Towards a three-level neo-Tinbergenian approach to object play: Structure, causes and consequences of a behavioral puzzle.

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.

A tool to act blind? Object-assisted eye-covering as a self-handicapping behavior and social play signal in Balinese long-tailed macaques.

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.

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.

Mechanisms of expression of object play: A comparative study of stone handling in two captive groups of long-tailed macaques (Macaca fascicularis fascicularis).

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.

Dyadic response facilitation of object play in Balinese long-tailed macaques.

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.

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

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.

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.

Stone affordances as potential for action expression in object play in long-tailed macaques (Macaca fascicularis).

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).

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

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'.

Animal Culture: How a New Birdsong Went Viral.

A new white-throated sparrow song has overtaken most of Canada in less than 20 years. The explanation for this remarkably fast spread may lie in the southern migratory grounds, where populations from across Canada converge each winter.

Is female-male mounting functional? An analysis of the temporal patterns of sexual behaviors in Japanese macaques.

In certain populations of Japanese macaques, adult females mount adult males in the context of heterosexual consortships (i.e., temporary but exclusive sexual associations between a male and a female). Previous research suggested that, in this primate species, female-male mounting (FMM) may be a behavioral adaptation. This functional hypothesis holds that FMM is a (special) courtship behaviour, or a (super) sexual solicitation, that serves the function of focusing the male's attention, preventing him from moving away, and expediting male-female mounting, in the context of high female competition for male mates. In this study, we aimed to test some of the proposed functional features of FMM in Japanese macaques by comparing the temporal structure of mating behavioral sequences, including various well-known sexual solicitations, exhibited during heterosexual consortships with and without FMM. To identify and compare recurring series of behavioral events within and across sequences, we used a temporal analysis known as "T-pattern detection and analysis". Our results (partly) supported the "FMM as a (super) sexual solicitation" hypotheses, and supported the "FMM as a sexual adaptation" hypothesis. The utilization of TPA allows for the detection of hidden features of primates' behaviors otherwise undetectable by using conventional quantitative approaches, such as the calculation of frequencies or durations of isolated behavioral components, disjointed from the comprehensive behavioral architecture. This study fits into the scheme of a broader investigation of the functionality of non-conceptive mounting patterns observed in Japanese macaques and a reconstruction of their evolutionary history.

Inferring functional patterns of tool use behavior from the temporal structure of object play sequences in a non-human primate species.

Inferring functional components of behavioral sequences is a crucial but challenging task. A systematic comparison of their temporal structure is a good starting point, based on the postulate that more functional traits are less structurally variable. We studied stone handling behavior (SH) in Balinese long-tailed macaques, a versatile form of stone-directed play. We tested the hypothesis that stones are used by male monkeys to stimulate their genitals in a sexual context (i.e., "sex toy" hypothesis). Specifically, two SH actions (i.e., "tap-on-groin" (TOG) and "rub-on-groin" (ROG), respectively the repetitive tapping and rubbing of a stone onto the genital area) gained functional properties as self-directed tool-assisted masturbation. Owing to the structural organization of playful activities, we predicted that SH sequences without TOG/ROG would exhibit higher levels of variability, repeatability and exaggeration than SH sequences with TOG/ROG. We also predicted that TOG/ROG would occur more often and last longer in SH sequences in which penile erection - a sexually-motivated physiological response in primates - was observed than in SH sequences in which penile erection was not observed. To identify and compare recurring series of SH patterns otherwise undetectable by using conventional quantitative approaches across SH sequences containing TOG/ROG or not, we used a temporal analysis known as "T-pattern detection and analysis" (TPA). Our predictions about variability, exaggeration and temporal association between TOG/ROG in males and penile erection were supported. As expected, SH sequences without TOG/ROG were, on average, more repeatable than SH sequences with TOG/ROG, but the difference was not statistically significant. Overall, the "sex toy" hypothesis was partly supported, and our results suggested that TOG and ROG are two forms of tool-assisted genital stimulation, possibly derived from the playful handling of stones. These findings are consistent with the view that tool use may evolve in stages from initially non-functional object manipulation, such as object play.

