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Special issue: Tool use among Ugandan forest fragment chimpanzees

‘Customary’ use of stick tools by chimpanzees in Bulindi, Uganda: update and analysis of digging techniques from behavioural observations

Utilisation « courante » d’outils par les chimpanzés de Bulindi, Ouganda : actualisation et analyse des techniques pour creuser le sol à partir d’observations comportementales
Matthew R. McLennan, Jacqueline Rohen, Zoe Satsias, Tom Sabiiti, John-Mary Baruzaliire et Marie Cibot

Résumés

Les chimpanzés sauvages utilisent couramment des bâtons comme outils dans leurs activités de fourragement, le plus souvent pour collecter du miel ou des insectes. Comparé à d’autres régions, les chimpanzés (Pan troglodytes schweinfurthii) de l’Ouganda de l’ouest n’utilisent qu’une petite palette d’outils. Les chimpanzés de la communauté de Sonso (forêt de Budongo), suivie sur le long terme, ne se servent même jamais de bâtons. À vingt-cinq kilomètres de Budongo, la communauté de Bulindi habite de petits fragments de forêts au milieu de terres agricoles et de villages. Des études précédentes ont montré des signes indirects d’utilisation d’outils par ces chimpanzés pour déterrer des nids souterrains d’abeilles sans dard (Meliponini) et collecter du miel. Cet article met à jour les dernières découvertes sur l’utilisation de bâtons comme outils à Bulindi, en analysant des observations opportunistes effectuées entre juin 2018 et mars 2020. Nous avons d’abord établi que l’utilisation de bâtons dans les activités de fourragement est « courante » à Bulindi, c.à.d. partagée par la plupart, voire la totalité des individus adultes, subadultes et juvéniles. Les chimpanzés utilisent des bâtons dans des contextes variés de fourragement. Par exemple, ils utilisent des baguettes pour sonder des branches ou des souches contenant des insectes ou leurs produits (ex : les nids d’abeilles Apis mellifera et de Xylocopa sp., des asticots ou larves non identifiés), mais aussi pour extraire les nids de Meliponini du sol. Ensuite, nous avons analysé des séquences vidéos d’utilisation d’outils pour creuser le sol, impliquant six individus et nous avons comparé leurs comportements avec les techniques hautement complexes (« actions ») réalisées par les chimpanzés (P. t. troglodytes) de Loango, Gabon – seul site où des données sur les techniques comportementales d’extraction de nids souterrains d’abeilles sont disponibles. Bien que les données de Bulindi soient préliminaires, la plupart des actions et des types de préhension décrits à Loango sont présents dans le répertoire des chimpanzés de Bulindi. Par ailleurs, nos observations indiquent une forte tolérance sociale dans le contexte d’utilisation d’outils pour creuser à Bulindi, avec des exemples de transfert d’outils entre les individus. Globalement, notre étude suggère une grande similitude dans les techniques utilisées pour accomplir ces tâches complexes d’utilisation d’outils entre les chimpanzés de Bulindi et les chimpanzés de l’Afrique de l’est et de Loango en Afrique Centrale, à 2 500 km de distance. Les pressions d’origine anthropiques incluant la perte de forêts, la fragmentation et la dégradation des habitats peuvent réduire les diversités comportementale et « culturelle » chez les chimpanzés, en diminuant les opportunités de transmission sociale des comportements. Pourtant, l’exemple des chimpanzés de Bulindi démontre que l’utilisation complexe de bâtons comme outils existe dans des populations occupant des habitats extrêmement perturbés, alors que ces comportements semblent absents de zones proches de forêts continues (ex : la forêt de Budongo).

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Notes de la rédaction

Submitted March 22, 2020, accepted after revisions June 10, 2020, published online July 22, 2020.

Texte intégral

1 Introduction

1Wild chimpanzees (Pan troglodytes) use sticks as tools in a variety of foraging contexts, often to harvest social insects and/or their products, i.e., ants, termites and honey, among other embedded or difficult to access foods such as nuts (e.g., Nishida and Hiraiwa, 1982; Goodall, 1986; Boesch and Boesch, 1990; McGrew, 1992; Fowler and Sommer, 2007; Sanz and Morgan, 2007; Humle, 2011; Koops et al., 2013; Hicks et al., 2019). However, chimpanzee populations vary markedly in the forms, functions and complexity of their tool-assisted foraging behaviour. For example, recent studies in Central Africa suggest that chimpanzees in this region may have the most complex stick tool technologies yet described for exploiting insect prey, e.g., in the number of behavioural elements needed to accomplish the task and the regular use of tool sets (e.g., Sanz et al., 2004; Sanz and Morgan, 2007; Boesch et al., 2009; Boesch, 2013). Some differences in chimpanzee tool use relate to variation in the availability of particular resources, such as nuts or insect prey (e.g., Koops et al., 2013), or to characteristics of prey species (Sanz et al., 2014). However, a complex interplay of ecological and social (i.e., ‘cultural’) factors is widely held to shape the tool use behaviours of chimpanzee populations (e.g., Möbius et al., 2008).

