Chimpanzee Tool Technology in the Goualougo Triangle, Republic of Congo

Journal of Human Evolution 52 (2007) 420e433

Chimpanzee tool technology in the Goualougo Triangle, Republic of Congo

Crickette M. Sanz a,*, David B. Morgan b,c

a Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany b Wildlife Conservation Society, Congo Program, B.P. 14537, Brazzaville, Republic of Congo c Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, 2001 N. Clark Street, Chicago, IL 60614, U.S.A. Received 30 April 2006; accepted 8 November 2006

Abstract

With the exception of humans, chimpanzees show the most diverse and complex tool-using repertoires of all extant species. Specific tool repertoires differ between wild chimpanzee populations, but no apparent genetic or environmental factors have emerged as definitive forces shaping variation between populations. However, identification of such patterns has likely been hindered by a lack of information from chimpanzee taxa residing in central Africa. We report our observations of the technological system of chimpanzees in the Goualougo Triangle, located in the Republic of Congo, which is the first study to compile a complete tool repertoire from the Lower Guinean subspecies of chimpanzee (Pan troglodytes troglodytes). Between 1999 and 2006, we documented the tool use of chimpanzees by direct observations, remote video monitoring, and collections of tool assemblages. We observed 22 different types of tool behavior, almost half of which were habitual (shown repeatedly by several individuals) or customary (shown by most members of at least one age-sex class). Several behaviors considered universals among chimpanzees were confirmed in this population, but we also report the first observations of known individuals using tools to perforate termite nests, puncture termite nests, pound for honey, and use leafy twigs for rain cover. Tool behavior in this chimpanzee population ranged from simple tasks to hierarchical sequences. We report three different tool sets and a high degree of tool-material selectivity for particular tasks, which are otherwise rare in wild chimpanzees. Chimpanzees in the Goualougo Triangle are shown to have one of the largest and most complex tool repertoires reported in wild chimpanzee populations. We highlight new insights from this chimpanzee population to our understanding of ape technological systems and evolutionary models of tool-using behavior. Ó 2006 Elsevier Ltd. All rights reserved.

Keywords: Chimpanzee; Pan troglodytes troglodytes; Tool use; Tool manufacture; Human evolution

Introduction van Schaik et al. (1999) attributed to differences in manual dexterity, capacity for social learning, and opportunities for Although tool use has been observed in various taxonomic social learning. Boesch and Boesch-Achermann (2000) further groups, complex and flexible tool use seems limited to the suggested that an understanding of causality between external order Primates, with humans showing extraordinary talent in objects is a key component for inventing and developing using objects to achieve their goals or change the environment. flexible tool repertoires, such as those of humans and chim- There is a great deal of variation among primate species that panzees. With the exception of humans, chimpanzees show the most diverse and complex tool-using repertoires of all extant species and are often used as models for the develop- * Corresponding author. Tel.: þ49 (0)341 35 50 243; fax: þ49 (0)341 35 50 299. ment of tool use in our common ancestors. It is essential E-mail addresses: [email protected] (C.M. Sanz), [email protected] that we have an understanding of intraspecific behavioral (D.B. Morgan). diversity in tool-using behaviors before this information is

0047-2484/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2006.11.001 C.M. Sanz, D.B. Morgan / Journal of Human Evolution 52 (2007) 420e433 421 used in comparative research or for constructing evolutionary a regional tradition of P. t. troglodytes. Chimpanzees in models. Although chimpanzee tool use has been well docu- Republic of Congo and Central African Republic use large mented at sites in western and eastern Africa, detailed clubs to open the hives of stingless bees (Fay and Carroll, information on tool-using behavior of the Lower Guinean 1994; Bermejo and Illera, 1999; Hicks et al., 2005), whereas subspecies (Pan troglodytes troglodytes) has not been avail- chimpanzees in other regions use different types of tools to able. The aim of this paper is to describe the chimpanzee access honey. Boesch and Boesch (1990) reported that chim- tool-using repertoire from the Goualougo Triangle, located panzees in the Tai Forest used tools to kill bees, inspect in the Ndoki forests of the Republic of Congo. We provide de- beehives, and fish for honey. Chimpanzees in the Bwindi tailed descriptions of each tool and compare the overall tool forests of Uganda use specific types of tools when preying repertoire to those reported from other chimpanzee sites. upon different bee species, but the diameter of these tools Field research on chimpanzees spanning the past four de- was relatively small compared to tools recovered from central cades has shown marked differences in tool technology within Africa (Stanford et al., 2000). and between populations (Goodall, 1973; McGrew, 1992; Aside from particular ecological opportunities or con- Boesch and Boesch-Achermann, 2000). Goodall (1964) first straints of some environments, it does not seem that particular documented the tool-using behavior of wild chimpanzees in habitat types have fostered or hindered tool-using dispositions Tanzania, and as reports accumulated from other sites, it in wild chimpanzees. Early models of human evolution and became clear that chimpanzee tool use was common and wide- initial documentation of tool use by chimpanzees in open spread across their range (Teleki, 1974; Boesch and Boesch, habitats promoted the idea that key human innovations were 1981; Nishida and Hiraiwa, 1982; McGrew and Rogers, driven by a transition to savanna habitats. However, recent 1983; Boesch and Boesch, 1990; Tutin et al., 1995). Tool-using geological and palaeontological data indicate that the earliest behaviors vary among populations in tool forms, materials hominids inhabited wet and wooded environments (Wolde- used, and goals of tool-using behaviors. These differences in Gabriel et al., 1994, 2001). The largest tool repertoires of tool diversity and complexity between sites are not easily at- chimpanzees are manifested by populations residing in differ- tributable to phylogenetic or ecological determinants (Boesch ent habitats, such as the rainforests of Tai in western Africa and Boesch, 1990; McGrew, 1992). One challenge to discern- and the savanna-woodlands of Gombe (Boesch and Boesch, ing patterns in the material culture of wild chimpanzees has 1990; Boesch-Achermann and Boesch, 1994). Further exami- been the distribution of field sites, which are found predomi- nation of the patterns of tool expression across ape populations nantly in western and eastern Africa. Reports on the tool reper- may provide insights for reconstructing the context of tool be- toires of the Lower Guinean and Nigerian subspecies are havior of our last common ancestor. needed to further our understanding of the tool technology of We report our observations of the technological system of chimpanzees. wild chimpanzees in the Goualougo Triangle, Republic of Several researchers have proposed regional differences in Congo. This study is the first to compile a tool repertoire chimpanzee tool technology (summarized by McGrew, from prolonged, direct observations of identified individuals 1994). In most of these scenarios, the nut cracking of west Af- representing the Lower Guinean subspecies of chimpanzee rican chimpanzees is contrasted with the technology used by that resides throughout the Congo Basin. We provide detailed P. t. troglodytes and P. t. schweinfurthii to gather social insects descriptions of use, manufacture, and modifications of each (Struhsaker and Hunkeler, 1971; Nishida, 1973; Teleki, 1974; tool type. The complete tool repertoire of this population is McGrew, 1992). However, all of these hypothesized regional compared to those from other sites to summarize our current differences in tool use have subsequently been challenged understanding of intraspecific variation in tool-using behaviors with evidence contradictory to predicted regional patterns. of wild chimpanzees. For example, Boesch et al. (1994) hypothesized that nut cracking was associated with the historical forest refugia on the Methods west side of the Sassandra River, Ivory Coast. Researchers reported that ecological conditions on the eastern side of this Study site and population natural geographic boundary could support nut-cracking (Boesch et al., 1994; McGrew et al., 1997), but the behavior The Goualougo Triangle is located within the southern sec- had not been observed beyond this river until recent reports tor of the Nouabale´-Ndoki National Park, which is located in from Cameroon (Morgan and Abwe, 2006). Although the hy- the Republic of Congo (Fig. 1). The study area covers 380 km2 pothesis of separate origins of termite fishing proposed by of evergreen and semideciduous lowland forest, with altitudes McGrew et al. (1979) has been shown to be invalid, the fact ranging between 330 and 600 m. The climate can be described remains that only chimpanzees within the Congo Basin seem as transitional between the Congo-equatorial and subequato- to use tool sets involving stout sticks and herbaceous probes rial climatic zones. Rainfall is bimodal, with a main rainy sea- to access and extract subterranean termites (Sanz et al., son from August through November and a short rainy season 2004). Further research is needed to determine if tool behavior in May. is related to the distribution of specific termite fauna or local Between February 1999 and April 2006, we spent a total of knowledge of the chimpanzees in this region. Hicks et al. 80 months in the Goualougo Triangle habituating and studying (2005) recently suggested that honey hammering may be wild chimpanzees. We conducted reconnaissance surveys in 422 C.M. Sanz, D.B. Morgan / Journal of Human Evolution 52 (2007) 420e433

