Sexual adaptation: is female-male mounting a supernormal courtship display in Japanese macaques?

Accepted author manuscriptWe analysed heterosexual consortships in a free-ranging group of Japanese macaques in which adult females routinely perform female-to-male mounting (FMM). We tested whether FMM is more efficient (i.e., a “supernormal courtship” behavioral pattern) than species-typical female-to-male sexual solicitations (FMSS) at prompting subsequent male-to-female mounts (MFM). In a context of high femalefemale competition for male mates, we found that (1) FMM functioned to focus the male consort partner’s attention as efficiently as FMSS and prevented him from moving away, and (2) FMM was more efficient than species-typical FMSS at expediting MFM (i.e., the most fitness-enhancing sexual behavior of a mating sequence). We concluded that FMM could be considered a supernormal courtship behavioral pattern in adult female Japanese macaques. This population-specific sexual adaptation may result from a combination of favorable socio-demographic conditions. This study has implications for the evolutionary history of non-conceptive mounting patterns in Japanese macaques and non-conceptive sexuality in humans

Acquisition of object-robbing and object/food-bartering behaviours: a culturally maintained token economy in free-ranging long-tailed macaques

Open access article. Creative Commons Attribution 4.0 International License (CC BY 4.0) appliesThe token exchange paradigm shows that monkeys and great apes are able to use objects as symbolic tools to request specific food rewards. Such studies provide insights into the cognitive underpinnings of economic behaviour in non-human primates. However, the ecological validity of these laboratory-based experimental situations tends to be limited. Our field research aims to address the need for a more ecologically valid primate model of trading systems in humans. Around the Uluwatu Temple in Bali, Indonesia, a large free-ranging population of long-tailed macaques spontaneously and routinely engage in token-mediated bartering interactions with humans. These interactions occur in two phases: after stealing inedible and more or less valuable objects from humans, the macaques appear to use them as tokens, by returning them to humans in exchange for food. Our field observational and experimental data showed (i) age differences in robbing/bartering success, indicative of experiential learning, and (ii) clear behavioural associations between value-based token possession and quantity or quality of food rewards rejected and accepted by subadult and adult monkeys, suggestive of robbing/bartering payoff maximization and economic decision-making. This population-specific, prevalent, cross-generational, learned and socially influenced practice may be the first example of a culturally maintained token economy in free-ranging animals.Ye

Structural analyses in the study of behavior: From rodents to non-human primates

The term "structure" indicates a set of components that, in relation to each other, shape an organic complex. Such a complex takes on essential connotations of functionally unitary entity resulting from the mutual relationships of its constituent elements. In a broader sense, we can use the word "structure" to define the set of relationships among the elements of an emergent system that is not determined by the mere algebraic sum of these elements, but by the interdependence relationships of these components from which the function of the entire structure itself derives. The behavior of an integrated living being can be described in structural terms via an ethogram, defined as an itemized list of behavioral units. Akin to an architectural structure, a behavioral structure arises from the reciprocal relationships that the individual units of behavior establish. Like an architectural structure, the function of the resulting behaving complex emerges from the relationships of the parts. Hence, studying behavior in its wholeness necessitates not only the identification of its constitutive units in their autarchic individuality, but also, and importantly, some understanding of their relationships. This paper aimed to critically review different methods to study behavior in structural terms. First, we emphasized the utilization of T-pattern analysis, i.e., one of the most effective and reliable tools to provide structural information on behavior. Second, we discussed the application of other methodological approaches that are based on the analysis of transition matrices, such as hierarchical clustering, stochastic analyses, and adjusted residuals. Unlike T-pattern analysis, these methods allow researchers to explore behavioral structure beyond its temporal characteristics and through other relational constraints. After an overview of how these methods are used in the study of animal behavior, from rodents to non-human primates, we discussed the specificities, advantages and challenges of each approach. This paper could represent a useful background for all scientists who intend to study behavior both quantitatively and structurally, that is in terms of the reciprocal relationships that the various units of a given behavioral repertoire normally weave together

