Published online (July 3rd, 2021)
Non-lethal handling of a captured duiker by a bonobo (Pan paniscus) at Wamba: Implications for prey image in bonobos
Primates Research Institute, Kyoto University, Japan
Wild bonobos hunt and consume the meat of small to medium-sized terrestrial mammals such as anomalures (e.g., Anomalurus derbianus, Anomalurus beecrofti), forest antelopes (e.g., bay duikers [Cephalophus castaneus], blue duikers [Philantomba monticola]), and other primates (e.g., galagos [Galago demidovii], red-tailed monkeys [Cercipithecus ascanius], and wolf guenons [Cercopithecus wolfi]) (Fruth & Hohmann 2002; Hohmann & Fruth 2008; Surbeck & Hohmann 2008; Sakamaki et al. 2016; Samuni et al. 2020). However, there are some differences in hunting and meat-eating behaviors among allopatric bonobo populations (Hohmann & Fruth 2003). As mentioned above, prey consumed by bonobos at some field sites include monkeys and duikers (Fruth & Hohmann 2002; Hohmann & Fruth 2008; Sakamaki et al. 2016; Samuni et al. 2020). On the other hand, at Wamba, in the Luo Scientific Reserve, Democratic Republic of the Congo, hunting and meat-eating behaviors by bonobos have been infrequent compared to those at other study sites (Hohmann & Fruth 2003; Sakamaki et al. 2016), and at this site bonobos have never been observed to hunt for mammals other than anomalures (Anomalurus spp.) (Ihobe 1992; Kano 1992; Hirata et al. 2010). Moreover, a recent study showed that there was a group preference for duiker or anomalure hunting even in a sympatric bonobo population (Samuni et al. 2020).
Some previous studies have described hunting and consuming other mammals that are recognized as food as prey image in the Pan genus (Boesch & Boesch 1989; Ihobe 1992). Boesch & Boesch (1989) suggested that chimpanzees at Taï Forest, Côte d‘Ivoire, have a specialized prey image in which monkeys, mostly colobus, are recognized as food, citing an observation that a juvenile male chimpanzee accidentally caught a blue duiker and handled with it as a toy, not as food. Therefore, these differences of prey profile between and within bonobo populations may likely be affected by prey image per respective population. Environmental conditions also contribute to the prey profile across bonobo populations (Wrangham 1975; Sakamaki et al. 2016), which suggests the necessity of studying predator–prey interactions at the specified population level.
Understanding the differences in prey images or prey preference in bonobos may be useful for interpreting the variety of bonobo cultures that previous studies have described (Hohmann & Fruth 2003; Samuni et al. 2020). Here, I report the first case of an adult female bonobo at Wamba capturing a blue duiker and carrying it around, alive, for approximately 30 min. This case report is important because it contributes to our understanding of the differences in prey profiles, inter-species interactions, and prey image among allopatric bonobo populations.
Observations were made at Wamba, where long-term studies on bonobos have been conducted since 1973 (Kano 1980; Furuichi 2011). At this time, there were three identified and fully habituated groups of bonobos at Wamba (E1, PE, and PW) (Sakamaki et al. 2018). In July 2018, the E1 group comprised of 41 individuals, including 12 adult females (parous, or ≥ 15 years old), and 2 adolescent females (nulliparous, 8 to < 15 years old), 8 adult males (≥ 15 years old), and 5 adolescent males (8 to < 15 years old) (age classes were categorized by Hashimoto 1997). An adult female known as Zn, who captured the duiker, immigrated to the E1 group from another group (not PE or PW) in October 2011 and was estimated to be 16 years old in 2018.
The duiker capture occurred on July 25, 2018, during regular ad libitum observations of bonobos in the E1 group. At 6:07 h two local assistants and I found a group of bonobos at the location where they had made their night beds the day before. There were ten adult females, two adolescent females, four adult males, and four adolescent males in this group.