2Compared to other regions where chimpanzees are studied, populations of P. t. schweinfurthii in mid-western Uganda have limited tool repertoires (Watts, 2008; Gruber et al., 2012; McLennan, 2014). Most notably, the well-studied chimpanzees of the Sonso ‘community’ in Budongo Forest do not use sticks for feeding at all (Gruber et al., 2011; Gruber, 2013), and evidence suggests communities elsewhere within Budongo may show a similar lack of stick tool use in foraging (Gruber et al., 2012; Mugisha et al., 2016). Gruber (2013) proposed that stick use may have disappeared among Budongo chimpanzees in response to changing ecological conditions that resulted in greater food availability and diversity. McLennan (2011), however, found evidence that chimpanzees in Bulindi, which inhabit unprotected forest fragments 25 km to the south of Budongo, use sticks to dig out and probe the underground nests of stingless bees (Meliponini). Subsequent analysis of faecal samples collected over a period of 22 months showed that honey from stingless bees and honey bees (Apis mellifera; Apini) is an occasional food item for the Bulindi chimpanzees, eaten throughout the year but most often during periods of low fruit availability (McLennan, 2015). However, behavioural data on the techniques used to access subterranean bee nests were previously unavailable. It was also unclear if the Bulindi chimpanzees used sticks in other foraging contexts, such as at Apis mellifera hives, although faecal analysis suggested they ignore certain species of ants (e.g., Dorylus spp., Camponotus spp.) and termites (Macrotermes sp., Pseudacanthotermes sp.), which are harvested with tools by some other chimpanzee populations (McLennan, 2014).

3Tools for accessing subterranean resources such as plant underground storage organs have been documented among some ancient hominin foragers as well as modern human foragers. More recently, it has become apparent that digging technology is also widespread in wild chimpanzees (e.g., Hernandez-Aguilar et al., 2007). Evidence of chimpanzees using sticks for digging (also referred to as ‘perforating’ or ‘puncturing’) to exploit honey stored in subterranean nests (reviewed in McLennan et al., 2019a) among other foods embedded underground, including termites and ants, has been reported widely at sites in Central Africa (e.g., Sugiyama, 1985; Fay and Carroll, 1994; Suzuki et al., 1995; Sanz et al., 2004; Fowler and Sommer, 2007; Boesch et al., 2009; Sanz et al., 2010; Dutton and Chapman, 2015; Estienne et al., 2017; Hicks et al., 2019), and may be a distinctive element of chimpanzee tool repertoires in that region. In comparison, tool-assisted digging has only rarely been described from the West and East of the species’ range (Yamagiwa et al., 1988; Hernandez-Aguilar et al., 2007; McLennan, 2011). As such, the occurrence of digging technology at Bulindi, and in at least one other nearby community outside the Budongo Forest (McLennan et al., 2019a), is noteworthy.

4Harvesting honey from stingless bee ground nests presents particular physical and cognitive challenges. Not only is the food hidden from view, but it is located up to 1 m below the ground and as far laterally from the bees’ tiny entrance tube at the surface, which is often the only visual clue of the nest’s presence (Boesch, 2013; see also Sommer et al., 2012). To date, behavioural data on the techniques employed by chimpanzees to excavate underground bee nests are available from a single site – Loango National Park in Gabon. Using camera trap footage, Estienne and colleagues (2017, 2019) showed that chimpanzees in Loango use a highly complex and flexible extraction technique, comprised of a diverse repertoire of discrete behavioural elements (or ‘actions’) (see also Boesch et al., 2009; Boesch, 2013). Moreover, successful honey extractions are normally achieved only after multiple visits to the same bee nest. The Loango study suggests that a strong social component is involved in the acquisition of this complex tool behaviour, with immatures observing the techniques performed by older, more experienced individuals – usually their mothers (Estienne et al., 2019). However, since data on ‘honey digging’ from other sites (including Bulindi) were based on indirect evidence, inter-site comparisons have not been possible previously.

5While earlier publications reported indirect evidence of tool-assisted foraging at Bulindi (McLennan, 2011, 2015), the chimpanzees are the focus of a long-term research project and behavioural data are accruing steadily. Thus, this article updates the earlier findings on tool use in Bulindi. While the chimpanzees use leaf tools in various contexts (e.g., for drinking or as napkins), as well as sticks in social contexts (e.g., during play, as clubs to threaten or strike another chimpanzee or other animal, or to throw at human observers), here we focus only on their use of sticks in a foraging context – primarily sticks used for digging into the ground (synonymous with ‘perforating’; Boesch et al., 2009; Estienne et al., 2017).

6Using opportunistically collected behavioural data, our first aim was to determine whether stick tool use in foraging contexts is ‘customary’, ‘habitual’, or merely ‘present’ behaviour (sensu Whiten et al., 1999, 2001; see definitions below) at Bulindi, with particular focus on the chimpanzees’ use of sticks for digging. Our second aim was to assess to what extent tool-assisted digging at Bulindi resembles techniques for excavating underground bee nests described previously for Central African chimpanzees P. t. troglodytes at Loango National Park, Gabon (Estienne et al., 2017, 2019).

