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Special issue: Tool use among Ugandan forest fragment chimpanzees

Digging for clues: Stick tools used for honey digging in a second community of ‘forest fragment chimpanzees’ outside the Budongo and Bugoma Forests, Uganda

A la recherche d’indices : Utilisation de bâtons comme outils pour creuser et collecter du miel par une seconde communauté de chimpanzés vivant dans des fragments forestiers voisins de Budongo et Bugoma, Ouganda
Matthew R. McLennan, Georgia A. Lorenti, Simon Mugenyi, Jonan Muganzi et Jacqueline Rohen

Résumés

Les chimpanzés (Pan troglodytes) sont les utilisateurs d’outils les plus fréquents parmi les primates non-humains. Documenter l’utilisation d’outils par des populations de chimpanzés nouvellement étudiées et identifier les variations technologiques parmi des groupes régionaux (« communautés ») permet de comprendre les diversités comportementale et « culturelle » de cette espèce. Certaines populations de chimpanzés utilisent des bâtons pour creuser à la recherche de miel dans des nids souterrains d’abeilles sans dard (Meliponini). Fourrager pour collecter du miel a été rapporté le plus souvent dans des sites d’Afrique Centrale et de l’Ouest mais apparaît moins fréquent en Afrique de l’Est. Les chimpanzés de l’ouest de l’Ouganda présentent un répertoire d’outils peu varié. En particulier, les chimpanzés bien étudiés de la forêt ougandaise de Budongo sont réputés pour ne pas utiliser de bâtons dans leurs activités de fourragement. Néanmoins, creuser avec des bâtons à la recherche de miel existe dans la communauté de Bulindi, qui habite des fragments rémanents de forêts riveraines, entre les forêts de Budongo et de Bugoma. Auparavant, il n’était pas certain que seule cette communauté utilise cette technique parmi les autres communautés de chimpanzés résidant dans le corridor Budongo-Bugoma. Dans cette étude, nous mettons en évidence que les chimpanzés d’une seconde communauté (nommée Mairirwe), dont le territoire comprend des fragments forestiers hors des forêts de Budongo et de Bugoma, utilisent des bâtons pour collecter du miel. Les bâtons ayant servi à creuser (ou « perforer ») deux nids de Meliponini dans le sol à Mairirwe sont remarquablement similaires en terme de dimension à ceux utilisés à Bulindi. Les bâtons utilisés par ces deux populations ougandaises voisines sont aussi similaires à ceux utilisés pour extraire du miel par les chimpanzés en Afrique Centrale, suggérant une relative uniformité dans les comportements d’utilisation d’outils à travers une large aire géographique. Notre étude montre aussi que les chimpanzés rentrent en compétition avec les humains pour accéder cette ressource souterraine à Mairirwe, puisque les populations locales utilisent des machettes pour déterrer les nids d’abeilles. Nos données suggèrent que creuser à l’aide d’un outil pour collecter du miel pourrait être un comportement de fourragement commun chez les chimpanzés présents dans les fragments forestiers riverains à l’extérieur des forêts de Budongo et de Bugoma. Cette étude souligne donc l’importance de ne pas ignorer les populations de chimpanzés qui survivent dans ces habitats dégradés et modifiés par l’Homme, hors des blocs forestiers majeurs, telles que les communautés de Mairirwe et de Bulindi. Ces groupes doivent être considérés comme des modèles régionaux expliquant les variations locales d’utilisation d’outils par les chimpanzés.

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Notes de la rédaction

Submitted December 1, 2019, accepted after revisions April 21, 2020, published online July 22, 2020.

Texte intégral

1 Introduction

1Chimpanzees (Pan troglodytes) are one of the most frequent tool users among nonhuman primates (McGrew, 1992; Sanz et al., 2013). Field studies of wild chimpanzees across the species’ distribution in tropical Africa have revealed striking differences among populations in the frequency, forms, functions and complexity of their tool use behaviour. Although regional patterns of tool use are apparent (‘behavioural realms’, Hicks et al., 2019), differences have been found among neighbouring groups (Luncz et al., 2012; O’Malley et al., 2012; Koops et al., 2015; Pascual-Garrido, 2019), and no two chimpanzee groups (known as ‘communities’) have yet been shown to possess identical tool repertoires. Environmental constraints (e.g., the absence or scarcity of a particular resource) inevitably influence the distribution of some tool behaviours, but an available resource accessed with tools by one community may not be accessed similarly by chimpanzees of another (McGrew et al., 1997; Humle and Matsuzawa, 2004; Möbius et al., 2008; Gruber et al., 2009). Where the acquisition of tool use involves some form of social learning, and the behaviour represents a group-level norm, tool use by chimpanzees is usually considered ‘cultural’ (see McGrew, 1992; Whiten et al., 1999; Whiten et al., 2005). Thus, documenting use of tools in newly-studied chimpanzee populations contributes to our understanding of the cultural diversity of this species. At more regional levels, identifying differences in tool use and foraging behaviour among nearby populations is useful for stimulating investigation into the causes of behavioural and cultural variation (Humle and Matsuzawa, 2001; Gruber et al., 2012; Luncz and Boesch, 2015).