Fig. 1. Location of the Nouabale´-Ndoki National Park and Goualougo Triangle study area in relation to other long-term chimpanzee study sites. several community ranges and spent more than 2,000 hours of an object (the tool), not part of the actor’s anatomical equip- observing chimpanzees. The majority of this time was spent ment and not attached to a substrate, to change the position, with the semihabituated Moto community, which consists of action, or condition of another object, either directly through 70 individuals, including immatures. In addition, we compiled the action of the tool on the object or of the object on the 63 hours of video recordings of chimpanzees visiting termite tool, or through action at a distance as in aimed throwing.’’ and ant nests in the study area between September 2003 and Objects used in play were not included in this study, with December 2005. the exception of ‘‘play start’’ and ‘‘self-tickle,’’ which have consistent actions and results. Tool making was defined as Data collection ‘‘all alterations actively accomplished on an object to modify its shape’’ (Boesch and Boesch, 1990: 94). Chimpanzee tool-using behaviors were documented by di- For all instances of tool-using behavior, we recorded the rect observation, remote video monitoring, and analysis of actor, behavior, type of object used, target of object, actions, chimpanzee tool assemblages. We adopted Parker and Gib- context and/or goal of the tool-using behavior, and the out- son’s (1977: 624e625) definition of tool use as ‘‘manipulation come. We recorded digital video of tool-using behaviors and C.M. Sanz, D.B. Morgan / Journal of Human Evolution 52 (2007) 420e433 423 collected tools whenever possible. For each tool, we recorded able-bodied members of at least one age-sex class) and habit- the location, use of the tool, materials used to make the tool, ual (observed repeatedly in several individuals) tool behaviors length, width, and any modifications. We compiled only obser- into a single category of ‘‘regular’’ tool use. In contrast, vations made by the authors for this report unless video re- ‘‘rare’’ tool use was observed in only a few individuals. cordings were available to confirm tool behaviors observed by research assistants. Tool use at termite and ant nests was also recorded with the Results aid of remote video monitoring units. Between four and eigh- teen remote monitoring/recording devices were used to Chimpanzee tool use in the Goualougo Triangle conduct surveillance at termite nests for chimpanzee visitation between 2003 and 2005. These devices consisted of a passive We observed 22 different types of tool use in the Goua- infrared motion sensor, a computer program developed for this lougo Triangle chimpanzee population (Table 1). Nine of these study (CHIMPCAM 1.0 and 2.0, Wildland Security), and a dig- tools were used by chimpanzees on a regular basis, which ital video recorder (SONY DCR-HC30). Immediately after the means that they were used by all members of at least one infrared sensor was triggered by animal movements, the com- age-sex class or repeatedly in several individuals. Regular puter program activated a digital video camera to record for tool use included extraction (ant dip, termite fish, leaf sponge), two minutes. If the sensor detected another movement within perforating (puncture termite nest, perforate termite nest), the two minutes of recording, the camera was immediately re- pounding (beehive pound), and display (aimed throw) behav- activated for another two minutes. This sequence was repeated iors. These customary or habitual tool behaviors were often until no motion was detected, at which point the recorder associated with food resources that occurred at specific local- would power down. ities, such as termite nests, ant nests, beehives, or water basins. Although some tools had similar overall goals, tool forms and Data analysis actions clearly differentiated each tool behavior. Less frequently observed tool behaviors were more likely to occur Data are presented using both a descriptive ethnographic instantaneously in response to specific situations, such as in- method based on Lemonnier’s (1992) ‘‘operational sequence’’ vestigating an object with a probe, wiping semen or feces and analytic comparative method following the coding of from oneself, whisking flies, or dabbing a fresh wound. Whiten et al. (1999, 2001). These data were compiled into All tools used by chimpanzees in the Goualougo Triangle tool-activity categories adopted from Boesch and Boesch were manufactured from perishable materials, including (1990). We further refine and define these categories as follows: leaves, herbs, lianes, twigs, sticks, and branches. Most tools were manufactured from suitable vegetation that was within arm’s reach of the chimpanzee, but three types of tools were Extract gathering an item or fluid with a tool for the fashioned from specific herb or tree species. Ninety-eight purpose of extracting it from a location that percent of sticks used to puncture subterranean termite nests is difficult to access manually. were made from Thomandersia hensii, which is very straight Probe use of tool to indirectly contact another and rigid with a uniform diameter, smooth stalk surface, and object or to inspect an area. few side branches. Although this is one of the most common Wipe leaf is used to swab body or wipe object to tree species in the study area, it is not always located in close remove another object or substance. proximity to the tool use site. By retracing the travel path of Whisk use of tool to displace another object from chimpanzees, we were often able to pinpoint the location environment. where raw materials had been gathered, which indicated that Scoop, hook tool is used to bring a distant item within the specific plants had been selected and transported to tool reach of the tool user. use sites. Several Thomandersia trees that were sources of Social object is used in social interaction (such as puncturing-stick materials were tens of meters from the ter- affiliation, display). mite nest, not visible from the tool-using location, and visited Pound percussion of tool onto another object or by chimpanzees on several occasions for gathering tool- substrate. making materials. Ninety-six percent of termite-fishing probes Perforate tool is used to open or gain access to interior were fashioned from Sarcophyrnium spp., with the remaining of an object. 4% from Haumania danckelmaniana, Ataenidia conferta, Meg- Cover, barrier object is placed so as to cover or shield body aphrynium sp., and other unidentified herbs. Preferred species from elements or injury. were characterized by sufficient stalk length, appropriate diam- Scratch, rub self rub or scratch object on self for grooming or eter, smooth surface, stalk flexibility, and fibers that fray into stimulation. a durable brush. We identified eight herb species at the study site that could function as fishing probes, and have confirmed Prevalence of tool-using behaviors was based upon occur- that their abundance is not correlated with use as raw materials rence categories defined by Whiten et al. (2001: 1488). (unpublished data). The majority of herbaceous ant-dipping However, we combined customary (observed in all or most tools were fashioned selectively from Sarcophrynium spp. or 424 C.M. Sanz, D.B. Morgan / Journal of Human Evolution 52 (2007) 420e433

Table 1 Tool behaviors observed in the Goualougo Triangle, Republic of Congo Tool use Target Tool material Tool length (range) Tool diameter (range) Termite ﬁsh n ¼ 273a Termites Herbb (n ¼ 852) 43.1 12.9 cm (11e104) 4.5 1.3 mm (1e11) Termite-nest perforating n ¼ 29 Termites Twig (n ¼ 54) 32.9 19.4 cm (5e91) 5.9 1.4 mm (3e9) Termite-nest puncturing n ¼ 96 Termites Stickb (n ¼ 332) 40.6 14.2 cm (11e95) 9.6 2.3 mm (1e18) Beehive pounding n ¼ 32 Honey Branch (n ¼ 27) 62.6 22.4 cm (25e107) 27.7 7.3 mm (18e45) Fluid dip n ¼ 7 Honey, water Twig (n ¼ 2) 43.2, 44.7 cm 6, 13 mm Lever open n ¼ 3 Honey Branch (n ¼ 1) 83.2 cm 20.2 mm Ant dip n ¼ 4 Ants Herbb (n ¼ 206) 63.6 17.6 cm 5.6 1.4 mm Twigb (n ¼ 61) 95.8 31.8 cm 7.5 1.9 mm Investigatory probe n ¼ 3 Other Twig, stick (n ¼ 2) 29.5, 78.8 cm 17, 11 mm Leaf sponge n ¼ 27 Water Leaves Marrow pick n ¼ 1 Marrow Twig segment Nut extraction n ¼ 2 Nuts, seeds Twig segment Rain cover n ¼ 6 Self Leafy twigs Leaf napkin n ¼ 4 Self Leaves Leaf dab n ¼ 1 Self Leaf Seat vegetation n ¼ 3 Self Leaves, twigs Comb n ¼ 1 Self Twig segment Self-tickle n ¼ 2 Self Fruit, seed pod Seat stick n ¼ 1 Self Twig Aimed throw n ¼ 5 Social Fruit, branch Branch drag n ¼ 2 Social Branch Play start with object n ¼ 3 Social Twig a Number of observations. b Includes only tools collected between December 2001 and February 2004.

