Captive female bonobos (Pan paniscus) tend to be more social during tool use than males 
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Daniel M. Goodkin-Gold1, Colin M. Brand1, Klaree J. Boose1, Frances J. White1, Audra Meinelt2 
1Department of Anthropology, University of Oregon, Eugene, OR 
..IS?.- ^ O Primate Osteology Laboratory University of Oregon 2 Columbus Zoo and Aquarium, Powell, OH 
Introduction: 
Tool use occurs in several non-human species, including 
primates. Within the genus Pan, chimpanzees (P. troglodytes) 
exhibit tool use in both the wild and captivity, while tool use in 
bonobos (P. pansiscus) has been documented in captivity and 
suggested to occur in the wild (White et al. 2008). Four 
conditions have been proposed to facilitate the evolution of 
material culture: 1) ecological opportunity, 2) motor dexterity, 3) 
cognition for problem solving and 4) social tolerance to allow for 
social learning of tool use behavior (van Schaik et al. 1999). 
Social tolerance behavior varies among the great apes and a 
recent captive study showed that bonobos had fewer neighbors 
present during tool use acquisition than what has been reported 
for chimpanzees and gorillas (Boose et al 2013, Lonsdorf et al. 
2009). These captive bonobos also exhibited a female bias in 
tool use acquisition that has been well documented in Pan 
(Boose et al. 2013, see also Gruber et al. 2010). We sought to 
investigate patterns of affiliation and association during tool use 
within this captive group of bonobos by analyzing sex and age 
differences. Based on what has been reported for bonobos 
regarding their affiliative patterns, we predicted females would 
be more social than males. 
Methods: 
Data were collected between June and August 2011 on 16 
bonobos housed at the Columbus Zoo and Aquarium, Columbus, 
OH. At the time, the population included 8 males and 7 females 
of various age classes. Individuals were videotaped and recorded 
using all-occurrence sampling for tool use. Videos were analyzed 
and coded later where party size within a 4 meter radius of the 
mound was determined for each fishing bout. We used ANOVA 
and a priori orthogonal planned comparisons (Sokal and Rohlf 
2012) to test for differences in party size between 1) males and 
females, 2) adult females and adolescent females, and 3) adult 
males and adolescent males. Individuals who fished infrequently 
(5 bouts total or less) as well as dependent offspring were 
excluded from our analyses. 
Results: 
Party size during tool use was not equally distributed across the 
population (Figure 1). The individuals who fished too 
infreq uently to be included (n=4) were all wild-born. Females 
fished in larger groups (avg.=2.8 individuals) than males (avg.=2.3 
individuals) (n=9, F=4.38, p<0.05) (See Figure 2). While there was 
no difference between adult and subadult males, adult females 
fished in significantly larger groups than subadult females (n=5, 
F=26.03, p < 0.0001) (See Figure 2). 
Adult male, Maiko, fishing. 
Figure 1. Mean Number of Neighbors During Tool 
Use by Individual 
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Female Adult Female Subadult Male Adult Male Subadult 
Sex/Age Class 
Figure 2. Mean Number of Neighbors During Tool 
Use by Age/Sex Class 
Discussion: 
Research on wild bonobos has revealed strong relationships 
between adult females, a stark contrast to the male-male social 
affiliation seen in chimpanzees. However, studies of captive 
bonobos have illustrated that male-female and male-male 
associations are just as frequent as female-female dyads 
(Stevens et al. 2006). Specifically, females may not always groom 
more frequently or occur in close proximity more than other sex 
combinations. This study demonstrates that female-female 
affiliation in captive bonobos may be evidenced in other 
behavioral contexts. These results also support previous 
knowledge of bonobo sociality. White (1988) reported that in 
wild bonobos, males tend to be more solitary than females, 
often traveling alone between food patches. Our results indicate 
that solitary behavior in males may extend into food acquisition 
behavior such as termite fishing. 
Acknowledgements: 
We thank Karen Huebel, Kelly Vineyard, Shannon Morarity, 
Shelly Roach, and the African Forest staff at the Columbus Zoo 
for their support, construction of the termite mound, and for 
allowing us to collect behavioral observations. We extend 
gratitude to Stephany Harris, Drew Enigk, Mary Fisher, Ashley 
Thoerner, Nicole Thoerner, and Patrick Hoehn for their 
assistance in video recording. 
References: 
Boose K, White F, Meinelt A. 2013. Sex differences in tool use acquisition 
in bonobos (Pan pansiscus). American Journal of Primatology 75:917— 
926. 
Gruber T, Clay Z, Zuberbuhler K. 2010. A comparison of bonobo and 
chimpanzee tool use: evidence for a female bias in the Pan lineage. 
Animal Behavior 80:1023-1033. 
Lonsdorf E, Ross S, Linick S, Milstein M, Melber T. 2009. An experimental, 
comparative investigation of tool use in chimpanzees and gorillas. 
Animal Behaviour 77:1119—1126. 
Sokal RR, Rohlf FJ. 2012. Biometry: the principles and practice of statistics 
in biological research. New York: W. H. Freeman and Co. p 937. 
Stevens JMG, Vervaecke H, De Vries H, Van Elsacker L. 2006. Social 
structures in Pan pansiscus: testing the female-bonding hypothesis. 
Primates 47:210-217. 
van Schaik CP, Deaner RO, Merrill MY. 1999. The conditions for tool use in 
primates: implications for the evolution of material culture. Journal of 
Human Evolution 36:719-741. 
White FJ. 1988. Party composition and dynamics in Pan paniscus. 
International Journal of Primatology. 9:179-193. 
White FJ, Waller MT, Cobden AK, Malone NM. 2008. Lomako bonobo 
population dynamics, habitat productivity, and the question of tool use. 
American Journal of Physical Anthropology 46:222.