Structural analyses in the study of behavior : From rodents to non-human primates

Ajuts: J-BL's research was funded by Natural Sciences and Engineering Research Council of Canada (NSERC, Discovery Grant #: 2015-06034 to J-BL). MC, SA, and GC's research was funded by a grant from the University of Palermo, Italy.The term " structure " indicates a set of components that, in relation to each other, shape an organic complex. Such a complex takes on essential connotations of functionally unitary entity resulting from the mutual relationships of its constituent elements. In a broader sense, we can use the word " structure " to define the set of relationships among the elements of an emergent system that is not determined by the mere algebraic sum of these elements, but by the interdependence relationships of these components from which the function of the entire structure itself derives. The behavior of an integrated living being can be described in structural terms via an ethogram, defined as an itemized list of behavioral units. Akin to an architectural structure, a behavioral structure arises from the reciprocal relationships that the individual units of behavior establish. Like an architectural structure, the function of the resulting behaving complex emerges from the relationships of the parts. Hence, studying behavior in its wholeness necessitates not only the identification of its constitutive units in their autarchic individuality, but also, and importantly, some understanding of their relationships. This paper aimed to critically review different methods to study behavior in structural terms. First, we emphasized the utilization of T-pattern analysis, i.e., one of the most effective and reliable tools to provide structural information on behavior. Second, we discussed the application of other methodological approaches that are based on the analysis of transition matrices, such as hierarchical clustering, stochastic analyses, and adjusted residuals. Unlike T-pattern analysis, these methods allow researchers to explore behavioral structure beyond its temporal characteristics and through other relational constraints. After an overview of how these methods are used in the study of animal behavior, from rodents to non-human primates, we discussed the specificities, advantages and challenges of each approach. This paper could represent a useful background for all scientists who intend to study behavior both quantitatively and structurally, that is in terms of the reciprocal relationships that the various units of a given behavioral repertoire normally weave together

Do monkeys use sex toys? Evidence of stone tool-assisted masturbation in free-ranging long-tailed macaques

Accepted author manuscriptRecent reports on tool use in nonforaging contexts have led researchers to reconsider the proximate drivers of instrumental object manipulation. In this study, we explore the physiological and behavioral correlates of two stone-directed and seemingly playful actions, the repetitive tapping and rubbing of stones onto the genital and inguinal area, respectively, that may have been co-opted into self-directed tool-assisted masturbation in long-tailed macaques (i.e., “Sex Toy” hypothesis). We predicted that genital and inguinal stone-tapping and rubbing would be more closely temporally associated with physiological responses (e.g., estrus in females, penile erection in males) and behavior patterns (e.g., sexual mounts and other mating interactions) that are sexually motivated than other stone-directed play. We also predicted that the stones selected to perform genital and inguinal stone-tapping and rubbing actions would be less variable in number, size, and texture than the stones typically used during other stone-directed playful actions. Overall, our data partly supported the “Sex Toy” hypothesis indicating that stone-directed tapping and rubbing onto the genital and inguinal area are sexually motivated behaviors. Our research suggests that instrumental behaviors of questionably adaptive value may be maintained over evolutionary time through pleasurable/self-rewarding mechanisms, such as those underlying playful and sexual activities

When males have females on their backs: male's tolerance, solicitation, and use of female-male mounting in Japanese macaques