Megaphrynium sp. stalks, which have a longer stalk length than chimpanzee sat and pulled the tool while using her foot to other herb species in the study area. break it in the middle section. McGrew and Collins (1985) Details of tool manufacture and modification are shown in reported that termite-fishing probes were occasionally stripped Table 2. Eleven types of tools were modified at least once, of bark, but there was only one indication of intentional bark- seven tools were modified twice, three tools were modified stripping in this study. We also observed a behavior similar to three times, and two tools were modified four or more times. what McGrew and Collins (1985) described as ‘‘stripping of The most common modifications involved cutting the length sedges,’’ but we prefer to describe the behavior in Goualougo of the tool with hands/mouth or shaping the tool by removing as ‘‘lengthwise splitting of herbs,’’ which involves pulling the extraneous parts. We observed a tool modification in the Goua- fibers of the tool apart so that the herb is split along its length. lougo Triangledthe brush tip modification to termite-fishing This reduces the diameter and increases the flexibility of a probesdthat was not previously documented at other long- termite-fishing probe. term study sites. Chimpanzees in this population intentionally We observed three different types of serial tool use in the premodified the end of herbaceous termite-fishing probes into Goualougo population, which is otherwise rare in wild chim- a brush, which aids in extraction of prey from their earthen panzee tool repertoires (Sugiyama, 1997). Two tool sets nests (Sanz et al., 2004). We observed almost every type of were regularly used to extract termites from their nests. At el- tool manufacture that has been reported from Tai, including evated nests, a perforating twig was first used to open a sealed detachment from a substrate, cutting to a specific length, re- termite exit hole on the surface of a nest, followed by the use moving leaves or bark, sharpening the end of a tool, modifying of a fishing probe to extract termites from the nest. A different length with teeth or hands, and breaking by pulling while tool set was used to extract termites from subterranean nests. standing on branch (Boesch and Boesch, 1990: 94). We did A puncturing stick was first used to create a canal into the cav- not observe breaking a tool by hitting it against a hard surface, ity of the termite nest, which was followed by the use of a fish- which is a modification directed towards nut-cracking tools ing probe to extract prey from the nest. These are the first (Boesch and Boesch, 1990). We observed a tool behavior serial tool-using behaviors that have been confirmed to be cus- equivalent to ‘‘pulling while standing on it’’ when a female tomary in a wild chimpanzee population (Sanz et al., 2004). C.M. Sanz, D.B. Morgan / Journal of Human Evolution 52 (2007) 420e433 425

Table 2 Details of tool manufacturing and modifications by chimpanzees in the Goualougo Triangle, Republic of Congo Tool Material selectivity Manufacture and modifications Tool reuse Cutting Shaping Termite-fishing probe Sarcophrynium spp. (96%) Clip with hands/mouth; Remove end leaf; Carried between Ataenidia conferta shorten length fabricate brush tip; nests Haumania danckelmaniana split tool lengthwise Megaphrynium sp. Termite-nest puncturing stick Thomandersia hensii (98%) Clip with hands/mouth Remove vegetation; Used on subsequent sharpen end nest visits; shared among individuals Termite-nest perforating twig Not selective Clip with hands/mouth Remove vegetation; sharpen end Ant-dipping rod/wand Sarcophrynium spp. (62%) Uproot stem from stand; Remove leaf; Megaphrynium sp. (6%) clip root from end remove frayed end Beehive-pounding club Not selective Remove vegetation; break with feet Fluid-dip stick Not selective Remove vegetation Lever-open stick Not selective Shorten length Remove vegetation Marrow pick Not selective Shorten length Remove vegetation Nut-extraction tool Not selective Shorten length Remove vegetation Leaf sponge Not selective Chew leaves Investigatory probe Not selective Remove vegetation

We also observed chimpanzees using several tools to access into the hive to extract honey. The tool set used in honey ex- honey from beehives, similar to observations by Bermejo traction seemed to be ﬂexible. The chimpanzee may create and Illera (1999) and Brewer and McGrew (1990). Chimpan- a large enough access hole by pounding to extract pieces of zees in the Goualougo Triangle were observed to use a pound- comb manually or to use their hands to dip for honey, which ing stick, which is a stout branch used to break open the does not necessitate a second or third tool. They may pound entrance of a bee hive, followed by a lever-open tool, which open a hive and use a lever-open tool to widen the hole or consists of a smaller twig used to widen the entrance to the a ﬂuid dip stick to extract honey (Fig. 2a,b). Or, they may hive; on two occasions, a dip-stick tool was then inserted use all three tools in succession.

Fig. 2. Use of a tool set to extract honey from a hive of stingless bees (Meliponini) on the underside of a large branch in the forest canopy. The chimpanzee (Dorothy) ﬁrst used a pounding club to open the entrance of the beehive (a). She repeatedly pounded the hive entrance with this large branch and then manufactured a second pounding tool. Between pounding bouts, Dorothy modiﬁed the length and shape of the second pounding tool by pulling on either end of the tool with her hands while using her foot to break it in the middle section. One of the pounding tools was placed in the forest canopy and another was dropped to the ground. After successfully opening the hive entrance, she used a dip stick to extract honey from the hive (b). Note that she held onto the main branch or twigs for support with her right hand, while manipulating the tools in her left hand. Photos courtesy of I. Nichols and the National Geographic Society (all rights reserved). 426 C.M. Sanz, D.B. Morgan / Journal of Human Evolution 52 (2007) 420e433

Specific tool behaviors straighten the fibers. This brush straightening was performed almost every time that the tool was inserted into the nest. Ant dip. Although tool traces have been recovered from ant The probe was withdrawn from the nest in one swift motion, nests at Lope´ Reserve in Gabon (Tutin et al., 1995) and the sometimes with the tool stalk resting on the opposite arm Ngotto Forest in Central African Republic (Hicks et al., for support. Termites were gathered into the chimpanzee’s 2005), this is the first study within the range of P. t. troglodytes mouth using either the pull-through or direct-mouthing to confirm tool use in ant dipping from direct observation. technique. Chimpanzees in the Goualougo Triangle used ant-dipping As mentioned previously, specific herbs were selected for probes made from herbaceous stems and twig tools made from the manufacture of termite-fishing probes. They were most small saplings to gather driver ants (Dorylus spp.). Tools were often clipped from the stand of herbs, rather than uprooted, inserted into the nest cavities or laid across the path of ants as which is the case for ant dipping. Termite-fishing probes they traveled. The chimpanzees ate the ants either directly may undergo several modifications before they are ready from the end of the tool (ant-dip-single or direct-mouthing) or for use. These may include removing the end leaf, fabricat- pulled the stem through their hand to sweep the ants into their ing the brush tip, shortening the length of the stem by clip- mouth (ant-dip-wipe or pull-through) (Whiten et al., 1999, ping off a short segment, or splitting the tool lengthwise to 2001; Humle and Matsuzawa, 2002; Yamakoshi and Myowa- reduce the diameter. Chimpanzees sometimes conserved Yamakoshi, 2004). Similar to reports from other sites, chimpan- these tools by carrying them between termite nests on the zees sat perched above the ant nest on bent saplings to access the same day. ants without being attacked. We determined that ant dipping was Termite-nest perforate. The Goualougo chimpanzee popula- customary based on ant remains in the fecal matter of identified tion is the first to be observed using two tools serially to access individuals and the abundance of tools collected at ant nests and extract prey from elevated termite nests (Sanz et al., throughout the study site. Presence of ants in feces does not in- 2004). Chimpanzees used a perforating twig to open the exit dicate how prey was obtained, but our direct observations and holes on the surface of a nest and then inserted a fishing probe remote video recordings confirmed that chimpanzees were us- to extract termites. Often after unsuccessfully attempting to ing tools to gather ants. open termite exit holes manually, chimpanzees manufactured The herbaceous ant-dipping tools were most commonly a perforating tool to open these holes. Tools were held be- manufactured from either Megaphrynium sp. or Sarcophry- tween the thumb and lateral side of the index finger, or be- nium spp. These herbs were also used as materials for termite- tween the index and middle fingers. The tip of the tool was fishing tools, but ant-dipping tools were significantly longer pressed into the surface of the nest and sometimes moved in than termite-fishing probes. Tools were often gathered for a circular motion until the exit hole had been cleared. The ant dipping by uprooting the entire stem, and thus it was com- chimpanzee then inserted a fishing probe into the cavities of mon to recover tools with roots intact at the unused end. This the nest to extract termites. The form of these tools varied was a distinction from termite-fishing tools, which were often from small, straight twig segments only a few centimeters clipped near the base within the herb stand. The broad leaf of long to large, unwieldy branches with several leafy twigs at- this stem was almost always removed before ant dipping. tached. Some chimpanzees premodified the tool by clipping These tools often have frayed ends, but we have not deter- the length and removing leafy material, while others left the mined if this is a premodification by the chimpanzees or tool unmodified. The ends of these tools were often slightly a by-product of removing ants from the end of the tool. The frayed (up to 2 cm) from the motions of pressing the stick other tool form consisted of a sapling, which had been broken into the exit hole and removing soil from the canal. We also at its base, 6e8 cm from the ground. Only one end of the twig observed chimpanzees intentionally sharpening the end of is used, with leafy vegetation often left intact on the other end. the tool by removing a part of the tool tip. In contrast to ter- Termite fish. Sanz et al. (2004) provide detailed descrip- mite-nest-puncturing sticks, perforating twigs were made tions of chimpanzees using fishing probes to extract termites from any suitable materials that were in close proximity to (Macrotermes spp.) from elevated and subterranean nests in the termite nest, regardless of species. the Goualougo Triangle. Previous reports described tool Although both perforating and puncturing tools were used assemblages recovered from termite nests and fleeting obser- to gain access to termites in their earthen nests, the forms vations (Muroyama, 1991; Fay and Carroll, 1994; Suzuki and functions of these tools were very distinct. Perforating et al., 1995; Bermejo and Illera, 1999), but ours was the first twigs were of variable form and made from any available study to describe this behavior from repeated observations of materials, whereas puncturing sticks were uniform and tool known individuals (Sanz et al., 2004). After taking a stem materials were specifically selected for this task. The tip of from the herb stand, the chimpanzee removed the leaf from perforating twigs were used to press or pick open a few centi- the distal end of the stem with his/her mouth. An end of the meters of soil, which seal existing termite exit passages on the tool was then pulled horizontally through partially clenched surface of an elevated termite nest. Puncturing sticks were teeth several times to fray the end of the herb into a brush held with a power grip by both hands and often a foot to tip. There was a specific technique for inserting the brush-tip push almost the entire length of the tool into the soil above tool into the termite nestdthe brush tip was wetted with saliva a subterranean termite nest, which may be approximately and then quickly pulled through the hands or mouth to 10e40 cm deep. C.M. Sanz, D.B. Morgan / Journal of Human Evolution 52 (2007) 420e433 427