2Chimpanzees (P. t. schweinfurthii) in mid-western Uganda are unusual: they exhibit rare or restricted insectivory and have meagre foraging tool kits compared to populations elsewhere (Watts, 2008; Gruber et al., 2012; McLennan, 2014; Webster et al., 2014). Most notably, well-studied chimpanzees in Uganda’s Budongo Forest have never been observed using stick tools in foraging contexts (Reynolds, 2005; Gruber et al., 2011, 2012; Gruber, 2013; Mugisha et al., 2016), despite availability of suitable insect prey (Hedges and McGrew, 2012). Recently, however, stick tool use was reported in chimpanzees living in unprotected forest fragments to the south of Budongo Forest, in Bulindi (McLennan, 2011). Specifically, evidence was found that Bulindi chimpanzees used sticks to dig out underground nests of stingless bees (Meliponini), involving a probable tool set composed of stout digging sticks and more slender probes (McLennan, 2011). Direct observations have since confirmed this tool-assisted foraging behaviour in Bulindi (McLennan et al., 2019). Besides Bulindi, however, tool use has not been investigated in chimpanzees ranging in forest fragments outside Uganda’s main forest blocks.

3The harvesting of honey and brood from nests of honeybees (Apis mellifera) and stingless bees occurs at sites throughout East, West, and Central Africa, and appears to be a universal foraging activity in chimpanzees (Sanz and Morgan, 2009; McLennan, 2015). In some instances, chimpanzees are able to gather honey with their hands without using sticks – as chimpanzees in Budongo do, for example (Reynolds, 2005; Gruber et al., 2011). More often, however, they employ a tool technology of varying sophistication to breach the bee’s defences and access the honey (Sanz and Morgan, 2009). Stingless bees nest both in tree cavities and underground (Kajobe, 2007). Accessing honey stored in subterranean nests poses special physical and cognitive challenges (Boesch, 2013): the chamber containing the honey is out of sight and located up to 1 m underground and as far laterally from the bees’ tiny entrance tube at the surface. Thus, a chimpanzee must use sticks to dig into the ground to locate the hidden honey chamber (Boesch et al., 2009; Boesch, 2013). Typically, multiple extraction attempts are required to successfully obtain honey (Estienne et al., 2017a).

4‘Honey digging’ with stick tools by chimpanzees has a patchy distribution geographically, but is reported mainly in the Central Africa region (P. t. troglodytes: Fay and Carroll, 1994; Hicks et al., 2005; Deblauwe, 2006; Boesch et al., 2009; Estienne et al., 2017a; P. t. ellioti: Sommer et al., 2012; Dutton and Chapman, 2015; P. t. schweinfurthii: Hicks et al., 2019) and, more rarely, further east (P. t. schweinfurthii: Yamagiwa et al., 1988; McLennan, 2011). Besides Bulindi, in Uganda honey digging reportedly occurs in the Sebitoli chimpanzee community in Kibale National Park (S. Krief, pers. comm.), but is seemingly absent in other long-term research communities there, and in Budongo (Watts, 2008; Gruber et al., 2012).

5The Bulindi chimpanzees are among multiple communities ranging in the human-dominated, mosaic landscape that separates Budongo Forest from the nearest main forest to the south, Bugoma Forest (a region known as the ‘Budongo–Bugoma corridor’; McLennan, 2008; McCarthy et al., 2015). Previously, it was unclear if chimpanzees elsewhere in this landscape use stick tools to dig for honey, or whether this behaviour was invented independently at Bulindi or else became extinct in nearby communities, including those within the main Budongo forest block (McLennan, 2011). In this article, we present preliminary data on the occurrence of honey digging with tools, including probable use of a tool set, in a second chimpanzee community residing in unprotected forest fragments between Budongo and Bugoma.

2 Methods

2.1 Study Site

6The Budongo and Bugoma forests in mid-western Uganda each support >500 chimpanzees (Plumptre et al., 2010). Between these main forest blocks, chimpanzees inhabit unprotected riverine forest fragments across an area covering roughly 1,200 km2, known as the ‘Budongo–Bugoma corridor’ (McLennan, 2008; McLennan and Plumptre, 2012). A recent genetic census confirmed the existence of a sizeable population of ‘forest fragment chimpanzees’: ≥260 individuals in 9 or more resident communities (McCarthy et al., 2015). Evidence of recent female dispersal was found among fragment communities, and also between the main Budongo forest block and fragments to the south (McCarthy et al., 2018). Thus, chimpanzees in the greater Budongo–Bugoma landscape, including the fragments, likely comprise one breeding population, at least until recently.

