Although tool use is known to occur in species ranging from naked mole rats [] to owls [], chimpanzees are the most accomplished tool users []. The modification and use of tools during hunting, however, is still considered to be a uniquely human trait among primates. Here, we report the first account of habitual tool use during vertebrate hunting by nonhumans. At the Fongoli site in Senegal, we observed ten different chimpanzees use tools to hunt prosimian prey in 22 bouts. This includes immature chimpanzees and females, members of age-sex classes not normally characterized by extensive hunting behavior. Chimpanzees made 26 different tools, and we were able to recover and analyze 12 of these. Tool construction entailed up to five steps, including trimming the tool tip to a point. Tools were used in the manner of a spear, rather than a probe or rousing tool. This new information on chimpanzee tool use has important implications for the evolution of tool use and construction for hunting in the earliest hominids, especially given our observations that females and immature chimpanzees exhibited this behavior more frequently than adult males.

Results and Discussion

4 McGrew W.C. Chimpanzee Material Culture: Implications for Human Evolution. 3 Whiten A.

Goodall J.

McGrew W.C.

Nishida T.

Reynolds V.

Sugiyama Y.

Tutin C.E.G.

Wrangham R.W.

Boesch C. Charting cultural variation in chimpanzees. 4 McGrew W.C. Chimpanzee Material Culture: Implications for Human Evolution. 3 Whiten A.

Goodall J.

McGrew W.C.

Nishida T.

Reynolds V.

Sugiyama Y.

Tutin C.E.G.

Wrangham R.W.

Boesch C. Charting cultural variation in chimpanzees. 4 McGrew W.C. Chimpanzee Material Culture: Implications for Human Evolution. 6 Huffman M.A.

Kalunde S.M. Tool-assisted predation on a squirrel by a female chimpanzee in the Mahale Mountains, Tanzania. Chimpanzees (Pan sp.), our closest living relatives, have been observed to use tools in over 25 different contexts across all populations that have been studied []. Most notably, chimpanzees use tools to acquire social insects and to pound open hard nuts with a hammer and anvil []. Generally, ape tool use in the wild occurs within a foraging context and is largely restricted to processing vegetable matter or invertebrates []. However, at a new site in the mosaic savanna habitat of southeastern Senegal, we observed chimpanzees (Pan troglodytes verus) of the Fongoli community fashion tools in attempts to extract lesser bushbabies (Galago senegalensis) from cavities in hollow branches or tree trunks. Only one other instance of such tool-assisted hunting has been reported for wild chimpanzees. In that case, an adolescent female at Mahale, Tanzania used a branch to rouse a squirrel from a hollow branch [].

7 Nekaris A.

Bearder S.K. The Lorisiform primates of Asia and mainland Africa. 8 Nash L.T.

Bearder S.K.

Olson T.R. Synopsis of Galago species characteristics. 4 McGrew W.C. Chimpanzee Material Culture: Implications for Human Evolution. 9 Stanford C.B. The Hunting Apes: Meat Eating and the Origins of Human Behavior. The observed hunts were recorded between March 2005 and July 2006. Bushbabies are small (weighing about 200 g []), nocturnal prosimians that sleep in hollow cavities or other shelters during the day []. Consumption of prosimian prey is itself rare for chimpanzees []. At most long-term study sites, red colobus monkeys (Piliocolobus sp.), which are absent from this dry site, are the most common prey recorded for chimpanzees [].

5 Beck B. Animal Tool Behavior: The Use and Manufacture of Tools by Animals. 10 Hunt G.R.

Gray R.D. The crafting of hook tools by wild New Caledonian crows. 4 McGrew W.C. Chimpanzee Material Culture: Implications for Human Evolution. 10 Hunt G.R.

Gray R.D. The crafting of hook tools by wild New Caledonian crows. 6 Huffman M.A.

Kalunde S.M. Tool-assisted predation on a squirrel by a female chimpanzee in the Mahale Mountains, Tanzania. 11 Goodall J. The Chimpanzees of Gombe: Patterns of Behavior. 12 Byrne R.W.

Byrne J.M. Complex leaf-gathering skills of mountain gorillas (Gorilla g. berengei): Variability and standardization. 13 Russon A.E. The nature and evolution of intelligence in orangutans (Pongo pygmaeus). 12 Byrne R.W.

Byrne J.M. Complex leaf-gathering skills of mountain gorillas (Gorilla g. berengei): Variability and standardization. 13 Russon A.E. The nature and evolution of intelligence in orangutans (Pongo pygmaeus). 12 Byrne R.W.

