Key words: great apes; termite fishing; social tolerance
INTRODUCTION
Many species of non‐human primates use tools inboth captivity [chimpanzee: Kohler, 1927; bonobo:Jordan, 1982; orangutan: Galdikas, 1982; sootymangabey: Kyes, 1988; capuchin: Visalberghi, 1990;gorilla: Fontaine et al., 1995; golden lion tamarin:Stoinski & Beck, 2001; ring‐tailed lemur and brownlemur: Santos et al., 2005; gibbon: Cunninghamet al., 2006; vervet: Santos et al., 2006; mandrill:Pansini & de Ruiter, 2011] and the wild [chimpanzee:van Lawick‐Goodall, 1970; red colobus: Struhsaker,1975; bonobo: Kano, 1982; orangutan: van Schaiket al., 1996; capuchin: Phillips, 1998, Boinski et al.,2000; gorilla: Breuer et al., 2005; spider monkey:Rodrigues & Lindshield, 2007; long‐tailed macaque:Gumert et al., 2011]. Tool use by great apes is ofparticular interest for modeling and identifyingpotential conditions that contributed to the evolutionof hominin tool use [Byrne, 2004; McGrew, 1992; vanSchaik et al., 1999]. Research on this topic hasrevealed a great deal of behavioral variation in tooluse behaviors both within and between the different
ape species [Boesch & Boesch‐Achermann, 2000;Galdikas, 1982; Gruber et al., 2010; Goodall, 1986;Kano, 1992; McGrew, 1992; Nishida, 1990; Reynolds,2005;Whiten et al., 2001]. Observations such as thesehave resulted in the description of and hypothesesrelated tomaterial culture in great apes [Hohmann&Fruth, 2003; McGrew, 1992; van Schaik et al., 2003;Whiten et al., 2001].
Addressing these differences, van Schaik et al.[1999] proposed four conditions that favor theevolution of material culture: (1) ecological opportu-nity, (2) motor dexterity (3), the cognitive ability to
Contract grant sponsor: Office of the Vice President of Researchat the University of Oregon.�Correspondence to: Klaree Boose, Department of Anthropology,1218 University of Oregon, Eugene, OR 97403.E‐mail: [email protected]
Received 20 November 2012; revised 2 February 2013; revisionaccepted 1 March 2013
DOI: 10.1002/ajp.22155Published online 19 April 2013 in Wiley Online Library(wileyonlinelibrary.com).
solve problems, and (4) a high degree of socialtolerance as a means to facilitate the social learningof such complex behaviors. In the captive setting,numerous tool use experiments and anecdotalevidence have demonstrated that all four species ofgreat apes posses the motor dexterity and cognitiveability to manufacture and use tools, even thoughthere is great variation in ability and behavioralrepertoires (gorillas: artificial fishing [Boysenet al., 1999]; orangutans: digging sticks and raincovers [Galdikas, 1982]; chimpanzees and bonobos:artificial fishing, aimed throwing, play, etc. [Gruberet al., 2010]). Even though chimpanzees and bonobosdiffer in their abilities to solve physical and socialcognitive problems [Herrmann et al., 2010], recentstudies also indicate that all of the great apes have asimilar understanding of the functional properties oftools [Herrmann et al., 2008].
Although ongoing research is continuing toreveal details and characteristics of tool use in allof the great ape species, chimpanzees remain themost prolific and diverse non‐human tool users (e.g.:Bentley‐Condit & Smith [2010]), showing the highestdegree of behavioral variation and complexity[Boesch & Boesch‐Achermann, 2000; Goodall, 1986;McGrew, 1992; Nishida, 1990; Reynolds, 2005;Whiten et al., 2001]. This behavioral variation intool use across chimpanzee study sites is thought tobe the result of distinct cultural differences betweengroups [McGrew, 1992], suggesting that sociallearning, facilitated by having a high degree of socialtolerance, plays a critical role in acquiring the tool usebehaviors present in a group [van Schaik et al., 1999].Recent research focusing on differences in tool usebehavior between chimpanzees and gorillas supportsthe hypothesis that social tolerance may play animportant role during acquisition [Lonsdorf et al.,2009]. A comparative study of tool use acquisition inthese two species at the Lincoln Park Zoo (LPZ)measured successful retrieval of bait from an artifi-cial termite mound together with the number ofneighbors present during tool use, as a measure ofsocial tolerance [Lonsdorf et al., 2009]. They foundthat chimpanzees used tools more quickly and had agreater percentage of possible neighbors presentthan did the gorillas. Later research on chimpanzeetool use acquisition demonstrated that the transmis-sion of novel tool use behaviors (the retrieval of baitfrom an apparatus called the “Panpipe” at the YerkesPrimate Center) was facilitated by the high socialtolerance exhibited by the two model individuals,each of whomwere trained to use a different retrievaltechnique [Horner, 2010]. Higher social tolerance inthe chimpanzees at LPZ, therefore, may havefacilitated a faster transmission of tool use behaviorsthan in the gorillas [Lonsdorf et al., 2009]. Lonsdorfet al. [2009] hypothesized that chimpanzees areespecially primed for social learning because of thenature of their fission–fusion ranging, where individ-
uals are routinely separated and reunited and mustbe highly socially tolerant to actively reform socialbonds during fusion events.