2 Methods

2.1 Study site

7Bulindi (1°29ʹN, 31°28ʹE) is situated in Hoima District, western Uganda, 25 km south of Budongo Forest and 42 km northeast of Bugoma Forest (Figure 1). The Bulindi chimpanzees are one of at least nine chimpanzee communities inhabiting remnant fragments of riverine forest between the main Budongo and Bugoma forest blocks across a human-dominated landscape, which covers roughly 1,200 km2, known as the ‘Budongo–Bugoma corridor’ (McLennan, 2008; McCarthy et al., 2015). Chimpanzees at Bulindi were first studied in 2006–2007; at that time, they were unhabituated and all data on tool use were indirect, i.e., inferred from examination of manufactured artefacts found in situ after chimpanzees had vacated a site (McLennan, 2011). Research was restarted in 2012 and is on-going. Between 2012 and 2019 community size has varied from 18–22 individuals. The chimpanzees’ home range (ca. 21 km2) consists primarily of farmland and villages, interspersed with small fragments of unprotected, degraded forest along streams and around papyrus swamps. Common trees in these fragments include Phoenix reclinata palms, Pseudospondias microcarpa and members of the Moraceae, e.g. Trilepisium madagascariensis, Antiaris toxicaria and figs Ficus spp. (McLennan and Plumptre, 2012). Similar to the status of unprotected forest elsewhere in the Budongo–Bugoma corridor (McLennan, 2008), deforestation at Bulindi has been extensive: between 2006 and 2014, ca. 80% of forest used by the chimpanzees was converted to farmland (McLennan et al., 2020). However, there was no significant change in the frequency of beeswax and Apis and Meliponini bees found in faecal samples during this period (McLennan, 2015), suggesting that the rapidly changing ecological conditions did not elicit a major change in the frequency of honey foraging by the chimpanzees. For information on climate and phenology at Bulindi, see McLennan (2015); for the chimpanzee diet, see McLennan (2013) and McLennan et al. (2020).

Figure 1

Figure 1

Map showing the approximate range of the Bulindi chimpanzee community (dashed yellow circle) in Hoima District, western Uganda; adapted from Google Earth™ 2018. Bulindi is located 12 km from Hoima town, mid-way between the Budongo and Bugoma Forest Reserves in the so-called ‘Budongo–Bugoma corridor’. At least 9 resident chimpanzee communities inhabit riverine forest fragments in this corridor landscape in close proximity to villages.

Carte situant le domaine vital approximatif des chimpanzés de la communauté de Bulindi (cercle jaune en pointillés) du district de Hoima, Ouganda de l'ouest ; adapté de Google Earth™ 2018. Bulindi est situé à 12 km du centre ville de Hoima, à mi-chemin entre les réserves forestières de Budongo et de Bugoma, appelé le “corridor de Budongo et Bugoma”. Au moins 9 communautés de chimpanzés vivent au sein des fragments de forêts riveraines de ce corridor, dans une proximité importante avec les villages.

8The chimpanzees were habituated to researcher presence by 2015 and were usually observable at distances of 10 m or less (Cibot et al., 2019; McLennan et al., 2019b). However, full day follows were initiated only from 2018. To investigate the techniques used by the chimpanzees during tool-assisted digging specifically, and to document their use of stick tools in foraging contexts more widely, we used opportunistic behavioural observations between June 2018 and March 2020, when we followed the chimpanzees throughout the day, usually for 5 days per week. Aside from 3 births, membership of age classes (see below) remained constant during this period. Where possible, we made video recordings of stick tool use for subsequent analysis. However, dense vegetation at ground level within the degraded forest in Bulindi (e.g., Lantana camara thickets and vine tangles) sometimes precluded making video recordings of tool use. In such cases, we noted the identity of the tool user, the behaviour observed and, where possible, we inspected tool sites after the departure of chimpanzees to gain additional information – for example, to help clarify the goal of the tool using behaviour and/or examine tools left behind. Not all instances of stick use observed by research assistants T.S. and J-M.B. were formally documented (i.e., when they were collecting other data); thus, we were unable to estimate how often stick tool use occurs and we have avoided comparing frequencies of observations among individuals. The current data are, however, sufficient for assessing to what extent stick tool use is shown by all age-sex classes at Bulindi. Thus, following Whiten et al. (1999, 2001), we considered stick tool use in any foraging context generally, and in a digging context specifically, as ‘customary’ if it occurred in all or most members of at least one age-sex class during this period; ‘habitual’ if it was not customary but occurred repeatedly in several individuals; and merely ‘present’ if the behaviour was neither customary nor habitual but clearly identified. Age classes at Bulindi follow Cibot et al. (2019): adult (≥ 12 years), adolescent (8–11 years), juvenile (4–7 years); we did not consider infants (0–3 years) because, while infants at Bulindi frequently manipulate sticks (unpublished data), goal-directed stick use in foraging has not been observed among individuals in this age class.

9Next, we analysed video recordings made opportunistically of chimpanzees using sticks for digging, in which the techniques employed by individuals could be assessed. We analysed two videos from 2019, supplemented by an earlier recording from 2015, showing tool-assisted digging behaviour by six individuals from the Bulindi community. None of the three recordings are complete since filming began only after an individual was noticed digging and in each case the chimpanzee(s) abandoned the activity before successfully locating the presumed target, i.e., a stingless bee ground nest. Long-term data, including extensive faecal sampling, confirm that the chimpanzees do not prey on termites or ants from subterranean or epigeal nests in Bulindi, though suitable prey species are present (McLennan, 2014). Thus, we assumed that a stingless bee ground nest was the intended target in instances of digging when we were unable to confirm the presence of an active bee nest.

10We assessed to what extent the techniques shown by Bulindi chimpanzees when digging resemble the complex behaviours used by chimpanzees to excavate stingless bee ground nests at Loango, Gabon. The behaviours of each individual in the three video recordings were coded independently by M.R.M. and M.C., according to behaviours (or ‘actions’) defined by Estienne et al. (2017, 2019). Of 197 actions identified in the videos, there was 93% agreement in coding between M.R.M. and M.C. The rare instances of divergence occurred when an individual’s behaviour was not clearly visible, for example when the chimpanzee was obscured by vegetation or had its back to the camera. We excluded all such ambiguous behaviour when determining the observed repertoire of techniques shown by each individual. Following Estienne et al. (2017), we grouped actions identified in the video recordings into three categories: exploration (including inspection of the ground or hole without tools); tool manufacture or modification; and extraction, which included all tool using behaviour (see Table A in Appendix for definitions). We distinguished tool-assisted digging (which includes extraction actions such as ‘perforate’ and ‘rotate’) from manual digging without tools. Additionally, we coded the type of grip shown by an individual during tool-assisted extraction actions (Appendix).

