Approche intégrée des comportements culturels

Dans la quête d’explications culturelles ou de propositions alternatives pour rendre compte de l’existence de variations comportementales entre des groupes de la même espèce, seule une approche intégrée, prenant en compte différentes perspectives et incorporant des types d’analyses complémentaires, permet d’établir la preuve de l’existence d’une forme de culture. L’objectif de cet article est de démontrer comment des études comparatives, longitudinales, et expérimentales du comportement de manipulation de pierres, une forme de jeu solitaire observée dans plusieurs groupes de macaques japonais, ont permis de caractériser la nature culturelle de cette pratique. L’approche comparative a révélé une importante variabilité du comportement de manipulation de pierres entre les groupes de cette espèce, mais aussi entre différentes espèces de macaques, avec un rôle limité des facteurs génétiques et environnementaux. L’approche longitudinale a permis de décrire les voies de transmission du comportement entre les membres d’un groupe et à travers les générations, d’évaluer le rôle de l’influence sociale directe de la mère dans l’acquisition du comportement de manipulation de pierres par le jeune lors des premiers mois de la vie, et de démontrer que la tradition de manipulation de pierres n’est pas figée, mais qu’au contraire, elle se transforme au cours du temps, avec une accumulation de diversité et de complexité comportementales, ainsi qu’une diversification des contextes au cours desquels le comportement de manipulation de pierres est pratiqué, des critères qui correspondent à la définition d’une culture cumulative. Enfin, l’approche expérimentale a prouvé que les produits de ce comportement engendrés par l’activité précédente d’un individu (des tas de pierres laissés au sol) stimulent de façon indirecte (c’est-à-dire même en l’absence de ce dernier) l’activité suivante des autres congénères, et participent certainement au maintien de cette tradition. Même si le comportement de manipulation de pierres ne remplit aucune fonction à l’heure actuelle, ce comportement pourrait servir, dans les conditions de faible pression de sélection qu’engendre le nourrissage régulier des singes, à maintenir dans une population un certain degré de diversité et de complexité comportementales associées à des pierres qui, sous réserve d’un changement des conditions environnementales, pourraient évoluer en utilisation des pierres comme outils. Cette recherche souligne l’importance d’une approche éthologique des comportements culturels, en considérant les quatre questions posées par Tinbergen (1963) : développement, mécanisme, fonction, et évolution.In the quest for cultural versus alternative explanations of behavioral variations between groups of the same species, only an integrative approach, considering different perspectives and incorporating complementary analyses, would allow to find evidence for a form of culture. The goal of this paper is to demonstrate how comparative, longitudinal, and experimental studies of stone handling behavior, a form of solitary object play observed in multiple groups of Japanese macaques, lead to characterize the cultural nature of this habit. The comparative approach revealed a considerable variability in stone handling between groups of this species and between different macaque species, with a limited effect of genetic and environmental factors. The longitudinal approach allowed to document the diffusion pathways of the behavior within a group and across generations, to evaluate the direct social influence of the mother in the acquisition of stone handling by young individuals during their first months of life, and to demonstrate that the stone handling tradition is not static but instead changes over time, with an accumulation of behavioral diversity and complexity, and a diversification of the contexts in which stone handling is practiced. Such criteria fit the definition of a cumulative culture. Finally, the experimental approach showed the indirect stimulating effect of stone handling by-products generated through the previous activity of other group members (piles of stones left on the ground) on the subsequent activity of conspecifics, and suggested how stone handling artefacts may contribute to the long-term maintenance of the stone handling tradition. Even though stone handling is currently functionless under the relaxed selective pressures of food provisioning, this behavior may simply serve the function of maintaining in some populations a set of behaviors and a high degree of familiarity with the properties of the stones that could evolve into stone tool-use in a different environment. This research urge for an ethological approach of cultural behaviors, taking into account the four Tinbergen’s (1963) questions: development, mechanism, function, and evolution

Blowing the lid off! Bottle-directed, extractive foraging strategies in synurbic bonnet macaques Macaca radiata in southern India