In addition to the observed differences in toolrepertoires between field sites, chimpanzees displaysignificant sex differences in complex foraging behav-ior. Females use tools to fish for termites morefrequently and for longer time periods than do males[McGrew, 1979]. Females are also more efficient atusing stone tools to crack open nuts, whereas maleshunt for prey and consume meat more frequently[Boesch & Boesch, 1984], although female chimpan-zees at Fongoli hunt with tools more frequently thanmales [Pruetz & Bertolani, 2007]. A study of tool useacquisition in wild chimpanzees at Gombe found thatyoung females spent more time watching theirmothers fish for termites, began fishing at an earlierage, and used tools more proficiently than did youngmales [Lonsdorf, 2005]. Although evidence of tool usefrom bonobo field sites is sparse [Hohmann &Fruth, 2003; Ingmanson, 1996; Kano, 1982], a recentsurvey of several captive groups found significant sexdifferences in tool use behaviors where females usedtoolsmore often and showed greater diversity in typesof tools used [Gruber et al., 2010]. This raises thequestion of whether there are sex differences in tooluse acquisition in bonobos and whether sex differ-ences in tool behavior are similar or different acrossthe ape species.
Differences in experimental methodology canmake direct comparisons among studies and speciesdifficult. This study, therefore, examines the acquisi-tion of tool use behavior in bonobos under anaturalistic setting using a protocol modeled on theexperiment comparing tool use acquisition in chim-panzees and gorillas at LPZ [Lonsdorf et al., 2009].We presented a captive group of bonobos at theColumbus Zoo and Aquarium (CZA) with an artificialtermite mound and recorded latency to attempt andto successfully use tools to extract bait. We firstpredict that, similar to other groups of captivebonobos [Gruber et al., 2010], this group of bonoboswill readily use tools. Chimpanzees that fish fortermites are selective in the types of tool materialused as well as themanner in which the rawmaterialis modified [McGrew et al., 1979]. Chimpanzees oftenchoose woody items in the form of tree and bushbranches that are modified through the employmentof several behaviors specific to tool‐making, such asdetachment of raw material, side‐branch removal,leave stripping, and bark peeling [McGrew et al.,1979]. Lonsdorf et al. [2009] describe a process ofallowing the chimpanzees and gorillas to select toolmaterial from the naturally occurring vegetationwithin the enclosure at LPZ. The bonobos at CZAwere also allowed to select tool material that grewwithin their enclosure. The task of selecting toolmaterial from natural vegetation, versus beingprovisioned with tools by the keepers, provided a
Am. J. Primatol.
918 / Boose et al.
novel task for all of the bonobos at CZA. We,therefore, predict that the bonobos at CZA will selecttool material and modify that material in a mannersimilar to what has been described for chimpanzeesin both the wild [McGrew et al., 1979] and captivesettings [Lonsdorf et al., 2009]. Following Gruberet al. [2010], we predict the bonobos will show similarsex differences in tool use behaviors with femaleslearning to use tools more quickly and using toolsmore frequently than males. Differences in socialtolerance between species have been suggested toexplain why a fission–fusion species like chimpan-zees use tools more readily than gorillas underidentical conditions [Lonsdorf et al., 2009]. Sincebonobos are also a fission–fusion species [Kano, 1992;White, 1996] and are, therefore, presumably moresocially tolerant than gorillas, we predict thatbonobos will be more similar to what has beenreported for chimpanzees than for gorillas [Lonsdorfet al., 2009] in both number of neighbors present andtool use behaviors.
METHODS
Ethical NoteThis study was conducted with approval at CZA,
an Association of Zoos and Aquariums (AZA) accred-ited institution in Columbus, Ohio, USA. CZAadheres to the welfare and husbandry standardsoutlined by the AZA. All data were collected usingobservations of spontaneous behavior. No animalswere separated from the group and no social groupswere manipulated for the purpose of this study. Alldata collection methods adhered to the AmericanSociety of Primatologists Principles for the EthicalTreatment of Nonhuman Primates and were ap-
proved by the University of Oregon InstitutionalAnimal Care and Use Committee (IACUC). Theauthors have no conflict of interest to declare.
Subjects and Housing
All data were collected on the captive group ofbonobos housed at CZA. Following Kano’s [1992] ageclass definitions (infant: 0–1; juvenile: 2–6; adoles-cent: 7–14; adult: �15), the group was composed offour adult males, four adult females, two adolescentfemales, two adolescentmales, one juvenilemale, onejuvenile female, one infant male, and one infantfemale (Table I). The bonobos were housed in acomplex of areas consisting of two large indoor publicviewing exhibits (54.8 m2 each) with multiple climb-ing structures, two off‐exhibit indoor enclosures(22.6 m2 each), two off‐exhibit outdoor enclosures(18.5 m2 each) and a large naturalistic outdoor publicviewing exhibit (57.9 m � 45.7 m, 2,647.7 m2) withgrass, mature trees, and an artificial stream andwaterfall. The keepers at CZA managed the bonobosto simulate the species typical fission–fusion processof variable party composition. In the morning,bonobos were allowed access to each other andparties were set based mostly on individual bonoboassociation preferences rather than parties that werepredetermined by the keepers. Most individuals hadequal access to each other, but two of the adult males(Jimmy and Donnie) were never allowed to betogether because of previous conflicts that hadresulted in serious injury. This management processusually resulted in three parties that lasted for2–3 days, and rarely changed on a daily basis orexceeded 4 days. Each sub‐group occupied differentpublic display areas.