11Finally, we made preliminary observations on the social context of tool use in the three video recordings, in particular the transfer of sticks between individuals (i.e., tool sharing). Following Musgrave et al. (2016) we defined a tool transfer as the change of possession of a stick tool from one individual to another (see also Pruetz and Lindshield, 2012). We further categorised the type of tool transfer according to definitions in Musgrave et al. (2020), i.e., whether or not the transfer was preceded by a request from the recipient (i.e., begging), and whether the transfer was initiated by the possessor of the tool (active transfer) or was simply tolerated without protest (tolerated take).

3 Results

3.1 Stick tool use is ‘customary’ in Bulindi

12Of 16 adult, subadult and juvenile individuals in the Bulindi community between June 2018 and March 2020, 11 individuals (69%) were documented using stick tools in foraging on at least one occasion (Table 1). Nine individuals (56%) were documented using sticks presumably to locate underground stingless bee nests (see below). Besides tool-assisted digging, individuals used sticks to probe holes or crevices in live or dead branches or logs, both in trees and on the ground (Figure 2; Supplementary Video 1). The purpose of tool-assisted probing could not always be determined. However, two subadult males used sticks to investigate carpenter bee (Xylocopa sp.) nests in dry branches and/or to rouse the adult bees; two individuals (a juvenile female and subadult male) used sticks to investigate dry branches in which unidentified grubs or larvae were present; a juvenile female and subadult female inserted sticks into a crevice in a branch that had been colonised by Apis mellifera bees; and one subadult male inserted a large stick into an abandoned Apis mellifera hive that was within the trunk of a felled tree and dislodged part of the hive wall. Two individuals used stick tools to ‘dip’ for fluids (i.e., extractive foraging): one subadult male repeatedly inserted a stick into a dry branch containing a Xylocopa nest and seemingly licked ‘honey’ (or ‘bee bread’) from the stick’s end; a subadult female pushed large leafy branches forcibly into a large tree hollow and subsequently extracted and ingested an unknown substance – possibly honey from an arboreal stingless bee nest.

Figure 2

Figure 2

Examples of probe tool use at Bulindi. (A): Subadult female manufacturing a probe tool from a leafy branch of a Trema orientalis tree; she used it to investigate a crevice in a branch of the tree that was colonised by Apis mellifera honey bees; (B): Five year old juvenile female using a small stick to probe a dry branch containing unidentified grubs or larvae; (C): Subadult male inserting a long stick (81 cm in length) into a hollow within the trunk of a felled Glenniea africana tree that contained an abandoned Apis mellifera nest – the presence of honeycomb and beeswax suggests the honey had been harvested previously by local people or the chimpanzees; he used the stick to dislodge part of the hive wall. Note that the grip type used (hand and foot together) resembles the grip used by some individuals to perforate the ground with sticks (i.e., digging).

Exemple d'utilisation d'outils à Bulindi. (A) : une femelle subadulte fabriquant une baguette à partir d'une branche feuillue de l'espèce d'arbre Trema orientalis ; elle utilise cet outil pour investiguer une crevasse dans une branche de l'arbre qui avait été colonisée par les abeilles mellifères Apis mellifera ; (B) : une femelle juvénile de 5 ans utilisant un petit bâton pour sonder une branche sèche contenant des asticots et/ou des larves non identifiés ; (C) : un mâle subadulte insérant un long bâton (81 cm de longueur) dans une cavité d'un tronc d'arbre tombé de l'espèce Glenniea africana contenant un nid abandonné d'Apis mellifera – la présence de structures alvéolaires et de cire d'abeilles suggère que du miel a été collecté précédemment par les populations humaines locales ou par les chimpanzés ; ce chimpanzé utilise un bâton pour dégager une partie de la cloison de la ruche. À noter que le type de préhension utilisée (main et pied conjointement) ressemble à celle utilisée par certains individus qui perforent le sol avec des bâtons (c.à.d. creuser).

13These preliminary data indicate that stick tool use for digging specifically, and in a foraging context generally, is ‘customary’ behaviour among chimpanzees in Bulindi (i.e., occurring in all or most members of at least one age-sex class; Table 1).

3.2 Techniques used for digging with sticks

14Table 2 lists the behavioural techniques (‘actions’) shown by 6 individuals of the Bulindi community from video analysis of tool-assisted digging (Figure 3). These 6 individuals comprised an adult female and adult male, a subadult female and a subadult male, as well as two juveniles aged 5 years; the subadult male (Araali) featured in two recordings. Further to the 18 actions in the behavioural categories exploration, tool manufacture / modification, and extraction defined by Estienne et al. (2017) and (2019) for the Loango chimpanzees, we recognised an additional 3 actions (‘taste’, ‘position tool’ and ‘probe’; see Table A in Appendix for definitions). Of these 21 actions, 16 were performed by at least one individual, with most performed by 3–6 individuals (Table 2; Supplementary Video 2). The absence of actions associated with honey extraction and consumption (i.e., ‘extract honey’, ‘eat’ and ‘lick’) is explained by the fact that chimpanzees were not successful in locating a bee nest and accessing the underground chamber containing the honey in any of the recordings.