Termite-nest puncture. Although assemblages of puncturing entrances, which may be located up to 30 m high. We also (also referred to as dig or perforate by Whiten et al., 2001) found tool assemblages at beehives located in natural tree tools had been recovered for more than twenty years at several falls. Once the hive was opened by pounding, the chimpanzee sites across central Africa (Sabater Pi, 1974; Sugiyama, 1985; reached into the hive to access the honey. We also observed Muroyama, 1991; Fay and Carroll, 1994; Suzuki et al., 1995; them to then use a lever open tool to widen the hive entrance Bermejo and Illera, 1999), this site is the first to provide full or a dip stick to extract honey (Fig. 2b). In some cases, all descriptions of puncturing tools being used to create access three tools were used sequentially to access honey. channels for fishing probes into subterranean termite nests Pounding tools were often placed on branches in the can- (Sanz et al., 2004). After having located a suitable digging opy or held in their feet between pounding bouts when the trench, the chimpanzee raked away the surface debris with chimpanzee rested or inspected the hive entrance visually or one hand. The chimpanzee then pointed the end of the digging manually. Chimpanzees held, sat on, or repeatedly reposi- stick at the location that had been cleared of leaves and began tioned the tool so it did not fall to the ground. Even after to push the stick tool into the ground with both hands grasping they finished attempting to open the hive or eating the honey, the midsection of the tool. They often used one foot to grasp the the pounding tool was often left in the canopy rather than base of the tool while their body weight was shifted over the dropped to the ground. One or both ends of the tool were tool to press it further into the ground. The chimpanzee then used to pound the hive. removed the tool and smelled the tip of the stick, which may Lever open. Goodall (1986) reported that chimpanzees used have pierced a termite-nest cavity. If a termite nest was hit tools to enlarge entrances to insect or bird nests. We observed by the puncturing stick, then the chimpanzee began to fish by chimpanzees use lever-open tools to widen hive entrances to inserting a fishing probe into the canal that was created by access honey. They inserted the end of the stick into the bee- the puncturing stick. If not, the puncturing process was hive and rapidly moved it side to side to widen the nest en- repeated. trance. After the entrance was widened, the chimpanzee Puncturing sticks were completely straight, smooth sticks either reached into the hive with their hand or used a dip stick that had a constant diameter along their entire length. Chim- to extract the honey. Lever-open tools were medium-sized panzees manufactured puncturing sticks almost exclusively twig tools, often with secondary vegetation removed. This from Thomandersia hensii. It is important to note that this tool was often made after the entrance of a hive had been tree species was not always available at the termite nest, and cracked or broken from pounding (see beehive pounding). chimpanzees traveled significant distances to gather appropri- The chimpanzee stopped pounding, traveled into the adjacent ate tool materials. Tool preparation required several modifica- canopy, gathered a small stick, removed the side and end tions to the raw vegetative materials, which may include twigs, and then inserted it into the hive entrance. The action clipping the length, removing vegetation, or sharpening the associated with this tool use was a powerful back-and-forth point of the tool. As had been suspected from tool assem- motion, using the side of the tool to widen the entrance into blages, we confirmed that chimpanzees reused puncturing the hive. In contrast to honey-pounding tools, we did not ob- sticks during 69% of visits recorded by remote video units. serve any conservation of these tools by a chimpanzee placing Beehive pound. We made repeated observations of known them in the canopy or holding them between pounding bouts. individuals using stout branches to break open the entrance Although relatively few direct observations of this tool behav- of beehives (African honey bee, Apis sp.; Stingless bees, ior have been made by the authors, assistants have observed Meliponula spp.) to gain access to honey. Honey-pounding, the behavior and encountered assemblages at beehives, indi- or ‘‘honey hammering,’’ tools have previously been recovered cating that lever-opening is common in this population. There in the Ngotto Forest (Hicks et al., 2005), and brief observa- have been previous reports of chimpanzees using tools as le- tions have been made at Bai Hokou and Ndakan (Fay and vers, bodkins, or chisels to open beehives (Brewer and Carroll, 1994), which are all located in Central African McGrew, 1990; Tutin et al., 1995; Bermejo and Illera, 1999). Republic. Serial tool use in honey gathering has been observed Aimed throw. Similar to past reports, chimpanzees in the in Republic of Congo by Bermejo and Illera (1999). Goualougo Triangle have been observed to throw various Chimpanzees in the Goualougo Triangle used relatively objects toward a target (Goodall, 1964). Intention of aim is in- large tools to open beehives. These tools had a diameter of ferred by an individual orienting toward a specific target while up to 45 mm, a length of 25e107 cm, and a weight of up to grasping and throwing an object. Although the initial swing of 1 kg (small tool ¼ 70 g, medium tool ¼ 195 g, large tool ¼ the arm was toward the target, the throw was often inaccurate. 875 g). There did not seem to be a preference for certain We have observed both overhand and underhand throwing in raw materials, and we observed that tool manufacture often this chimpanzee population. The active swinging of the arm occurred in trees adjacent to the beehive. Manufactured tools differentiates this behavior from dropping, pushing, or kicking were carried for up to 30 minutes while foraging for other down objects from the forest canopy. food items before the tool was actually used to pound Leaf sponge. Leaf-sponging to gather water from tree ba- a beehive. The tool action involved repeatedly pounding the sins is considered a universal chimpanzee behavior (Whiten end of the stick against the entrance of the hive, as shown in et al., 1999, 2001), and we confirmed its presence at this Fig. 2a. Chimpanzees suspended themselves at precarious site. A chimpanzee gathered fresh leaves and placed them in angles in the forest canopy to deliver forceful blows to hive his/her mouth. We estimated that between 2 to 5 leaves of 428 C.M. Sanz, D.B. Morgan / Journal of Human Evolution 52 (2007) 420e433 medium size were necessary for effective sponging. Chimpan- them across his penis to collect remaining ejaculate. Material zees gathered these leaves from vegetation that was near the on leaves may or may not be inspected. Leaves were discarded water source without preference for particular plant species. after a single use. Leaves were placed in the chimpanzee’s mouth and chewed Branch drag. It is a universal chimpanzee behavior to drag to make a mass that was then transferred to the hand. The branches as an enhancement to threat displays (Whiten et al., chimpanzees dipped the leafy mass into a tree basin of water. 1999, 2001). The broken end of a detached branch was The chewed leaves functioned as a sponge in absorbing water grasped with one hand and dragged along the ground. in the recessed basin. The soggy leaf mass was then trans- Seat vegetation. Hirata et al. (1998) first reported chimpan- ferred to the mouth and the fluid sucked or squeezed from zees placing vegetation under themselves when sitting. Chim- the leaves. panzees picked large leaves, detached twigs, or bent down Marrow pick. While consuming duiker meat, we observed twigs to cover a substrate and then sat on the vegetation. a chimpanzee using a small twig segment as a pick to extract Seat stick. Vegetation may also be used to protect oneself marrow from bones. This is similar to marrow-pick tools used from a thorny substrate such as branches of Ceiba pentandra by chimpanzees in the Tai Forest, Ivory Coast (Boesch and (Alp, 1997). This was observed in canopies of trees with Boesch, 1990). thorny branches, where chimpanzees arranged vegetation so Fluid dip. Twigs may be used to dip honey from beehives or as to protect themselves from sitting directly on thorns. water from tree hollows (Boesch and Boesch, 1990). Chim- Comb. We observed a chimpanzee using a small twig to panzees inserted a stick into the nest cavity or tree hollow, comb through his hair while self-grooming. The end of a small extracted the probe, and then licked or sucked the fluid from detached twig segment was brushed horizontally across the the stick. An example of honey dipping is shown in Fig. 2b. hair. The twig was pushed slowly over a specific area, and These wooden tools are often straight or slightly bent branches the chimpanzee inspected the exposed skin with his lips and or twigs. Chimpanzees often removed the leafy side-branches fingers of the other hand. Use of an object as a comb has from the tool. One or both ends of the tool were used for dip- been reported by Whiten et al. (2001). ping. Dipping for honey often resulted in a somewhat blunted Play start. Goodall (1986) reported that chimpanzees may end with resin in the wood fibers. The fluid-dip stick may be use objects to initiate or maintain play with another individual. the second or third tool used in a tool set to extract honey. They detached a small twig and held it in their mouth or hand Investigatory probe. Stick or twig probes may be used to in- while approaching or retreating from a playmate. spect items or inaccessible areas (Goodall, 1968). The probe Self-tickle. Objects may also be used to tickle oneself was unimanually held and oriented toward the object or area (Goodall, 1986). Chimpanzees rubbed an object against the of interest. The end of the tool was used to prod the item of body (neck, groin, or inner thigh), which evoked a response interest or inserted into the recessed area. The end was re- similar to being tickled by another individual. tracted or removed and then visually inspected and/or smelled. Nut extraction. Chimpanzees sometimes used a small twig Comparing tool behaviors between study sites segment to dislodge seeds from within the thick pods of Eribroma oblongum. Similar tool behavior was frequently There was a wide range of tool behaviors between chimpan- observed in Tai chimpanzees extracting Detarium seeds and zee study sites, which showed repertoires ranging from six to in certain populations of orangutans when feeding on Neesia 22 tool behaviors (Fig. 3). Goualougo had one of the largest fruits (Boesch and Boesch, 1990; van Schaik et al., 2003). tool repertoires with 22 different types of tools, but less than Leaf dab. Detached leaves were held unimanually and half of these were used on a regular basis. Tai and Gombe gently touched to a wound surface, similar to descriptions in showed similar levels of tool diversity with more than 20 types Whiten et al. (2001). The surface of the leaves that touched of tools, but more regular tool behaviors. This is in contrast to the wound was examined by the chimpanzee. Leaves were Assirik, Lope´, Budongo, and Kibale, which have less than ten then discarded. tools total and five tools that are used on a regular basis. In Rain cover. Detached leafy twigs were used as a rain cover. contrast to the expectation that tool diversity would be corre- Chimpanzees detached twigs and placed them directly over lated with observation time, we found that study duration for their back/shoulders during heavy rains. Twigs were placed the ten chimpanzee study sites was not correlated with either in direct contact with the chimpanzee’s body, rather than being the total number of tools or the number of regularly used used as a shelter or umbrella. One or more twigs were used tools in the tool repertoires (PearsonAll tools ¼ 0.51, p ¼ 0.134; and repositioned during the rain. This behavior has not been PearsonRegularly used tools ¼ 0.63, p ¼ 0.053). observed in any other population of Pan troglodytes, but bono- The tool repertoire of wild chimpanzees was expressed in bos (Pan paniscus) have been observed to use leafy twigs in a variety of behavioral contexts (Table 3). Fifty-three percent a similar manner and also to cover their nests (Kano, 1982). of tool behaviors shown by all wild chimpanzee populations Leaf napkin. Chimpanzees used leaves to wipe substances were directed towards food gathering. Tools were most often from their bodies, similar to behavior reported by Goodall used in gathering otherwise inaccessible items, such as nuts, (1964). Leaves were used to wipe feces or urine from hair insects, bone marrow, honey, and water. Tools were also or skin, or fruit pulp from hands or other body parts. Immedi- used by several populations in self-care [e.g., grooming and ately after copulation, a male may detach leaves and wipe comfort (32%)] and social contexts [e.g., display and play C.M. Sanz, D.B. Morgan / Journal of Human Evolution 52 (2007) 420e433 429

