<NOTE> Published online (July 12, 2021)
Use of a novel human object as a masturbatory tool by a wild male chimpanzee at Bulindi, Uganda

Matthew R. McLennan1,2,3 & Kim van Dijk1,4
1 Bulindi Chimpanzee and Community Project, Hoima, Uganda
1 Faculty of Social Sciences, Oxford Brookes University, Oxford, UK
1 Centre for Ecology and Conservation, University of Exeter, Cornwall, UK
1 Animal Behaviour and Cognition, Utrecht University, Utrecht, The Netherlands


INTRODUCTION

Besides humans, self-stimulation of the genitalia (masturbation) has been documented in many primate species (Dixson 2012; Thomsen & Sommer 2017). Although masturbation by captive nonhuman primates is sometimes considered abnormal or, at least, undesirable behaviour (e.g., Mallapur & Choudhury 2003), masturbation also occurs under natural conditions and may represent a phylogenetically ancient and widespread trait in primates (Thomsen & Sommer 2017). Several studies have reported masturbation in wild male primates living in multimale–multifemale groups where sperm competition occurs (e.g., Temminck’s red colobus, Piliocolobus badius temminckii; Starin 2004; Japanese macaque, Macaca fuscata; Thomsen & Soltis 2004; rhesus macaque, Macaca mulatta; Dubuc et al. 2013). While the hypothesis that male masturbation functions to increase sperm quality (Baker & Bellis 1993) received support in one study of Japanese macaques (Thomsen & Soltis 2004), masturbation leading to ejaculation was observed rather rarely in most reports, suggesting alternative explanations require consideration (Starin 2004; Dubuc et al. 2013).

In chimpanzees, masturbation occurs commonly in captive settings where it has been linked to restricted rearing, which can impede development of speciestypical social and sexual behaviour (Kollar et al. 1968; Rogers & Davenport 1969; Lopresti-Goodman et al. 2013). Masturbation by captive chimpanzees is performed by hand, foot or mouth, against a cage wall or screen, or sometimes using a manipulable object (Shefferly & Fritz 1992). In the wild, object-assisted masturbation occurs in male long-tailed macaques (Macaca fascicularis), which stimulate their genitals using stones (Cenni et al. 2020). Such self-directed employment of a manipulable object meets the criteria of an animal ‘tool’ (Shumaker et al. 2011).

In contrast to captivity, masturbation appears to be rare among male chimpanzees in the wild. Male chimpanzees of all ages at Gombe and Mahale, Tanzania, manipulated (or ‘fumbled’ or ‘fiddled’ with) their erect penises occasionally, but this was never observed to lead to ejaculation (van Lawick-Goodall 1968; Nishida 1997). Recently, Nakamura (2018) described an infant chimpanzee at Mahale ‘copulating’ with a discarded fruit wadge, which was likened to a ‘sex toy’. Besides this, there seem to be no other reports of wild male chimpanzees using manipulable objects as tools in sexual behaviour.

We observed a wild subadult male chimpanzee at Bulindi, Uganda, using a novel human object—a discarded plastic bottle—as a masturbatory tool. While anecdotal (Ramsay & Teichroeb 2019), this unusual observation raises questions about the function of masturbation in male chimpanzees, and contributes to an understanding of the range in behavioural responses of wild apes to novel objects.



METHODS
Study site

Chimpanzees Pan troglodytes schweinfurthii in Bulindi (1°29′N, 31°28′E) were first studied during 2006–2007 (McLennan & Hill 2010) and subsequently from 2012 to the present. They inhabit a human-modified environment comprising fragments of riverine forest amidst farmland and villages (McLennan et al. 2020). The chimpanzees feed habitually on agricultural crops and encounter local people on a daily basis (McLennan et al. 2019a; 2020). They also encounter discarded human objects, including plastic bottles and other litter items.

The Bulindi chimpanzees use leaf or stick tools in various contexts including foraging (McLennan 2011; McLennan et al. 2019b) and hygiene. For example, males sometimes use leaf tools as napkins to wipe their penises after mating (unpubl. data). Bulindi males also handle or inspect their erect penises occasionally (Figure 1), typically after copulation or when females with anogenital swellings are nearby. This behaviour is not accompanied by pelvic thrusts, as occurs during copulation, and has not been observed to result in ejaculation. Thus, it appears similar to penis ‘fumbling’ described at other sites (van Lawick-Goodall 1968; Nishida 1997).

During the present observation in August 2018, chimpanzees were habituated and observable at distances of ≤10 m (Cibot et al. 2019). Community size was 19 including 3 adult and 3 subadult males, 5 adult and 1 subadult females, and 7 immature individuals. The subject of this report is a subadult male named ‘Araali’. In 2018, Araali was estimated to be 9-years old (Figure 1). He had descended testicles, an adult-sized penis, and displayed rhythmic contractions during mating, suggesting he was sexually mature and able to ejaculate.



Figure 1. Subadult male ‘Araali’ in August 2018. The image shows him inspecting his penis after he had mated with an adult female (Photo by Matthew McLennan).