Table 1

Table 1

The number (and %) of chimpanzees in each age-sex class documented using stick tools at least once (A) in any foraging context, and (B) in the context of digging at a presumed ground bee nest specifically; behavioural data are from June 2018–March 2020.

Nombre (%) de chimpanzés de chaque classe d’âge et de sexe ayant été répertoriés utilisant des bâtons comme outils, au moins une fois, (A) pour fourrager, et (B) pour creuser le sol à la recherche présumée de nids d’abeilles et de miel ; ces données comportementales ont été collectées de juin 2018 à mars 2020.

Figure 3

Figure 3

Two examples of tool-assisted digging; the presumed target in both cases is a Meliponini ground nest. (A): Subadult female using a stick tool to perforate the ground. She is holding the tool under her chin with one hand, enabling her to apply greater force to the action by using her upper body; this grip type was not described from Loango (Estienne et al., 2017); (B): Subadult male using a stick tool to perforate the ground, initially using a ‘hands only’ grip; (C): He subsequently switched grip to use both hands and a foot simultaneously while performing the action ‘rotate’; (D): Throughout this sequence the subadult male’s behaviour was watched closely by two immature individuals, a 5-year old juvenile male and an infant female aged 3 years. The subadult male subsequently allowed the juvenile to take the stick (tolerated tool transfer), which the latter used to perforate the ground (see Supplementary Video 3). The subadult and juvenile are not maternal relatives (unpublished data).

Deux exemples d’utilisation d’outils pour creuser le sol ; le but présumé dans les deux cas est d’extraire du miel d’un nid au sol de Meliponini. (A) : une femelle subadulte utilisant un bâton comme outil pour perforer le sol. Elle cale l’outil sous son menton avec une main, lui permettant d’appliquer une force plus importante sur le bâton en faisant peser la partie supérieure de son corps sur ce dernier ; ce type de préhension n’est pas décrit à Loango (Estienne et al., 2017) ; (B) : un mâle subadulte utilisant un bâton comme outil pour perforer le sol, initialement en se servant uniquement de ses mains – prise définie comme « hands only / mains seulement » ; (C) : Il change ensuite de type de préhension en utilisant ses deux mains ainsi que son pied simultanément alors qu’il réalise une « rotation » de l’outil ; (D) : tout le long de cette séquence, un mâle juvénile de 5 ans et une enfant femelle de 3 ans observent de façon rapprochée le comportement du mâle subadulte. Par la suite, le mâle adolescent a autorisé le juvénile à prendre le bâton (transfert d’outil toléré) dont il se servait pour perforer le sol (voir la vidéo 3). Le subadulte et le juvénile ne sont pas apparentés du côté maternel (données non publiées).

15A notable difference between the Loango and Bulindi communities concerns the extractive action ‘pound’, which occurs when an individual at Loango strikes the ground with a stick repeatedly: this action was not shown by any individual at Bulindi and may be absent from individual repertoires at this site.

Behaviours (‘actions’) performed by 6 individuals of the Bulindi community during 3 video-recorded episodes of tool-assisted digging. Behavioural categories and actions follow definitions in Estienne et al. (2017, 2019); see Appendix. Grip types used by each individual for tool-assisted extraction actions are also shown. An ‘X’ indicates that the individual performed the action or grip type.

Catégories de comportements et actions réalisés par 6 individus de la communauté de Bulindi au cours de 3 épisodes d’utilisation d’outils pour creuser le sol, enregistrés par vidéo. Les actions suivent les définitions d’Estienne et al. (2017, 2019) ; voir annexe. Les types de préhension utilisés par chaque individu lors des actions utilisant un outil sont aussi notés. Un « X » indique que l’individu a réalisé l’action ou le type de préhension.

16Among 4 grip types used for tool-assisted extraction actions at Loango, we confirmed the grips ‘hands only’, ‘both (hands and feet together)’ and the grip modifier ‘amplify strength’ among Bulindi individuals (Table 2). Additionally, we recognised a grip type not described from Loango, i.e. ‘hands with tool under chin’: at Bulindi a subadult female and juvenile female held a tool beneath their chin with one or both hands, respectively, when perforating the ground with the stick’s other end (Figure 3a). This grip apparently enabled them to utilise increased upper body strength and apply greater force to the action (Supplementary Video 2).

3.3 Tool transfers

17In video recordings #2 and #3 (Supplementary Video 3) multiple individuals were present at digging sites simultaneously. Non-tool using individuals generally showed interest in the activity of tool users, while tool users showed a high level of tolerance towards other individuals in close proximity. In particular, immature individuals (two infants and two juveniles) showed strong interest in the activity of older tool-using individuals, in their tools, and in holes made in the ground (Figure 3). Tool transfers occurred in the recordings on 7 occasions. On separate occasions a juvenile female and a juvenile male (both aged 5 years) picked up sticks and used them to perforate the ground after an older individual – a subadult male who was the manufacturer of each tool – discarded the tool and left the vicinity. An adult female also reused a discarded stick that had been manufactured by the same subadult male. Three other tool transfers corresponded to Musgrave and colleagues’ (2020) ‘tolerated take’ (or ‘share-allowed’ in Estienne et al., 2019) and occurred when a male possessor allowed another individual to take a tool that was in his possession. In no case was the transfer preceded by a request (i.e., begging) and each case was tolerated by the possessor. Twice an immature individual took a stick tool from an unrelated older male. In one of these cases, a 2.5 year old infant manipulated and played with the stick but did not use it as a tool (this stick was subsequently retrieved by the infant’s mother who used it to perforate the ground herself); in the other case a juvenile male immediately used the stick to perforate the ground (Supplementary Video 3). In the remaining case, the older male repossessed his stick from the juvenile male, after the latter paused while digging with it.