Nonhuman individuals and groups, living in anthropogenic landscapes, often adopt adaptive foraging strategies, mediated by their day-to-day interactions with humans and their artefacts. Exploring such novel behavioral manifestations, especially in the Anthropocene, offers us insights into behavioral innovations and their transmission in such rapidly changing ecologies. In this study, employing field experiments, we investigated an example of human-induced, extractive foraging behavior – the extraction of liquid contents from plastic bottles – in a synurbic bonnet macaque Macaca radiata population. The main aims of the study were to examine the distribution, diversity, inter-individual variability and intra-individual flexibility of bottle-directed manipulative behaviors, and to explore the social and environmental factors driving this behavioral practice. We video-recorded the manipulation of partially filled plastic bottles and the extraction of liquid across four groups of bonnet macaques in southern India. Two socio-demographic factors – age class and group membership – and one environmental factor – food provisioning – were identified as major determinants of inter-individual variation in the performance of sophisticated manipulative techniques and in bottle-opening success. Our results also suggest that age-related physical maturation, experiential trial-and-error learning, and possibly social learning contributed to the acquisition of foraging competence in this task. These findings illuminate the mechanisms underlying inter-individual behavioral variability and intra-individual behavioral flexibility amongst free-ranging individuals of a cercopithecine primate species, traditionally known for its ecological adaptability and behavioral plasticity. Finally, this study documents how the presence of humans, their artefacts and their activities facilitate the development of certain behavioral traditions in free-ranging nonhuman populations, thus providing valuable insights into how human–alloprimate relations can be restructured within the increasingly resource-competitive environments of the Anthropocene

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

Two types of withdraw-to-eat movement related to food size in long-tailed macaques (Macaca fascicularis): insights into the evolution of the visual control of hand shaping in anthropoid primates

Open access article. Creative Commons Attribution 3.0 Unported License (CC BY 3.0) appliesThe details of the evolutionary steps in the transition from nonvisual guidance of hand movements for feeding, as displayed by many non-primate species, to visual guidance of hand movements in primates are sparse. Contemporary theory holds that a small-bodied stem primate evolved visual control of the reach to guide a hand to obtain small insects and fruit items from the terminal branches of trees. The subsequent evolution of the visual control of hand and finger shaping movements of the grasp of anthropoids is uncertain. The present study finds that Balinese long-tailed macaques (Macaca fascicularis), video recorded while spontaneously eating at the Sacred Monkey Forest Sanctuary in Ubud in Indonesia, displayed two types of hand movements associated with two types of withdraw movements to place food items in the mouth. Small food items were brought directly to the mouth with hand supination, often with no visual monitoring after grasping. Large food items that protruded from the hand were visually monitored to orient the food item on the initial part of the withdraw but visually disengaged with a head movement and often a blink before the item was placed in the mouth. The results are discussed in relation to the idea that visual information related to orientating food items of varying sizes to an appropriate position in the mouth contributed to the evolution of the visual control of hand shaping skills in anthropoid primates.Ye

Inter-group variation in non-conceptive sexual activity in female Japanese macaques: could it be cultural?

Open access distributed under the Creative Commons Attribution 3.0 License.We compared two non-conceptive sexual behavioral patterns (female-male mounting – FMM – and female-female mounting – FFM) across four free-ranging groups of Japanese macaques (Macaca fuscata) living at three different field sites in Japan (Arashiyama, Minoo, and Jigokudani). We found marked inter-group differences and covariation in the frequency and form of FMM and FFM. This result supports the view that FMM and FFM in Japanese macaques are developmentally and evolutionarily linked. The customary occurrence, high prevalence, and great diversity of FMM and FFM at Arashiyama may be the result of combined favorable socio-demographic conditions, namely few resident males, most of them being old, sexually under-motivated, and less aggressive and controlling than the average male Japanese macaques. We suggest that FMM and FFM may be cultural sexual practices in the Arashiyama-E group. In most other populations, all the aforementioned favorable sociodemographic conditions are not met, and although female mounting may occasionally be expressed by several group members, it does not reach the group-level tradition status. Our cultural interpretation of female mounting in Japanese macaques is consistent with evidence of the social transmission of courtship behaviors and mating preferences in various animal taxa, including nonhuman primates and humans. Our study may have implications for the evolution of non-conceptive sexuality in humans, including sexual fluidity in women.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

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

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