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Self-handicapping behaviors evolved as honest signals that reliably reflect the quality of their performers. In playful activities, self-handicapping is described as intentionally and unnecessarily putting oneself into disadvantageous positions and situations. Self-handicapping during play may allow individuals to learn to cope with unexpected events by improving sensori-motor coordination, as well as function as a play solicitation signal. One such self-handicapping behavior involves moving about while deliberately covering one's eyes. We conducted a quantitative study of object-assisted eye-covering (OAEC) in a population of free-ranging Balinese macaques. After evaluating the frequency, form, distribution, and context of OAEC, we measured the responses this behavior elicited (1) in the performers with a focus on sensori-motor self-handicapping, and (2) in their conspecifics, with an emphasis on whether, and if so how, OAEC may facilitate social play. Our data provided some support for several hypotheses: OAEC is a sensori-motor self-handicapping behavior, an attention-getting cue, a social play signal, and a socially self-handicapping tactic during social play. We discuss our results from the perspective of tool-assisted self-handicapping behavior, propose a scenario to account for the emergence of this behavioral innovation, and speculate on the cultural nature of OAEC.
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Comportamento Animal , Macaca fascicularis , Comportamento Social , Animais , Jogos e BrinquedosRESUMO
Previous 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 nonconceptive but intense and powerful female mating tactic.
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Macaca fuscata , Comportamento Sexual Animal , Animais , Feminino , Japão , Macaca/fisiologia , Masculino , Reprodução , Comportamento Sexual Animal/fisiologiaRESUMO
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.
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Macaca fascicularis , Aprendizado Social , Animais , Indonésia , AprendizagemRESUMO
INTRODUCTION: SMG9 deficiency is an extremely rare autosomal recessive condition originally described in three patients from two families harboring homozygous truncating SMG9 variants in a context of severe syndromic developmental disorder. To our knowledge, no additional patient has been described since this first report. METHODS: We performed exome sequencing in a patient exhibiting a syndromic developmental delay and in her unaffected parents and report the phenotypic features. RESULTS: Our patient presented with a syndromic association of severe global developmental delay and diverse malformations, including cleft lip and palate, facial dysmorphic features, brain abnormalities, heart defect, growth retardation, and severe infections. She carried a novel SMG9 homozygous variant NM_019108.3:c.1177C>T, p.(Gln393*), while her unaffected parents were both heterozygous. CONCLUSIONS: We confirm that bi-allelic truncating SMG9 variants cause a severe developmental syndrome including brain and heart malformations associated with facial dysmorphic features, severe growth and developmental delay with or without ophthalmological abnormalities, severe feeding difficulties, and life-threatening infections.
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Deficiências do Desenvolvimento/diagnóstico , Deficiências do Desenvolvimento/genética , Estudos de Associação Genética , Predisposição Genética para Doença , Peptídeos e Proteínas de Sinalização Intracelular/genética , Mutação , Alelos , Encéfalo/anormalidades , Encéfalo/diagnóstico por imagem , Pré-Escolar , Consanguinidade , Feminino , Estudos de Associação Genética/métodos , Homozigoto , Humanos , Linhagem , Fenótipo , SíndromeRESUMO
We assessed the effect of a progestin-based contraceptive treatment (chlormadinone acetate) on female heterosexual and homosexual behaviors in a free-ranging group of Japanese macaques (Macaca fuscata) living at Arashiyama-Kyoto, Central Japan. The data included estimated intensity of fertility cues, sexual solicitations and mounting behaviors collected daily during 17 consecutive mating seasons (1995-2012) from 159 females. Females that were on contraception: (1) exhibited less intense cues of putative fertility and for shorter periods; (2) were solicited by fewer males, and those males that did solicit them did so less often (i.e., lower heterosexual attractivity); (3) solicited fewer males and when they did perform sexual solicitations they did so less often (i.e., lower heterosexual proceptivity); (4) engaged in shorter heterosexual consortships with fewer male partners (i.e., lower heterosexual receptivity), compared with females that were not on contraception. In contrast, contraceptive treatment had no significant effect on the prevalence, occurrence, frequency, or duration of female homosexual behaviors. Even though heterosexual and homosexual behaviors can both be considered sexual in character and under hormonal control, our results suggested they are, to some extent, dissociable. Because females engaging in homosexual interactions showed less intense cues of putative fertility than those engaging in heterosexual interactions, regardless of contraceptive treatment, we argued that the hormonal threshold required for the expression of heterosexual behavior by females was associated with elevated sex hormones levels compared to homosexual behavior. We discussed the hormonal correlates of sexual behavior and partner preferences in Japanese macaques.