7Between July and December 2018 we made an ecological study of a previously unstudied group of chimpanzees, here referred to as the ‘Mairirwe community’. These chimpanzees range in the southern portion of the corridor, approximately 11 km northeast of Bugoma Forest and 25 km southwest of Bulindi, which is closer to Budongo Forest (Figure 1). Their range covers a minimum of 11.3 km2 in the vicinity of 7 villages (1°21–23'N, 31°12–14'E), estimated via a minimum convex polygon encompassing the locations of sightings of identified individuals from the Mairirwe community (see below) during the study period. The habitat consists of a main 150-acre fragment of riverine forest, and a network of small remnant forest patches along watercourses amidst a patchwork of farmland, homes, and other village areas (Figure 2). In 2014 there were 147 persons per km2 in Kiziranfumbi subcounty, the administrative division of local government which includes most villages in these chimpanzees’ range (Hoima District Local Government, 2015). Most village residents are farmers who practice a combination of subsistence and commercial farming, with sugarcane (Saccharum officinarum) being the main cash crop regionally. All forest patches are privately owned and degraded. Common trees in fragments include Phoenix reclinata, Funtumia africana, Pseudospondias microcarpa, Ficus vallis-choudae and Macaranga schweinfurthii (unpublished data), similar to degraded riverine forest elsewhere regionally (McLennan and Plumptre, 2012). The Mairirwe chimpanzees are unhabituated; to supplement direct observations and to help estimate community size and composition we placed 3 remote sensor camera traps (Bushnell Trophy Cam HD 14MP Aggressor, set to record for 1 min per video) on chimpanzee trails within the 150-acre forest fragment. Over the course of the study we identified a minimum of 17 mature individuals (5 adult males, 9 adult females, and 3 subadult females); considering that 8 of the adult females was each accompanied by 1–2 dependant offspring and the likelihood that not all individuals were identified, we expect total community size numbered about 30 individuals. Like chimpanzees throughout the Budongo–Bugoma corridor (McLennan, 2008, 2013), the Mairirwe chimpanzees eat agricultural crops frequently – notably the commercially farmed sugarcane – in the village matrix surrounding forest patches (unpublished data). While our data are preliminary, their natural diet includes tree fruits of figs (Ficus spp.), Phoenix reclinata, Pseudospondias microcarpa and Caloncoba crepiniana, similar to the chimpanzee diet in nearby Bulindi (McLennan, 2013; McLennan et al., 2020).

Figure 1

Figure 1

Map showing the Budongo and Bugoma Forests in western Uganda and the intervening ‘corridor’ landscape (approximated by the dashed oval), where 9 or more resident chimpanzee groups (‘communities’) inhabit degraded fragments of unprotected riverine forest amidst villages. The range of the Mairirwe community – the focus of this report – is indicated by the solid green circle, near Bugoma; the dashed circle shows the range of the long-term study community at Bulindi, closer to Budongo. The star at centre indicates the location of Hoima town, a major urban centre.

Carte représentant les forêts de Budongo et Bugoma à l’ouest de l’Ouganda et le « corridor » entre les deux (approximativement l’ovale en tirets), où au moins 9 groupes de chimpanzés (« communautés ») résident dans des fragments de forêt riveraines dégradées, non protégées, au milieu de villages. Le territoire de la communauté de Mairirwe – l’objet de ce rapport – est indiqué par un cercle vert, près de Bugoma ; le cercle en tirets correspond au territoire de la communauté de Bulindi, étudiée sur le long terme, près de Budongo. L’étoile au centre indique la localisation de la ville de Hoima, un centre urbain majeur.

Figure 2

Figure 2

Map showing the local landscape within the range of the Mairirwe community of chimpanzees, adapted from Google Earth™ 2018. Their confirmed range during this study (July–December 2018) is approximated by the white oval within the vicinity of 7 villages (italicised names); local people report that the chimpanzees also sometimes cross the main road in the southeast of their range. Dark green areas are fragments of riverine forest, comprising a main 150-acre fragment (at centre) and thin strips of remnant forest and wetlands. The surrounding matrix is a patchwork of agricultural fields, homesteads, roads and tracks, and other village areas. The locations of the two tool sites featured in this article are indicated by the letter ‘T’.

Carte montrant le paysage au sein du territoire des chimpanzés de la communauté de Mairirwe, adaptée à partir de Google Earth™ 2018. Le territoire utilisé par les chimpanzés pendant cette étude (Juillet-Décembre 2018) est représenté approximativement par l’ovale blanc comprenant 7 villages (noms en italiques) ; les populations locales rapportent que les chimpanzés traversent aussi de temps en temps la route principale au sud-ouest de leur territoire. Les zones en vert foncé représentent les fragments de forêts riveraines, comprenant un fragment principal de 150 acres (au centre) et de minces bandes de forêts rémanentes et de marécages. La matrice environnante est un patchwork de champs cultivés, de fermes, de routes et de chemins, et d’autres zones appartenant aux villages. La localisation des deux sites d’utilisation d’outils décrits dans l’article sont indiqués par la lettre « T ».

8No instances of tool use were observed directly. Instead, evidence of tool use was indirect, i.e., inferred from examination of manufactured artefacts found in situ and left behind by chimpanzee users (McGrew et al., 2003). We found tool assemblages opportunistically at disturbed stingless bee ground nests that showed evidence of excavation; the nest sites examined at Mairirwe closely resembled excavated Meliponula ground nests at nearby Bulindi (McLennan, 2011; McLennan et al., 2019). We inspected sticks recovered in the immediate vicinity of nests for signs of use (e.g., soil-covered and/or frayed ends) and modification (e.g., neatly trimmed ends, stripped bark, side branches snapped off). These criteria enabled us to identify sticks as tools. We measured the dimensions of each stick tool (length and width calculated from the average of its two ends) that was associated with honey digging by Mairirwe chimpanzees and compared these with sticks recovered from digging sites in Bulindi (McLennan, 2011; and unpublished data). We tested for between-site differences in the dimensions of sticks used for digging using independent t-tests, having verified that assumptions of normality and homogeneity of variance were met by running Kolmogorov–Smirnov and Levene’s tests, respectively. The analysis was performed using SPSS Version 25.0 (SPSS Inc., Chicago, IL, USA).

3 Results

9We found evidence of chimpanzee honey digging with stick tools at two stingless bee ground nests within forest patches (hereafter ‘Site 1’ and ‘Site 2’).