4 Discussion

18Tool using behaviour at Bulindi awaits systematic investigation. Even so, current data allow us to confirm that stick use in foraging contexts is ‘customary’ in this community, i.e., occurring in all or most members of most age-sex classes (sensu Whiten et al., 1999; 2001) (Table 1). While similar to most studied chimpanzee populations, customary stick tool use at Bulindi contrasts with the leaf-based tool repertoires of the well-known Sonso community (Reynolds, 2005; Gruber et al., 2011; Hobaiter et al., 2014) and also the neighbouring Waibira community (Mugisha et al., 2016) in the Budongo Forest. Remarkably, Sonso chimpanzees do not use stick tools in foraging at all (Gruber et al., 2011, 2012; Gruber, 2013), with individuals showing ‘a complete disregard for sticks’ before reaching adulthood (Lamon et al., 2018). In contrast, evidence of stick tool use by chimpanzees inhabiting forest fragments at several sites outside the main Budongo and Bugoma forest blocks is accumulating (Mairirwe: McLennan et al., 2019a; Kasongoire: Oxley and Jovan, 2019). The updated findings from Bulindi, along with preliminary data from these newer sites, contribute to our understanding of the variability in ‘cultural’ behaviours including tool use among western Ugandan populations, and call for microecological and hypothesis-driven studies to help explain this regional variation (Gruber, 2013). Subtle ecological differences likely influence aspects of the technological variation observed among chimpanzees in the Budongo–Bugoma landscape, and throughout western Uganda more generally (see below). Even so, Hedges and McGrew (2012) found no evidence that insect prey occurred at low densities in the Sonso region of Budongo, and concluded that the absence of extractive foraging in resident chimpanzees most likely reflects their lack of ‘cultural knowledge’. Similar findings were also reported from Semliki (located southwest of Bugoma), where tool-assisted insectivory appears to be rare (Webster et al., 2014).

19Prior to recent insights from Loango, Gabon (Estienne et al., 2017, 2019), all previous data on use of sticks by chimpanzees to dig out stingless bee ground nests were indirect (e.g., Yamagiwa et al., 1988; Fay and Carroll, 1994; Fowler and Sommer, 2007; Boesch et al., 2009; McLennan, 2011; Sommer et al., 2012; Dutton and Chapman, 2015; Hicks et al., 2019). Thus, the behavioural data presented here provide the first opportunity for a cross-site comparison with Loango. Given the anecdotal nature of observations from Bulindi, however, our comparison with the techniques used by chimpanzees in Loango is necessarily preliminary. Nevertheless, we confirmed that most of the actions and grip types described from Loango are present at Bulindi. Even so, individual repertoires are undoubtedly larger than indicated by our preliminary data (Table 2). For example, only two individuals performed actions related to manufacturing new tools (‘break’ and ‘remove side branches’), since in most cases individuals had already manufactured tools by the time the video recordings started, or reused tools previously manufactured by other chimpanzees. Moreover, previous analysis of tools recovered from stingless bee ground nests at Bulindi indicate that tool-making and modifying actions, i.e., ‘break’, ‘cut-off’, ‘strip bark’ and ‘remove side branches’, are applied routinely to digging sticks (McLennan, 2011). At Bulindi, we recognised a grip type used to perforate the ground that was not described from Loango, i.e., ‘hands with tool under chin’. While the absence of this grip type from individual repertoires at Loango needs verifying, it potentially represents a behavioural variant that is unlikely to be related to ecological differences.

20One common extractive action used at ground bee nests by Loango chimpanzees (‘pound’) was not observed in Bulindi. Pounding (i.e., percussion of a tool onto another object or substrate; Sanz and Morgan, 2007) appears to be a common component of honey gathering techniques for P. t. troglodytes in Central Africa, most often in an arboreal context (e.g., Fay and Carroll, 1994; Bermejo and Illera, 1999; Hicks et al., 2005; Sanz and Morgan, 2007; Boesch et al., 2009; Wilfried and Yamagiwa, 2014), but seems rare or absent elsewhere or in other chimpanzee subspecies. Since the chimpanzees at Bulindi were unsuccessful at locating the honey chamber in the video recordings analysed, we did not score any actions associated with honey extraction and consumption (i.e., ‘extract honey’, ‘eat’ and ‘lick’). The occurrence, however, of stingless bees and beeswax in faecal samples, and occasional beeswax sign at excavated bee nests, confirms that the chimpanzees are at times successful (see McLennan, 2011, 2015). Estienne et al. (2017) reported that successful extractions were relatively rare at Loango and achieved only after multiple visits to a bee nest; similar use of camera traps at stingless bee ground nests in Bulindi could reveal how often the chimpanzees successfully obtain honey.

21Overall, our data suggest close alignment between the techniques used to perform a complex tool-assisted task in a population of P. t. schweinfurthii in East Africa and a population of P. t. troglodytes in Central Africa, separated by almost 2,500 km. McLennan et al. (2019a) further showed that digging sticks (synonymous with ‘perforating sticks’) used to excavate stingless bee ground nests at Bulindi and the nearby Mairirwe site (located 25 km from Bulindi) were remarkably similar in length to digging sticks used by several chimpanzee populations in the Central African region, i.e., Gashaka and Ngel Nyaki in Nigeria, and Bili-Uéré in the Democratic Republic of Congo; however, they were somewhat shorter than sticks used at Loango.