TABLE I. Subjects (CZA), Number of Trials, and Latencies to Investigate, Attempt, and Succeed
Subject Sex Age (years) Offspring No. of trials
Latencies
Investigate Attemptb Succeedb
Lola F 7 19 1 1 1Gilda F 5 20 3 1 1Unga F 18 Gander, Jerry 12 4 1 1Ana Neema F 19 Bila Isia, Gilda, Wilbur 19 2 2 2Donnie M 18 Jerry 14 1 3 3JoT F 9 17 1 4 4Maiko M 27 23 — 9 9Gander M 8 15 1 10 10Jerry M 3 12 1 12 12Bila Isia M 10 20 2 11 20Toby M 32a Lola 22 16 1 —
Mary‐Rose F 1.5 16 2 14 —
Susie F 29a Donnie, Lola, Mary‐Rose 16 1 — —
Lady F 29a JoT 16 1 — —
Wilbur M 0.5 19 5 — —
Jimmy M 32a Donnie 21 — — —
Note: aEstimated age for wild‐caught individuals; blatency to attempt and to succeed after first investigation; italicized individuals are under 5 years old andwere excluded from data analyses.
Am. J. Primatol.
Bonobo Sex Differences in Tool Use / 919
During the study period, the bonobos werereleased into the outdoor exhibit each morning atapproximately 0730 hr and were brought backinto the indoor enclosures at approximately1900 hr. The bonobos were rarely brought insidebetween these hours, except for extenuating circum-stances (i.e. dangerous inclement weather or anemergency). Each night the party that occupied theoutdoor exhibit was brought into one of the indoorenclosures and the outdoor exhibit remained emptyuntil the following morning. The bonobos werefed each morning and evening at approximately0730 and 1900 hr. Additional supplemental enrich-ment feedings were sometimes given throughoutthe day.
An artificial termite mound was installed in theoutdoor enclosure near Viewing Area 1 (Fig. 1) forthe purpose of this study and provided a novelstructure and tool related task for this group at CZA.From the knownhistories of the study group (Table I),all but two individuals (Ana‐Neema and Unga) werenaïve to an artificial extractive foraging structure.Ana‐Neema had previously resided at theMilwaukeeZoo in Milwaukee, WI where she was exposed to anartificial structure and had learned to successfullyfish for bait using tools provided by the staff asenrichment. Finding a tool from the naturalistichabitat and modifying it for use on this new deviceprovided this subjectwith anovel task for the purposeof this study. Unga previously resided at thePlanckendael Zoo in Belgium where she was pre-sented with several tool use opportunities, includingthose involving extractive foraging using devices, butnot an artificial termite mound.
Testing Apparatus and Bait
An artificial termitemoundwas constructed fromconcrete, rebar, wire mesh, and paint (Fig. 2). Themound was constructed by the CZA staff and wasfashioned to resemble those naturally occurring inthe wild. Eight bait holes were bored into the moundand fitted with removable polyvinyl chloride (PVC)tubes that measured 15.0 cm in length and 4.5 cm indiameter. The mound had a small locked access door
Fig. 1. Composite maps of the a) bonobo enclosures at CZA and b) gorilla and chimpanzee enclosures at LPZ. Maps not to scale. (Originalfigures courtesy of the Columbus Zoo and Aquarium and the Lincoln Park Zoo.)
Fig. 2. Juvenile female bonobo using a tool to fish bait from anartificial termite mound at the Columbus Zoo (Photo: DrewEnigk).
Am. J. Primatol.
920 / Boose et al.
to allow the staff to remove and replace the bait tubes.The unbaited mound was installed in the outdoorhabitat in front of a large public display windowduring November of 2010. The subjects were free toexplore the unbaited mound both before and afterJune 29, 2011, the first day of baited trials. Allsubjects were considered habituated (i.e. did notdisplay avoidance behavior and readily approachedthe apparatus) to the mound before trials began.Beginning June 29, 2011, the mound was baited eachmorning by CZA staff during their regular morningcheck of the enclosure. The baited tubes remained inthe mound throughout the day until the followingmorning when they were replaced by new tubes withfresh bait. Bait included honey and/or pureed blue-berries, raspberries, bananas, and cooked sweetpotatoes and carrots. All subjects readily consumedthese food items as part of their regular diet. No toolsor raw material were explicitly provided to theanimals, instead, individuals were allowed to con-struct tools out of the naturally occurring vegetationgrowing in the enclosure (i.e. tree branches, grass,bushes, etc.).
Data Collection and DefinitionsData were collected most days between June 29,
2011 and August 29, 2011. Data collection beganwhen the first individual was released into theoutdoor enclosure in the morning and ended whenthe last individual was shut out of the enclosure forthe night. Each day that a subject had exposure to thebaited mound was scored as one trial for that subject.Individuals within 1 m of the mound were scored asbeing within proximity of the mound. All presencedata and behaviors within 1 m of the mound werevideotaped and coded by K.J.B. Continuous datawere collected from the videotapes and includedfrequencies and durations of all predeterminedmound‐related behaviors (i.e. investigate, poke, toolbehavior, and fish as defined byLonsdorf et al. [2009])for each subject. Attempting the task was defined asinserting a tool into the bait tubes without accessingthe bait and successful fishing was defined asinserting a tool into the bait tubes and retrievingbait [Lonsdorf et al., 2009]. Lonsdorf et al. [2009]defined latency as the number of trials with thebaited mound experienced by each individual beforethey attempted the task or successfully fished.