3.1 Site 1

10On 28 September 2018, we found evidence of digging at a hole in the ground, which was surrounded by an area of freshly flattened vegetation (approximately 2 m x 2 m) where chimpanzees had apparently sat or rested. The hole (29 cm deep x 3 cm wide at surface) was at the centre of a shallow circular area that had been cleared of leaf litter (Figure 3a). Twelve stick tools were recovered in the immediate vicinity of the hole. Most were sturdy and soiled with mud on one or both ends, and had evidently been used for digging. Heavily soiled ends were typically frayed (Figure 4a). One stick in the assemblage was slender and flexible, with only light soil traces on the tips of each end, and may have been used as a probe to investigate the hole. The tool site appeared fresh, i.e., from earlier that morning or the previous afternoon. Five newly broken shrubs and saplings (including Croton sp., Glenniea africana, Ficus asperifolia and Oxyanthus speciosus) were within 0.5–2 m of the hole and were the source of most, or all, stick tools. Several medium-sized stingless bees (unidentified sp.) were noted around the hole, supporting the conclusion that the target was an underground bee nest. The edges of the hole were very smooth, suggesting considerable time and effort had been expended in digging and potentially enlarging the hole. There was no sign of honeycomb or beeswax around the hole or on the sticks.

Figure 3

Figure 3

Two chimpanzee digging sites at stingless bee ground nests in Mairirwe. (A) Site 1: Fresh digging site discovered on 28 September 2018. The stick tools visible above the hole were handled by researchers before this photograph was taken, and are thus not in the exact position left behind by chimpanzees. The ground vegetation surrounding the hole was apparently flattened by chimpanzees. (B) Site 2: The second digging site on 8 October 2018. Stick tools are visible above the excavated hole. The bees’ tiny wax entrance tube is visible near the base of the hole (indicated by white arrow).

Deux sites de nids souterrains d’abeilles sans dard, utilisés par les chimpanzés à Mairirwe. (A) Site 1 : site frais où les chimpanzés ont creusé, découvert le 28 septembre 2018. Les bâtons utilisés comme outils, visibles au-dessus du trou, ont été manipulés par les chercheurs avant d’être photographiés, et ne sont donc pas dans la position où ils ont été trouvés. La végétation au sol autour du trou a été aplatie par les chimpanzés (B) Site 2 : second site où les chimpanzés ont creusé datant du 8 octobre 2018. Les bâtons sont visibles au-dessus du trou fouillé. Un petit tube en cire servant d’entrée aux abeilles est visible dans le trou (indiqué par la flèche blanche).

11On 4 October 2018, we found two large sticks next to the same hole in the ground. The sticks appeared fresh, most likely from the previous day. One end of each stick was thickly encrusted with soil indicating it had been used for digging. A broken sapling (unknown sp.) within 1 m of the hole was identified as the source of the sticks. Compared to the previous occasion, the vegetation surrounding the hole was not flattened, suggesting fewer chimpanzees had been present. No obvious change in the dimensions of the hole was apparent. However, a narrower stick was discovered still inside the excavated hole (Figure 4b). When retracted, small clumps of beeswax were visible on the stick, suggesting it may have been used as a probe to locate the chamber, and/or to extract honey. More traces of beeswax were discovered inside the hole. However, no traces of honey or wax were noted outside the hole. Several stingless bees were observed in its vicinity.

Figure 4

Figure 4

A–c: three tool assemblages collected at two stingless bee ground nests in Mairirwe, (a) Tools collected at Site 1 on 28 September 2018. The assemblage was comprised mainly of sturdy digging sticks; one stick (indicated by arrow) was slender and flexible, and may have been used as a probe; (b) Stick tools collected at Site 1 on 4 October 2018. Two sticks were likely used for digging, while the third (indicated by arrow) had traces of beeswax and may have been used to probe the nest chamber and/or to extract honey; (c) Large tool assemblage collected at Site 2 on 6 October 2018. Most sticks were sturdy with soil-encrusted ends and had evidently been used for digging; one stick (indicated by arrow) was more slender, with only light soil traces on one end, and was possibly used as a probe; (d) Tool assemblage from a stingless bee ground nest in Bulindi, comprised of sturdy digging sticks (collected 29 April 2015).

A-c : trois ensembles d’outils collectés auprès de deux nids souterrains d’abeilles sans dard à Mairirwe, (a) outils collectés au Site 1 le 28 septembre 2018. L’ensemble se compose principalement de bâtons robustes pour creuser ; un bâton (indiqué par la flèche) est fin et flexible, et a pu être utilisé comme une sonde ; (b) bâtons collectés au Site 1 le 4 octobre 2018. Les deux bâtons semblent avoir été utilisés pour creuser, alors que le troisième (indiqué par la flèche) porte des traces de cire d’abeilles et a pu être utilisé pour sonder la cavité du nid et/ou pour extraire du miel ; (c) grand ensemble d’outils collectés sur le Site 2 le 6 octobre 2018. La plupart des bâtons sont robustes avec les extrémités recouvertes de terre et avaient visiblement été utilisés pour fourrager ; un bâton (indiqué par la flèche) est plus fin, avec seulement quelques légères traces de terre sur une extrémité, et a été potentiellement utilisé comme une sonde ; (d) ensemble d’outils provenant d’un nid souterrain d’abeilles sans dard à Bulindi, comprenant des bâtons rigides pour creuser (collecté le 29 avril 2015).

12By 10 October 2018, no further sign of tool use activity was evident at the hole, which appeared to have been abandoned by bees.