Accepted author manuscript. Embargo in effect until May 25, 2023Previous research on Japanese macaques has shown that female-to-male mounting (FMM) is performed by some females as an exaggerated form of sexual solicitation that may occur in the context of high female competition for male mates. This supernormal courtship behavior functions to prompt subsequent male-to-female mounting. In this report, we focused on the male consort partners’ responses to FMM. We studied a free-ranging population of Japanese macaques at Arashiyama, Japan, in which FMM is frequent and prevalent. We analyzed 240 consortships involving 31 females and 19 males. We tested three hypotheses regarding male’s tolerance, solicitation, and use of FMM. First, we found that FMM was tolerated by male mountees who were no more likely to aggress their female partners during a short time window around a FMM, than they were during the rest of the consortship period. Second, we showed that FMM could be triggered by male recipients, via explicit male-to-female sexual solicitations. Third, we found that some males may utilize FMM in a quest for their own sexual stimulation, which sometimes culminated in masturbation by the male during FMM. Our findings indicate that male partners facilitate the expression of FMM both passively (via their tolerance) and actively (via their solicitation). In addition, FMM appears to enhance the sexual arousal of male partners during consortships. We argued that, for females to have expanded their repertoire of sexual solicitations by adopting FMM, male mates must have played a role in the evolutionary origins and maintenance of this non-conceptive, but intense and powerful female mating tactic.Ye

Social influence on the expression of robbing and bartering behaviours in Balinese long‑tailed macaques

Animals use social information, available from conspecifics, to learn and express novel and adaptive behaviours. Amongst social learning mechanisms, response facilitation occurs when observing a demonstrator performing a behaviour temporarily increases the probability that the observer will perform the same behaviour shortly after. We studied “robbing and bartering” (RB), two behaviours routinely displayed by free-ranging long-tailed macaques (Macaca fascicularis) at Uluwatu Temple, Bali, Indonesia. When robbing, a monkey steals an inedible object from a visitor and may use this object as a token by exchanging it for food with the temple staff (bartering). We tested whether the expression of RB-related behaviours could be explained by response facilitation and was influenced by model-based biases (i.e. dominance rank, age, experience and success of the demonstrator). We compared video-recorded focal samples of 44 witness individuals (WF) immediately after they observed an RB-related event performed by group members, and matched-control focal samples (MCF) of the same focal subjects, located at similar distance from former demonstrators (N = 43 subjects), but in the absence of any RB-related demonstrations. We found that the synchronized expression of robbing and bartering could be explained by response facilitation. Both behaviours occurred significantly more often during WF than during MCF. Following a contagion-like effect, the rate of robbing behaviour displayed by the witness increased with the cumulative rate of robbing behaviour performed by demonstrators, but this effect was not found for the bartering behaviour. The expression of RB was not influenced by model-based biases. Our results support the cultural nature of the RB practice in the Uluwatu macaques

Behavior Systems Approach to Object Play: Stone Handling Repertoire as a Measure of Propensity for Complex Foraging and Percussive Tool Use in the Genus Macaca

Stone handling (SH), has been identified in four closely related primate species of the Macaca genus. We provide the first ethogram of SH in long-tailed macaques (Macaca fascicularis), a primate species known to use stones for extractive foraging. A total of 62.7 hrs of video recorded data were scored from a population of Balinese long-tailed macaques living in Ubud, Bali, Indonesia, and a total of 36 stone handling patterns were identified. Behavior discovery curves were generated and showed that the minimum threshold of completeness was exceeded for the SH repertoire in this group. A “foraging substitute” hypothesis for the expression of SH was proposed, suggesting that SH consists of performing foraging-like actions on non-edible objects. We used a “behavior systems” framework to test this prediction, finding that all 36 stone handling patterns could be reliably categorized in a foraging behavior system, supporting the hypothesis that stone handling can be considered pseudo-foraging behavior. Our “behavior systems” approach will serve as a foundation for the future testing of the motivational basis of stone handling. Additionally, a comparison of 39 stone handling patterns performed by three macaque species (M. fascicularis, M. fuscata and M. mulatta) showed overlapping behavioral propensities to manipulate stones; however, the differences suggest that long-tailed macaques might be more prone to use stones as percussive tools in a foraging context. This work could offer insights into the development and evolution of complex activities such as percussive stone tool use in early humans