There is currently much debate about the origins of animal culture, including why some animals have acquired the ability to use tools. Ecological problems often lead to the innovation of new tools. For example, a particular desirable food item may not be reachable without using a tool, or environmental conditions may make it difficult for an animal to find food without help.

Gruber et al. investigated how particular ecological factors influenced the use of tools in wild chimpanzees by combining controlled field experiments and observational data. When the ecological conditions were the most demanding, wild chimpanzees engaged most with the honey-trap experiment, an experiment where they had to use a tool to extract honey from a cavity dug in a log. Chimpanzees spent a longer time engaging with the apparatus when not much food was available and they had to travel more to obtain it. However, actual tool use during the experiments was only influenced by the travel effort made by the chimpanzees before they engaged with the log, not by how much fruit they had eaten beforehand.

In a larger analysis that included data from all of the long-term field sites with habituated chimpanzees, Gruber et al. found that chimpanzee communities that travel further on a daily basis use a wider range of tools to acquire food. These results suggest that travel is an important factor to consider when studying how tool use evolved. Furthermore, these results can be extrapolated to humans, who both travel further and use a greater variety of tools than chimpanzees.

Although innovation and culture are closely linked, innovation is mostly performed by individuals whereas culture is a social process. However, both are shaped by the environment. The next step will therefore be to disentangle and quantify the different contributions of environmental, individual and group factors in explaining how culture evolves.

What evolutionary pressures have favoured tool use in some species, including chimpanzees and humans, but not others? Recent work in non-human primate species has focussed on the role of ecological variables for the emergence of tool use (Fox et al., 1999; Humle and Matsuzawa, 2002; Möbius et al., 2008; Spagnoletti et al., 2012; Sanz and Morgan, 2013). These studies have enlightened our understanding of how ecology influences animal culture (Whiten et al., 1999; Laland and Janik, 2006) and are also informative for modelling early hominin lifestyle (Susman and Hart, 2015).

For non-human primates, Fox and colleagues proposed three hypotheses to test the relation between ecological factors and the innovation of feeding-related tool use in primates, i.e., the ‘invention’, ‘necessity’, and ‘opportunity’ hypotheses (Fox et al., 1999). While the invention hypothesis states that new forms of tool use are rare chance events, which spread through social learning (Fox et al., 2004), the necessity and opportunity hypotheses state that ecological factors can have an additional influence (Sanz and Morgan, 2013). While the necessity hypothesis predicts that tool use emerges as a response to food scarcity, the opportunity hypothesis predicts this emergence as a response to encounters with either the material needed to make a tool or the resources to be extracted by the tools (Koops et al., 2013). The current literature has generated conflicting and inconclusive results concerning the different ecological hypotheses, even within the same species (chimpanzees (Pan troglodytes verus; necessity: Yamakoshi, 1998; opportunity: Koops et al., 2013; inconclusive: Furuichi et al., 2015); capuchins (Sapajus spp., necessity: Moura and Lee, 2004; opportunity: Spagnoletti et al., 2012); bonobos (Pan paniscus; inconclusive: Furuichi et al., 2015); see (Sanz and Morgan, 2013) for a review).

Research on non-primates has generated an additional ecological hypothesis, the ‘relative profitability hypothesis’ to explain the emergence of tool use, which is based on optimal foraging theory and work on New Caledonian crows (Corvus moneduloides). This hypothesis states that tool use can develop as a strategy to obtain dietary components difficult to obtain without tools, but only if this is more profitable than non-tool-based strategies and as long as the ecological conditions, such as low predation pressure, allow it (Rutz and St Clair, 2012).

Koops et al. (2014) proposed an enlarged opportunity hypothesis, which includes not only ecological but also social and cognitive opportunities as drivers of tool use innovation and maintenance. In this view, necessity cannot explain tool use in animals because of the lack of correlations between selected environmental indicators and tool use. In particular, in a study with unhabituated chimpanzees of Nimba forest, Guinea, there was no correlation between fruit availability and ant remains in faeces, a proxy for stick use (Koops et al., 2013). Additionally, there was no relation between feeding-related tool use variants and the number of dry months across chimpanzee sites through Africa, further suggesting that tool use did not emerge out of necessity (Koops et al., 2014). In contrast, support for the necessity hypothesis comes from another study with the nearby habituated chimpanzees of Bossou, Guinea, where nut-cracking increased when fruit availability was low, suggesting that tool use is a fall back strategy during periods of food scarcity (Yamakoshi, 1998).