The bonobos at CZA had access to the unbaitedmound for approximately 6 months before the firstbaiting and were housed outside of the visual andauditory range of the mound during baiting. Becausethe mound was baited out of sight of the bonobos, nosubjects had visual information that the mound wasbaited until they approached and investigated thestructure. The mound was not baited unless observ-ers were present and the baited mound was observedfor the entire time that bonobos were in the
enclosures. We recorded latency to investigate themound as the number of baited trails until firstinvestigation. Latency to attempt and latency tosucceed were then recorded as the number of trialsafter this initial investigation before they attemptedthe task or successfully fished.
A tool use bout was defined as the time duringwhich an individual continuously fished or attemptedto extract bait.When an individual left 1 m proximityof the mound, or stopped tool use behaviors for morethan 30 sec but remained within 1 m proximity ofthe mound, the bout was scored as finished. Tocompare the time spent fishing between individuals,we first summed the duration of each successfulfishing bout for each individual and then divided thistotal time by the number of trials for that individualto control for variation in number of trials (Table I).To compare rate of fishing between individuals, wefirst calculated the total number of bouts and thendivided this number by the total number of trials forthat individual to again control for variation innumber of trials.
Each group member within 1 m of the mound wasscored as a “neighbor” [Lonsdorf et al., 2009] for eachfocal individual on each day during each bout. Thenumber of neighbors was recorded for each individualthat was within 1 m of the mound, regardless ofwhether or not that individual, or their “neighbors,”were engaged in mound related behaviors. Groupcomposition in the outdoor enclosure at CZA wasvariable (see “Subjects and Housing Section”) and,following Lonsdorf et al. [2009], we controlled fordifferences in group sizes by calculating the number ofneighbors as a percentage based on presence data(number of neighbors/number of groupmembers in theenclosure � 1). The percentage of neighbors wascalculated for all individuals for all approaches towithin 1 m proximity of the mound including fishingbehavior, attempts tofish, andnon‐fishing approaches.
Data Analyses
Frequency data were compared using G tests ofGoodness of Fit with Williams correction applied[Sokal & Rohlf, 2012] and ANOVAs were used to testfor significant differences in means [Sokal &Rohlf, 2012]. All data were tested for fit to theassumptions of ANOVAs, including normality, andno transformationswere required. Data on individualchimpanzee and gorilla latencies to attempt and tosucceed published in Table I of Lonsdorf et al. [2009]were used for comparison with the bonobo datacollected onmean latencies to attempt and to succeedfor the purpose of this study. In addition, we obtainedN’s, means, and standard errors for percentage ofpossible neighbors for chimpanzees and gorillasduring baited trials using Figure 3 from Lonsdorfet al. [2009]. Wemade the assumption that, althoughthe enclosures at CZA and LPZ differed in size, each
The first individual to both attempt and success-fully fish was a naïve juvenile female, Lola, whoinvestigated the mound, manufactured a tool,attempted, and successfully fished on the first baitedtrial presented to the bonobos. Groupmean latency toinvestigate the mound was 3.00 � SE 1.335 trials.Seven individuals (four females and three males)investigated the mound on their first trial, and sevenindividuals (four females and three males) investi-gated the mound after their first trial (range ¼ 2–16trials, mean ¼ 4.86 trials, Table I). Two adult males,Jimmy and Maiko, never investigated the moundduring the study period and although Maiko success-fully learned to fish for bait, he was never observed toinvestigate the mound. Group mean latency toattempt after investigation was 4.300 � SE 1.291trials (range ¼ 1–11, N ¼ 10, individuals <5 yearsexcluded: N ¼ 2), although some individuals neverattempted the task (N ¼ 3, one male and twofemales, individuals <5 years excluded: N ¼ 1).Group mean latency to succeed after investigation
was 5.67 � SE 2.121 trials (range ¼ 1–20, N ¼ 9,individuals <5 years excluded: N ¼ 1) trials.
After 60 days, 62.5% (N ¼ 10, including oneindividual <5 years) of the subjects had successfullyperformed fishing behavior (Table I). Of thesesubjects, 50.0% (N ¼ 5) successfully modified rawmaterials into tools and 50.0% (N ¼ 5) only usedmaterial that had been modified by another individ-ual or material that did not requiremodification to besuccessfully used as a tool (i.e. straight piece of woodymaterial with no side branches or leaves, etc.). A totalof 901 tool use bouts were recorded, of which 99.7%(N ¼ 898) included tools made from woody material(tree and bush branches). Other tools used includedgrass, leaves, and wood–wool nesting material.