3.2 Site 2

13On 8 October 2018 we identified a second digging site, located 200 m from Site 1. It included an irregularly shaped hole (approximately 40 cm deep and up to 30 cm wide at surface) surrounded by flattened vegetation (approximately 1 m x 1 m). A tiny wax entrance tube (about 5 mm in diameter) was visible near the base of the hole, in which several small bees were visible (Figure 3b). Nineteen stick tools were recovered within a 1 m radius of the hole (Figure 4c). Sticks appeared to vary in age, suggesting chimpanzees had potentially excavated the site over multiple visits. The most recent sticks (2–3 days old) had been detached from a Drypetes sp. sapling, 40 cm from the hole. Most sticks were sturdy and soil-encrusted, indicating they had been used for digging. As before, however, a slender stick was present in the assemblage that might have been used as an investigatory probe, rather than to dig. We noted no sign of honeycomb or beeswax within or around the hole. This, together with the presence of an active bee entrance tube, suggests the chimpanzees had not successfully located the chamber and extracted the honey.

14We positioned a camera trap overlooking the site in an effort to capture further digging behaviour by the chimpanzees. On 11 November 2018, the camera captured two unidentified men attempting to dig out the honey. One of the men excavated the hole to a depth of roughly 50 cm using a panga (machete), removing the earth by hand and piling it to the side, and at one point examining a clump of soil possibly for signs of the bees’ wax tube (Figure 5a). After 3 min they abandoned their effort and left the site, having failed to locate the honey chamber. By 15 November 2018, a new bee entrance tube was visible near the base of the hole.

Images from camera trap footage at Site 2. (a): Unidentified men (pixilated for anonymity) attempting to dig out the bee nest using pangas (machetes) on 11 November 2018. The man on the left used his panga to chop vertically into the soil at the hole previously excavated by chimpanzees (indicated by white arrow); he removed the loosened earth with his hands and piled it at the side of the nest; (b–d): An adult female chimpanzee at the excavated nest site on 23 November 2018; she first stood looking at the hole (b), then looked at the camera (c), before squatting to closely inspect the excavated area manually, with her back to the camera (d).

Images provenant d’une séquence vidéo prise par piège-vidéo sur le Site 2. (a) : des hommes non-identifiés (images pixélisées pour l’anonymat) essayant de déterrer le nid d’abeilles en utilisant des machettes le 11 novembre 2018. L’homme à gauche donne des coups verticaux de machette sur le sol au niveau du trou préalablement creusé par les chimpanzés (indiqué par la flèche blanche) ; il retire la terre meuble avec ses mains et l’empile sur le côté du nid ; (b-d) : une femelle chimpanzé adulte au niveau du site du nid déterré, le 23 novembre 2018 ; elle reste tout d’abord debout à regarder le trou (b), puis regarde la caméra (c), avant de s’accroupir pour inspecter manuellement la zone déterrée, le dos tourné à la caméra (d).

15On 23 November 2018, the camera captured an adult female chimpanzee at the bee nest for 1 min (Figure 5b-d); she stared at the excavated hole and then at the camera, before examining the cavity manually for 10 s before the recording ended. On two further occasions, on 24 and 26 November, chimpanzees (including an adult male, two adult females with dependent offspring, and a subadult female) passed the digging site, but only one individual (an older infant) paused to inspect the hole briefly. The chimpanzees showed awareness of the camera (i.e., glancing at it), suggesting its presence may have inhibited them from remaining at the nest site. Signs of disturbance by humans might also have affected their willingness to investigate the hole further. On 29 November, a large soil-encrusted stick was found 30 cm from the nest. Though the tool did not appear old, the camera had not recorded any tool use activity at the nest site.

3.3 Analysis of digging sticks

16We recovered 35 sticks showing clear signs of use from the two stingless bee nest sites. All had been stripped of leaves and twigs (Figure 4a-c). Most showed ≥1 additional modification, i.e., they were partially or entirely stripped of bark, had ends that were neatly trimmed or snapped to length, and/or were split lengthways. Six sticks collected at Site 2 appeared to have been manufactured from a single large stem, indicating multiple modifications. Four sticks were probable offcuts and may have been discarded following division. We ascribed a probable function to the remaining 31 tools based on wear pattern (e.g., extent of soil cover and fraying on ends) and sturdiness (cf. McLennan, 2011). Twenty-eight (90%) had evidently been used to dig into the ground and were categorised as digging sticks (synonymous with ‘perforating sticks’; Boesch et al., 2009; Estienne et al., 2017b). Two (6.5%) were slender with only light soil traces and were categorised as investigatory probes. Only one stick (3%) had traces of beeswax, and may have been used to probe the nest chamber and, potentially, to extract honey (i.e., a ‘collector’; Boesch et al., 2009).

17We compared the dimensions of digging sticks from Mairirwe (n = 28) with sticks used for digging at Bulindi (n = 47; McLennan, 2011; and unpublished data). Digging sticks made by chimpanzees of the two populations were remarkably uniform. Mean length (± SD) of sticks from Mairirwe was 36.9 ± 10.6 cm, compared to 38.4 ± 13.5 cm at Bulindi (t = -0.484, df = 73, p = 0.630). The mean width of digging sticks from Mairirwe was 1.2 ± 0.3 cm, compared to 1.2 ± 0.4 cm at Bulindi (t = -0.605, df = 73, p = 0.547). Table 1 compares dimensions of tools categorised as digging sticks (or ‘perforating’ sticks) used by chimpanzees to excavate stingless bee ground nests from 7 sites with available data. The average length of digging sticks from Mairirwe and Bulindi in Uganda were similar to those used by chimpanzees in the Central Africa region at Gashaka and Ngel Nyaki (Nigeria) and Bili-Uéré (Democratic Republic of Congo) (36–43 cm); only digging sticks used by P. t. troglodytes in Loango (Gabon) and Dja (Cameroon) differed by being longer (69–70 cm). However, this might be an artefact of small sample size for these two sites (Table 1). Width of digging sticks was also similar across sites; only sticks from P. t. ellioti in Nigeria (Gashaka and Ngel Nyaki) differed in having a relatively small diameter size (both averaged 0.8 cm; other sites averaged 1.1–1.4 cm).

