Behavioral, physiological, and genetic drivers of coping in a non-human primate.

Animals experience stressful situations, from predation to social conflicts, but mostly deal with them successfully. This adaptive mechanism, coping, reduces the adverse effects of stressors, and its failure may result in reduced fitness. Substantial inter-individual variation in coping is observed, yet little is known about how behavioral, physiological and genetic drivers regulate coping holistically and contribute to such variations. We assessed behavioral coping styles (n=30), emotional arousal (n=12), and personalities (n=32) of long-tailed macaques (Macaca fascicularis) and also investigated the association of coping with a valine/methionine polymorphism encoded by a critical human stress regulatory gene, catechol-O-methyltransferase (COMT) (n=26). Personality and the human equivalent COMT Val/Met polymorphism were associated with "nonaggression-based" and "aggression-based" coping styles. Compared to nonaggression-based, aggression-based copers maintained higher average facial temperatures, indicating potentially lower emotional arousal, as measured using infrared thermography. These findings demonstrate a complex interplay of various proximate mechanisms governing coping in a non-human primate.

Prosociality in a despotic society.

Prosociality is the intent to improve others' well-being. Existing hypotheses postulate that enhanced social tolerance and inter-individual dependence may facilitate prosocial preferences, which may favor the evolution of altruism. While most studies are restricted to "tolerant" (cooperatively breeding and self-domesticated) species, despotic societies provide an alternative opportunity to investigate prosociality due to nepotism and ample inter-individual dependencies. Japanese macaques live in hierarchical matrilineal societies, with strong kin bonds. Besides, tolerance among non-kin may persist through reciprocity. Using a group service food-provision paradigm, we found prosocial preferences in a semi free-ranging group of Japanese macaques. The extent of provisioning was at levels comparable to tolerant species. Dyadic tolerance predicted the likelihood and magnitude of provisioning, while kinship predicted the magnitude. We emphasize the role of a complex socio-ecology fostering individual prosocial tendencies through kinship and tolerance. These findings necessitate a framework including different forms of interdependence beyond the generally tolerant species.

A novel methodological approach for group classification during fission of a semi-free-ranging group of Japanese macaques (Macaca fuscata).

The self-initiated split of a social group, known as fission, is a challenge faced by many group-living animals. The study of group fission and the social restructuring process in real time provides insights into the mechanism of this biologically important process. Previous studies on fission in Japanese macaques (Macaca fuscata) assigned individuals to newly reorganized groups mainly using behavioral observations and group attendance records based on periods before or after fission itself. Here, we present a novel framework for group classification during the process of fission that uses quantifiable behavioral variables and statistical analyses. The framework was tested on a group fission process at Affenberg Landskron (Austria), a park that housed around 160 semi-free-ranging Japanese macaques. The behavioral data were collected for 26 days during fission. We analyzed three behavioral developments recurrent in fissions in Japanese macaques, that is, independence of behavior, participation in group movements, and separation of nomadic ranges. These analyses were combined to assign individuals to different groups. Our study resulted in one main group (N = 33), one subgroup (N = 36) and 56 individuals whose group membership was still undefined. The demographic characteristics of these newly formed groups were comparable with those of fissioned groups in wild populations. Furthermore, we found that these newly forming groups showed early social dynamics of fission five months before group level movements, that is: grouping based on spatial proximity and spatial withdrawal of the subgroup to the periphery. These results underline the validity of our novel framework to study social dynamics in Japanese macaques during the process of fission. It represents an important addition to existing methods, and we recommend testing its scope in other primate societies.

Evaluation of thermal infrared imaging from uninhabited aerial vehicles for arboreal wildlife surveillance.

An important component of wildlife management and conservation is monitoring the health and population size of wildlife species. Monitoring the population size of an animal group can inform researchers of habitat use, potential changes in habitat and resulting behavioral adaptations, individual health, and the effectiveness of conservation efforts. Arboreal monkeys are difficult to monitor as their habitat is often poorly accessible and most monkey species have some degree of camouflage, making them hard to observe in and below the tree canopy. Surveys conducted using uninhabited aerial vehicles (UAVs) equipped with thermal infrared (TIR) cameras can help overcome these limitations by flying above the canopy and using the contrast between the warm body temperature of the monkeys and the cooler background vegetation, reducing issues with impassable terrain and animal camouflage. We evaluated the technical and procedural elements associated with conducting UAV-TIR surveys for arboreal and terrestrial macaque species. Primary imaging missions and analyses were conducted over a monkey park housing approximately 160 semi-free-ranging Japanese macaques (Macaca fuscata). We demonstrate Repeat Station Imaging (RSI) procedures using co-registered TIR image pairs facilitate the use of image differencing to detect targets that were moving during rapid sequence imaging passes. We also show that 3D point clouds may be generated from highly overlapping UAV-TIR image sets in a forested setting using structure from motion (SfM) image processing techniques. A point cloud showing area-wide elevation values was generated from TIR imagery, but it lacked sufficient point density to reliably determine the 3D locations of monkeys.