All Observed Tool Use 20 Customary/Habitual Tool Use

10 Tool Behaviors

0 Goualougo Tai Gombe Bossou Mahale-M Mahale-K Kibale Budongo Assirik Lope (P.t.t.) (P.t.v.) (P.t.s.) (P.t.v.) (P.t.s.) (P.t.s.) (P.t.s.) (P.t.s.) (P.t.v.) (P.t.t.) Chimpanzee Study Sites

Fig. 3. Comparison of tool diversity between chimpanzee study sites. The size of the complete tool-using repertoire, including rarely used tools, is compared to tool behaviors that are regularly observed in these populations. Abbreviations: P.t.s. ¼ Pan troglodytes schweinfurthii, P.t.t. ¼ P. t. troglodytes, P.t.v. ¼ P. t. verus.

(14%)]. In the Goualougo Triangle, 50% of chimpanzee tool populations. This relatively young study site ranks as one of behaviors occurred in a feeding context. Tools used in foraging the highest among chimpanzee study sites in overall repertoire were most often aimed toward gathering social insects and size and number of regularly used tools. Several behaviors honey. Four tool types (18%) were used in self-grooming or considered universals among chimpanzee populations were stimulation, but none of these tools were used on a regular ba- confirmed to occur in this population, but we also identified sis. Three tool behaviors (14%) were used to cover or protect several new tool-using behaviors and described behaviors the body from the elements or injury, which were also ob- that were previously known only from indirect evidence or served rarely in the Goualougo chimpanzee population. Three limited observations. From this site, we have reported the first tools (14%) were used in social interactionsdtwo in aggres- direct observations of identified individuals using tools to sive contexts and one in play initiation. One tool was used perforate or puncture termite nests, pound for honey, and use in an exploratory context. Across all study sites, most chim- leafy twigs for rain cover. The material culture of the Goua- panzee tool behaviors were extractive, which was followed lougo chimpanzee population was used to exploit food re- in frequency by tools used in social activities (Table 4). All sources, enhance their social interactions, clean and protect studied chimpanzee populations showed at least one type of their bodies, and investigate their environment. Tool actions tool used for extraction or social activities. Many populations ranged from simple tasks to hierarchical sequences, often also exhibited a type of wiping, but this was only habitual or involving tool manufacture and several tool modifications. customary at a few sites. This is in contrast to probing, perfo- This initial report of the tool repertoire of chimpanzees in rating, and pounding, which were less consistent across sites. the Goualougo Triangle not only enhances our knowledge of Comparison of specific tool-using behaviors across study the tool-using behavior of the Lower Guinean subspecies, sites did not confirm any previously posited regional hypothe- but also contributes to our understanding of tool diversity in ses of tool use or yield any new regional trends. There was not this species. a single tool use behavior that was shown exclusively by all Almost half of the tools in the repertoire of the Goualougo the populations representing a particular subspecies. Prior to chimpanzees were exhibited on a habitual or customary basis, recent findings from Cameroon, nut hammer was the closest which means that these tool behaviors were observed in most candidate (Boesch et al., 1994; Morgan and Abwe, 2006). members of at least one age-sex class. Most regular tool Tool sets used to extract subterranean termites may be unique behaviors were food-directed, with the exception of aimed to chimpanzees in western equatorial Africa, but it has not throwing, which occurs in a social context. Tools used in feed- been determined if this behavior is elicited by particular ing were often directed at food items that were difficult to termite species or climatic factors in this region. Similarly, obtain manually, such as gathering social insects or opening assessment of regional patterns in honey pounding (or beehives to extract honey. Tool use was an important aspect hammering) awaits further information on its distribution of the feeding ecology of these chimpanzees, as demonstrated and underlying ecological conditions. by the significant proportion of tool use that was customary or habitual. Further, the regularity and diversity in these tool- Discussion using skills indicates that chimpanzees were aware of objects in their environment and have the skills to manipulate them. Chimpanzees of the Goualougo Triangle have one of the Rarely observed tool-using behaviors seemed to arise in re- largest and most diverse tool kits among studied ape sponse to a particular stimulus, such as the immediate need 430 C.M. Sanz, D.B. Morgan / Journal of Human Evolution 52 (2007) 420e433

