter zijn dan mannetjes. Dat laatste komt mogelijk doordat deze soort ‘meiden aan de macht’ in het vaandel draagt, en de bondgenotes maar beter op goede voet staan met elkaar. Het is natuurlijk ook mogelijk dat die mannetjes net knorrig worden van het leven onder de knoet van de vrouwen, al is dat voorlopig een wilde hypothese.

Bibliografie

Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49, 227–267.Amici, F., Call, J., & Aureli, F. (2012). Aversion to violation of expectations of food distribution: the role of social tolerance and relative dominance in seven primate species. Behaviour, 149(3), 345–368.Aragón, P., López, P., & Martín, J. (2007). Familiarity modulates social tolerance between male lizards, Lacerta monticola, with size asymmetry. Ethology, Ecology & Evolution, 19, 69–76. doi:10.1080/08927014.2007.9522582Balasubramaniam, K. N., Dittmar, K., Berman, C. M., Butovskaya, M., Cooper, M. a., Majolo, B., … de Waal, F. B. M. (2012). Hierarchical steepness and phylogenetic models: phylogenetic signals in Macaca. Animal Behaviour, 83(5), 1207–1218. doi:10.1016/j.anbehav.2012.02.012Behringer, V., Deschner, T., Deimel, C., Stevens, J. M. G., & Hohmann, G. (2014). Age-related changes in urinary testosterone levels suggest differences in puberty onset and divergent life history strategies in bonobos and chimpanzees. Hormones and Behavior, 66(3), 525–33. doi:10.1016/j.yhbeh.2014.07.011Boesch, C., Head, J., Tagg, N., Arandjelovic, M., Vigilant, L., & Robbins, M. M. (2007). Fatal chimpanzee attack in Loango National Park, Gabon. International Journal of Primatology, 28, 1025–1034. doi:10.1007/s10764-007-9201-1Boose, K. J., White, F. J., & Meinelt, A. (2013). Sex differences in tool use acquisition in bonobos (Pan paniscus). American Journal of Primatology, 75(9), 917–26. doi:10.1002/ajp.22155Brosnan, S. F. (2006). Nonhuman species’ reactions to inequity and their implications for fairness. Social Justice Research, 19(2), 153–185. doi:10.1007/s11211-006-0002-zBudaev, S. V. (2010). Using principal components and factor analysis in animal behaviour research: Caveats and guidelines. Ethology, 116(5), 472–480. doi:10.1111/j.1439-0310.2010.01758.xBullinger, A. F., Burkart, J. M., Melis, A. P., & Tomasello, M. (2012). Bonobos, Pan paniscus, chimpanzees, Pan troglodytes, and marmosets, Callithrix jacchus, prefer to feed alone. Animal Behaviour, 85(1), 51–60. doi:10.1016/j.anbehav.2012.10.006Burkart, J. M., Hrdy, S. B., & Van Schaik, C. P. (2009). Cooperative breeding and human cognitive evolution. Evolutionary Anthropology, 18(5), 175–186. doi:10.1002/evan.20222Burkart, J. M., & van Schaik, C. (2013). Group service in macaques (Macaca fuscata), capuchins (Cebus apella) and marmosets (Callithrix jacchus): A comparative approach to identifying proactive prosocial motivations. Journal of Comparative Psychology, 127(2), 212–225. doi:10.1037/a0026392Clark, C. W., & Mangel, M. (1986). The evolutionary advantages of group foraging. Theoretical Population Biology, 30(1), 45–75.Clay, Z., & de Waal, F. B. M. (2013). Development of socio-emotional competence in bonobos. Proceedings of the National Academy of Sciences of the United States of America, 110(45), 18121–6. doi:10.1073/pnas.1316449110Coolidge, H. J. (1933). Pan paniscus, pigmy chimpanzee from south of the congo river. American Journal of Physical Anthropology.52Cords, M., & Aureli, F. (2000). Reconciliation and relationship