One explanation for these conflicting results is that the necessity hypothesis is difficult to test. For instance, Sanz and Morgan (2013) argue that the abundance of preferred food is a poor proxy for necessity and that even low levels of these foods may not be sufficient to trigger significant behavioural changes. Second, necessity may be driven by the lack of particular micronutrients essential for survival but that do not account for a major part of the diet (Sanz and Morgan, 2013). Necessity-based tool inventions, in other words, may not always function to compensate for low caloric intake. A third problem with the necessity hypothesis may also be due to the narrow focus of the analyses conducted to test it, e.g. feeding opportunities determined through phenological surveys, with no data on (a) whether animals actually seize these opportunities, (b) their variation across large timescales (Gruber et al., 2012a), (c) the energetic costs incurred to benefit from them (Pontzer and Wrangham, 2004; Lehmann et al., 2007; Amsler, 2010), and (d) the differential needs of individuals across time. In this respect, while analysing entire communities or populations can be useful, for instance by correlating phenological variables with tool use frequencies or tool repertoire sizes of entire communities (see below), individual needs may differ substantially within groups, suggesting that additional levels of analysis may be necessary to test the necessity hypothesis.

In this study, we were interested in the role of ecological factors in the emergence of chimpanzee tool use at the individual level. We studied how individuals of a chimpanzee community known for its limited tool use behaviour, the Sonso community of Budongo Forest (Pan troglodytes schweinfurthii), behaved in an experimental foraging task that required tool use. Although Sonso chimpanzees use tools in non-feeding contexts, such as for personal hygiene or communication, they have only been observed to use one type of tool to access resources, which consists of folding and chewing a handful of leaves to make a sponge, usually to collect water (Reynolds, 2005). Recently, some members of the Sonso community have learned a new technique, moss-sponging, to access mineral-rich suspensions from a clay pit (Hobaiter et al., 2014).

The Sonso community is part of a larger population of about 700 chimpanzees living in Budongo Forest, which most likely show the same limitations in tool use behaviour (Gruber et al., 2012a). For this reason, they constitute ideal subjects to study the emergence of new tool use behaviours, unlike other populations that already have complex food-related tool repertoires (Whiten et al., 1999).

We analysed data from a long-term field experiment, the honey-trap experiment, in which subjects were exposed to a novel foraging task that could only be solved with a tool. In doing so, we controlled for opportunity-based ecological aspects by presenting subjects with a standardised apparatus, which consisted of a small cavity drilled into a portable log, filled with liquid honey (Gruber et al., 2009, 2011). Our goal was to test individuals under conditions of high ecological validity, over an extended period of time (2009–2015), with an unprecedented subject pool of over 50 individuals of a fully habituated community. In contrast to previous studies, our experimental approach allowed us to carry out analyses at the individual level, by comparing individuals in their interactions with the apparatus (Gruber et al., 2009, 2011).

In our previous work, we found that 10 of 52 individuals (19.2%) who engaged with the apparatus proceeded to manufacture a leaf-sponge to extract artificially provided honey (Gruber et al., 2009, 2011; Gruber, 2016). This behaviour is customarily used by wild chimpanzees to drink water, but there are no reports of chimpanzees using this behaviour to collect naturally available honey from bee nests. During our experiments, we also recorded two individuals using a stick to access the honey, but only after much exposure and experimental facilitation (see Material & Methods), and in contrast to another Ugandan chimpanzee community, where stick use was customary to access experimentally provided honey (Gruber et al., 2009, 2011).

In the current study, we combined our long-term experimental data and behavioural observations to determine the natural parameters that influenced individual variation in engagement with the apparatus and the use of tools. As our experimental design controlled for opportunity, we were able to assess the influence of two key necessity-related variables, feeding time spent on ripe fruits (a proxy for food availability) and travel effort (a proxy for energetic demands), measured as the proportion of travel in the activity budget, on individuals’ (a) engagement time with the apparatus and (b) probability of tool use. As we had no specific predictions concerning the relevant time intervals, we carried out these analyses incorporating data from different time periods prior to interaction with the apparatus.