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Anticoncepcionais Orais Hormonais/farmacologia , Heterossexualidade/efeitos dos fármacos , Homossexualidade Feminina , Macaca , Comportamento Sexual Animal/efeitos dos fármacos , Animais , Acetato de Clormadinona/farmacologia , Comportamento de Escolha/efeitos dos fármacos , Feminino , Heterossexualidade/fisiologia , Japão , Masculino , Casamento , Reprodução/efeitos dos fármacos , Estações do AnoRESUMO
This is the first quantitative study of heterospecific sexual behavior between a non-human primate and a non-primate species. We observed multiple occurrences of free-ranging adolescent female Japanese macaques (Macaca fuscata) performing mounts and sexual solicitations toward sika deer (Cervus nippon) at Minoo, central Japan. Our comparative description of monkey-deer versus monkey-monkey interactions supported the "heterospecific sexual behavior" hypothesis: the mounts and demonstrative solicitations performed by adolescent female Japanese macaques toward sika deer were sexual in nature. In line with our previous research on the development of homospecific sexual behavior in immature female Japanese macaques, this study will allow us to test other hypotheses in the future, such as the "practice for homospecific sex," the "safe sex," the "homospecific sex deprivation," the "developmental by-product," and the "cultural heterospecific sex" hypotheses. Further research will be necessary to ascertain whether this group-specific sexual behavior was a short-lived fad or an incipient cultural phenomenon and may also contribute to better understanding the proximate and ultimate causes of reproductive interference.
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Cervos , Comportamento Sexual Animal/fisiologia , Animais , Estudos de Avaliação como Assunto , Feminino , Japão , Macaca , MasculinoRESUMO
We used cross-sectional focal data collected in adolescent and adult females to elucidate the comparative development of heterosexual and homosexual behaviors in female Japanese macaques (Macaca fuscata) living at Arashiyama, Japan, in a group where adult females routinely exhibit sexual interactions with both males and females. Our data fully or partially supported most of our predictions (20 out of 30) related to the "learning hypothesis," which postulated that adolescence would serve to provide young females with a period in which to practice, and gradually acquire, three types of adult female-like heterosexual and homosexual behavioral patterns, namely sexual solicitations, sexual mounts, and spatio-temporal coordination during consortships. However, there were marked differences in the development of heterosexual and homosexual behaviors. The percentage of homosexual mounts was significantly higher in adolescent than in adult females. Of the fully or partially supported predictions, 13 of 15 pertained to heterosexual activity whereas only seven of 15 pertained to homosexual activity. A number of sexual behavioral patterns (e.g., demonstrative solicitations, range of solicitation patterns and mounting postures, and grasping behavior during consortships) emerged earlier and developed faster when directed to females than when directed to males. We explain such differences in terms of risk of male aggression, males' disinterest in adolescent females' sexual solicitations, presence of motivated same-sex sexual partners, social facilitation, and sexual reward.
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Macaca/fisiologia , Preferência de Acasalamento Animal/fisiologia , Adaptação Fisiológica , Agressão , Animais , Estudos Transversais , Feminino , Japão , Macaca/psicologia , Recompensa , Facilitação SocialRESUMO
We aimed to explain the frequent and prevalent female homosexual behavior in the context of female-biased operational sex ratios (OSR) and qualified sex ratios (Q) in a free-ranging group of Japanese macaques (Macaca fuscata) living at Arashiyama-Kyoto, Japan. Our data included the average availability of sexually mature males during females' putative fertile period (OSR), the ratio of sexually mature males to sexually mature females (Q), as well as heterosexual and female homosexual solicitations and consortships collected during 13 mating seasons from 136 females. Our results did not support the "heterosexual deprivation hypothesis," which holds that female homosexual behavior is attributable to a shortage of male mates. Likewise, our results did not support the "lack of opposite-sex sexual competitor hypothesis," which holds that females have more access to female mates when male sexual rivals are scarce. Of the 11 predictions tested, only one yielded statistically significant results: we found that higher ratios of availability of preferred female partners to preferred male partners were associated with female homosexual consortships rather than female heterosexual consortships. This result supported the "bisexual preference hypothesis," which holds that female homosexual behavior is attributable to female preference for certain female mates relative to certain male mates. We conclude that when a female targets another female as a mate, it is an active choice for a female sexual partner over available male alternatives, rather than a by-default situation that occurs because males are not available as sexual partners, or because females are better able to access female sexual partners due to a scarcity of male sexual competitors.