qualities. In F. Aureli & F. B. M. de Waal (Eds.), Natural Conflict Resolution (pp. 177–198). Berkeley, CA: University of California press.Coussi-Korbel, S., & Fragaszy, D. M. (1995). On the relation between social dynamics and social learning. Animal Behaviour, 50(6), 1441–1453. doi:10.1016/0003-3472(95)80001-8Cronin, K. A. (2012). Prosocial behaviour in animals: The influence of social relationships, communication and rewards. Animal Behaviour, 84(5), 1085–1093. doi:10.1016/j.anbehav.2012.08.009Cronin, K. A., De Groot, E., & Stevens, J. M. G. (2015). Bonobos show limited tolerance in a group setting: A comparison with chimpanzees and a test of the Relational Model. Folia Primatologica, 86, 164–177. doi:10.1159/000373886Cronin, K. A., & Sánchez, A. (2012). Social Dynamics and Cooperation: the Case of Nonhuman Primates and Its Implications for Human Behavior. Advances in Complex Systems, 15(supp01), 1250066 1–21. doi:10.1142/S021952591250066XCronin, K. A., van Leeuwen, E. J. C., Vreeman, V., & Haun, D. B. M. (2014). Population-level variability in the social climates of four chimpanzee societies. Evolution and Human Behavior, 35(5), 389–396. doi:10.1016/j.evolhumbehav.2014.05.004D’Eath, R. B., & Keeling, L. J. (2003). Social discrimination and aggression by laying hens in large groups: From peck orders to social tolerance. Applied Animal Behaviour Science, 84, 197–212. doi:10.1016/j.applanim.2003.08.010De Vries, H., Stevens, J. M. G., & Vervaecke, H. (2006). Measuring and testing the steepness of dominance hierarchies. Animal Behaviour, 71(3), 585–592. doi:10.1016/j.anbehav.2005.05.015De Vries, H., Stevens, J., Van Elsacker, L., & Vervaecke, H. (2005). The influence of the steepness of dominance hierarchies on reciprocity and interchange in captive groups of bonobos (Pan paniscus). Behaviour, 142(7), 941–960. doi:10.1163/1568539055010075De Waal, F. (1989). Dominance style and primate social organization. In V. Standen & R. A. Foley (Eds.), Comparative socioecology; The behavioural ecology of humans and other mammals (pp. 243–263). Blackwell scientific publications.De Waal, F. B. M. (1986a). Class structure in a rhesus monkey group: the interplay between dominance and tolerance. Animal Behaviour, (34), 1033–1040.De Waal, F. B. M. (1986b). The integration of dominance and social bonding in primates. The Quarterly Review of Biology, 61(4), 459–478.De Waal, F. B. M. (1988). The communicative repertoire of captive bonobos (Pan paniscus), compared to that of chimpanzees. Behaviour, 107, 183–251.De Waal, F. B. M. (1991). The chimpanzee’s sense of social regularity and its relation to the human sense of justice. American Behavioral Scientist, 34(3), 335–349. doi:10.1177/0002764291034003005De Waal, F. B. M. (1992). Appeasement, celebration, and food sharing in the two Pan species. Topics in Primatology, 37–50.De Waal, F. B. M. (1996). Conflict as negotiation. In W. C. McGrew, L. F. Marchant, & T. Nishida (Eds.), Great ape societies (pp. 159–172). Cambridge: Cambridge University Press.De Waal, F. B. M. (2000). Primates - a natural heritage of conflict resolution. Science, 289, 586–590.53De Waal, F. B. M., & Luttrell, L. M. (1989). Toward a comparative socioecology of the genus Macaca: different dominance styles in rhesus and stumptail moleys. American Journal of Primatology, 19, 83–109.Doran, D. M., Jungers, W. L., Sugiyama, Y., Fleagle, J. G., & Heesy, C. P. (2002). Multivariate and