22While stick tool use occurs in various contexts in Bulindi, we were unable to estimate the frequency of foraging tool use in the present study. This will require future systematic research. Thick vegetation in the heavily disturbed forest has hindered good observations of the chimpanzees’ behaviour at ground-level, despite most individuals being well-habituated since 2015 (Cibot et al., 2019). We expect that additional individuals use stick tools besides those documented doing so during the period considered here (e.g., several adult females; Table 1). Even so, we do not think tool-assisted foraging is especially common at Bulindi when compared to some other populations that use tools to harvest social insects frequently, at times on a daily basis (e.g., Macrotermes termite-fishing at Gombe, Tanzania: McGrew, 1979; and at Fongoli, Senegal: Bogart and Pruetz, 2011; Camponotus ant-fishing at Mahale, Tanzania: Nishida and Hiraiwa, 1982). Additionally, we have never seen Bulindi chimpanzees making and using tools to harvest edible species of ants and termites, which is consistent with data from faecal analysis (McLennan, 2014), and is similar to other populations in mid-western Uganda (Budongo: Reynolds, 2005; Mugisha et al., 2016; Kibale: Watts, 2008; Semliki: Webster et al., 2014); however, this pattern contrasts with at least one Ugandan population further south, where the chimpanzees dip for Dorylus sp. ants (Kalinzu: Hashimoto et al., 2015). More generally, chimpanzees that exhibit one or more forms of tool-assisted insectivory – whether termite-fishing, ant dipping or ant-fishing, or honey digging – often lack other forms shown by populations elsewhere, despite availability of insect prey (for a recent review see Wondra et al., 2016). For example, chimpanzees in Gashaka and Bili-Uéré use sticks to dig and probe for honey and to capture multiple ant species, but neither population fishes for termites (Fowler and Sommer, 2007; Hicks et al., 2019).

23Broad regional patterns of chimpanzee tool use are nevertheless apparent (‘behavioural realms’, Hicks et al., 2019). In the case of honey digging at Meliponini ground nests, this technological behaviour might have been invented independently by some Ugandan populations. Alternatively, honey digging might represent a formerly large scale behavioural realm that extended from West-Central Africa eastward to the Albertine Rift, but went extinct in many Ugandan populations – such as those in Budongo Forest – for unknown reasons.

24Our preliminary observations suggest that tool users at Bulindi are highly tolerant of others, particularly younger, less competent individuals. We observed several instances of passive tool transfer in both video recordings in which multiple individuals were present at digging sites. Under some conditions, transfer of tools has been proposed to constitute a form of teaching in chimpanzees (Musgrave et al., 2016, 2020). We confirmed that transfer of tools from older more skilled individuals to younger less competent individuals occurs at Bulindi (Supplementary Video 3). At Loango, immature chimpanzees acquired the techniques for accessing stingless bee ground nests over a long period, which involved both non-social (i.e., physical maturation) and social learning processes (Estienne et al., 2019). While more data are needed, we anticipate that social influences play a similarly important role in the acquisition of this complex tool-assisted task at Bulindi.

25The Bulindi chimpanzees inhabit one of the most human-modified and deforested environments in which chimpanzees have been studied (McLennan et al., 2019b, 2020). Human impacts including forest loss, fragmentation and degradation might reduce opportunities for cultural transmission in chimpanzees, potentially leading to a loss of behavioural and cultural diversity (Kühl et al., 2019). The occurrence of complex stick tool use in Bulindi, and its apparent absence in the nearby main forest block, cautions that we should not assume that modified habitats result in impoverished behavioural repertoires (or low ‘cultural value’) in chimpanzees in the absence of long-term ecological and ethological field studies (Hockings and McLennan, 2019).

Acknowledgements

26We thank the Uganda National Council for Science and Technology, the President’s Office, and the Uganda Wildlife Authority for permission to study the chimpanzees of Bulindi. We are grateful for the assistance of many local residents and local leaders in the range of the chimpanzees. Field staff of the Bulindi Chimpanzee and Community Project helped in various ways during this research; we extend our particular thanks to the Project Manager, Moses Ssemahunge. Research and conservation at Bulindi was supported by funding from Blair Drummond Safari Park, Born Free Foundation, European Outdoor Conservation Association, Friends of Chimps, the Jane Goodall Institute–Switzerland, Leverhulme Trust UK, and Prince Bernard Nature Fund. We are grateful to Cleve Hicks and Alejandra Pascual-Garrido for their helpful feedback on the draft manuscript.

27This article is dedicated in loving memory of Jackie Rohen, author and co-director of the Bulindi Chimpanzee and Community Project, who worked passionately to conserve the chimpanzees of Bulindi and improve the lives of the people living alongside them.

Declaration of Competing Interests

28The authors declare that they have no competing interests.

Appendix

29Supplementary videos for this article are available in the online version of the article on the website of the Revue de Primatologie (Varia 10 | 2019).
https://journals.openedition.org/​primatologie/​

Ethogram used for coding behaviours (‘actions’) performed during video-recorded episodes of tool-assisted digging by chimpanzees in Bulindi, and grip types used (adapted from Estienne et al., 2017, 2019).

Ethogramme utilisé pour coder les comportements (« actions ») réalisés par les chimpanzés de Bulindi durant les épisodes d’utilisation d’outils pour creuser, et les types de préhension utilisés (adaptés à partir d’Estienne et al., 2017, 2019) (enregistrements par vidéo).

