Sex Differences in Tool Use Acquisition in Bonobos (Pan Paniscus)
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American Journal of Primatology 75:917–926 (2013) RESEARCH ARTICLE Sex Differences in Tool Use Acquisition in Bonobos (Pan paniscus) 1 1 2 KLAREE J. BOOSE *, FRANCES J. WHITE , AND AUDRA MEINELT 1Department of Anthropology, University of Oregon, Eugene, Oregon 2Columbus Zoo and Aquarium, Powell, Ohio All the great ape species are known tool users in both the wild and captivity, although there is great variation in ability and behavioral repertoire. Differences in tool use acquisition between chimpanzees and gorillas have been attributed to differing levels of social tolerance as a result of differences in social structure. Chimpanzees also show sex differences in acquisition and both chimpanzees and bonobos demonstrate a female bias in tool use behaviors. Studies of acquisition are limited in the wild and between species comparisons are complicated in captivity by contexts that often do not reflect natural conditions. Here we investigated tool use acquisition in a captive group of naïve bonobos by simulating naturalistic conditions. We constructed an artificial termite mound fashioned after those that occur in the wild and tested individuals within a social group context. We found sex differences in latencies to attempt and to succeed where females attempted to fish, were successful more quickly, and fished more frequently than males. We compared our results to those reported for chimpanzees and gorillas. Males across all three species did not differ in latency to attempt or to succeed. In contrast, bonobo and chimpanzee females succeeded more quickly than did female gorillas. Female bonobos and female chimpanzees did not differ in either latency to attempt or to succeed. We tested the social tolerance hypothesis by investigating the relationship between tool behaviors and number of neighbors present. We also compared these results to those reported for chimpanzees and gorillas and found that bonobos had the fewest numbers of neighbors present. The results of this study do not support the association between number of neighbors and tool behavior reported for chimpanzees. However, bonobos demonstrated a similar sex difference in tool use acquisition, supporting the hypothesis of a female bias in tool use in Pan. Am. J. Primatol. 75:917–926, 2013. © 2013 Wiley Periodicals, Inc. Key words: great apes; termite fishing; social tolerance INTRODUCTION ape species [Boesch & Boesch‐Achermann, 2000; Many species of non‐human primates use tools in Galdikas, 1982; Gruber et al., 2010; Goodall, 1986; both captivity [chimpanzee: Kohler, 1927; bonobo: Kano, 1992; McGrew, 1992; Nishida, 1990; Reynolds, Jordan, 1982; orangutan: Galdikas, 1982; sooty 2005; Whiten et al., 2001]. Observations such as these mangabey: Kyes, 1988; capuchin: Visalberghi, 1990; have resulted in the description of and hypotheses gorilla: Fontaine et al., 1995; golden lion tamarin: related to material culture in great apes [Hohmann & Stoinski & Beck, 2001; ring‐tailed lemur and brown Fruth, 2003; McGrew, 1992; van Schaik et al., 2003; lemur: Santos et al., 2005; gibbon: Cunningham Whiten et al., 2001]. et al., 2006; vervet: Santos et al., 2006; mandrill: Addressing these differences, van Schaik et al. Pansini & de Ruiter, 2011] and the wild [chimpanzee: [1999] proposed four conditions that favor the van Lawick‐Goodall, 1970; red colobus: Struhsaker, evolution of material culture: (1) ecological opportu- 1975; bonobo: Kano, 1982; orangutan: van Schaik nity, (2) motor dexterity (3), the cognitive ability to et al., 1996; capuchin: Phillips, 1998, Boinski et al., 2000; gorilla: Breuer et al., 2005; spider monkey: Contract grant sponsor: Office of the Vice President of Research Rodrigues & Lindshield, 2007; long‐tailed macaque: at the University of Oregon. Ã Gumert et al., 2011]. Tool use by great apes is of Correspondence to: Klaree Boose, Department of Anthropology, 1218 University of Oregon, Eugene, OR 97403. particular interest for modeling and identifying E‐mail: [email protected] potential conditions that contributed to the evolution Received 20 November 2012; revised 2 February 2013; revision of hominin tool use [Byrne, 2004; McGrew, 1992; van accepted 1 March 2013 Schaik et al., 1999]. Research on this topic has DOI: 10.1002/ajp.22155 revealed a great deal of behavioral variation in tool Published online 19 April 2013 in Wiley Online Library use behaviors both within and between the different (wileyonlinelibrary.com). © 2013 Wiley Periodicals, Inc. 918 / Boose et al. solve problems, and (4) a high degree of social uals are routinely separated and reunited and must tolerance as a means to facilitate the social learning be highly socially tolerant to actively reform social of such complex behaviors. In the