At 6:30 h, while I was observing the bonobos at this location, I heard the shriek of a blue duiker and found that Zn was in a tree, grasping an immature blue duiker (Video 1). Zn lightly swung the duiker in her right hand for a few minutes. While Zn was in the tree with the duiker, other bonobos watched her from other trees or from the ground, and they attempted to approach her but did not interfere. Zn then left the tree and wandered around on the ground, carrying the duiker, for approximately 30 min. The duiker continued to shriek throughout the incident. Zn did not try to eat the duiker during our observations. Several group members (five adult females, two adolescent females, one adult male, and one adolescent male) followed Zn as she moved about, but Zn seemed to run away from these individuals. During observations, I did not observe any aggressive behaviors (e.g., hit, kick, bite) by Zn toward the captured duiker. At 7:00 h, Zn was lost from sight. At that time, the two local assistants and I verified the presence of all group members that had been seen at the beginning of observations, with the exception of Zn, one adolescent female, and one adolescent male. When I found Zn again at 8:50 h, she did not have the duiker anymore. There was no blood or duiker fur around her mouth, on her hands, or on her body. During the observations, I did not hear any specific bonobo vocalizations expressing anxiety, stress, or social tension (Hayashi et al. 2012; Yokoyama & Yasumoto 2019).
In the current case, the female bonobo seemed to manipulate the duiker in a manner that might be described as play, which was similar to the bonobo and chimpanzee behaviors described in previous studies (Sabater-Pi et al. 1993; Hirata et al. 2001; Carvalho et al. 2010). Thus the duiker did not seem to be included in the prey image of bonobos at Wamba, although they captured and toyed with it.
Bonobos at Wamba have been observed in non-lethal interactions with other primates, including mutual grooming between bonobos and red colobus (Colobus badius) (Ihobe 1990) and a bonobo carrying the corpse of a red-tailed monkey (Toda et al. 2017). In addition, there was a single previous report of bonobos interacting with, but not killing or eating, a trapped blue duiker (e.g., approaching, sniffing, touching) (Hayashi et al. 2012). Multiple similar incidents have been observed in the habituated groups at Wamba (N. Tokuyama, personal observation; T. Yokoyama, personal observation). A case report at Lilungu (Ikela), Zaire by Sabater-Pi et al. (1993) described three observed incidents of bonobos handling, but not eating, captured primates: an angola colobus (Colobus angolensis), and a red-tailed monkey (Cercopithecus ascanius). In the case of chimpanzees, at Bossou, Guinea, they captured western tree hyraxes (Dendrohyrax dorsalis, order Hyracoidea) and West African wood-owls (Ciccaba woodfordi), but did not eat them (Hirata et al. 2001; Carvalho et al. 2010).
Continuing observations of hunting and carnivorous behaviors among bonobo populations will shed light on the factors that cause local differences in prey images in bonobos. Variations in social and ecological factors (e.g., food availability, overlapped range areas among species, human interference) among field sites might affect the different prey images in bonobos that are part of their local traditions or cultures. This case report will be helpful in confirming the differences in prey images and inter-species interactions among allopatric bonobo populations.
I am grateful to the Research Center for Ecology and Forestry, Ministry of Scientific Research, DRC, and field assistants for supporting our field research. I especially appreciate Mr. Shohei Shibata, Dr. Shintaro Ishizuka, Dr. Kazuya Toda, Dr. Nahoko Tokuyama, Dr. Tetsuya Sakamaki, Dr. Chie Hashimoto, and Dr. Takeshi Furuichi for contributing to the continuous observations and camp management at Wamba and giving valuable comments on the manuscript. I was supported by the Japan Society for the Promotion of Science (JSPS) Grants-in-Aid for Scientific Research (26257408, 16H02753, and 18KK0204).
Boesch C, Boesch H 1989. Hunting behavior of wild chimpanzees in the Taï National Park. Am J Phys Anthropol 78: 547–573. https://doi.org/10.1002/ajpa.1330780410
Carvalho S, Yamanashi Y, Yamakoshi G, Matsuzawa T 2010. Bird in the hand: Bossou chimpanzees (Pan troglodytes) capture west african wood-owls (Ciccaba woodfordi) but not to eat. Pan Afr News 17: 6–9. https://doi.org/10.5134/143514
Fruth B, Hohmann G 2002. How bonobos handle hunts and harvests: why share food? In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural Diversity in Chimpanzees and Bonobos. Cambridge University Press, Cambridge, pp 231–243.