Table 3 Comparison of specific tool-using behaviors across chimpanzee study sites (comparative data are from Whiten et al., 1999, 2001) Context Tool use P. t. verus P. t. troglodytes P. t. schweinfurthii Tai Bossou Assirik Goualougo Lope´ Gombe MahaleM MahaleK Kibale Budongo Feeding Algae scoop þþ ?? ? Ant dip, single þþ þþ þþ þ Ant dip, wipe þ þþ þþ þþ Ant fish þ þþ ? þþ þ þþ þþ Bee probe þþ ?? ? þ Branch hook þ ?? ? Dig þ ? Expel/stir þþ ?? ?þþ þþ þþ Fluid dip þþ þþ þ þþ þþ þþ þþ þþ Insect pound þ ?? ? Leaf sponge þþ þþ ? þþ þ þþ þ þþ þþ Leaf wipe þ ?? ?þ Leaf brush ?? ?þ Leaf mop ?? ?þ þ Lever open þþ ? þþ þþ þþ Marrow pick þþ ? þ ? Nut-extraction toola þþ ??þ ?? ? ? ? ? Nut hammer þþ þþ Perforate termite nest ? þþ Pestle pound þþ Pound beehive þþ Puncture termite nest ? þþ Resin pound þ ?? ? Sponge push-pull þþ ?? ?þþ Termite fish þ þþ þþ þþ þþ Self-groom, stimulate Comb ? þ ? þ Leaf dab þ ? þ ? þ þþ Leaf napkin þ þ þ ? þþ þ þþ þþ Nasal probe ?? ?þ Self-tickle ? þ ? þþ Comfort, protection Fly whisk þþ ?? ?þ þþ Rain cover ? þ ? Seat vegetation þþ þ ? þþ Seat stick ? þ ? Social Aimed throw þþ þþ þ þþ ? þþ þþ þ þ Branch drag þþ þþ ? þþþþþþþþþþþþþ Club þþ þ ?? ?þþ þ Leaf clip þþ þþ ?? þþ þþ þþ þþ Play start þþ þ þ þ þþ þþ þþ þþ þþ þþ Other Investigatory Probe þþ þþ ? þ ? þþ þþ þþ þ ? Anvil prop þþ ? Container ?? ?þ Notes: þ¼rare, þþ ¼ regular, ¼absent, ? ¼ insufficient observations; MahaleM ¼ Mahale M Community, MahaleK ¼ Mahale K Community, aNut-extraction tools were described by Boesch and Boesch (1990), but their prevalence at other sites was not addressed by Whiten et al. (1999, 2001). to wipe the body or swat at insects. This indicates that chim- to the types of modifications shown by chimpanzees at other panzees recognize even rare situations that can be tool- sites, chimpanzees in the Goualougo Triangle showed a tool mediated and readily generalized tool use to new settings. modification that has not previously been reported from other We observed chimpanzees in the Goualougo Triangle study sites. They manufactured fishing probes with brush manufacturing 12 different types of tools. In contrast to pas- stems by fraying the end of the tool with their teeth before sive modification through use, these were active alterations use. In the authors’ experiences with termite fishing, this to modify the shape of the object (Table 2). Several different brush-tip modification increased the number of termites ex- tools were modified between one to four times. In addition tracted by up to ten times that of an unmodified termite-fishing C.M. Sanz, D.B. Morgan / Journal of Human Evolution 52 (2007) 420e433 431 probe. Unmodified stems of other herb species can be used to for different tool tasks. When gathering herb stems for termite gather termites from their earthen nests, but the brush-tip mod- fishing, the chimpanzees often clipped them a few centimeters ification seems to be a technological enhancement adopted by from the ground with the hands or mouth. The same species chimpanzees in this region (Suzuki et al., 1995; Sanz et al., were gathered for ant dipping by pulling up the entire stem 2004). and root. This change in treatment of the raw materials allows Our results support Boesch and Boesch’s (1990) assertion the same herb species to be prepared for either termite-fishing that reuse occurs most often for tools that require specific or ant-dipping applications. Chimpanzees occasionally used materials and modifications. Chimpanzees in the Goualougo the same tool for both tasks, which demonstrates an under- Triangle showed a high degree of material selectivity for three standing of tool generalization. particular tool types and reuse of tools in two of these tasks We documented three different types of sequential tool use (Table 2). Chimpanzees reused wooden puncturing sticks in the Goualougo Triangle. Two tools sets were used to extract during more than half of their visits to subterranean termite termites from their nests (perforating and termite fishing; nests. Visitation to a termite nest that has a store of puncturing puncturing and termite fishing) on a regular basis in this pop- tools supports the notion of a tool cache, i.e., a location where ulation. We also observed chimpanzees using another tool set specific tools that are difficult to procure may be reused during to access honey from beehives (honey pound, lever open, and/ subsequent visits. This is thought to reduce the energetic costs or honey dip). Due to the prevalence and standardization associated with searching for raw materials and manufacturing across several communities, it seems unlikely that such se- new tools (Potts, 1984). When chimpanzees in the Goualougo quences were singularly innovated. Although this study did Triangle brought new puncturing tools to the subterranean ter- not investigate specific learning processes, it was apparent mite nests, they often arrived carrying both a stick tool for that tool acquisition was facilitated by tool sharing of mothers puncturing the nest and an herb stem for termite extraction with their infants, attention to the tool use of another individ- tools. We also observed that termite-fishing probes may be ual, and sequential structuring of skills. It is also interesting to conserved and transported between nests within a single day. note that two customary and complex tool sequences in wild To fabricate a fishing probe, chimpanzees must locate the chimpanzees occurred at fixed locations where resources are appropriate herb species and then may perform several modi- exploited, termite nests in Goualougo and nut-cracking centers fications to prepare the tool for use. Marantaceae is the dom- in Tai Forest. We have subsequently documented that social inant undergrowth in this forest, but the particular species networks differed between tool tasks, which could affect selected by chimpanzees for termite fishing and ant dipping success in transmitting relevant tool information between are not the most abundant herbs (Sanz et al., unpublished individuals. An increase in foraging efficiency as a result of data). The chimpanzees in Goualougo showed awareness for tool-using centers, where specific information is learned, could the different herbs by using them when the preferred species increase fitness advantages and promote the social inheritance were not available, but we detected consistent preferences of such technological systems. for the most appropriate tool materials, which is similar to Addition of the Goualougo chimpanzee tool repertoire to the tool-material selectivity observed by McBeath and the previously compiled data on chimpanzee cultures does McGrew (1982) in Senegal. The same herbs were used for not indicate the presence of any new regional tool traditions. ant dipping and termite fishing, but we have observed differ- Indeed, the tool sets used by these chimpanzees to extract ences in the manufacture and modification of these materials termites from their nests has dispelled the notion of exclusive