Second, to determine whether any eventual patterns characterised chimpanzees as a species, we ran a cross-population comparison of travel behaviour and fruit feeding in relation to differences in food-related tool repertoires comparing data from all long-term chimpanzee communities. Finally, we discuss how our findings can shed light on the different hypotheses outlined above, and how they can contribute to a unifying model of the emergence of tool use.

We analysed a total of 292 experimental trials (N = 52 subjects, mean/median number of trials per individual: 5.6/3.0, range: 1–39). Mean engagement time with the apparatus was 111 s (N = 292 trials, range: 1–1275 s). In 21 of these trials (7.2%), subjects also used a tool. These cases were distributed over 16 different experimental days (11 with a single tool-user, five with two successive tool-users). For each trial, we determined the preceding travel and ripe fruit feeding behaviour of the subject by systematically varying the time periods before each experiment (ranging from 1 to 13 weeks). To this end, we determined the proportion of all scans that contained travel and ripe fruit feeding for the focal individual of the test subject’s party. This is a reasonable approach since members of a chimpanzee party typically engage in the same behaviour at a given time (see Material and methods).

The first model assessed how a subject’s engagement time with the apparatus was related to ripe fruit feeding, travel time and time period. This model was significant overall (linear mixed-effects model, likelihood ratio test (LRT): _X² = 188.1, df = 10, p<0.0001, R²_m = 0.33, Table 1), with a significant three-way interaction between ripe fruit feeding, travel time and time period (LRT: _X² = 5.77, df = 1, p = 0.0163, Figure 1A). Specifically, when subjects fed little on ripe fruits, they engaged more with the apparatus, provided they also travelled much. This effect was modulated by the duration the subject was recorded in the same condition. For example, chimpanzees engaged more with the apparatus if they had travelled more and had consumed less ripe fruits for longer than shorter periods of time (Figure 1A, lower panel). However, when subjects spent much time feeding on ripe fruits, there was less variation in time spent engaging with the apparatus, regardless of prior travel time. In addition, older individuals and males engaged less with the apparatus than young individuals and females.

Figure 1

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Figure 1—source data 1

Engagement data.

https://doi.org/10.7554/eLife.16371.005

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Figure 1—source data 2

Tool data 1 week.

https://doi.org/10.7554/eLife.16371.006

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Figure 1—source data 3

Tool data 7 weeks.

https://doi.org/10.7554/eLife.16371.007

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Figure 1—source data 4

Tool data 13 weeks.

https://doi.org/10.7554/eLife.16371.008

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Concerning the occurrence of tool use (observed in 21 of 292 trials; 7.2%), we built three generalized linear mixed models at three different time periods (1 week, 7 weeks and 13 weeks) because a single model analogous to the one presented above did not converge. Each of these models included the interaction between ripe fruit feeding and travel. We found that only the 1-week model was significantly different from its corresponding null model (LRT: 1 week: _X² = 12.0, df = 5, p = 0.0346, R²_m = 0.30; 7 weeks: _X² = 7.6, df = 5, p = 0.1810, R²_m = 0.19; 13 weeks: _X² = 8.5, df = 5, p = 0.1299, R²_m = 0.18). Contrary to the previous engagement time model, we did not find any effect of the interaction between ripe fruit feeding and travel time on the likelihood of tool use (all p>0.1, Table 2). However, we found a significant main effect of travel time on the probability of tool use, which increased with travel time (Table 3, Figure 1B top panel). No such result was found for ripe fruit feeding, although the effect went into the expected direction (i.e., more tool use with less ripe fruit feeding). For the other two time periods, the estimated effects of travel time and ripe-fruit feeding also went into the expected directions (Table 3, Figure 1B).

Finally, we analysed our data set on published estimates of diet and travel related behaviour of nine habituated wild chimpanzee communities (Table 4). In accordance with the results found in our analysis, we found that larger tool repertoires were associated with lower percentages of fruit consumption (Spearman’s rho = −0.43, N = 9, Figure 2A) and higher percentages of travel (rho = 0.61, N = 9, Figure 2B). When using average distance travelled per day, we found again a positive relationship with size of tool repertoire (rho = 0.77, N = 7, Figure 2C). Similar to our experimental data, the effect of the travel-related variables was larger than the effect of ripe fruit feeding.