captive setting, bonds during fusion events. numerous tool use experiments and anecdotal In addition to the observed differences in tool evidence have demonstrated that all four species of repertoires between field sites, chimpanzees display great apes posses the motor dexterity and cognitive significant sex differences in complex foraging behav- ability to manufacture and use tools, even though ior. Females use tools to fish for termites more there is great variation in ability and behavioral frequently and for longer time periods than do males repertoires (gorillas: artificial fishing [Boysen [McGrew, 1979]. Females are also more efficient at et al., 1999]; orangutans: digging sticks and rain using stone tools to crack open nuts, whereas males covers [Galdikas, 1982]; chimpanzees and bonobos: hunt for prey and consume meat more frequently artificial fishing, aimed throwing, play, etc. [Gruber [Boesch & Boesch, 1984], although female chimpan- et al., 2010]). Even though chimpanzees and bonobos zees at Fongoli hunt with tools more frequently than differ in their abilities to solve physical and social males [Pruetz & Bertolani, 2007]. A study of tool use cognitive problems [Herrmann et al., 2010], recent acquisition in wild chimpanzees at Gombe found that studies also indicate that all of the great apes have a young females spent more time watching their similar understanding of the functional properties of mothers fish for termites, began fishing at an earlier tools [Herrmann et al., 2008]. age, and used tools more proficiently than did young Although ongoing research is continuing to males [Lonsdorf, 2005]. Although evidence of tool use reveal details and characteristics of tool use in all from bonobo field sites is sparse [Hohmann & of the great ape species, chimpanzees remain the Fruth, 2003; Ingmanson, 1996; Kano, 1982], a recent most prolific and diverse non‐human tool users (e.g.: survey of several captive groups found significant sex Bentley‐Condit & Smith [2010]), showing the highest differences in tool use behaviors where females used degree of behavioral variation and complexity tools more often and showed greater diversity in types [Boesch & Boesch‐Achermann, 2000; Goodall, 1986; of tools used [Gruber et al., 2010]. This raises the McGrew, 1992; Nishida, 1990; Reynolds, 2005; question of whether there are sex differences in tool Whiten et al., 2001]. This behavioral variation in use acquisition in bonobos and whether sex differ- tool use across chimpanzee study sites is thought to ences in tool behavior are similar or different across be the result of distinct cultural differences between the ape species. groups [McGrew, 1992], suggesting that social Differences in experimental methodology can learning, facilitated by having a high degree of social make direct comparisons among studies and species tolerance, plays a critical role in acquiring the tool use difficult. This study, therefore, examines the acquisi- behaviors present in a group [van Schaik et al., 1999]. tion of tool use behavior in bonobos under a Recent research focusing on differences in tool use naturalistic setting using a protocol modeled on the behavior between chimpanzees and gorillas supports experiment comparing tool use acquisition in chim- the hypothesis that social tolerance may play an panzees and gorillas at LPZ [Lonsdorf et al., 2009]. important role during acquisition [Lonsdorf et al., We presented a captive group of bonobos at the 2009]. A comparative study of tool use acquisition in Columbus Zoo and Aquarium (CZA) with an artificial these two species at the Lincoln Park Zoo (LPZ) termite mound and recorded latency to attempt and measured successful retrieval of bait from an artifi- to successfully use tools to extract bait. We first cial termite mound together with the number of predict that, similar to other groups of captive neighbors present during tool use, as a measure of bonobos [Gruber et al., 2010], this group of bonobos social tolerance [Lonsdorf et al., 2009]. They found will readily use tools. Chimpanzees that fish for that chimpanzees used tools more quickly and had a termites are selective in the types of tool material greater percentage of possible neighbors present used as well as the manner in which the raw material than did the gorillas. Later research on chimpanzee is modified [McGrew et al., 1979]. Chimpanzees often tool use acquisition demonstrated that the transmis- choose woody items in the form of tree and bush sion of novel tool use behaviors (the retrieval of bait branches that are modified through the employment from an apparatus called the “Panpipe” at the Yerkes of several behaviors specific to tool‐making, such as Primate Center) was facilitated by the high social detachment of raw material, side‐branch removal, tolerance exhibited by the two model individuals, leave