Table 4 Comparison of chimpanzee tool activities across sites, with counts of all observed and regular tool behaviors listed Extract Social Wipe Probe Perforate Whisk Cover, Scoop, Pound Scratch, Other Total barrier hook rub self P. t. verus Tai, Ivory Coast 5/5 5/5 3/0 2/2 1/1 2/2 1/1 1/0 1/1 dd21/17 Bossou, Guinea 7/2 5/3 d 1/1 dd1/0 3/1 2/2 d 2/1 21/10 Assirik, Senegal 4/4 2/0 1/0 dd dddddd7/4 P. t. troglodytes Goualougo, Rep. Congo 7/4 3/1 2/0 1/0 3/3 d 3/0 d 1/1 2/0 d 22/9 Lope´, Gabon 3/2 2/2 dd 1/1 dddd dd6/5 P. t. schweinfurthii Gombe, Tanzania 6/4 4/4 4/1 2/2 1/1 2/0 d 1/0 d 1/1 1/0 22/13 Mahale-M, Tanzania 3/2 5/4 1/0 3/2 ddd1/0 ddd13/8 Mahale-K, Tanzania 3/3 3/3 1/0 2/2 d 1/0 ddd dd10/8 Kibale, Uganda 2/2 4/3 2/2 1/0 dd1/0 dd dd10/7 Budongo, Uganda 1/1 4/3 1/1 dd1/1 ddd1/0 d 8/6 Totals (all/regular) 41/29 37/28 15/4 12/9 6/6 6/3 6/1 6/1 4/4 4/1 3/1 140/87 Regular (%) 71% 76% 27% 75% 100% 50% 17% 17% 100% 25% 33% 62% 432 C.M. Sanz, D.B. Morgan / Journal of Human Evolution 52 (2007) 420e433 regional traditions for termite fishing and digging (Sanz et al., (such as shown in termite fishing) or locations where tools are 2004). We confirm the absence of nut cracking in this popula- cached (termite-puncturing sticks and nut-cracking hammers tion, but cannot exclude ecological constraints on this behav- and anvils). Data from all chimpanzee study sites suggest ior. Panda oleosa, which is cracked by chimpanzees in the Tai that a proportion of tool-using behaviors are regularly ex- Forest, is present in the Goualougo study area, but there are hibited, while others are manifested only rarely and in re- few stones in the Goualougo study area, which could be a lim- sponse to specific stimuli. It is certain that there is a high iting factor for nut cracking. Honey gathering with the aid of degree of variation between sites. In contrast to the rigid pat- tools has been observed in several chimpanzee populations, terns of tool use observed in other taxa, apes respond to partic- but the use of large pounding clubs to open beehives seems ular situations with adaptive solutions, which may demonstrate thus far to be unique to central Africa (Fay and Carroll, an understanding of causality in external objects. However, 1994; Bermejo and Illera, 1999; Hicks et al., 2005). This is there remains a large gap in our knowledge of the specific a candidate regional tradition, but it requires further research mechanisms that promote innovation and maintenance of on its distribution and ecological determinants. specific traditions within and between communities. Most Although there are many hypotheses regarding the origin of comparisons have studied behaviors between sites that are sep- tool behavior, it is widely supported that the particular feeding arated by several hundreds if not thousands of kilometers, with niches of primates have promoted tool-using behaviors. Parker little research focusing on differences among groups or local and Gibson (1977) hypothesized that tertiary sensorimotor in- populations. Future research needs to follow the multicom- telligence is driven by particular high-protein resources that munity approach of Mahale and Tai, which have both shown are only seasonally available and embedded in protective intriguing differences among groups that are not clearly attrib- casings. Trial-and-error foraging strategies to access these re- utable to ecological differences (Collins and McGrew, 1987; sources were thought to have promoted an enhanced under- Boesch, 2003). standing of causality in certain taxa. This intelligence is then This study provides a snapshot of the tool-using behavior in applied to the taxon’s object-manipulation skills to produce the Goualougo chimpanzee population. Tool-using behaviors complex and flexible tool-using behaviors. Although this study are dynamic and susceptible to drift, modification, replace- was not equipped to examine the evolutionary forces driving ment, and attrition. The Goualougo chimpanzee population re- tool use, our summary both supports and contradicts this the- sides within an intact ecosystem that is surrounded by other oretical framework. The majority of chimpanzee tool-using communities. Therefore, it is likely that new information will behaviors occurred in feeding contexts that involved using intermittently be introduced via the transfer of new individuals. tools to gain access to otherwise inaccessible food items, Opportunities to study such traditions within intact populations which has been shown to yield significant caloric return for are decreasing as chimpanzees habitats are degraded or de- the energy expended (Gunther and Boesch, 1993). However, stroyed. Although much remains to be learned from chimpan- our results also show that objects were frequently used by zees residing in the Congo Basin (Wrangham, 2006), the great apes in social interactions or to enhance self-comfort, survival of these apes and their traditions are in jeopardy. As protection, or stimulation. The selective advantages of these we continue to make discoveries of new tool behaviors, it is behavioral contexts are not as immediate as enhanced foraging also our responsibility to ensure that others do not disappear. efficiency, but may provide indirect benefits to ape health. It has been observed that some populations of orangutans use Acknowledgements tools to exploit food resources, while others show tool use that is related only to self-comfort and physical protection We are deeply appreciative of the opportunity to work in (van Schaik et al., 2003). The reported tool-using repertoire the Nouabale´-Ndoki National Park and especially the Goua- of bonobos currently contains few feeding-related tool lougo Triangle. This work would not have been possible with- behaviors; rather, their tool use seems driven by promoting out the continued support of the Ministere de l’Economie self-comfort and communicating information within a social Forestiere et de l’Environment of the Government of the Re- context (Ingmanson, 1996; Hohmann and Fruth, 2003). It public of Congo and Wildlife Conservation SocietyeCongo. has been hypothesized that foraging strategies promoted the Special thanks to J.M. Fay, P. Elkan, S. Elkan, M. Gately, emergence of tool-using behaviors, but observations of tool E. Stokes, and P. Ngouembe. We also express our gratitude use across various contexts in extant apes prompt reexamina- to C. Boesch for his mentorship and support of this project. tion of the forces shaping tool use. S. Gulick is to be credited for the remote-monitoring technol- It is likely that the tool-using repertoire of early hominins ogy that was used in this study. We thank J.R. Onononga for was far more complex than that of any extant ape population. his continuing commitment to chimpanzee research and con- Models based on living primates suggest that tools were used servation in Congo. I. Nichols and the National Geographic not only in foraging, but in a variety of other contexts, such as Society generously provided the photos for this manuscript. self-comfort and protection, personal hygiene, and social ac- We gratefully acknowledge the U.S. Fish and Wildlife Service, tivities. Data from Goualougo and Tai chimpanzee populations National Geographic Society, Wildlife Conservation Society, suggest that reuse of tools would occur in situations that re- Columbus Zoological Park, Brevard Zoological Park, and quire specific materials or several modifications to produce. Lowry Zoological Park for funding. During the preparation This reuse could occur as tools were transported between sites of the manuscript, C. Sanz was supported by a Richard Carley C.M. Sanz, D.B. Morgan / Journal of Human Evolution 52 (2007) 420e433 433