phylogenetic approaches to understanding chimpanzee and bonobo behavioral diversity. In C. Boesch, G. Hohmann, & L. F. Marchant (Eds.), Behavioural diversity in in Chimpanzees and Bonobos.Estevez, I., Keeling, L. J., & Newberry, R. C. (2003). Decreasing aggression with increasing group size in young domestic fowl. Applied Animal Behaviour Science, 84, 213–218. doi:10.1016/j.applanim.2003.08.006Field, A. (2009). Discovering statistics using SPSS (3th editio.). London: SAGE Publications Ltd.Fraser, O. N., Schino, G., & Aureli, F. (2008). Components of relationship quality in chimpanzees. Ethology, 114(9), 834–843. doi:10.1111/j.1439-0310.2008.01527.xFuruichi, T. (1989). Social interactions and the life history of female Pan paniscus in Wamba, Zaire. International Journal of Primatology, 10(3), 173–197.Furuichi, T. (1997). Agonistic interactions and matrifocal dominance rank of wild bonobos (Pan paniscus) at Wamba. International Journal of Primatology, 18(6), 855–876.Furuichi, T. (2011). Female contributions to the peaceful nature of bonobo society. Evolutionary Anthropology, 20(4), 131–42. doi:10.1002/evan.20308Ganem, G., & Bennett, N. C. (2004). Tolerance to unfamiliar conspecifics varies with social organization in female African mole-rats. Physiology and Behavior, 82, 555–562. doi:10.1016/j.physbeh.2004.05.002Gardner, A., Griffin, A. S., & West, S. A. (2009). Theory of cooperation. In Encyclopedia of life sciences. Chichester: John Wiley & Sons, Ltd. doi:10.1002/9780470015902.a0022548Goodall, J. (1986). The Chimpanzees of Gombe. Cambridge: The Belknap Press of Harvard University Press.Hamai, M., Nishida, T., Takasaki, H., & Turner, L. a. (1992). New records of within-group infanticide and cannibalism in wild chimpanzees. Primates, 33(2), 151–162. doi:10.1007/BF02382746Hare, B., & Kwetuenda, S. (2010). Bonobos voluntarily share their own food with others. Current Biology : CB, 20(5), R230–1. doi:10.1016/j.cub.2009.12.038Hare, B., Melis, A. P., Woods, V., Hastings, S., & Wrangham, R. (2007). Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Current Biology, 17(7), 619–23. doi:10.1016/j.cub.2007.02.040Hare, B., Wobber, V., & Wrangham, R. (2012). The self-domestication hypothesis: evolution of bonobo psychology is due to selection against aggression. Animal Behaviour, 83(3), 573–585. doi:10.1016/j.anbehav.2011.12.007Healey, M. C. (1967). Aggression and self-regulation of population size in deermice. Ecological Society of America, 48(3), 377–392. doi:10.2307/1932673Hinde, R. A. (1976). Interactions, relationships and social structure. Man, New Series, 11(1), 1–17.54Hohmann, G., & Fruth, B. (1996). Food sharing and status in unprovisioned bonobos. In P. Wiessner & W. Schiefenhövel (Eds.), Food and the status quest, an interdisciplinary perspective.Hohmann, G., & Fruth, B. (2000). Use and function of genital contacts among female bonobos. Animal Behaviour, 60(1), 107–120. doi:10.1006/anbe.2000.1451Hohmann, G., & Fruth, B. (2002). Dynamics in social organization of bonobos (Pan paniscus). In C. Boesch, L. Marchant, & G. Hohmann (Eds.), Behavioural diversity in chimpanzee.Huffman, M. a., & Hirata, S. (2004). An experimental study of leaf swallowing in captive chimpanzees: Insights into the origin of a self-medicative behavior and the role of social learning. Primates, 45, 113–118. doi:10.1007/s10329-003-0065-5Hurst, J. L., & Barnard, C. J. (1995). Kinship and social tolerance