Table 1

Table 1

Cross-site comparison of digging (or ‘perforating’) sticks used by chimpanzees to excavate subterranean stingless bee nests1

Comparaison des sites d’utilisation de bâtons par les chimpanzés pour extraire (ou « perforer ») les nids souterrains d’abeilles sans dard1

18The small number of tools categorised as investigatory probes in the Mairirwe assemblages (n = 2) precluded comparison with probe sticks from Bulindi or other study sites.

4 Discussion

19The use of stick tools by chimpanzees to dig out underground stingless bee nests for honey has been documented widely in Central and West-Central Africa (Fay and Carroll, 1994; Hicks et al., 2005; Deblauwe, 2006; Boesch et al., 2009; Fowler et al., 2011; Sommer et al., 2012; Boesch, 2013; Dutton and Chapman, 2015; Estienne et al., 2017a,b; Hicks et al., 2019). The behaviour seems less common further east (Yamagiwa et al., 1988; McLennan, 2011; McLennan, 2015), while there seem to be no published reports of honey digging from far West Africa. In fact, use of sticks to dig into (or ‘perforate’ or ‘puncture’) the ground to exploit subterranean insect prey (i.e., termites, bees, and ants) appears characteristic of tool repertoires of chimpanzees in Central Africa generally (e.g., Sanz and Morgan, 2007; Boesch et al., 2009; Dutton and Chapman, 2015; Estienne et al., 2017b; Hicks et al., 2019). We found that sticks used by chimpanzees of the Mairirwe and Bulindi communities to excavate Meliponini ground nests in Uganda were similar in dimensions to those used by populations in Central Africa, suggesting relative uniformity across a wide geographical area in the tools required to accomplish this task.

20Several studies have suggested that chimpanzees use more than one type of tool to access honey from stingless bee ground nests, i.e., a tool set. Besides digging sticks, which are used to perforate the soil and locate the underground nest chamber, chimpanzees may use probes to investigate the excavated holes and/or ‘collectors’ to extract honey and brood (e.g., Boesch et al., 2009; Fowler et al., 2011; McLennan, 2011; Sommer et al., 2012; Boesch, 2013; Dutton and Chapman, 2005). Tools from Mairirwe included a small number of slender and/or flexible sticks with only light traces of soil in addition to the more numerous, sturdier soil-encrusted digging sticks – including one narrow tool with traces of beeswax. Thus, the Mairirwe chimpanzees seem to also employ a tool set when foraging for honey from subterranean nests, although direct behavioural data are needed to establish the techniques used precisely. Until recently, behavioural observations of honey digging were entirely lacking. Recent camera trap data from Loango (Gabon), however, show that chimpanzees at that site demonstrate a highly complex and flexible sequence of actions when digging for honey with sticks (Estienne et al., 2017b; see also preliminary behavioural data from Bulindi; McLennan et al., 2019). For these reasons, the occurrence of this complex tool-assisted foraging behaviour in mid-western Uganda – a region notorious for the limited tool repertoires of its chimpanzees (Gruber, 2013) – is notable.

21Mairirwe is the second site (after Bulindi) within the forest–farm matrix outside the main Budongo and Bugoma forests where chimpanzee honey digging has been documented. The dimensions of sticks used in this task by the Mairirwe chimpanzees were remarkably similar to those used by the Bulindi community (Figure 4d; Table 1). However, the Mairirwe and Bulindi communities are not neighbours: their ranges are 25 km apart on opposite sides of Hoima Town, an expanding urban centre (Figure 1). Female chimpanzees are generally more frequent and skilled tool users than males in foraging tasks (McGrew, 1979; Gruber et al., 2010). McCarthy et al. (2018) confirmed recent female dispersal among ‘forest fragment chimpanzee’ communities in the northern portion of the Budongo–Bugoma corridor, suggesting conditions for cultural transfer of behaviours such as honey digging via female migration (cf. O’Malley et al., 2012 for an example of probable inter-community transmission of tool-assisted foraging by a migrating female). Other chimpanzee communities occur to the north and northeast of Mairirwe and west of Bulindi (McLennan, 2008; McCarthy et al., 2015). At least until recently, therefore, the Bulindi and Mairirwe communities were presumably linked via migration of females among these intervening fragment communities. Our data suggest that honey digging with sticks may be a cultural behaviour common to chimpanzees inhabiting riverine forest regionally.