Sex Differences in BonobosThere was a significant sex difference in mean
latency to attempt to use tools to fish in this bonobogroup. Females attempted the task after fewer trials(mean ¼ 1.80 � SE 0.583 trials, N ¼ 5, individuals<5 years excluded: N ¼ 1) than did the males(mean ¼ 6.80 � SE 2.010 trials, N ¼ 5, individuals<5 years excluded: N ¼ 1, ANOVA: F ¼ 5.71, df¼ 1,8, P < 0.05, Fig. 3). There was also a significantsex difference in mean latency to succeed in thisbonobo group, where females succeeded in fishingafter significantly fewer trials (mean ¼ 1.80 � SE0.583 trials, N ¼ 5, individuals <5 years excluded:N ¼ 1) than did the males (mean ¼ 10.50 � SE3.524 trials, N ¼ 4, ANOVA: F ¼ 7.56, df ¼ 1,7,P < 0.05, individuals <5 years excluded: N ¼ 1).There was no significant difference in the numbertrials experienced by males and females (F ¼ 0.66,df ¼ 1,14, P ¼ 0.4301, Table I). Females engaged insignificantly more fishing bouts than did the males(488 female bouts, 74 male bouts, Goodness of Fit:G ¼ 325.737, P < 0.001). There was no significantdifference in the mean duration of bouts per trialbetween females (mean ¼ 408.6 � SE 159.7 sec/tri-al) and males (mean ¼ 223.2 � SE 194.3 sec/trial,ANOVA: F ¼ 0.55, df ¼ 1,11, P ¼ 0.472).
Sex Differences Across Species
The comparison of results for males and femalesamong the three ape species (excluding individualsunder 5 years old) demonstrated that there were nosignificant differences among the species in meanlatency to attempt or to succeed in males (attempt—ANOVA: F ¼ 0.64, df ¼ 2,5, P ¼ 0.5636; succeed—ANOVA:F ¼ 0.73, df ¼ 2,4,P ¼ 0.5364) or in latencyto attempt in females (ANOVA: F ¼ 3.61, df ¼ 2,12,P ¼ 0.0593, Table II). There were significant differ-ences among the species in latency to succeed infemales (ANOVA: F ¼ 12.34, df ¼ 2,12, P < 0.005).The multiple comparisons within this statisticallysignificant ANOVA show that there was no
Fig. 3. Mean number of trials in latency to attempt and tosucceed for male and female bonobos. �Significant differences(P < 0.05). Attemptmeans forfivemales (N ¼ 34 total trials) andfive females (N ¼ 9 total trials). Succeed means for four males(N ¼ 42 total trials) and five females (N ¼ 9 total trials).
Am. J. Primatol.
922 / Boose et al.
significant difference within Pan, between femalebonobos and female chimpanzees, in latency tosucceed (F ¼ 0.02, df ¼ 1, P ¼ 0.8864), but therewas a significant difference between female gorillasand female Pan in latency to succeed (F ¼ 24.63,df ¼ 1, P < 0.001).
Numbers of NeighborsWe recorded the number of neighbors for 1,192
observations of 15 focal animals engaged in allmound‐related behaviors. We tested for differencesin the number of neighbors during mound relatedbehaviors by focal bonobos in this group using aNested ANOVA. Therewere significant differences innumber of neighbors between individuals (F ¼ 10.61,df ¼ 13,1177, P < 0.0001) but there was no signifi-cant sex difference in number of neighbors (F ¼ 0.21,df ¼ 1,13, P ¼ 0.6521). There was, however, asignificant difference in mean number of neighborspresent between bonobos (CZA), chimpanzees (LPZ),and gorillas (LPZ) (ANOVA: F ¼ 25.793, df ¼ 2,26,P < 0.001, Table III). Bonobos had the fewest meanpercentage of possible neighbors present at themound.
DISCUSSION
The results presented in this study confirmprevious studies and our prediction that bonobosposses the motor dexterity and cognitive ability to
manufacture and use appropriate tools. Althoughrecent studies also indicate that all of the great apeshave a similar understanding of the functionalproperties of tools [Herrmann et al., 2008; but seeHerrmann et al., 2010], other studies have suggestedthat species aswell as sexesmay showdiffering levelsof propensity or aptitude in constructing and usingtools [Gruber et al., 2010; Lonsdorf et al., 2004;Lonsdorf et al., 2009; McGrew, 1992; Reynolds, 2005;Whiten et al., 2001].We found that, comparable to thechimpanzees at LPZ, several individuals in thisgroup of bonobos rapidly became proficient inmanufacturing tools and extracting bait from theartificial termite mound. Tools were mostly con-structed out of woody material harvested primarilyfrom the nearby trees and bushes within thenaturalistic outdoor enclosure. Tool constructionwas remarkably similar to what has been describedfor termite fishing in wild chimpanzees [McGrewet al., 1979], including detachment of raw material,side branch removal, leaf stripping, and bark peeling.Both the individual that constructed the tool as wellas other members of the group often reused tools thatwere constructed out of woody branch‐type material.On several occasions, individuals were observedcarrying tools away from the mound and returningsome time later with the same tool to begin anotherfishing bout.