Figure 2

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Our results indicate that travel is directly related to the probability of tool use behaviour in wild chimpanzees. Our data first showed that the combination of low ripe-fruit availability and high travel effort increased their motivation to engage with a foraging problem that required tool use. Specifically, in situations of low fruit availability, the subjects spent more time engaging with the apparatus than at times of high ripe fruit availability, suggesting that they were possibly more inclined to explore alternative hard-to-get food possibilities. Our second finding was that tool use was mainly driven by short-term changes in daily travel, and less so by fruit availability. Specifically, tool use increased with increasing amounts of travel before the experiment, but this was mostly a short-term effect, up to one week prior to an experiment (Figure 1B, Table 3). Taken together, these results suggest that travel generates extra energetic costs in situations of low fruit abundance and that tool use is more likely to appear if ecological situations force chimpanzees to explore alternative feeding options in situations of high energy expenditures.

In this respect, tool use itself does not appear to be fostered by resource limitation, but rather by increased energetic costs. While tool use was interpreted as a fall back strategy in response to food scarcity in Bossou (Yamakoshi, 1998), in line with the original definition of necessity (Fox et al., 1999), this effect may not be observed in communities that do not display habitual feeding-related tool use behaviour, such as Sonso. The Budongo Forest has been described as a rich habitat where periods of extreme food scarcity are absent (Newton-Fisher, 1999), which may prevent chimpanzees from experiencing extreme necessity. Food availability nevertheless undergoes seasonal fluctuations (Reynolds, 2005) and, over the last decade, the food supply has noticeably gone down, in part due to anthropogenic activities (Babweteera et al., 2012). The Sonso chimpanzees have responded with behavioural adaptations to the disappearance of their original food resources (Reynolds et al., 2015), which suggests that detailed analyses are needed to better understand how food variation affects chimpanzee behaviour. Overall, our results suggest that chimpanzees are more eager to exploit difficult resources when the ecological conditions are more demanding relative to average conditions, both in terms of low food availability and high amounts of energy required to obtain the food. While high travel effort in itself is not necessarily linked with low diet quality in chimpanzees (e.g. Riedel et al., 2011), our analyses show that a combination of the two favours the exploration of alternative food resources, which creates opportunities for acquiring new tool behaviours. We interpret these findings as support for the more general idea that necessity can also drive invention in wild chimpanzees, when energetic demands are high. Necessity, in other words, is likely to be a major factor in driving the emergence of tool use behaviour in chimpanzees, if it is redefined to take into account both energetic costs and opportunities to compensate these costs. These results underline the importance of individual-based analyses that take into account data on both energetic expenditure and intake, with potentially important implications for theories about the origin of tool use behaviour.

Our results are in line with the ‘relative profitability hypothesis’, which states that extractive tool use will occur if it is relatively more profitable than other alternative foraging strategies that do not rely on tool use (Rutz and St Clair, 2012). If increased travel effort represents an extra energetic cost, then tool use is a relatively more profitable strategy, especially if this occurs in ecologically challenging situations, which may trigger the switch from non-tool to tool-based foraging. Interestingly, the chimpanzees of Budongo Forest have increased their crop raiding habits over the last decade (Tweheyo et al., 2005), a probable response to a general decrease in food availability in the forest (Babweteera et al., 2012). As such, the innovation of novel tool use may only be one possible reaction to a changing environment, highlighting the flexibility of chimpanzees in dealing with changes in food availability (Hockings et al., 2015). Another facet of the relative profitability hypothesis is that tool use may provide individuals with a selective advantage over non-tool-using individuals (Patterson and Mann, 2011), as it provides them access to an energetically valuable resource, although in only 7% of trials did subjects succeed to do so. Perhaps this is not so surprising as tool use innovation is itself rarely observed in the animal kingdom (Shumaker et al., 2011) and only some species will develop tool use under identical ecological conditions (Rutz and St Clair, 2012), a reasoning that may apply at the population or individual level, as suggested by the current study.