among female and juvenile wild house mice: Kin bias but not kin discrimination. Behavioral Ecology and Sociobiology, 36(5), 333–342. doi:10.1007/s002650050155Hutcheson, G., & Sofroniou, N. (1999). The multivariate social scientist. In B. G. Tabachnick & L. S. Fidell (Eds.), Using multivariate statistics (5th ed.).Idani, G. (1990). Relations between unit-groups of bonobos at Wamba, Zaire: encounters and temporary fusions. African Study Monographs, 11(3), 153–186.Idani, G. (1991). Social relationships between immigrant and resident bonobo (Pan paniscus) females at Wamba. Folia Primatologica, 57, 83–95.Jaeggi, A. V, Stevens, J. M. G., & Van Schaik, C. P. (2010). Tolerant food sharing and reciprocity is precluded by despotism among bonobos but not chimpanzees. American Journal of Physical Anthropology, 143(1), 41–51. doi:10.1002/ajpa.21288Kano, T. (1982). The social group of pygmy chimpanzees (Pan paniscus) of Wamba. Primates, 23(2), 171–188.Kano, T. (1992). The last ape; Pygmy chimpanzee behavior and ecology. Stanford: Stanford University Press.Kummer, H. (1978). On the value of social relationships to nonhuman primates: A heuristic scheme. Social Science Information, 17(4-5), 687–705. doi:10.1177/053901847801700418Kuznetsova, A., Brockhoff, B., & Christensen, H. B. (2015). lmerTest: tests in linear mixed effects models. Retrieved from http://cran.r-project.org/package=lmerTestLacambra, C., Thompson, J., Furuichi, T., Vervaecke, H., & Stevens, J. (2005). Bonobo (Pan paniscus). In J. Caldecott & L. Miles (Eds.), World Atlas of Great Apes and their Conservation.Langergraber, K. E., Boesch, C., Inoue, E., Inoue-Murayama, M., Mitani, J. C., Nishida, T., … Vigilant, L. (2011). Genetic and “cultural” similarity in wild chimpanzees. Proceedings of the Royal Society B, 278, 408–416. doi:10.1098/rspb.2010.1112Leiva, D., & De Vries, H. (2014). Steepness: testing steepness of dominance hierarchies. R package version 0.2-2. Retrieved from http://cran.r-project.org/package=steepnessLührs, M. L., & Kappeler, P. M. (2013). Simultaneous GPS tracking reveals male associations in a solitary carnivore. Behavioral Ecology and Sociobiology, 67(11), 1731–1743. doi:10.1007/s00265-013-1581-y55Madison, D. M., & McShea, W. J. (1987). Seasonal Changes in Reproductive Tolerance , Spacing , and Social Organization in Meadow Voles : A Microtine Model. American Zoologist, 27(3), 899–908.McShea, W. J. (1990). Social tolerance and proximate mechanisms of dispersal among winter groups of meadow voles, Microtus pennsylvanicus. Animal Behaviour, 39, 346–351. doi:10.2307/3503976Melis, A. P., Hare, B., & Tomasello, M. (2006). Engineering cooperation in chimpanzees: tolerance constraints on cooperation. Animal Behaviour, 72(2), 275–286. doi:10.1016/j.anbehav.2005.09.018Miller, R., Schiestl, M., Whiten, A., Schwab, C., & Bugnyar, T. (2014). Tolerance and social facilitation in the foraging behaviour of free-ranging crows (Corvus corone corone). Ethology, 120, 1248–1255. doi:10.1111/eth.12298Mitani, J. C., & Watts, D. P. (2001). Why do chimpanzees hunt and share meat? Animal Behaviour, 61, 915–924. doi:10.1006/anbe.2000.1681Pagel, M., & Dawkins, M. S. (1997). Peck orders and group size in laying hens: “Futures contracts” for non-aggression. Behavioural Processes, 40, 13–25. doi:10.1016/S0376-6357(96)00761-9Palagi, E., Paoli, T., & Tarli, S. B. (2004). Reconciliation and consolation in captive bonobos (Pan paniscus). American