Following Lonsdorf et al. [2009], “investigation”of the mound was defined as using visual andolfactory senses to examine the contents of the baitholes in order to identify when subjects were firstclearly aware that the termite mound contained bait.This definition appeared appropriate for most indi-viduals, except for one. Maiko, a low‐ranking male,did not investigate the mound under this definition,but was in the vicinity of fishing individuals onseveral occasions prior to his first attempt. In thissingle case, it appears that Maiko used informationfrom observing the behaviors of other groupmembersto identify that the mound contained bait. Alsofollowing Lonsdorf et al. [2009], “attempt” wasdefined as non‐successful use of tools, however, allof the bonobos except Maiko frequently poked at theholes in the termite mound with their fingers beforetheir first attempt to use tools to extract bait. It ispossible, therefore, that Maiko learned to successful-ly fish by observing other group members from adistance rather than through a standard method oftrial‐and‐error that involved very close proximity togroup members that were fishing and frequentlypoking. It is not surprising that, because the bonoboswere tested within social groups, a low‐ranking malewould not approach the mound while multipleindividuals were engaged inmound related behaviorssurrounding a high‐value food source. Maiko’sbehavior highlights the importance of conductingresearch within the social context in order to observepotential variation in behavioral strategies.
TABLE II. Latencies to Attempt and to Succeed forMales and Females in Chimpanzeesa, Gorillasa, andBonobos
aNote: Data for chimpanzees and gorillas from Lonsdorf et al. [2009].
Am. J. Primatol.
Bonobo Sex Differences in Tool Use / 923
As has been observed in chimpanzees[Lonsdorf, 2005; McGrew, 1979], there were similarsignificant sex differences in tool use behaviors in thisgroup of bonobos. We found that the female bonoboswere much quicker to attempt to use tools andsuccessfully fished more quickly than did the males.This result is similar to the description of theacquisition of termite fishing in chimpanzees[Lonsdorf, 2005]. Although Lonsdorf [2005] observedlearning in young chimpanzees, whereas we mea-sured tool acquisition in bonobos ranging in age from6 months to 32 years, the result that mean time toacquisition in females was significantly shorter thanin males is similar to what we observed in thebonobos. In addition, once successful, the femalebonobos returned to the artificial termite mound andfished significantly more frequently than did themale bonobos. Together our results support previousresearch demonstrating a female bias in tool use inPan [Gruber et al., 2010].
The observed sex differences in this group ofbonobos highlight important variations in tool useaptitude and propensity across the ape species andbetween the sexes. When comparing our results withthose published by LPZ, we found that there was nosignificant difference among the males of the threespecies in latency to attempt or to succeed. Althoughcaution must be applied when considering smallsample sizes, the males in these groups of chimpan-zees, bonobos, and gorillas demonstrated similaraptitudes in tool use acquisition. Further research isneeded to determine if these results accurately reflectaptitude among the males and the degree to whichpropensity to use tools affects successful acquisitionin males. There were also important similarities andsome differences among the females of the threespecies. Females from all three species had similarmean latencies to attempt to use tools to extract baitsuggesting that female chimpanzees, bonobos, andgorillas share a similar propensity to use tools.However, while chimpanzee and bonobo femalesalso had similar latencies to successfully use tools,the two Pan species were significantly quicker tosucceed than were the gorilla females. Our resultsdemonstrate similarity between chimpanzees andbonobos in these attributes of tool use acquisition,and verify a key difference in tool use aptitudebetween the Pan genus and gorillas.
Differences in ecological constraints have beensuggested to explain why chimpanzees and gorillasdiffer in their tool using abilities [Breuer et al., 2005].Chimpanzees use tools to extract resources that areotherwise difficult to attain, whereas gorillas aremore able to use physical strength to acquire hard toobtain food items [Breuer et al., 2005]. Lonsdorf et al.[2009] reported significant differences in propensityto investigate the artificial termite mound at LPZ.Prior to baiting the structure, the chimpanzeesengaged in mound‐related behaviors significantly
more frequently than did the gorillas. In addition, thechimpanzees were faster to use tools to successfullyretrieve bait and had a greater percentage of possibleneighbors present than did the gorillas. Lonsdorfet al. [2009] suggested that social tolerance, asmeasured by number of neighbors present, mightimpact the social learning necessary for successfultool use acquisition. The authors concluded thatdifferences in tool use behavior among species may,therefore, be related to differences in social structureas party or group sizes, stability, and social dynamicscan differ significantly both within and betweenspecies. We tested this hypothesis with the inclusionof number of neighbors data from the CZA bonobosduring their first 60 days of exposure to the baitedtermite mound. Bonobos also exhibit a fission‐fusionsocial system and previous studies have demonstrat-ed that they have a high degree of social tolerance inthe form of lower aggression, higher cohesion, andgreater cofeeding during food sharing opportunitiescompared to chimpanzees [Hare et al. 2007; Kano,1992; White, 1996]. Because we found that bonobofemales, like chimpanzee females, were faster thangorilla females to succeed in this tool use experiment,we expected that the mean percentage of number ofneighbors in bonobos to be similar to the numberreported in chimpanzees. Instead, we found that thebonobos had the lowestmean percentage of number ofneighbors than either chimpanzees or gorillas aftercontrolling for differences in group and party sizes.Our data, therefore, do not support the hypothesisthat this measure of social tolerance is a facilitator ofthe transmission of tool use behaviors in bonobos.However, it is possible that differences in the socialmanagement of the groups, at CZA fission–fusion issimulated whereas at LPZ all the chimpanzee andgorilla groups are stable, may have impacted theresults.