Twenty-three-year demographic history of the Affenberg Japanese macaques (Macaca fuscata), a translocated semi-free-ranging group in southern Austria.

Demographic studies on translocated primate groups provide a unique opportunity to study population dynamics, social strategies, and reproductive parameters of a species adapting to new environments. In 1996, 38 Japanese macaques (Macaca fuscata) of the Minoo-H group (Osaka Prefecture, Japan) were translocated to Affenberg Landskron, a four-hectare naturally forested park in southern Austria. By January 2020, the population had increased to 160 individuals, and a total of 223 births were recorded. Births peaked in late April to late May, and the timing was influenced by neither offspring sex nor parity status of the mother. Infant mortality was low (8.97%), mostly involving primiparous females, and the average interbirth intervals were shorter following the death of an infant (1.10 years) than a surviving infant (1.77 years). Females rarely had offspring with the same males repeatedly, and the reproductive success among males declined with increasing years of presence in the group. The main aspects of reproduction, mortality, and mate choice are consistent with published data on natural and provisioned populations in Japan and those translocated to other countries. The life expectancy for females, however, was relatively high (11.72% chance of reaching the age of 20), whereas birth control prevented them from using their lifetime reproductive potential. By January 2020, the number of old individuals (> 18 years; 17.5%) was close to that of juveniles (< 4 years; 22.5%). The specific group composition, along with the inability of males to emigrate out of their natal group, may affect the social dynamics of the population, which merits further attention in future studies.

Exploring the Cognitive Capacities of Japanese Macaques in a Cooperation Game.

Cooperation occurs amongst individuals embedded in a social environment. Consequently, cooperative interactions involve a variety of persistent social influences such as the dynamics of partner choice and reward division. To test for the effects of such dynamics, we conducted cooperation experiments in a captive population of Japanese macaques (Macaca fuscata, N = 164) using a modified version of the loose-string paradigm in an open-experiment design. We show that in addition to becoming more proficient cooperators over the course of the experiments, some of the macaques showed sensitivity to the presence of potential partners and adjusted their behavior accordingly. Furthermore, following an unequal reward division, individuals receiving a lesser reward were more likely to display aggressive and stress-related behaviors. Our experiments demonstrate that Japanese macaques have some understanding of the contingencies involved in cooperation as well as a sensitivity to the subsequent reward division suggestive of an aversion to inequity.

On the sunny side of (new) life: Effect of sunshine duration on age at first reproduction in Japanese macaques (Macaca fuscata).

To produce offspring early in life is energetically demanding and depends greatly on environmental conditions. In female primates, age at first reproduction (AFR) has been associated with social parameters (e.g., population density and social rank), food availability and meteorological conditions (e.g., photoperiod, rainfall patterns, and temperature). Regarding the latter, less attention has been given to the influence of sunshine. In nonhuman primates, including the northern-most distributed Japanese macaque (Macaca fuscata), sunbathing is an effective thermoregulatory strategy to maintain sufficient energy intake during harsh winter months. Furthermore, the energetic value of sunshine and its role in the synthesis of essential vitamins important for sexual development and overall fertility is well investigated using human and animal models. In the present study, we hypothesized that female's AFR is influenced by the amount of sunshine in a semi-free-ranging, provisioned a group of Japanese macaques. To test this, we gathered data on sunshine duration in the year females theoretically experienced the onset of puberty. This phase of the female life cycle is particularly prone to the effects of environmental conditions. In addition to the investigation of sunshine duration and other meteorological conditions (i.e., rainfall and temperature) we controlled for social parameters (i.e., group size and sex ratio) as potential covariates. We found a clear effect of sunshine duration on female AFR: Females who entered puberty in years with more sunshine reproduced for the first time at significantly younger ages than females who experienced less sunshine during this specific period of their development. Possible mechanisms for how the sunshine influences sexual maturation in Japanese macaques are discussed.