While alternate strategies, such as crop-raiding, may contribute in part to the general lack of tool use inventions in this community, it is equally possible that psychological mechanisms can explain some of the observed patterns, offering insights into the ‘invention hypothesis’. Here, one important result of our study is that the large majority of the tool-using individuals (19 of 21 cases, 90.5%) applied a familiar technique, leaf-sponging, in the experiment, behaving much different from when extracting honey from natural bee nests with their hands. Nevertheless, while adapting an existing behaviour to a novel context may be considered an innovation (Reader and Laland, 2003; Reader et al., 2016), only two individuals chose a different technique by attempting to use sticks. However, these two individuals did not incorporate this behaviour into their repertoire, raising questions about how wild chimpanzees represent artefacts as potentially useful tools (Gruber et al., 2015; Gruber, 2016). Additional studies are needed to explore the cognitive processes underlying chimpanzee tool use and, particularly, to decipher how ecological pressures and cognitive factors interact to lead to tool use innovation.

A neglected aspect in this study were the social opportunities for individuals to engage with the device or observe others to do so (see Koops et al. (2014)). In our study, engagement with the apparatus overlapped between social contexts (Figure 3), suggesting that the presence of others did not prevent subjects from engaging with it. However, it is less clear how the presence of others influenced the use of tools. Six individuals used a tool while being alone, seven others while in the company of family members, and eight in the company of other group members, to the effect that the current study cannot disentangle the relative role of social competition. Although tool-users spent more time with the apparatus and consumed more honey (Gruber (2016) and see Table 1), it is unlikely that this was because they monopolized the log. Rather, these individuals had developed a successful technique to recover the honey, compared to others who abandoned the apparatus earlier (Gruber, 2016). However, social influences are also in terms of social learning opportunities. As described elsewhere (Gruber, 2016), chimpanzees were generally tolerant to each other, but it is unclear whether they learnt from each other that leaf-sponge use was a suitable solution to extract honey. Social learning is a reasonable explanation for three individuals, but individual learning cannot be ruled out, largely because leaf-sponging was already part of their behavioural repertoire. Nevertheless, wild chimpanzees can learn socially from each other, even in a competitive context, and it is equally possible that this may even enhance social learning as it facilitates close observations of the novel behaviour (Hobaiter et al., 2014).

Figure 3

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From our data, we conclude that the emergence of tool use in our group was due to a combination of necessity (energetic demands), opportunity (inaccessible honey) and relative profitability (lack of alternatives), suggesting that ecological and temporal aspects of resources availability as well as individual efforts all played a role (Gruber, 2013). While it is important to quantify the food available over the entire home range, it is also important to take into account the temporal variation of food availability and its consequences on the relative attractiveness of alternative foods simultaneously available to individuals, even for foods as attractive as honey. We concur with Koops et al. (2014) that individuals must be exposed to the right ecological opportunities, in our case the honey-trap apparatus, and that the probability of tool use may directly depend on the frequency with which they will encounter this challenge, a parameter we controlled for in our experiment. For tool acquisition and spread to appear, the right social settings may also have to be present (Sanz and Morgan, 2013), under the form of opportunities for close observation (Hobaiter et al., 2014). In our case, encountering tools left by others (i.e. discarded sticks) did not appear to constitute a sufficient condition for social learning (Gruber et al., 2011). Our data also suggest that individual differences need to be taken into account. Finally, while cognitive abilities are likely to play a part in innovation and learning (Gruber, 2016), the emergence of tool use may also depend on whether it is relatively more profitable to do so, at any given time (Rutz and St Clair, 2012). Here, our data suggest that energetic demands resulting from individual variation in diet and travel effort directly influence the probability of tool use.

Is the relationship between travel and tool use generally found in the Hominidae? Our analysis of nine chimpanzee communities, although limited by the availability of published data on travel effort and tool use, suggests that our findings represent a general pattern. This analysis corroborated our empirical findings that travel effort and fruit consumption have opposing effects on tool repertoire size, and that travel effort, which arguably is best represented by the average daily distance walked by the chimpanzees, is likely to be more important than fruit consumption in explaining variation in tool repertoires between chimpanzee populations. In the long run, with more chimpanzee communities being currently habituated spanning across their entire ecological range (e.g. savanna in Fongoli, Pruetz, 2006), future studies will have to disentangle how environmental changes influence the relationship between tool use, energy intake and expenditure across a larger sample of chimpanzee populations. Regarding other great apes, both gorillas (genus Gorilla) and most orangutans (genus Pongo) show limited to no feeding-related tool use and interestingly they spend significantly less time travelling per day compared to chimpanzees, which suggests that their energy requirements are lower (Pontzer and Wrangham, 2004; Pontzer et al., 2016). Nevertheless, because travel is mostly arboreal in orangutans, more work is needed to estimate how this compares to chimpanzees, particularly with respect to Sumatran orangutans (Pongo abelii) for whom interesting variation in feeding-related tool use behaviour has been described (van Schaik et al., 2003; Gruber et al., 2012b).