22McCarthy et al. (2018) also found evidence of contemporary gene flow between chimpanzee communities in the northern part of the corridor and the southwestern region of Budongo Forest (Busingiro region), where preliminary research by Gruber et al. (2012) found no evidence of stick tool use among its resident chimpanzees. Thus, the occurrence of tool-assisted honey digging in at least two forest fragment communities, and its possible absence among communities within the main Budongo forest block, seems unlikely to have resulted from separation of these populations. Future research should aim to establish if honey digging is present in forest fragment communities closest to the southern border of Budongo, as well as communities ranging between Mairirwe and Bulindi. Elsewhere in mid-western Uganda, the finding that chimpanzees of the Sebitoli community in the northern part of Kibale National Park also dig for honey, whereas well-studied chimpanzees elsewhere in the park seemingly do not (S. Krief, pers. comm.), implies we should not exclude the possibility that other unstudied communities within Budongo Forest use sticks in this foraging task. Furthermore, while Bulindi is located closer to Budongo in the northern half of the Budongo–Bugoma corridor, Mairirwe lies in the southern portion close to Bugoma Forest where chimpanzee tool repertoires are not yet established (Figure 1). Assuming recent female migration occurred between Bugoma and chimpanzee communities outside the reserve, this raises the possibility that honey digging may also be present in the main Bugoma forest block.

23Our study also showed that chimpanzees compete with humans to access this underground food source in the Mairirwe area, with local people using machetes to excavate the bee nests. While it is interesting to speculate about the possible influence of humans on honey digging by chimpanzees in the forest fragments, its occurrence at multiple sites from East to West-Central Africa (including sites with far lower human impact) suggests it is most likely that the chimpanzees invented this tool-assisted foraging behaviour independently of people. Further research will establish whether the Mairirwe community use sticks in other foraging contexts besides honey digging. However, since chimpanzees in Bulindi use stick tools in various contexts (McLennan et al., 2019), and stick probe use has been reported from another fragment community close to Budongo (Kasongoire; Oxley and Jovan, 2019), we predict that Mairirwe chimpanzees exhibit additional forms of stick tool use. The absence of stick-assisted foraging in multiple well-studied communities in Budongo Forest remains a puzzle (Reynolds, 2005; Gruber et al., 2011, 2012; Gruber, 2013; Mugisha et al., 2016). Gruber et al. (2012) and Gruber (2013) proposed that a high diversity of edible plants (influenced in part by past human activities) might help explain the absence of stick-based foraging in Budongo communities, by buffering chimpanzees against seasonal food shortages which could reduce the need to engage in extractive tool use. In possible support of this, riverine forest in Bulindi had a high density of fruit trees (McLennan and Plumptre, 2012), but fruit availability was strongly seasonal (McLennan, 2013). Indeed, the chimpanzees consumed honey at a highest frequency during fruit-poor months (McLennan, 2015). Whether chimpanzees at Mairirwe similarly show a seasonal pattern of honey foraging is not yet known. The structure and species composition of riverine fragments in Bulindi and Mairirwe are overall similar (unpublished data). However, tree species differed markedly between Bulindi riverine fragments and the main Budongo forest block (McLennan and Plumptre, 2012), implying these are dissimilar habitats for chimpanzees despite close geographical proximity. Clearly, additional microecological studies are needed to explain the distribution of tool-assisted foraging, including honey digging, among communities inhabiting the greater Budongo–Bugoma landscape. For example, while stingless bees occur in Budongo (Kajobe and Echazarreta, 2005) and presumably also in Bugoma, it remains possible that stingless bee ground nests are less common there compared to riverine forest outside the main forest blocks.

24The fragmentation and conversion of forest habitats for other land uses can exert a strong influence on great ape behaviour and ecology (Hockings et al., 2015; McLennan et al., 2020). Recently, Kühl et al. (2019) suggested that chimpanzees most impacted by human activities show reduced behavioural and cultural diversity. Therefore, our finding that chimpanzees in highly degraded, human-dominated habitat outside the main Budongo–Bugoma forest blocks exhibit frequent tool-assisted foraging including honey digging, while those in the main Budongo forest block seemingly do not, goes against expectation. Thus, our study also underscores the need to consider chimpanzees in unprotected and human-modified habitat – which are not normally the focus of research or conservation efforts – as well as those inhabiting Uganda’s largest forest blocks such as Budongo, Bugoma, Kibale and Kalinzu, in regional models to explain variation in chimpanzee tool use.

Acknowledgements

25We thank the Uganda National Council for Science and Technology, the President’s Office, and the Uganda Wildlife Authority for permission to conduct this research. We are grateful for the assistance of many local residents in the range of the Mairirwe chimpanzees, particularly in the villages of Kyaisamba, Kicaaya, Kitagasa, Kyakiiza, Nyabuhere, Kyabakahuna and Mairirwe. We thank especially Mr John Bagumirabingi and Philip Baguma of Mairirwe Farm for encouraging this study, and for their support and assistance throughout field data collection. We also thank the local chairpersons of the above-mentioned villages for granting us permission to work in their areas. The field staff of the Bulindi Chimpanzee and Community Project helped in various ways during the study. Thanks also go to Dr Nancy Merrick, Gary Lairmore and Dr Marie Cibot for encouraging us to carry out this research. Funding support was provided by the European Outdoor Conservation Association, Born Free Foundation, Friends of Chimps, the Jane Goodall Institute–Switzerland, Prince Bernard Nature Fund, and the Swiss Foundation for Solidarity in Tourism. Hjalmar Kühl and Paula Diequez (Max Planck Institute for Evolutionary Anthropology) kindly provided camera traps, and Maureen McCarthy and Jack Lester helped with the initial camera set-up. We thank Sabrina Krief and an anonymous reviewer for insightful feedback that helped us improve the manuscript. Marie Cibot kindly translated portions of the text into French.