Byrne J.M. Complex leaf-gathering skills of mountain gorillas (Gorilla g. berengei): Variability and standardization. Figure 1 Steps Involved in Making Tools for Hunting by Fongoli Chimpanzees In only one of the 22 recorded cases was the chimpanzee successful in finding and acquiring prey, but the observed tool making and associated hunting behavior was systematic and consistent. A common definition of tool use requires “the external employment of an unattached environmental object to alter more efficiently the form, position, or condition of another object, another organism, or the user itself when the user … is responsible for the proper and effective orientation of the tool” ([], p. 10]). We analyzed specific modifications made during the process and divided the behaviors into a stepwise progression of tool manufacture and use, which indicates “crafting” by Fongoli chimpanzees, a behavior previously attributed only to humans and other sophisticated tool users such as crows [] ( Figure 1 ). In fact, termite-fishing and ant-dipping behaviors by chimpanzees should also be considered examples of “crafting” given the similar number of steps involved in making and refining these types of tools []. Although each step observed in hunting with tools by Fongoli chimpanzees has been recorded for chimpanzees at other study sites in different tool-using contexts, the combination of these steps within a hunting context is unique, having been observed in only a few isolated cases []. The number of steps completed during this task by Fongoli chimpanzees is similar to what has been observed during foraging on difficult-to-process plant foods by wild gorillas (Gorilla gorilla beringei) [] and ex-captive orangutans (Pongo pygmaeus) [] and is considered hierarchical in organization []. The sequence of steps is hierarchically organized, with some steps that can be occasionally omitted and others that can be repeated. This structure is similar to what has been described as a branching tree [], demonstrating the flexibility involved in an otherwise standardized process.

14 Boesch C.

Boesch-Achermann H. The Chimpanzees of the Tai Forest: Behavioural Ecology and Evolution. 15 Nishida T. The ant-gathering behaviour by the use of tools among wild chimpanzees of the Mahali Mountains. Figure 2 Tip of Hunting Tool Sharpened with Teeth Show full caption Tool length approximately 70 cm. In most cases, Fongoli chimpanzees completed four or more steps of tool manufacture and use during hunting. In all cases but one, chimpanzees broke off living branches to make their tool. In every case, individuals trimmed side branches and leaves from the main branch/tool. In many cases, chimpanzees further trimmed both the proximal and distal ends and sometimes stripped the entire tool of bark (n = 8). Trimming off the smaller distal end appears to effectively strengthen the tool. In only one case was an individual observed to break a tool while using it. Individuals also sharpened the tip of the tool with their incisors (n = 4, Figure 2 ), sometimes using multiple bites to trim the tool end to a point. The function of this trimming appears to differ from similar behavior seen in other tool-using contexts, where it is usually done to obtain items that are within a small space (e.g., to extract the kernel from within a nut after it has been pounded open) and cannot be reached otherwise []. The average diameter of cavities chimpanzees exploited with tools was estimated to be 11 cm (9–12 cm, n = 7), large enough for a chimpanzee to insert its arm up to the shoulder. However, tools did not function simply as an extension of the arm. Tools, but not hands and arms, were first forcefully inserted into cavities. In this way, tools functioned as spears.

16 Marlowe F.W. Hunter-gatherers and human evolution. 3 Whiten A.

Goodall J.

McGrew W.C.

Nishida T.

Reynolds V.

Sugiyama Y.

Tutin C.E.G.

Wrangham R.W.

Boesch C. Charting cultural variation in chimpanzees. 17 Napier J. Hands. 7 Nekaris A.

Bearder S.K. The Lorisiform primates of Asia and mainland Africa. 6 Huffman M.A.

Kalunde S.M. Tool-assisted predation on a squirrel by a female chimpanzee in the Mahale Mountains, Tanzania. Chimpanzees forcibly “jabbed” (sensu Marlowe []) tools into hollow trunks or branches multiple times and smelled and/or licked them upon extraction. In only two of 22 cases was tool use playful (in the case of the infant male) or exploratory in nature (“investigatory probe” []). In all other cases, chimpanzees were judged to use such force in inserting the tool that prey within the cavity could have been injured. In all observed cases, chimpanzees used one hand in a “power grip” [] to jab the tool downward multiple times into the cavity. In the single instance in which a chimpanzee was observed to extract a bushbaby, it was unknown whether the prey was alive or dead after the use of the tool, but it made no attempts to escape, nor did it utter any vocalization. In that case, the chimpanzee ultimately broke off the terminal end of the hollow branch by moving several meters up the large (>10 cm diameter) branch and jumping on the branch until it broke off. She then climbed down, reached into the cavity, and pulled out the bushbaby. This same behavioral sequence was also seen in two other cases. The opening of cavities after using a tool, especially after the chimpanzee has moved some distance from the cavity opening to do so, suggests that the tool is used to immobilize prey rather than for extraction. Bushbabies move rapidly, using a vertical clinging and leaping form of locomotion [], and opening a nest cavity before immobilizing this prey would presumably result in frequent escape. Given these lines of evidence, the tools used by Fongoli chimpanzees can better be described as spearing as opposed to rousing tools [].

14 Boesch C.

Boesch-Achermann H. The Chimpanzees of the Tai Forest: Behavioural Ecology and Evolution. 18 Stanford C.B. Chimpanzee and Red Colobus: The Ecology of Predator and Prey. 14 Boesch C.

