Introduction

Aimed throwing behavior requires a series of coordinated movements, associated with adjusting the angle and timing of an object's release in order to successfully hit the target [1]–[4]. Aimed throwing probably played an important role in the aggressive and defensive behavior of protohominids against predators and cospecifics, and certainly did so in the subsequently in hunting [5], [6], leading to the development of tool-using technologies such as projectiles and spears [3], [7]. Selection for object throwing capabilities during human evolution (of great importance to allow defense and hunting) may have led to neural structures including time sequencers (to control the release of objects) and enlarged areas of the brain - such as the motor cortex, which has been speculated to secondarily have been used for fine manual gestures, tool manufacture, and even language processing [1], [8], [9]. Moreover, accurate throwing behavior in humans may have been an important adaptation for hunting during human evolution (perhaps around 2My ago [5]), initially involved in the throwing of natural objects and later in the throwing of hunting tools such as spears and javelins [7].

Capuchin monkeys (Cebus spp and Sapajus spp – the latter one previously referred to as the tufted species of the genus Cebus) are New World monkeys characterized by high brain/body size ratios and enhanced manipulative abilities and manual dexterity that enable them to solve problems in a wide range of manipulative tasks [10]. They also are reported to have social traditions in foraging and affiliative behavior [11]–[13].

In captivity, there are many reports of spontaneous object throwing, but most are anecdotal and lack detailed behavioral descriptions [14]–[16]. There are, though, reports of experimental situations, like Westergaard et al [17], that reported that capuchin monkeys (Sapajus sp) threw food as a means to share it with other monkeys housed in cages 1 m apart. Moreover, in an experimental situation, capuchin monkeys (Sapajus sp) successfully used stones to solve a foraging problem throwing stones into a syrup container and then retrieving them - coated with syrup. Over 83% of these episodes involved overarm throws, and success was positively correlated with individual hand preference. Sex based differences in throwing accuracy were not found [18]. In a stone throwing task that required tufted capuchins to select and throw a stone toward a bucket containing food, Cleveland et al. [19] found that individuals exhibited a strong preference for stones of a given mass, performing better when using stones of the preferred mass. Finally, in an experiment designed to test the capuchins' understanding of the difference between functionally appropriate or inappropriate tools, Evans and Westergaard [20] reported that the monkeys choose the appropriate throwing tools more frequently to recover food (i.e. a projectile attached to a line) than an inappropriate tool (i.e. a non-attached projectile, a projectile attached to shorter line, a projectile without line or a line without a projectile tool).

Capuchin monkeys have been observed pushing or dropping stones and sticks in inter- and intraspecific threat episodes, both in captivity [14], [21] and in the wild [22]–[24; personal observation]. In these cases, though, the release is rarely aimed, the movement is not ballistic, and the object usually ends up far from the threat display target. Stone banging to enhance a threat display was also reported [25], but there are no reports of aimed throwing by wild capuchin monkeys.

In the case of apes, there is evidence that some species use tools for communication purposes in the wild, including sexual displays. Male chimpanzees of Mahale, Tanzania, use leaf-clipping to attract females during courtship [26], while those in the Ngogo community (Kibale National Park, Uganda) use both leaf-clipping and branch-waving for the same purpose [27]. Chimpanzees were also described throwing stones in charging displays and during play, and also throwing rocks into streams, thereby producing loud splash sounds that intimidate others [28]. Orangutans have been seen to use branches to hit other animals [29]. This involved the use of sticks or branches agitated or thrown at the other individual.

Female capuchins exhibit a broad repertoire of behaviors during the proceptive phase, including facial expressions, vocalizations, stereotyped bodily postures, and touch-and-run behavior - where the female touches, grabs, or pulls a part of the male's body and then retreats. These behavioral changes are external manifestations of sexual proceptivity and subsequent receptivity [30]. Initially, the male may ignore the female displays and avoid her. On other occasions, he may threaten and briefly chase the female, especially in response to touch-and-run behavior. Later, the male may respond with similar facial and bodily displays leading to copulation. During a female's proceptive period (estimated from 1 to 7 days, depending on the study [10], she follows a male (usually the dominant male) and directs most of her solicitations to him [10], [31]. If the female is not impregnated, the cycle restarts after +/−21 days [10].