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Comportamento de Escolha , Homossexualidade Feminina , Macaca , Preferência de Acasalamento Animal/fisiologia , Animais , Bissexualidade , Feminino , Heterossexualidade , Humanos , Japão , Masculino , Razão de Masculinidade , Comportamento Sexual Animal/fisiologia , Parceiros SexuaisRESUMO
We explored the role that sexual and social partners play in the expression of female homosexual behavior among adolescent female Japanese macaques at Arashiyama, Japan. Our data fully or partially supported all the predictions related to four non-mutually exclusive hypotheses, namely the "adult male disinterest in adolescent females" hypothesis, the "numerous homosexual adult females" hypothesis, the "safer homosexual interactions" hypothesis and the "same-sex sexual interactions" hypothesis. Our results show that both sexual context (e.g., lack of adolescent female attractivity toward adult males, presence of motivated same-sex sexual partners), and social context (e.g., risk of aggression) help explain the high frequency and prevalence of homosexual behavior in adolescent females in the Arashiyama group of Japanese macaques. As with adult females, whose homosexual consortships do not reflect generalized patterns of social affiliation or kinship, we found that adolescent females' same-sex sexual partners were neither kin, nor were they non-kin individuals with whom adolescent females were closely affiliated outside of a consortship context. Our study furthers the growing database of female homosexual behavior in Japanese macaques and provides additional evidence that homosexual behavior as expressed by adolescent female Japanese macaques is, like heterosexual behavior, sexual in nature. We discuss the relevance of our findings to a broader comparative approach that may shed light upon the development and evolution of human homosexuality.
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Macaca/fisiologia , Comportamento Sexual Animal , Comportamento Social , Agressão , Animais , Feminino , Homossexualidade Feminina , Japão , Masculino , Meio SocialRESUMO
We documented nine male homosexual consortships within three different male-male dyads in a free-ranging all-male group of Japanese macaques (Macaca fuscata), at Minoo, Japan. A total of 63 male-male mounts were observed during these consortships. Male homosexual interactions shared most of the behavioral components that have been reported to characterize heterosexual and female homosexual consortships in this species. Convergent behavioral data, including analysis of male-male solicitations, mounting postures, body orientations, inter-mount activities, and third-party male intrusions supported the conclusion that male-male consortships are a sexual phenomenon. We discussed a series of proximate and ultimate hypotheses that purport to account for the occurrence of male homosexual behavior in all-male groups of primates, including humans. This first report of male homosexual interactions in an all-male group of Japanese macaques contributes to the growing database used to provide insights into the developmental processes, causal mechanisms, adaptive significance, and phylogenetic pathways of same-sex sexual behavior.
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Homossexualidade Masculina , Macaca/psicologia , Comportamento Sexual Animal , Animais , Corte , Japão , MasculinoRESUMO
We studied the development of sexual behaviors in female Japanese macaques (Macaca fuscata) living at Arashiyama, Japan, in a group where adult females routinely exhibit sexual interactions with both males and females. Our cross-sectional data on juvenile, adolescent, and adult females supported most of our predictions related to the learning hypothesis, which holds that adolescence serves to provide females with a period in which to practice adult female-like sexual behavioral patterns, including sexual solicitations, sexual mounts, and spatio-temporal coordination during consortships. We found evidence for a gradual acquisition of adult-like behavioral patterns (e.g., more frequent solicitations with body contact, more frequent complete mounts, more diverse solicitation patterns and complete mounting postures, and longer consortships involving prolonged inter-mount grasping behavior between partners), and a gradual disappearance of less effective immature behavioral patterns (e.g., less frequent non-contact solicitations, ambiguous mounting initiations, and incomplete mounts). We distinguished between three major categories of sexual behavioral patterns based on their speed of development, ranging from fast (e.g., diversity in mounting postures and genital stimulation during mounting) to slow (e.g., contact solicitations and grasping behavior between consortship partners), with some being intermediate (e.g., range of solicitation patterns and expression of complete mounts). This study showed that the emergence of both conceptive and non-conceptive adult sexual behaviors can be traced back to immature behavioral patterns in adolescent female Japanese macaques, with a major threshold occurring at the age of 4 years.