Furuichi T 2011. Female contributions to the peaceful nature of bonobo society. Evol Anthropol 20: 131–142. https://doi.org/10.1002/evan.20308
Hashimoto C 1997. Context and development of sexual behavior of wild bonobos (Pan paniscus) at Wamba, Zaire. Int J Primatol 18: 1–21. https://doi.org/10.1023/A:1026384922066
Hayashi M, Ohashi G, Ryu H 2012. Responses toward a trapped animal by wild bonobos at Wamba. Anim Cogn 15: 731–735. https://doi.org/10.1007/s10071-012-0478-x
Hirata S, Yamakoshi G, Fujita S, Ohashi G, Matsuzawa T 2001. Capturing and toying with hyraxes (Dendrohyrax dorsalis) by wild chimpanzees (Pan troglodytes) at Bossou, Guinea. Am J Primatol 53: 93–97. https://doi.org/10.1002/1098-2345(200102)53:2<93::AID-AJP5>3.0.CO;2-X
Hirata S, Yamamoto S, Takemoto H, Matsuzawa T 2010. A case report of meat and fruit sharing in a pair of wild bonobos. Pan Afr News 17: 21–23. https://doi.org/10.5134/143519
Hohmann G, Fruth B 2003. Culture in bonobos? Between-species and within-species variation in behavior. Curr Anthropol 44: 563–609. https://doi.org/10.1086/377649
Hohmann G, Fruth B 2008. New records on prey capture and meat eating by bonobos at Lui Kotale, Salonga National Park, Democratic Republic of Congo. Folia Primatol 79: 103–110. https://doi.org/10.1159/000110679
Ihobe H 1992. Observations on the meat-eating behavior of wild bonobos (Pan paniscus) at Wamba, Republic of Zaire. Primates 33: 247–250. https://doi.org/10.1007/BF02382754
Ihobe H 1990. Interspecific interactions between wild pygmy chimpanzees (Pan paniscus) and red colobus (Colobus badius). Primates 31: 109–112. https://doi.org/10.1007/BF02381033
Kano T 1992. The Last Ape: Pygmy Chimpanzee Behavior and Ecology. Stanford University Press, Stanford, CA.
Kano T 1980. Social behavior of wild pygmy chimpanzees (Pan paniscus) of Wamba: A preliminary report. J Hum Evol 9: 243–260. https://doi.org/10.1016/0047-2484(80)90053-6
Sabater-Pi J, Bermejo M, Illera G, Vea JJ 1993. Behavior of bonobos (Pan paniscus) following their capture of monkeys in Zaire. Int J Primatol 14: 797–804. https://doi.org/10.1007/BF02192191
Sakamaki T, Maloueki U, Bakaa B, et al. 2016. Mammals consumed by bonobos (Pan paniscus): New data from the Iyondji forest, Tshuapa, Democratic Republic of the Congo. Primates 57: 295–301. https://doi.org/10.1007/s10329-016-0529-z
Sakamaki T, Ryu H, Toda K, Tokuyama N, Furuichi T 2018. Increased frequency of intergroup encounters in wild bonobos (Pan paniscus) around the yearly peak in fruit abundance at Wamba. Int J Primatol 39: 685–704. https://doi.org/10.1007/s10764-018-0058-2
Samuni L, Wegdell F, Surbeck M 2020. Behavioural diversity of bonobo prey preference as a potential cultural trait. Elife 9: 1–10. https://doi.org/10.7554/ELIFE.59191
Surbeck M, Hohmann G 2008. Primate hunting by bonobos at LuiKotale, Salonga National Park. Curr Biol 18: 906–907. https://doi.org/10.1016/j.cub.2008.08.040
Toda K, Tokuyama N, Furuichi T 2017. An old female bonobo carried a dead red-tailed monkey for over a month. Pan Afr News 24: 19–21. https://doi.org/10.5134/228896
Wrangham RW 1975. The behavioural ecology of chimpanzees in Gombe National Park, Tanzania. Ph.D. thesis, University of Cambridge, Cambridge.
Yokoyama T, Yasumoto S 2019. Behavioral responses toward a conspecific corpse of wild bonobos (Pan paniscus) at Wamba. Pan Afr News 26: 16–18. https://doi.org/10.5134/245544
Received: 23 March 2021
Accepted: 16 May 2021
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