Boesch-Achermann H. The Chimpanzees of the Tai Forest: Behavioural Ecology and Evolution. 14 Boesch C.

Boesch-Achermann H. The Chimpanzees of the Tai Forest: Behavioural Ecology and Evolution. 19 Stevens J.R.

Gilby I.C. A conceptual framework for nonkin food sharing: timing and currency of benefits. Individuals observed fashioning or using hunting tools included one adult female, one adult male, three adolescent females, two adolescent males, one juvenile female, one juvenile male, and one infant male. Multiple immatures were associated with tool-assisted hunting several times. One adolescent female was observed fashioning such tools a total of five times and was successful in removing and eating a bushbaby once, for a success rate of 0.20, similar to solitary male chimpanzee hunters at Tai, Ivory Coast (17% success rate []) but less successful than single hunters' success rates at Gombe, Tanzania during red colobus hunts (30%–40% []). In addition to the aforementioned case in which an adolescent female acquired a bushbaby with a tool, two other individuals were seen eating bushbabies, but the method of procuring the prey was not seen. An adult male was observed eating a bushbaby but was not observed to share meat with any other individuals, although several chimpanzees approached him and briefly watched him consume the prey. The adult female was seen to eat the largest portion of a bushbaby while her juvenile daughter fed on meat, presumably of this same bushbaby. The adolescent female who captured a bushbaby consumed her prey without sharing, although she was surrounded by a number of adult males. Extensive meat sharing, as characterizes monkey eating at other sites [], was not observed in this context but had been seen in the same individual adult male chimpanzees with green monkey (Chlorocebus aethiops) prey at this same site just ten days previous. Sharing meat among chimpanzees correlates with coordination during hunts in most cases [], although this view is disputed []. Regardless, given the small size of bushbaby prey and the lack of necessity for coordinated hunting in order to secure them, it is not surprising that more meat sharing does not occur.

9 Stanford C.B. The Hunting Apes: Meat Eating and the Origins of Human Behavior. 14 Boesch C.

Boesch-Achermann H. The Chimpanzees of the Tai Forest: Behavioural Ecology and Evolution. 18 Stanford C.B. Chimpanzee and Red Colobus: The Ecology of Predator and Prey. 20 Mitani J.C.

Watts D.P. Why do chimpanzees hunt and share meat?. 6 Huffman M.A.

Kalunde S.M. Tool-assisted predation on a squirrel by a female chimpanzee in the Mahale Mountains, Tanzania. 21 Smolker R.A.

Richards A.F.

Connor R.C.

Mann J.

Berggren P. Sponge-carrying by Indian Ocean bottlenose dolphins: Possible tool use by a delphinid. 16 Marlowe F.W. Hunter-gatherers and human evolution. 22 McGrew W.C. The female chimpanzee as a human evolutionary prototype. Behavioral studies at Fongoli focus on the 11 adult males in this community of 35 chimpanzees, yet most of our observations of tool-assisted hunting are of females and immature individuals, underscoring its importance in these sex-age classes. This is in stark contrast to chimpanzee hunting behavior in general, a predominantly male activity []. Immature chimpanzees at Fongoli appear to exploit a niche relatively ignored by adult males. This supports the proposal that individuals whose access to preferred resources such as meat is limited by social or physical factors respond by developing alternative means with which to acquire them []. Social factors have also been proposed to explain why female but not male bottlenose dolphins use tools []. Our findings at Fongoli may support the hypothesis that female hominids play a role in the evolution of the earliest tool technology [], and we suggest that these technologies included hunting-related behavior, in addition to gathering-related activities.

23 Panger M.A.

Brooks A.S.

Richmond B.G.

Wood B. Older than the Oldowan? Rethinking the emergence of Hominin tool use. 24 Byrne R.W. The maker not the tool: The cognitive significance of great ape manual skills. 25 Thieme H. Lower Paleolithic hunting spears from Germany. 26 Semaw S.

Renne P.

Harris J.W.K.

Feibel C.S.

Bernor R.L.

Fesseha N.

Mowbray K. 2.5-million-year-old stone tools from Gona, Ethiopia. 27 Goodall J. Tool-using and aimed throwing in a community of free-living chimpanzees. 16 Marlowe F.W. Hunter-gatherers and human evolution. The multiple steps taken by Fongoli chimpanzees in making tools to dispatch mammalian prey involve the kind of foresight and intellectual complexity that most likely typified early human relatives, e.g., Australopithecines. The observed utility of materials that do not fossilize further indicates that our assessment of the cognitive capacity of relatively small-brained hominids is most likely underestimated, as has been suggested elsewhere []. The oldest known weapons of organic material are 400,000-year-old wooden spears [], approximately 2 million years younger than the earliest evidence for stone-tool use by hominids []. Although we have long known that chimpanzees are efficient tool users [], the observation of such behavior in a hunting context has significant implications for the way we have traditionally viewed hominid hunting. The suggestion that the earliest tool technology likely consisted of pounding or throwing rocks and hitting and jabbing sticks at about 6 million years ago [] is supported by our findings.