Declaration of Competing Interests

26The authors declare that they have no competing interests.

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Table des illustrations

Titre Figure 1
Légende Map showing the Budongo and Bugoma Forests in western Uganda and the intervening ‘corridor’ landscape (approximated by the dashed oval), where 9 or more resident chimpanzee groups (‘communities’) inhabit degraded fragments of unprotected riverine forest amidst villages. The range of the Mairirwe community – the focus of this report – is indicated by the solid green circle, near Bugoma; the dashed circle shows the range of the long-term study community at Bulindi, closer to Budongo. The star at centre indicates the location of Hoima town, a major urban centre.
URL http://journals.openedition.org/primatologie/docannexe/image/6718/img-1.jpg
Fichier image/jpeg, 362k
Titre Figure 2
Légende Map showing the local landscape within the range of the Mairirwe community of chimpanzees, adapted from Google Earth™ 2018. Their confirmed range during this study (July–December 2018) is approximated by the white oval within the vicinity of 7 villages (italicised names); local people report that the chimpanzees also sometimes cross the main road in the southeast of their range. Dark green areas are fragments of riverine forest, comprising a main 150-acre fragment (at centre) and thin strips of remnant forest and wetlands. The surrounding matrix is a patchwork of agricultural fields, homesteads, roads and tracks, and other village areas. The locations of the two tool sites featured in this article are indicated by the letter ‘T’.
URL http://journals.openedition.org/primatologie/docannexe/image/6718/img-2.jpg
Fichier image/jpeg, 491k
Titre Figure 3
Légende Two chimpanzee digging sites at stingless bee ground nests in Mairirwe. (A) Site 1: Fresh digging site discovered on 28 September 2018. The stick tools visible above the hole were handled by researchers before this photograph was taken, and are thus not in the exact position left behind by chimpanzees. The ground vegetation surrounding the hole was apparently flattened by chimpanzees. (B) Site 2: The second digging site on 8 October 2018. Stick tools are visible above the excavated hole. The bees’ tiny wax entrance tube is visible near the base of the hole (indicated by white arrow).
URL http://journals.openedition.org/primatologie/docannexe/image/6718/img-3.jpg
Fichier image/jpeg, 769k
Titre Figure 4
Légende A–c: three tool assemblages collected at two stingless bee ground nests in Mairirwe, (a) Tools collected at Site 1 on 28 September 2018. The assemblage was comprised mainly of sturdy digging sticks; one stick (indicated by arrow) was slender and flexible, and may have been used as a probe; (b) Stick tools collected at Site 1 on 4 October 2018. Two sticks were likely used for digging, while the third (indicated by arrow) had traces of beeswax and may have been used to probe the nest chamber and/or to extract honey; (c) Large tool assemblage collected at Site 2 on 6 October 2018. Most sticks were sturdy with soil-encrusted ends and had evidently been used for digging; one stick (indicated by arrow) was more slender, with only light soil traces on one end, and was possibly used as a probe; (d) Tool assemblage from a stingless bee ground nest in Bulindi, comprised of sturdy digging sticks (collected 29 April 2015).
URL http://journals.openedition.org/primatologie/docannexe/image/6718/img-4.jpg
Fichier image/jpeg, 376k
Titre Figure 5
URL http://journals.openedition.org/primatologie/docannexe/image/6718/img-5.jpg
Fichier image/jpeg, 298k
Légende Images from camera trap footage at Site 2. (a): Unidentified men (pixilated for anonymity) attempting to dig out the bee nest using pangas (machetes) on 11 November 2018. The man on the left used his panga to chop vertically into the soil at the hole previously excavated by chimpanzees (indicated by white arrow); he removed the loosened earth with his hands and piled it at the side of the nest; (b–d): An adult female chimpanzee at the excavated nest site on 23 November 2018; she first stood looking at the hole (b), then looked at the camera (c), before squatting to closely inspect the excavated area manually, with her back to the camera (d).
URL http://journals.openedition.org/primatologie/docannexe/image/6718/img-6.jpg
Fichier image/jpeg, 347k
Titre Table 1
Légende Cross-site comparison of digging (or ‘perforating’) sticks used by chimpanzees to excavate subterranean stingless bee nests1
URL http://journals.openedition.org/primatologie/docannexe/image/6718/img-7.jpg
Fichier image/jpeg, 280k
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Référence électronique

Matthew R. McLennan, Georgia A. Lorenti, Simon Mugenyi, Jonan Muganzi et Jacqueline Rohen, « Digging for clues: Stick tools used for honey digging in a second community of ‘forest fragment chimpanzees’ outside the Budongo and Bugoma Forests, Uganda », Revue de primatologie [En ligne], 10 | 2019, mis en ligne le 22 juillet 2020, consulté le 02 mars 2021. URL : http://journals.openedition.org/primatologie/6718 ; DOI : https://doi.org/10.4000/primatologie.6718

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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
mmclennan@brookes.ac.uk; mclennan.bccp@gmail.com

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Georgia A. Lorenti

Bulindi Chimpanzee and Community Project, Hoima, Uganda
glorenti@gmail.com

Simon Mugenyi

Bulindi Chimpanzee and Community Project, Hoima, Uganda

Jonan Muganzi

Bulindi Chimpanzee and Community Project, Hoima, Uganda

Jacqueline Rohen

Bulindi Chimpanzee and Community Project, Hoima, Uganda

Articles du même auteur

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