The most promising comparison may come from the chimpanzees’ closest relatives, the bonobos (Pan paniscus), where the lack of tool use has been connected to smaller travel distance between food patches and reduced feeding competition (Wrangham and White, 1988). The estimated daily travel effort for bonobos (2.6 km, Furuichi et al. (2008)) is comparable with some chimpanzee communities, incidentally the ones with the smallest tool repertoires for the species (Kanyawara, Ngogo and Sonso, all in Uganda), underlining a possible convergence in ecological pressures faced by these populations (Gruber et al., 2010). Interestingly, some convergence can also be found with modern humans. For instance, modern human hunter-gatherers walk on average 11.4–14.1 km/day (Marlowe, 2005; Pontzer et al., 2012, 2016) and have the most diverse tool repertoire of all Hominidae, much beyond anything reported from the great apes (Marlowe, 2010). Combined, the results of the present study and the data from the three living hominines (Homo, Pan) reviewed here suggest an important role of travel in the emergence of tool use, but this needs to be tested across more study groups in different habitats and species. Whether this pattern holds for larger taxonomic groups beyond hominines remains to be investigated, taking into account the various ecological conditions faced by each species.

In conclusion, our findings suggest that tool use in hominids evolved in reaction to environmental changes that made preferred food harder to obtain. By extension, our results have direct implications for understanding hominid technological evolution, particularly in relation to the evolution of locomotor behaviour in the early stages of human evolution, as hominids faced similar ecological pressures. In effect, a number of major biogeographic events in the human lineage occurred at times of climate instability and it has been suggested that the development of tool use and sociality in hominins could constitute adaptive responses to heightened habitat instability (Potts, 2013). Australopithecines, for instance, evolved in a changing environment at the beginning of the Pliocene, where they faced more patchy resources of potentially lower quality (Foley and Gamble, 2009; Potts, 2013). Our findings support the view that tool use is connected to energy gain in a changing environment and that using tools is a response to increased costs of travel and lower quality of available food. In parallel, the adoption of bipedalism, which is less energetically costly than the quadrupedal and bipedal locomotion of chimpanzees, also allowed minimizing energy expenditure (Pontzer et al., 2009). Efficient, human-like bipedalism and tool use may have had complementary effects on travel costs, allowing both energy gain through the exploitation of novel ecological niches and energy economy during locomotion. Whether their development to unrivalled levels is what led to the dispersal of early humans throughout Africa and the advent of complex technology around 3.0 million years ago (Foley and Gamble, 2009; Harmand et al., 2015) remains to be investigated.

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Author details

1. Thibaud Gruber

   1. Department of Comparative Cognition, University of Neuchâtel, Neuchâtel, Switzerland
   2. Budongo Conservation Field Station, Masindi, Uganda
   3. Swiss Center for Affective Sciences, University of Geneva, Geneva, Switzerland

   Contribution

   TG, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   For correspondence

   thibaud.gruber@gmail.com

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0002-6766-3947

2. Klaus Zuberbühler

   1. Department of Comparative Cognition, University of Neuchâtel, Neuchâtel, Switzerland
   2. Budongo Conservation Field Station, Masindi, Uganda
   3. School of Psychology and Neuroscience, University of St Andrews, St Andrews, United Kingdom

   Contribution

   KZ, Drafting or revising the article, Contributed unpublished essential data or reagents

   Competing interests

   The authors declare that no competing interests exist.

3. Christof Neumann

   Department of Comparative Cognition, University of Neuchâtel, Neuchâtel, Switzerland

   Contribution

   CN, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0002-0236-1219

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