OBSERVATIONS

At midday on 13th August 2018, we followed a party of 11 chimpanzees to a Lantana camara thicket. (L. camara is an invasive weed that forms dense thickets that the chimpanzees use for resting and shade). The party included the alpha male and 3 adult females, none of whom had anogenital swellings. We could hear a chimpanzee manipulating a plastic object under the Lantana. At 12:10 h we approached and observed Araali in possession of a medium-sized plastic bottle, which he was ‘copulating’ with. It is unclear how long he was engaged in this behaviour prior to our approach. The bottle was approximately 1–1.5 L, empty, and without a label or cap (Figure 2); field assistants suggested it was a discarded herbicide bottle of the kind used by local farmers.



Figure 2. The discarded plastic bottle used as a masturbatory ‘tool’ by Araali, photographed the following day (Photo by Bulindi Chimpanzee and Community Project).

We made a 1-min video of Araali’s behaviour (Video1). At the start of the recording, Araali had inserted his erect penis into the bottle’s open top. For 25 sec he made pelvic thrusting movements into the bottle, which he had positioned flat on the ground in front of him (Figure 3a). Once, he repositioned the bottle after his penis came out. At times he showed a relaxed open-mouth expression (or ‘play face’; van Lawick-Goodall 1968). After 30 sec, Araali inspected his erect penis manually before sniffing his fingers. Lifting the bottle, he peered into the open top. He then reinserted his penis into the bottle, which he held in position with one hand while holding a branch with the other (Figure 3b). For the remaining 8 sec of the recording, Araali sat with a play face, apparently with his penis still inside the bottle. Shortly after the recording ended, Araali walked away leaving the bottle behind. It was collected immediately by a juvenile male who, with other youngsters, played with it until we left the chimpanzees at 12:35 h. Therefore, we could not determine if Araali ejaculated into the bottle during the observation. We located the bottle the following evening; however, we did not collect it to test for traces of semen.




Video 1



Figure 3 a.b. Illustrations of Araali ‘copulating’ with the plastic bottle, based on still images taken from video (Illustrations by Kim van Dijk)

DISCUSSION

We observed a wild sexually-mature chimpanzee using a human object as a tool in autoerotic behaviour, i.e. as a ‘sex toy’. Our observation shares similarities with a previous report of an infant male at Mahale, which used a fruit wadge as a masturbation tool (Nakamura 2018). Araali’s tool-assisted masturbation was further distinct from ordinary penis handling or ‘fumbling’ by male chimpanzees at Bulindi, which does not involve pelvic thrusting. While we cannot exclude the possibility that Araali ejaculated into the bottle, it seems doubtful: intromission in sexually-mature males is ordinarily short (mean: 7 sec; Nishida 1997), whereas Araali thrust into the bottle for over 20 seconds.

How should Araali’s masturbatory behaviour be explained? Male primates in multimale–multifemale social groups, including chimpanzees, may not always be able to copulate because of competition with higher-ranking males. Thus, masturbation could improve semen quality by discarding old sperm (Baker & Bellis 1993). However, no sexually receptive females were present during the observation, making such an adaptive explanation unlikely. In multimale–multifemale groups where sperm competition occurs, males might have neuroendocrine specializations for enhanced sexual arousal and copulatory performance; thus, masturbation could provide a sexual outlet for subordinate males with little or no access to receptive females (Dixson 2012). Although Araali occasionally mated with receptive females, he was subordinate to three adult males. In particular, the alpha male successfully monopolised receptive females (McCarthy et al. 2020). Nevertheless, given the rarity of reports of male masturbation in wild chimpanzees, including an absence of reports of masturbation leading to ejaculation (and the lack of evidence for ejaculation in our observation), this ultimate explanation for Araali’s behaviour is also doubtful.

Wild great apes including chimpanzees were reported to show generally indifferent or neophobic responses to novel objects (Forss et al. 2015; Kalan et al. 2019). However, where chimpanzees and other wild primates encounter human artefacts frequently, as at Bulindi, novel human items can elicit interest, leading to object handling and, potentially, novel behaviours (cf. van de Waal & Bshary 2010; le Roux et al. 2019). Young chimpanzees at Mahale manipulated and played with long-abandoned clay pots (Matsusaka 2012) and attempted to touch or inspect human belongings (Matsusaka et al. 2015). Similarly, the enthusiastic play with the bottle by immature chimpanzees in Bulindi is consistent with previous findings that younger apes are more curious of objects than adults (Ramsey & McGrew 2005; Kalan et al. 2019).

Araali’s masturbatory behaviour most likely resulted from his motivation to inspect and play with a novel human object. Male chimpanzees exhibit penile erections in various contexts besides sexual arousal, such as food excitement and during some social interactions including play (pers. observ.). The physical properties of the open bottle presumably elicited Araali’s autoerotic response, suggesting he recognized its suitability for that purpose. Considering he exhibited a play face while ‘copulating’ with the bottle indicates his masturbatory behaviour was ‘pleasurable’ or ‘fun’.



ACKNOWLEDGEMENTS

We thank the Uganda National Council for Science and Technology and Uganda Wildlife Authority for permission to study chimpanzees in Bulindi. For field assistance, we thank John-Mary Baruzaliire and Tom Sabiiti. Conservation and research at Bulindi was supported by Blair Drummond Safari Park, Born Free Foundation, Friends of Chimps and Jane Goodall Institute-Switzerland. We thank Kimberley Hockings and the reviewers for helpful feedback on previous versions of the manuscript. We dedicate this article in loving memory of Jackie Rohen who was devoted to conserving the chimpanzees of Bulindi.



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Received: 9 May 2021
Accepted: 21 June 2021




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