Hunt Fellowship from the Wenner-Gren Foundation for An- McGrew, W.C., Collins, D.A., 1985. Tool use by wild chimpanzees (Pan trog- thropological Research. lodytes) to obtain termites (Macrotermes herus) in the Mahale Mountains, Tanzania. Am. J. Primatol. 9, 47e62. McGrew, W.C., Ham, R.M., White, L.J.T., Tutin, C.E.G., Fernandez, M., 1997. Why don’t chimpanzees in Gabon crack nuts? Int. J. Primatol. 18, References 353e374. McGrew, W.C., Rogers, M.E., 1983. Chimpanzees, tools, and termites: New Alp, R., 1997. ‘‘Stepping-sticks’’ and ‘‘seat-sticks’’: New types of tools used record from Gabon. Am. J. Primatol. 5, 171e174. by wild chimpanzees (Pan troglodytes) in Sierra Leone. Am. J. Primatol. McGrew, W.C., Tutin, C.E.G., Baldwin, P.J., 1979. Chimpanzees, tools, and 41, 45e52. termites: Cross-cultural comparisons of Senegal, Tanzania, and Rio Bermejo, M., Illera, G., 1999. Tool-set for termite-fishing and honey extraction Muni. Man 14, 185e214. by wild chimpanzees in the Lossi Forest, Congo. Primates 40, 619e627. Morgan, B.J., Abwe, E.E., 2006. Chimpanzees use stone hammers in Came- Boesch, C., 2003. Is culture a golden barrier between human and chimpanzee? roon. Curr. Biol. 16, R632eR633. Evol. Anthropol. 12, 82e91. Muroyama, Y., 1991. Chimpanzees’ choice of prey between two sympatric Boesch, C., Boesch, H., 1981. Sex differences in the use of natural hammers species of Macrotermes in the Campo Animal Reserve. Hum. Evol. 6, by wild chimpanzees: A preliminary report. J. Hum. Evol. 10, 585e593. 143e151. Boesch, C., Boesch, H., 1990. Tool use and tool making in wild chimpanzees. Nishida, T., 1973. The ant-gathering behaviour by the use of tools among wild Folia Primatol. 54, 86e99. chimpanzees of the Mahali Mountains. J. Hum. Evol. 2, 347e370. Boesch, C., Boesch-Achermann, H., 2000. The Chimpanzees of the Tai Forest: Nishida, T., Hiraiwa, M., 1982. Natural history of a tool-using behavior by Behavioural Ecology and Evolution. Oxford University Press, Oxford. wild chimpanzees in feeding upon wood-boring ants. J. Hum. Evol. 11, Boesch, C., Marchesi, N., Fruth, B., Julian, F., 1994. Is nut cracking in wild 73e99. chimpanzees a cultural behaviour? J. Hum. Evol. 26, 325e338. Parker, S.T., Gibson, K.R., 1977. Object manipulation, tool use, and sensori- Boesch-Achermann, H., Boesch, C., 1994. Hominization in the rainforest: The motor intelligence as feeding adaptations in Cebus monkeys and great chimpanzee’s piece of the puzzle. Evol. Anthropol. 3, 9e16. apes. J. Hum. Evol. 6, 623e641. Brewer, S.M., McGrew, W.C., 1990. Chimpanzee use of a tool-set to get Sabater Pi, J., 1974. An elementary industry of the chimpanzees in the honey. Folia Primatol. 54, 100e104. Okorobiko Mountains, Rio Muni (Republic of Equatorial Guinea), West Collins, D.A., McGrew, W.C., 1987. Termite fauna related to differences in Africa. Primates 15, 351e364. tool use between groups of chimpanzees (Pan troglodytes). Primates 28, Sanz, C., Morgan, D., Gulick, S., 2004. New insights into chimpanzees, tools, 457e471. and termites from the Congo Basin. Am. Nat. 164, 567e581. Fay, J.M., Carroll, R.W., 1994. Chimpanzee tool use for honey and termite Stanford, C.B., Gambaneza, C., Nkurunungi, J.B., Goldsmith, M.L., 2000. extraction in central Africa. Am. J. Primatol. 34, 309e317. Chimpanzees in Bwindi-Impenetrable National Park, Uganda, use different Goodall, J., 1964. Tool-using and aimed throwing in a community of free- tools to obtain different types of honey. Primates 41, 337e341. living chimpanzees. Nature 201, 1264e1266. Struhsaker, T.T., Hunkeler, P., 1971. Evidence of tool-using by chimpanzees in Goodall, J., 1968. The behaviour of free-living chimpanzees in the Gombe the Ivory Coast. Folia Primatol 15, 212e219. Stream Reserve. Anim. Behav. Monogr. 1, 161e311. Sugiyama, Y., 1985. The brush-stick of chimpanzees found in south-west Goodall, J., 1973. Cultural elements in the chimpanzee community. In: Cameroon and their cultural characteristics. Primates 26, 361e374. Menzel, E.W. (Ed.), Precultural Primate Behaviour. S. Karger, Basel. Sugiyama, Y., 1997. Social tradition and the use of tool-composites by wild Goodall, J., 1986. The Chimpanzees of Gombe: Patterns of Behavior. Belknap chimpanzees. Evol. Anthropol. 6, 23e27. Press., Cambridge. Suzuki, S., Kuroda, S., Nishihara, T., 1995. Tool-set for termite-fishing by Gunther, M., Boesch, C., 1993. Energetic costs of nut-cracking behavior in chimpanzees in the Ndoki Forest, Congo. Behaviour 132, 219e234. wild chimpanzees. In: Chivers, D., Preuschoft, H. (Eds.), Evolution of Teleki, G., 1974. Chimpanzee subsistence technology: Materials and skills. Hands. Gustav Fisher Verlag, Stuttgart, pp. 109e129. J. Hum. Evol. 3, 575e594. Hicks, T.C., Fouts, R.S., Fouts, D.H., 2005. Chimpanzee (Pan troglodytes Tutin, C.E.G., Ham, R., Wrogemann, D., 1995. Tool-use by chimpanzees (Pan troglodytes) tool use in the Ngotto Forest, Central African Republic. t. troglodytes) in the Lope´ Reserve, Gabon. Primates 36, 181e192. Am. J. Primatol. 65, 221e237. van Schaik, C.P., Deaner, R.O., Merrill, M.Y., 1999. The conditions for tool Hirata, S., Myowa, M., Matsuzawa, T., 1998. Use of leaves as cushions to sit use in primates: Implications for the evolution of material culture. on wet ground by wild chimpanzees. Am. J. Primatol. 44, 215e220. J. Hum. Evol. 36, 719e741. Hohmann, G., Fruth, B., 2003. Culture in bonobos? Between-species and van Schaik, C.P., Ancrenaz, M., Borgen, G., Galdikas, B., Knott, C.D., within-species variation in behavior. Curr. Anthropol. 44, 563e571. Singleton, I., Suzuki, A., Utami, S.S., Merrill, M., 2003. Orangutan Humle, T., Matsuzawa, T., 2002. Behavioral diversity among the wild chim- cultures and the evolution of material culture. Science 299, 102e105. panzee populations of Bossou and neighboring areas, Guinea and Cote Whiten, A., Goodall, J., McGrew, W.C., Nishida, T., Reynolds, V., d’Ivoire, west Africa. Folia Primatol. 72, 57e68. Sugiyama, Y., Tutin, C.E.G., Wrangham, R.W., Boesch, C., 1999. Cultures Ingmanson, E.J., 1996. Tool-using behaviors in wild Pan paniscus: Social and in chimpanzees. Nature 399, 682e685. ecological considerations. In: Russon, A.E., Bard, K.A., Parker, S.T. Whiten, A., Goodall, J., McGrew, W.C., Nishida, T., Reynolds, V., (Eds.), Reaching into Thought: The Minds of the Great Apes. Cambridge Sugiyama, Y., Tutin, C.E.G., Wrangham, R., Boesch, C., 2001. Charting University Press, Cambridge, pp. 190e210. cultural variation in chimpanzees. Behaviour 138, 1481e1516. Kano, T., 1982. The use of leafy twigs for rain cover by the pygmy chimpan- WoldeGabriel, G., Haile-Selassie, Y., Renne, P.R., Hart, W.K., Ambrose, S.H., zees of Wamba. Primate 23, 453e457. Asfaw, B., Heiken, G., White, T., 2001. Geology and palaeontology of the Lemonnier, P., 1992. Elements for an Anthropology of Technology. University late Miocene middle Awash valley, Afar rift, Ethiopia. Nature 412, of Michigan, Ann Arbor. 175e178. McBeath, N.M., McGrew, W.C., 1982. Tools used by wild chimpanzees to WoldeGabriel, G., White, T.D., Suwa, G., Renne, P., de Heinzelin, J., obtain termites at Mt. Assirik, Senegal: The influence of habitat. J. Hum. Hart, W.K., Heiken, G., 1994. Ecological and temporal placement of early Evol. 11, 65e72. Pliocene hominids at Aramis, Ethiopia. Nature 371, 330e333. McGrew, W.C., 1992. Chimpanzee Material Culture: Implications for Human Wrangham, R.W., 2006. Chimpanzees: The culture-zone concept becomes Evolution. Cambridge University Press, Cambridge. untidy. Curr. Biol. 16, R634eR635. McGrew, W.C., 1994. Tools compared. In: Wrangham, R.W., McGrew, W.C., Yamakoshi, G., Myowa-Yamakoshi, M., 2004. New observations of ant- de Waal, F.B.M., Heltne, P.G. (Eds.), Chimpanzee Cultures. Harvard dipping techniques in wild chimpanzees at Bossou, Guinea. Primates 45, University Press, Cambridge, pp. 25e39. 25e32.