Corrigendum: Pulling Rank: Military Rank Affects Hormone Levels and Fairness in an Allocation Experiment.

[This corrects the article on p. 1750 in vol. 7, PMID: 27891109.].

Pulling Rank: Military Rank Affects Hormone Levels and Fairness in an Allocation Experiment.

Status within social hierarchies has great effects on the lives of socially organized mammals. Its effects on human behavior and related physiology, however, is relatively little studied. The present study investigated the impact of military rank on fairness and behavior in relation to salivary cortisol (C) and testosterone (T) levels in male soldiers. For this purpose 180 members of the Austrian Armed Forces belonging to two distinct rank groups participated in two variations of a computer-based guard duty allocation experiment. The rank groups were (1) warrant officers (high rank, HR) and (2) enlisted men (low rank, LR). One soldier from each rank group participated in every experiment. At the beginning of the experiment, one participant was assigned to start standing guard and the other participant at rest. The participant who started at rest could choose if and when to relieve his fellow soldier and therefore had control over the experiment. In order to trigger perception of unfair behavior, an additional experiment was conducted which was manipulated by the experimenter. In the manipulated version both soldiers started in the standing guard position and were never relieved, believing that their opponent was at rest, not relieving them. Our aim was to test whether unfair behavior causes a physiological reaction. Saliva samples for hormone analysis were collected at regular intervals throughout the experiment. We found that in the un-manipulated setup high-ranking soldiers spent less time standing guard than lower ranking individuals. Rank was a significant predictor for C but not for T levels during the experiment. C levels in the HR group were higher than in the LR group. C levels were also elevated in the manipulated experiment compared to the un-manipulated experiment, especially in LR. We assume that the elevated C levels in HR were caused by HR feeling their status challenged by the situation of having to negotiate with an individual of lower military rank. This would be in line with the observation that unequally shared duty favored HR in most cases. We conclude that social status, in the form of military rank affects fairness behavior in social interaction and endocrine levels.

Allelic variation of the COMT gene in a despotic primate society: A haplotype is related to cortisol excretion in Macaca fuscata.

Sequence variations in genes of the monoamine neurotransmitter system and their common function in human and non-human primate species are an ongoing issue of investigation. However, the COMT gene, coding for the catechol-O-methyltransferase, has not yet attracted much scientific attention regarding its functional role in non-human primates. Considering that a polymorphism of the human COMT gene affects the enzyme activity and cortisol level in response to a social stressor, this study investigated the impact of COMT on endocrine stress and behavioural parameters in Japanese macaques (Macaca fuscata). The species exemplifies a despotic hierarchy in which males' social rank positions require an adaptation of behaviour strategies. During the mating period steroid secretion and the frequency of aggressive encounters between males increase. We addressed i) whether this species exhibits potential functional COMT variants, ii) whether these variants are associated with faecal cortisol excretion of males, iii) how they are distributed among different social rank positions and iv) whether they are associated with behavioural strategies during times of mate competition. By genotyping 26 males we identified three COMT haplotypes (HT), including a putative splice mutant (HT3). This variant was associated with increased cortisol excretion. Given the observed inverse correlation between cortisol and physical aggression, we assume that different COMT haplotypes may predispose individuals to pursue more or less aggressive strategies. How these gene-stress effects might favour a specific social role is discussed. Our study of non-invasive genotyping in combination with behavioural and endocrine parameters represents an important step towards the understanding of gene-stress effects in a hierarchically organised primate society.

Using eye tracking to test for individual differences in attention to attractive faces.

We assessed individual differences in visual attention toward faces in relation to their attractiveness via saccadic reaction times. Motivated by the aim to understand individual differences in attention to faces, we tested three hypotheses: (a) Attractive faces hold or capture attention more effectively than less attractive faces; (b) men show a stronger bias toward attractive opposite-sex faces than women; and (c) blue-eyed men show a stronger bias toward blue-eyed than brown-eyed feminine faces. The latter test was included because prior research suggested a high effect size. Our data supported hypotheses (a) and (b) but not (c). By conducting separate tests for disengagement of attention and attention capture, we found that individual differences exist at distinct stages of attentional processing but these differences are of varying robustness and importance. In our conclusion, we also advocate the use of linear mixed effects models as the most appropriate statistical approach for studying inter-individual differences in visual attention with naturalistic stimuli.