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.

Are the roots of human economic systems shared with non-human primates?

We review and analyze evidence for an evolutionary rooting of human economic behaviors and organization in non-human primates. Rather than focusing on the direct application of economic models that a priori account for animal decision behavior, we adopt an inductive definition of economic behavior in terms of the contribution of individual cognitive capacities to the provision of resources within an exchange structure. We spell out to what extent non-human primates' individual and strategic decision behaviors are shared with humans. We focus on the ability to trade, through barter or token-mediated exchanges, as a landmark of an economic system among members of the same species. It is an open question why only humans have reached a high level of economic sophistication. While primates have many of the necessary cognitive abilities (symbolic and computational) in isolation, one plausible issue we identify is the limits in exerting cognitive control to combine several sources of information. The difference between human and non-human primates' economies might well then be in degree rather than kind.

Confirmation and further delineation of the SMG9-deficiency syndrome, a rare and severe developmental disorder.

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.

Is play a behavior system, and, if so, what kind?

Given that many behavior patterns cluster together in sequences that are organized to solve specific problems (e.g., foraging), a fruitful perspective within which to study behaviors is as distinct 'behavior systems'. Unlike many behavior systems that are widespread (e.g., anti-predator behavior, foraging, reproduction), behavior that can be relegated as playful is diverse, involving behavior patterns that are typically present in other behavior systems, sporadic in its phylogenetic distribution and relatively rare, suggesting that play is not a distinct behavior system. Yet the most striking and complex forms of play have the organizational integrity that suggests that it is a behavior system. One model that we develop in this paper, involves three stages of evolutionary transition to account for how the former can evolve into the latter. First, play-like behavior emerges from the incomplete development of other, functional behavior systems in some lineages. Second, in some of those lineages, the behavior patterns typical of particular behavior systems (e.g., foraging) are reorganized, leading to the evolution of specific 'play behavior systems'. Third, some lineages that have independently evolved more than one such play behavior system, coalesce these into a 'super system', allowing some animals to combine behavior patterns from different behavior systems during play. Alternative models are considered, but irrespective of the model, the overall message from this paper is that the conceptual framework of the behavior system approach can provide some new insights into the organization and diversity of play present in the animal kingdom.

Hormonal contraceptive affects heterosexual but not homosexual behavior in free-ranging female Japanese macaques over 17 mating seasons.

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.

Deer Mates: A Quantitative Study of Heterospecific Sexual Behaviors Performed by Japanese Macaques Toward Sika Deer.

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.

Intergroup variation in robbing and bartering by long-tailed macaques at Uluwatu Temple (Bali, Indonesia).

Robbing and bartering (RB) is a behavioral practice anecdotally reported in free-ranging commensal macaques. It usually occurs in two steps: after taking inedible objects (e.g., glasses) from humans, the macaques appear to use them as tokens, returning them to humans in exchange for food. While extensively studied in captivity, our research is the first to investigate the object/food exchange between humans and primates in a natural setting. During a 4-month study in 2010, we used both focal and event sampling to record 201 RB events in a population of long-tailed macaques (Macaca fascicularis), including four neighboring groups ranging freely around Uluwatu Temple, Bali (Indonesia). In each group, we documented the RB frequency, prevalence and outcome, and tested the underpinning anthropogenic and demographic determinants. In line with the environmental opportunity hypothesis, we found a positive qualitative relation at the group level between time spent in tourist zones and RB frequency or prevalence. For two of the four groups, RB events were significantly more frequent when humans were more present in the environment. We also found qualitative partial support for the male-biased sex ratio hypothesis [i.e., RB was more frequent and prevalent in groups with higher ratios of (sub)adult males], whereas the group density hypothesis was not supported. This preliminary study showed that RB is a spontaneous, customary (in some groups), and enduring population-specific practice characterized by intergroup variation in Balinese macaques. As such, RB is a candidate for a new behavioral tradition in this species.