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Table des illustrations

Titre Figure 1
Légende Map showing the approximate range of the Bulindi chimpanzee community (dashed yellow circle) in Hoima District, western Uganda; adapted from Google Earth™ 2018. Bulindi is located 12 km from Hoima town, mid-way between the Budongo and Bugoma Forest Reserves in the so-called ‘Budongo–Bugoma corridor’. At least 9 resident chimpanzee communities inhabit riverine forest fragments in this corridor landscape in close proximity to villages.
URL http://journals.openedition.org/primatologie/docannexe/image/6706/img-1.jpg
Fichier image/jpeg, 4,5M
Titre Figure 2
Légende Examples of probe tool use at Bulindi. (A): Subadult female manufacturing a probe tool from a leafy branch of a Trema orientalis tree; she used it to investigate a crevice in a branch of the tree that was colonised by Apis mellifera honey bees; (B): Five year old juvenile female using a small stick to probe a dry branch containing unidentified grubs or larvae; (C): Subadult male inserting a long stick (81 cm in length) into a hollow within the trunk of a felled Glenniea africana tree that contained an abandoned Apis mellifera nest – the presence of honeycomb and beeswax suggests the honey had been harvested previously by local people or the chimpanzees; he used the stick to dislodge part of the hive wall. Note that the grip type used (hand and foot together) resembles the grip used by some individuals to perforate the ground with sticks (i.e., digging).
URL http://journals.openedition.org/primatologie/docannexe/image/6706/img-2.jpg
Fichier image/jpeg, 1,3M
Titre Table 1
Légende The number (and %) of chimpanzees in each age-sex class documented using stick tools at least once (A) in any foraging context, and (B) in the context of digging at a presumed ground bee nest specifically; behavioural data are from June 2018–March 2020.
URL http://journals.openedition.org/primatologie/docannexe/image/6706/img-3.jpg
Fichier image/jpeg, 1,5M
Titre Figure 3
Légende Two examples of tool-assisted digging; the presumed target in both cases is a Meliponini ground nest. (A): Subadult female using a stick tool to perforate the ground. She is holding the tool under her chin with one hand, enabling her to apply greater force to the action by using her upper body; this grip type was not described from Loango (Estienne et al., 2017); (B): Subadult male using a stick tool to perforate the ground, initially using a ‘hands only’ grip; (C): He subsequently switched grip to use both hands and a foot simultaneously while performing the action ‘rotate’; (D): Throughout this sequence the subadult male’s behaviour was watched closely by two immature individuals, a 5-year old juvenile male and an infant female aged 3 years. The subadult male subsequently allowed the juvenile to take the stick (tolerated tool transfer), which the latter used to perforate the ground (see Supplementary Video 3). The subadult and juvenile are not maternal relatives (unpublished data).
URL http://journals.openedition.org/primatologie/docannexe/image/6706/img-4.jpg
Fichier image/jpeg, 5,6M
Titre Table 2
URL http://journals.openedition.org/primatologie/docannexe/image/6706/img-5.jpg
Fichier image/jpeg, 1,9M
Légende Behaviours (‘actions’) performed by 6 individuals of the Bulindi community during 3 video-recorded episodes of tool-assisted digging. Behavioural categories and actions follow definitions in Estienne et al. (2017, 2019); see Appendix. Grip types used by each individual for tool-assisted extraction actions are also shown. An ‘X’ indicates that the individual performed the action or grip type.
URL http://journals.openedition.org/primatologie/docannexe/image/6706/img-6.jpg
Fichier image/jpeg, 2,6M
Titre Table A
URL http://journals.openedition.org/primatologie/docannexe/image/6706/img-7.jpg
Fichier image/jpeg, 1,9M
Légende Ethogram used for coding behaviours (‘actions’) performed during video-recorded episodes of tool-assisted digging by chimpanzees in Bulindi, and grip types used (adapted from Estienne et al., 2017, 2019).
URL http://journals.openedition.org/primatologie/docannexe/image/6706/img-8.jpg
Fichier image/jpeg, 1,9M
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Référence électronique

Matthew R. McLennan, Jacqueline Rohen, Zoe Satsias, Tom Sabiiti, John-Mary Baruzaliire et Marie Cibot, « ‘Customary’ use of stick tools by chimpanzees in Bulindi, Uganda: update and analysis of digging techniques from behavioural observations », Revue de primatologie [En ligne], 10 | 2019, mis en ligne le 21 juillet 2020, consulté le 01 mars 2021. URL : http://journals.openedition.org/primatologie/6706 ; DOI : https://doi.org/10.4000/primatologie.6706

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Auteurs

Matthew R. McLennan

Bulindi Chimpanzee and Community Project, Hoima, Uganda
Department of Social Sciences, Oxford Brookes University, Oxford, UK
Centre for Ecology and Conservation, University of Exeter, Cornwall, UK
Email: mmclennan@brookes.ac.uk; mclennan.bccp@gmail.com

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Jacqueline Rohen

Bulindi Chimpanzee and Community Project, Hoima, Uganda

Articles du même auteur

Zoe Satsias

Centre for Ecology and Conservation, University of Exeter, Cornwall, UK

Tom Sabiiti

Bulindi Chimpanzee and Community Project, Hoima, Uganda

John-Mary Baruzaliire

Bulindi Chimpanzee and Community Project, Hoima, Uganda

Marie Cibot

Bulindi Chimpanzee and Community Project, Hoima, Uganda
Department of Social Sciences, Oxford Brookes University, Oxford, UK
Anicoon Vétérinaires, Ploemeur/Larmor-Plage, France
E-mail: marie.cibotchemin@gmail.com

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