In this study we describe stone throwing as a communicative behavior exhibited as part of the proceptive display in female Sapajus libidinosus inhabiting Serra da Capivara National Park (SCNP) in Northeastern Brazil. Although most tool use in this population is foraging-related, we describe here the use of stone throwing as a socio-sexual behavior. We observed this behavior in only one of the two groups we studied in the park. This group has been studied for 4 years. In two other groups of S. libidinosus studied in SCNP by Mannu and Ottoni [32] for 2 years, stone throwing as a courtship behavior has not been reported. Bearded capuchin monkeys at SCNP exhibit a unique tool-kit. In addition to the use of “hammer” stones to crack hard fruits or seeds, often observed in savannah and dry bush populations [13], all studied groups in SCNP frequently use stones as “hammer” to loosen the soil for digging, and sometimes as a “hoe” to cut plant parts and pull the soil when digging. They also use stones as “hammers” to pulverize or dislodge rocks, and sticks as probes to remove prey such as lizards and bees from cavities [32], [33].

Methods

Results

During a total contact time of 1290.2 h with PF group and 426.3 h with BC group, we recorded 49 proceptive periods for at least 17 of the 23 adult females in the groups (Table 1). During 28.5% of contact time, one or more females in our study groups were in estrus (PF: 385.1 h; BC: 106.2 h). Three of 13 females in the PF group (but none in the BC group) were seen throwing stones at males during their proceptive phases. All throwing postures were overarm: the females held the stones at or above shoulder level before throwing it (Figure 1 and Video S1). They usually stood bipedally while throwing, but there were cases (not quantified) of throwing using a tripedal stance. The target males were always high-ranking individuals, but not always the alpha males (who were the targets in 22.2% events). Low-ranking males were never targets of stone throwing.

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Figure 1. Stills from video recordings, showing moments of two throwing events.

(a) Pedrita running with a stone just before throwing it at Beiçola;(b) Pedrita picking up a stone, (c, d) running, and (e) throwing the stone at Bochechudo. The video is available as supplementary material - Video S1.

https://doi.org/10.1371/journal.pone.0079535.g001

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Table 1. Proceptive periods recorded for the capuchin monkeys of PF and BC groups from Serra da Capivara National Park.

https://doi.org/10.1371/journal.pone.0079535.t001

When hit by a stone (N = 10), the males looked towards the female and, on two occasions, briefly threatened and chased her. This behavior response could be exhibited even if when the stone hit the ground near him (<1 m,). After that, they usually resumed their ongoing activities. The threats were not very severe and the male's response was not different from when a female grabbed the male's tail during touch-and-run behavior.

No female was observed throwing stones outside of her proceptive period. The three females from PF group that exhibited throwing behavior did so at different frequencies (Table 2). Pedrita was the most frequent thrower (76.2%). She was observed on 5 days during 2 proceptive periods. She threw stones at 2 different males.

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Table 2. Throwing events by capuchin monkey females of PF group.

https://doi.org/10.1371/journal.pone.0079535.t002

In Table 3 we present data collected between 01/2012 and 08/2012 for the PF group, using the same methods as in the previous study period. We found that 3 additional females in the group were also performing stone throwing behavior during their proceptive period. Two of these females were immatures during the original study (Vesga - 8 events and Alice - 13 events), and the other was an adult during the 2007–2009 study period (Gorda - 1 event), but was not seen throwing stones in either of the two proceptive periods we observed (Table 1).

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Table 3. Throwing events by female capuchin monkeys of PF group after the original research period (01/2012–07/2012).

https://doi.org/10.1371/journal.pone.0079535.t003

In 2007–2008, we collected eight stones used as projectiles by two of the females (Pedrita and Ninfa). We only collected stones that we were able to identify were thrown by a female. The average weight of the stones was 52.0 g (+/−27.1 - range 19–84), and the average length, width and thickness were, respectively, 4.6 cm (+/−0.9 - range: 3.6–5.9), 3.1 cm (+/−0.52 - range: 2.1–3.8) and 2.2 cm (+/−0.64 - range: 1.1–3.1).

Discussion

The sexual display of female capuchin monkeys is a very conspicuous behavior. It has been described in Sapajus spp., C. capucinus and C. albifrons, and varies in form from a simple display in the two Cebus species to very elaborate and extensive display in Sapajus spp. While C. capucinus do not present a high variety of displays, it includes a unique facial expression described as duck face in which monkeys protrude their lips during sexual display [34]. A duck face display has not been reported in Sapajus spp., but this genus appears to include the species that have the most diverse sexual displays [10]. The incorporation of stone throwing, which has been reported only in S. libidinosus, further suggests that among tufted capuchins there is a great plasticity in display behaviors.