Journal of Primatology, 62, 15–30. doi:10.1002/ajp.20000Parish, A. R. (1994). Sex and food control in the “uncommon chimpanzee”: How Bonobo females overcome a phylogenetic legacy of male dominance. Ethology and Sociobiology, 15(3), 157–179. doi:10.1016/0162-3095(94)90038-8Range, F., Ritter, C., & Range, F. (2015). Testing the myth: tolerant dogs and aggressive wolves. Proceedings of the Royal Society B, 282, 0–7.Rilling, J. K., Scholz, J., Preuss, T. M., Glasser, M. F., Errangi, B. K., & Behrens, T. E. (2012). Differences between chimpanzees and bonobos in neural systems supporting social cognition. Social Cognitive and Affective Neuroscience, 7(4), 369–79. doi:10.1093/scan/nsr017Schwarz, E. (1929). Das Vorkommen des Schimpansen auf den linken Kongo-Ufer. Revue de Zoologie et de Botananique Africaines.Scott, E. M., Mann, J., Watson-capps, J. J., Sargeant, B. L., & Connor, R. (2005). Aggression in Bottlenose Dolphins: Evidence for Sexual Coercion, Male-Male Competition, and Female Tolerance through Analysis of Tooth-Rake Marks and Behaviour. Behaviour, 142(1), 21–44.Seed, A. M., Clayton, N. S., & Emery, N. J. (2008). Cooperative problem solving in rooks (Corvus frugilegus). Proceedings. Biological Sciences / The Royal Society, 275, 1421–1429. doi:10.1098/rspb.2008.0111Silk, J. B. (2007). The adaptive value of sociality in mammalian groups. Philosophical Transactions of the Royal Society of London. Series B, 362(1480), 539–559. doi:10.1098/rstb.2006.1994Smith, J. E. (2014). Hamilton’s legacy: kinship, cooperation and social tolerance in mammalian groups. Animal Behaviour, 92, 291–304. doi:10.1016/j.anbehav.2014.02.029Staes, N., Stevens, J. M. G., Helsen, P., Hillyer, M., Korody, M., & Eens, M. (2014). Oxytocin and Vasopressin Receptor Gene Variation as a Proximate Base for Inter- and Intraspecific Behavioral Differences in Bonobos and Chimpanzees. PloS One, 9(11), e113364. doi:10.1371/journal.pone.011336456Stanford, C. B. (1998). The Social Behavior of Chimpanzees and Bonobos. Current Anthropology, 39(4), 399–420.Sterck, E. H. M., Watts, D. P., & van Schaik, C. P. (1997). The evolution of female social relationships in nonhuman primates. Behavioural Ecology and Sociobiology, 41(5), 291–309.Stevens, J. M. G., de Groot, E., & Staes, N. (2015). Relationship quality in captive bonobo groups. Behaviour, 152(3-4), 259–283. doi:10.1163/1568539X-00003259Stevens, J. M. G., Vervaecke, H., De Vries, H., & Van Elsacker, L. (2006). Social structures in Pan paniscus: testing the female bonding hypothesis. Primates; Journal of Primatology, 47(3), 210–7. doi:10.1007/s10329-005-0177-1Stevens, J. M. G., Vervaecke, H., de Vries, H., & van Elsacker, L. (2007). Sex Differences in the Steepness of Dominance Hierarchies in Captive Bonobo Groups. International Journal of Primatology, 28(6), 1417–1430. doi:10.1007/s10764-007-9186-9Stevens, J. M. G., Vervaecke, H., & Elsacker, L. Van. (2008). The bonobo’s adaptive potential : Social relations under captive conditions. In T. Furuichi & J. Thompson (Eds.), The Bonobos: Behavior, Ecology and Conservation (pp. 19–38). New York: Springer.Stumpf, R. (2011). Chimpanzees and bonobos: Inter- and intra-species diversity. In C. Campbell, A. Fuentes, K. MacKinnon, S. Bearder, & R. Stumpf (Eds.), Primates in Perspective, 2nd Edition.Surbeck, M., Mundry, R., & Hohmann, G. (2011a). Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus). Proceedings. Biological Sciences / The Royal Society, 278(1705), 590–598. doi:10.1098/rspb.2010.1572Surbeck, M., Mundry, R., & Hohmann, G. (2011b). Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus). Proceedings of the Royal Society B, 278(1705), 590–598. doi:10.1098/rspb.2010.1572Tan, J., & Hare, B. (2013). Bonobos share with strangers. PLoS ONE, 8(1), e51922. doi:10.1371/journal.pone.0051922Team, R. C. (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Retrieved from http://www.r-project.org/.Van Schaik, C. P., & Burkart, J. M. (2011). Social learning and evolution: the cultural intelligence hypothesis. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 366, 1008–1016. doi:10.1098/rstb.2010.0304Vervaecke, H., De Vries, H., & Van Elsacker, L. (2000a). Dominance and its behavioral measures in a captive group of bonobos (Pan paniscus). International Journal of Primatology, 21(1), 47–68.Vervaecke, H., De Vries, H., & Van Elsacker, L. (2000b). Function and distribution of coalitions in captive bonobos (Pan paniscus). Primates, 41(3), 249–265.Vervaecke, H., Van Elsacker, L., Möhle, U., Heistermann, M., & Verheyden, R. F. (1999). Inter-menstrual intervals in captive bonobos (Pan paniscus). Primates, 40(2), 283–289.Vervaecke, H., Vries, H. De, & Elsacker, L. Van. (2000c). Dominance and its Behavioral Measures in a Captive Group of Bonobos ( Pan paniscus ), 21(1).Watts, P. D., Muller, M., Amsler, S. J., Mbabazi, G., & Mitani, J. C. (2006). Lethal intergroup aggression by chimpanzees in Kibale National Park, Uganda. American Journal of Primatology, 68, 161–180.57White, F. J. (1992). Pygmy chimpanzee social organization, variation with party size and between study site. American Journal of Primatology, 26, 203–214.White, F. J. (1994). Food sharing in wild pygmy chimpanzees, Pan paniscus. In J. J. Roeder, B. Thierry, J. R. Anderson, & N. Herrenschmidt (Eds.), Current Primatology Volume II, Social development, Learning and behaviour.White, F., & Wood, K. (2007). Female Feeding Priority in Bonobos, Pan paniscus, and the Question of Female Dominance. American Journal of Primatology, 69, 837–850. doi:10.1002/ajpWilson, E. O. (1975). Sociobiology, The new synthesis (25th Anniv.). Cambridge (MS, USA), London (UK): The Belknap Press of Harvard University Press.Wilson, M. L., Boesch, C., Fruth, B., Furuichi, T., Gilby, I. C., Hashimoto, C., … Wrangham, R. W. (2014). Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature, 513, 414–417. doi:10.1038/nature13727Wittemyer, G., & Getz, W. M. (2007). Hierarchical dominance structure and social organization in African elephants, Loxodonta africana. Animal Behaviour, 73, 671–681. doi:10.1016/j.anbehav.2006.10.008Wobber, V., Hare, B., Maboto, J., Lipson, S., Wrangham, R., & Ellison, P. T. (2010a). Differential changes in steroid hormones before competition in bonobos and chimpanzees. Proceedings of the National Academy of Sciences of the United States of America, 107(28), 12457–62. doi:10.1073/pnas.1007411107Wobber, V., Wrangham, R., & Hare, B. (2010b). Bonobos exhibit delayed development of social behavior and cognition relative to chimpanzees. Current Biology : CB, 20(3), 226–30. doi:10.1016/j.cub.2009.11.070Yamamoto, S., Humle, T., & Tanaka, M. (2009). Chimpanzees help each other upon request. PLoS ONE, 4(10), 1–7. doi:10.1371/journal.pone.0007416

Universiteit of Hogeschool
Biologie, afstudeerrichting 'Evolutie & gedrag'
Publicatiejaar
2015
Kernwoorden