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Aprendizagem/fisiologia , Macaca/fisiologia , Comportamento Sexual Animal/fisiologia , Maturidade Sexual/fisiologia , Animais , Estudos Transversais , Feminino , JapãoRESUMO
My main goal in this paper is to propose a reformulation of foundational models in behavioral research, including Tinbergen's (1963) well-known four levels of analysis (namely, ontogenetic, mechanistic, functional, and evolutionary questions) and Mayr's (1961) dichotomy between proximate and ultimate causations. After critically evaluating these influential but problematic models, I present a three-level neo-Tinbergenian approach to behavior that considers the triadic integration of behavioral causes, structure, and consequences along a single temporal continuum. I then argue that object-directed play is a good candidate behavior to apply this new paradigm by presenting significant examples of the combined analysis of at least two of these three levels. Finally, I show how stone handling, a form of culturally-transmitted object play in macaques, is perfectly amenable to this unified three-level explanatory framework. My proposed approach fits recent theoretical and empirical advances in behavioral biology, has a heuristic value, and may provide numerous benefits to a range of behavioral scientists.
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Evolução Biológica , Macaca , Animais , Causalidade , Pesquisa ComportamentalRESUMO
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.
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Social influence is at the core of the emergence and maintenance of behavioral traditions in various animal taxa. Response facilitation is a mechanism of social influence whereby observing a demonstrator performing a behavior temporarily increases the probability that the observer will perform the same behavior. We focused on stone handling (SH) behavior, a form of object-directed play routinely displayed by free-ranging long-tailed macaques (Macaca fascicularis) in Ubud, Bali, Indonesia. We tested whether the expression of SH was subject to dyadic response facilitation. We compared video-recorded focal samples of an individual immediately after they had witnessed a SH bout performed by a conspecific, and matched-control focal samples of the same witness in the absence of any surrounding SH bouts. We found converging evidence that SH was facilitated within pairs of individuals. First, SH occurred significantly more often and lasted significantly longer in the post-witnessing condition than in the matched-control condition. Second, a monkey initiated SH more rapidly in the former than in the latter, and this significant facilitation effect mainly occurred during the first two minutes after witnessing SH. By demonstrating that the expression of SH was socially mediated, we provided further support for the cultural nature of this behavior.
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Macaca fascicularis , AnimaisRESUMO
Stone handling (SH) is a form of solitary object play that is socially learned and culturally maintained. We studied two captive groups (Modena, N = 20; Padova, N = 20) of common long-tailed macaques housed in a sanctuary in Italy. Our research goal was two-fold: (1) establish the first SH repertoire in captive-raised long-tailed macaques, and (2) explain major differences in the expression of SH between the two study groups. Despite being of identical size and sharing similar environmental conditions, we found that SH was performed by most group members in Modena, whereas SH was absent in Padova. We aimed to explain this inter-group variation by exploring the role of proximate factors that are known to affect the occurrence of SH: demography, dominance, stone availability, activity budget, and food provisioning. The atypical age structure of Padova (i.e., no immature individuals) may have impaired the emergence of SH in this group. In Modena, we found no significant effect of hierarchical rank on SH frequency and duration and no temporal relationship between SH and feeding. Regarding the activity budget, SH filled in for a portion of affiliative and resting behaviours in Modena. Our findings lend support to the cultural nature of SH.
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Alimentos , Animais , Macaca fascicularis , ItáliaRESUMO
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.
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Object affordances play a major role in action expression: (a) providing opportunities to generate potential solutions to instrumental problems and (b) shaping and constraining the motor actions available to an individual. The playful manipulation of objects can facilitate individual acquisition of functional object-assisted actions through affordance learning. We tested the "object affordance" hypothesis in free-ranging long-tailed macaques. This hypothesis holds that the physical properties associated with stone size afford different stone-directed actions, in the context of stone handling (SH) behavior, a form of culturally maintained stone play from which stone tool use can emerge. We predicted that higher SH versatility (i.e., total number of different SH behavioral elements expressed) and higher duration of the SH behavioral element "Pound" would be associated with the manipulation of medium-sized stones, followed by small stones, and then large stones. Our data partly supported these predictions. Both medium-sized and small-sized stones afforded the highest SH versatility, and a higher duration of "Pound" than large stones. As expected, duration of "Pound" was higher with medium than small stones, but the difference was not statistically significant. Our results were consistent with Newell's constraint model, which emphasizes the role of objects' physical properties in limiting and enhancing the expression of actions directed to these objects. The relaxed selective pressures acting on SH behavior may enhance the expression of a range of actions directed toward stones of different sizes that could facilitate the emergence of instrumental solutions and may contribute to explaining the evolution of lithic technology in early humans. (PsycInfo Database Record (c) 2021 APA, all rights reserved).