It is interesting that, given the sex differences inthe bonobos in latency to attempt and to succeed, wefound no significant difference between the sexes insocial tolerance at the mound as measured by thenumber of neighbors present. There were, however,significant individual differences indicating thatsome males and females were more social thanothers. For example, the adult male that fished themost frequently and for the longest duration per bout(Maiko) rarely fished at the mound when any otherindividuals were present, exhibiting a preference tofish alone. Maiko also seemingly learned to fish byobserving others from a distance. One female (Unga),in contrast, rarely fished alone, and when approach-ing the mound, would often loud call to out‐of‐sightmembers of her party who would then join her at themound a short time after. This further suggests thatthe social tolerance hypothesis does not universallyfunction at the individual level in this bonobo group.Observations of this group, in contrast, suggest to usthat there may be inter‐individual differences in
Am. J. Primatol.
924 / Boose et al.
propensity that did not appear to be strictly sex‐based. Although females in this group fished signifi-cantly more frequently than did the males, somefemales showed little interest in the mound (e.g.Lady, Susie, and JoT), whereas some males fishedregularly (e.g. Maiko, Gander, and Jerry). Furtherstudies are needed to test whether it may bedifferences in propensity and aptitude, rather thansocial tolerance, which are driving sex differences,and possibly species differences, in tool usebehaviors.
ACKNOWLEDGMENTSWe gratefully acknowledge Karen Huebel, Kelly
Vineyard, Shannon Morarity, Shelly Roach, and theentire African Forest staff at the Columbus Zoo fortheir institutional support, construction of thetermite mound, and for allowing us to collectbehavioral observations. We thank Stephany Harris,Drew Enigk, Mary Fisher, Ashley Thoerner, NicoleThoerner, and Patrick Hoehn for their assistance invideo recording, and Thomas Dick for providinggraphic design work. We also wish to thank twoanonymous reviewers for their helpful comments andinsightful suggestions.
REFERENCES
Bentley‐Condit VK, Smith E. 2010. Animal tool use: currentdefinitions and an updated comprehensive catalog. Behav-iour 147:185–221.
Boesch C, Boesch H. 1984. Possible causes of sex differences inthe use of natural hammers by wild chimpanzees. J HumEvol 13:415–440.
Boesch C, Boesch‐Achermann H. 2000. The chimpanzees of theTai forest: behavioural ecology and evolution. New York:Oxford University Press. p 316.
Boinski S, Quatrone RP, Swartz H. 2000. Substrate and tooluse by brown capuchins in Suriname: ecological contexts andcognitive bases. Am Anthropol 102:741–761.
Boysen ST, Kuhlmeier VA,Halliday P,HallidayYM. 1999. Tooluse in captive gorillas. In: Parker ST,Mitchell RW,MilesHL,editors. The mentalities of gorillas and orangutans: compar-ative perspectives. Cambridge: Cambridge University Press.p 179–187.
Breuer T, Ndoundou‐Hockemba M, Fishlock V. 2005. Firstobservation of tool use in wild gorillas. PLoS Biol 3:2041–2043.
Byrne RW. 2004. The manual skills and cognition that liebehind hominid tool use. In: Russon AE, Begun DR, editors.The evolution of thought: evolutionary origins of great apeintelligence. Cambridge: Cambridge Univ Press. p 31–44.
Cunningham CL, Anderson JR, Mootnick AR. 2006. Objectmanipulation to obtain a food reward in hoolock gibbons(Bunopithecus hoolock). Anim Behav 71:621–629.
Fontaine B, Moisson PY, Wickings EJ. 1995. Observations ofspontaneous tool making and tool use in a captive group ofwestern lowland gorillas (Gorilla gorilla gorilla). FoliaPrimatol 65:219–223.
Galdikas BMF. 1982. Orang‐utan tool‐use at Tanjung PutingReserve, central Indonesian Borneo (Kalimantan Tengah). JHum Evol 11:19–33.
Goodall J. 1986. The chimpanzees of Gombe: patterns ofbehavior. Cambridge: Harvard University Press. p 673.
Gruber T, Clay Z, Zuberbühler K. 2010. A comparison of bonoboand chimpanzee tool use: evidence for a female bias in thePan lineage. Anim Behav 80:1023–1033.
Gumert MD, Hoong LK, Malaivijitnond S. 2011. Sex differ-ences in the stone tool‐use behavior of a wild population ofburmese long‐tailed macaques (Macaca fascicularis aurea).Am J Primatol 73:1239–1249.
Hare B, Melis A, Woods V, Hastings S, Wrangham R. 2007.Tolerance allows bonobos to outperform chimpanzees on acooperative task. Curr Biol 17:619–623.
Herrmann E, Wobber V, Call J. 2008. Great apes’ (Pantroglodytes, Pan paniscus, Gorilla gorilla, Pongo pygmaeus)understanding of tool functional properties after limitedexperience. J Comp Psychol 122:220–230.
Herrmann E, Hare B, Call J, Tomasello M. 2010. Differences inthe cognitive skills of bonobos and chimpanzees. PLoS ONE5(8):e12438.
Hohmann G, Fruth B. 2003. Culture in bonobos? Between‐species and within‐species variation in behavior. CurrAnthropol 44:563–571.
Horner V. 2010. The cultural mind of chimpanzees: how socialtolerance can shape the transmission of culture. In: LonsdorfEV, Ross SR, Matsuzawa T, Goodall J, editors. The mind ofthe chimpanzee: ecological and experimental perspectives.Chicago: University of Chicago Press. p 101–115.