We have studied 4 groups of S. libidinosus at SCNP over the course of 5 years, however, only females of PF group have been observed throwing stones [32], [35]. Moreover, during a 5-day field trip to SCPN in July/2012, we observed stone throwing by two other adult females from PF group during their proceptive period. Gorda was observed throwing a stone at Torto once, and Vesga (a juvenile not observed in estrus in the original period of research) was seen throwing stones 7 times (2 hits) on 2 days of observed estrus. Vesga also was seen throwing stones during one of her proceptive periods, on June/2012 [Camila Coelho, pers. comm.], and, in July/2012, another female (Alice) exhibited the throwing behavior (N = 13) during her proceptive period [Raphael Cardoso, pers. comm.]. In each case, the male hit with the stone copulated with the sexually displaying female. We have no data on whether stone throwing has any effect on a female's success in soliciting copulations from an adult male (e.g. decreasing the male latency to mate).

All adult individuals in our study groups (even in the groups in which we did not observe females' stone throwing) are proficient at using stones (and other objects) as tools in various contexts [35, Falótico & Ottoni, unpublished data]. In this regard, it is possible that some females of PF group could have independently added stone throwing to their sexual display.

The only similar observation is a recent report from captives in a zoo [36]: in that study a single female S. libidinosus threw stones (N = 6) at males during estrus, in a similar manner to the cases reported here. This could indicate that stone throwing during sexual solicitation is more widespread in S. libidinosus than previously thought or is a commonly “reinvented” behavioral pattern. In our study groups, we believe that the possibility that 6 females in the same group independently added stone throwing to their sexual display is unlikely, since females from other groups in SCNP have access to stones, use stones in foraging contexts, but were never observed throwing stones during sexual displays. In addition, Mannu and Ottoni [32] studied two groups of bearded capuchins in the same area over a two year period and did not observe stone throwing in this context, nor has this behavior been reported in another long-term study site where stone tool use by bearded capuchins is common, Fazenda Boa Vista [37], [38].

One possible explanation for the presence of this behavior in the repertoire of several females in PF is that this behavior was disseminated through social influences. Although stone throwing was not very frequent, occurring at an average rate of 7.8 times per throwing female proceptive period, non-throwing females could observe it performed by others on several occasions. The pattern of occurrence of the behavior, restricted to just one group and with an increasing number of females performing it, suggests that social learning played an important role in behavioral transmission. That is, the behavior was independently ‘invented’ by one or more females, and then copied by others as a form of “enhanced” display. It is not possible to determine when this behavior appeared in PF, but it was already exhibited by some females from the beginning of our study, and appears to be slowly spreading in the group: we first observed only 3 of 14 individual females exhibit this behavior (Table 1), and 3 years after the original research, an additional 3 females (1 who was and 2 who were not adults during our original study) were seen throwing stones at males.

If the social learning hypothesis is correct, this behavior is likely to remain limited to its original group, since S. libidinosus females are strongly philopatric, and seldom leave their natal group [39]. Moreover, during intergroup encounters, males from neighboring groups were seen to interact, whereas adult females appeared to remain apart and avoid contact.

It's also important to note that most tool use by capuchins (and primates in general) is foraging-related [10], and is a predominantly male activity [35], [37], [40], [41, Falótico & Ottoni, unpublished data]. As a communicative behavior, it is reminiscent of object percussion as a male sexual signaling [42] or threat display [24] in capuchins, as well as the leaf-clipping behavior by Mahale male chimpanzees reported by Nishida [26].

Continuing observation of the PF group and other nearby groups will help us determine whether the stone throwing behavior will spread to more or all adult females in the PF group, and eventually appear in other groups - either by independent invention or diffusion by a rare migrating female. We have perhaps, a unique opportunity to document the early phase of the diffusion of a new behavior, whose potential future dissemination history we are looking forward to following.

Supporting Information

Acknowledgments

We would like to thank the FUMDHAM staff, particularly their Director Niède Guidon, who provided us with logistical support during the fieldwork. We also thank our field assistant Francisco “Chico” Reinaldo for his help in data collection, and Camila Coelho and Raphael Cardoso for the reports of other throwing events. We acknowledge the critical reviews by Paul Garber and two anonymous reviewers on an earlier version of the manuscript.