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Comportamento de Utilização de Ferramentas , Animais , Humanos , Macaca fascicularisRESUMO
The 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. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.
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Aprendizagem , Macaca fascicularis/psicologia , Recompensa , Comportamento Social , Animais , Feminino , Indonésia , Masculino , Reforço por RecompensaRESUMO
The preferential use of one hand over the other is considered the primary behavioral expression of structural and functional asymmetry in cerebral structures, which is a decisive factor in human evolution. We present the first analysis of manual laterality in a form of object play-stone handling (SH) behavior-in a free-ranging group of Japanese macaques. Defined as a stone-directed manipulative activity, and comprised of multiple one-handed SH patterns (e.g., grabbing a stone in one hand and cradling it against its chest), as well as coordinated two-handed SH patterns with manual role differentiation (e.g., holding a stone with one hand and rubbing it with the other), SH behavior is a good candidate for the study of hand lateralization. We systematically followed the methodological framework developed by McGrew and Marchant (1997) to measure and analyze the presence, strength, and direction of manual preference in the performance of SH behavior and in various SH patterns, both at the individual and group level. Some individuals showed a significant manual lateral bias on a single SH pattern (hand preference), whereas others showed consistency in laterality across all or most of the SH patterns they performed (hand specialization). At the group level, we found that, although their collective distribution of left versus right remained random, most subjects were either significantly but incompletely lateralized, or completely lateralized within particular SH patterns (pattern specialization), but not across all SH patterns (no handedness for SH behavior as a whole). As predicted by the task-complexity model, hand specialization and handedness were stronger in the coordinated bimanual SH patterns than in the unimanual patterns. We discuss the implications of our findings for the evolution of manual preferences in noninstrumental object manipulation versus stone tool use in nonhuman primates and hominins.
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Lateralidade Funcional , Macaca/psicologia , Fatores Etários , Animais , Ecossistema , Feminino , Lateralidade Funcional/genética , Japão , Macaca/fisiologia , Masculino , Postura , Fatores Sexuais , Comportamento de Utilização de FerramentasRESUMO
Demonstrating the ability to 'copy' the behavior of others is an important aspect in determining whether social learning occurs and whether group level differences in a given behavior represent cultural differences or not. Understanding the occurrence of this process in its natural context is essential, but can be a daunting task in the wild. In order to test the social learning hypothesis for the acquisition of leaf swallowing (LS), a self-medicative behavior associated with the expulsion of parasites, we conducted semi-naturalistic experiments on two captive groups of parasite-free, naïve chimpanzees (Pan troglodytes). Individuals in the group were systematically provided appropriate stimuli (rough hispid leaves) identical to those used by chimpanzees in the wild. Individuals initially responded in a variety of ways, ranging from total aversion to normal chewing and swallowing. Over time, however, the two groups adopted different variants for inserting and folding the leaves in the mouth prior to swallowing them (complete and partial LS), following the specific method spontaneously displayed by the first and primary LS models in their respective groups. These variants were similar to LS displayed by chimpanzees in the wild. Using the option-bias method, we found evidence for social learning leading to group-level biased transmission and group-level stabilization of these two variants. This is the first report on two distinct cultural variants innovated in response to the introduction of natural stimuli that emerged and spread spontaneously and concurrently within two adjacent groups of socially housed primates. These observations support the assertion that LS may reflect a generalized propensity for ingesting rough hispid leaves, which can be socially induced and transmitted within a group. Ingesting an adequate number of these leaves induces increased gut motility, which is responsible for the subsequent expulsion of particular parasite species in the wild. Cultural transmission and maintenance of LS within a group and associative learning by the individual of the positive consequences of this otherwise non-nutritive mode of ingestion is proposed to be the pivotal link between this feeding propensity and its maintenance as a self-medicative behavior by great apes in the wild.