Ingmanson EJ. 1996. Tool‐using behavior in wild Pan paniscussocial and ecological considerations. In: Russon AE, BardKA, Parker ST, editors. Reaching into thought: the minds ofthe great apes. New York: Cambridge University Press. p190–210.
Jordan C. 1982. Object manipulation and tool‐use in captivepygmy chimpanzees (Pan paniscus). J Hum Evol 11:35–39.
Kano T. 1982. The social group of pygmy chimpanzees (Panpaniscus) of Wamba. Primates 23:171–188.
Kano T. 1992. The last ape: pygmy chimpanzee behavior andecology. Stanford: Stanford University Press. p 248.
Kohler W. 1927. The mentality of apes. London: Routledge &Kegan Paul. p 286.
Kyes RC. 1988. Grooming with a stone in sooty mangabeys(Cercocebus atys). Am J Primatol 16:171–175.
Lonsdorf E, Eberly L, Pusey A. 2004. Sex differences inlearning in chimpanzees. Nature 428:715–716.
Lonsdorf E, Ross S, Linick S, Milstein M, Melber T. 2009. Anexperimental, comparative investigation of tool use inchimpanzees and gorillas. Anim Behav 77:1119–1126.
Lonsdorf EV. 2005. Sex differences in the development oftermite‐fishing skills in the wild chimpanzees, Pan troglo-dytes schweinfurthii, of Gombe National Park, Tanzania.Anim Behav 70:673–683.
McGrew WC. 1979. Evolutionary implications of sex differ-ences in chimpanzee predations and tool use. In: HamburgDA, McCown ER, editors. The great apes. Menlo Park:Benjamin Cummings. p 441–463.
McGrew WC. 1992. Chimpanzee material culture. Cambridge:Cambridge University Press. p 424.
McGrew WC, Tutin CEG, Baldwin PJ. 1979. Chimpanzees,tools, and termites: cross‐cultural comparisons of Senegal,Tanzania, and Rio Muni. Man 14:185–214.
Nishida T. 1990. The chimpanzees of the Mahale Mountains:sexual and life history strategies. Tokyo: University of TokyoPress. p 328.
Pansini R, de Ruiter J. 2011. Observation of tool use andmodification for apparent hygiene purposes in a mandrill.Behav Process 88:53–55.
Phillips KA. 1998. Tool use in wild capuchin monkeys (Cebusalbifrons trinitatis). Am J Primatol 46:259–261.
Pruetz JD, Bertolani P. 2007. Savanna chimpanzees, Pantroglodytes verus, hunt with tools. Curr Biol 17:412–417.
Reynolds V. 2005. The chimpanzees of the Budongo Forest:ecology, behaviour, and conservation. Oxdord: OxfordUniversity Press. p 297.
Am. J. Primatol.
Bonobo Sex Differences in Tool Use / 925
Rodrigues MR, Lindshield SL. 2007. Scratching the surface:observations of tool use in wild spider monkeys. Am J PhysAnthropol 44:201–202.
Santos LR, Mahajan N, Barnes JL. 2005. How prosimianprimates represent tools: experiments with two lemurspecies (Eulemur fulvus and Lemur catta). J Comp Psychol119:394–403.
Santos LR, PearsonHM, SpaepenGM,Tsao F,HauserM. 2006.Probing the limits of tool competence: experiments with twonon‐tool‐using species (Cercopithecus aethiops andSaguinusoedipus). Anim Cognit 9:94–109.
Stoinski TS, Beck BB. 2001. Spontaneous tool use in captive,free‐ranging golden lion tamarins (Leontopithecus rosaliarosalia). Primates 42:319–326.
Sokal RR, Rohlf FJ. 2012. Biometry: the principles and practiceof statistics in biological research. NewYork:W. H. Freemanand Co. p 937.
Struhsaker TT. 1975. The red colobus monkey. Chicago:University of Chicago Press. p 326.
van Lawick‐Goodall J. 1970. Tool‐using in primates and othervertebrates. Adv Study Behav 3:195–249.
van Schaik CP, Fox E, Sitompul A. 1996. Manufacture and useof tools in wild Sumatran orangutans. Naturwissenschaften83:186–188.
van Schaik CP, Deaner RO, Merrill MY. 1999. The conditionsfor tool use in primates: implications for the evolution ofmaterial culture. J Hum Evol 36:719–741.
van Schaik CP, Ancrenaz M, Borgen G, et al. 2003. Orangutancultures and the evolution of material culture. Science299:102–105.
Visalberghi E. 1990. Tool use in Cebus. Folia Primatol 54:146–154.
White FJ. 1996. Comparative socioecology of Pan paniscus.In: McGrew WC, Nishida T, Marchant L, editors. Greatape societies. Cambridge: Cambridge University Press.p 29–41.
Whiten A, Goodall J, McGrewW, et al. 2001. Charting culturalvariation in chimpanzees. Behaviour 138:1481–1516.
![3 sex differences-in_bronchiolar_epithelial_injury.5[1]](https://static.documents.pub/doc/80x56/55ab96151a28abb2588b4632/3-sex-differences-inbronchiolarepithelialinjury51.jpg)
