Oil palm cultivation critically affects sociality in a threatened Malaysian primate.

Human-induced habitat alterations globally threaten animal populations, often evoking complex behavioural responses in wildlife. This may be particularly dramatic when negatively affecting social behaviour, which fundamentally determines individual fitness and offspring survival in group-living animals. Here, we provide first evidence for significant behavioural modifications in sociality of southern pig-tailed macaques visiting Malaysian oil palm plantations in search of food despite elevated predation risk. Specifically, we found critical reductions of key positive social interactions but higher rates of aggression in the plantation interior compared to the plantation edge (i.e. plantation areas bordering the forest) and the forest. At the plantation edge, affiliation even increased compared to the forest, while central positions in the macaques' social network structure shifted from high-ranking adult females and immatures to low-ranking individuals. Further, plantations also affected mother-infant relationships, with macaque mothers being more protective in the open plantation environment. We suggest that although primates can temporarily persist in human-altered habitats, their ability to permanently adapt requires the presence of close-by forest and comes with a trade-off in sociality, potentially hampering individual fitness and infant survival. Studies like ours remain critical for understanding species' adaptability to anthropogenic landscapes, which may ultimately contribute to facilitating their coexistence with humans and preserving biodiversity.

Temperament in rhesus, long-tailed, and pigtailed macaques varies by species and sex.

Temperament differs among individuals both within and between species. Evidence suggests that differences in temperament of group members may parallel differences in social behavior among groups or between species. Here, we compared temperament between three closely related species of monkey-rhesus (Macaca mulatta), long-tailed (M. fascicularis), and pigtailed (M. nemestrina) macaques-using cage-front behavioral observations of individually housed monkeys at a National Primate Research Center. Frequencies of 12 behaviors in 899 subjects were analyzed using a principal components analysis to identify temperament components. The analysis identified four components, which we interpreted as Sociability toward humans, Cautiousness, Aggressiveness, and Fearfulness. Species and sexes differed in their average scores on these components, even after controlling for differences in age and early-life experiences. Our results suggest that rhesus macaques are especially aggressive and unsociable toward humans, long-tailed macaques are more cautious and fearful, and pigtailed macaques are more sociable toward humans and less aggressive than the other species. Pigtailed males were notably more sociable than any other group. The differences observed are consistent with reported variation in these species' social behaviors, as rhesus macaques generally engage in more social aggression and pigtailed macaques engage in more male-male affiliative behaviors. Differences in predation risks are among the socioecological factors that might make these species-typical behaviors adaptive. Our results suggest that adaptive species-level social differences may be encoded in individual-level temperaments, which are manifested even outside of a social context. Am. J. Primatol. 75:303-313, 2013. © 2012 Wiley Periodicals, Inc.

Sparse code of conflict in a primate society.

Animals living in groups collectively produce social structure. In this context individuals make strategic decisions about when to cooperate and compete. This requires that individuals can perceive patterns in collective dynamics, but how this pattern extraction occurs is unclear. Our goal is to identify a model that extracts meaningful social patterns from a behavioral time series while remaining cognitively parsimonious by making the fewest demands on memory. Using fine-grained conflict data from macaques, we show that sparse coding, an important principle of neural compression, is an effective method for compressing collective behavior. The sparse code is shown to be efficient, predictive, and socially meaningful. In our monkey society, the sparse code of conflict is composed of related individuals, the policers, and the alpha female. Our results suggest that sparse coding is a natural technique for pattern extraction when cognitive constraints and small sample sizes limit the complexity of inferential models. Our approach highlights the need for cognitive experiments addressing how individuals perceive collective features of social organization.

Multiple time-scales and the developmental dynamics of social systems.

To build a theory of social complexity, we need to understand how aggregate social properties arise from individual interaction rules. Here, I review a body of work on the developmental dynamics of pigtailed macaque social organization and conflict management that provides insight into the mechanistic causes of multi-scale social systems. In this model system coarse-grained, statistical representations of collective dynamics are more predictive of the future state of the system than the constantly in-flux behavioural patterns at the individual level. The data suggest that individuals can perceive and use these representations for strategical decision-making. As an interaction history accumulates the coarse-grained representations consolidate. This constrains individual behaviour and provides the foundations for new levels of organization. The time-scales on which these representations change impact whether the consolidating higher-levels can be modified by individuals and collectively. The time-scales appear to be a function of the 'coarseness' of the representations and the character of the collective dynamics over which they are averages. The data suggest that an advantage of multiple timescales is that they allow social systems to balance tradeoffs between predictability and adaptability. I briefly discuss the implications of these findings for cognition, social niche construction and the evolution of new levels of organization in biological systems.

Aggression in pigtailed macaque (Macaca nemestrina) breeding groups affects pregnancy outcome.

Past research has shown that aggressive behaviors can affect female reproductive outcome in nonhuman primate captive breeding programs. In this study, aggressive behaviors were recorded in a colony of pigtailed macaque monkeys (Macaca nemestrina) and related to pregnancy outcome. For 22 weeks, behavioral data were collected from nine breeding groups, consisting of zero to one male (some males were removed after a cycle of conceptions for husbandry reasons) and four to eight females. Observations included all occurrences of 11 aggressive behaviors during 15 min observation sessions, 1-3 times a week. Mean weekly aggression levels during the study period were determined for each group as well as for each pregnancy. Aggression data were summarized with Principal Components Analyses. Results indicate that pigtailed macaque aggression falls into five distinctive categories: warn, engage, threaten, pursue, and attack. Breeding groups differed in their levels of aggression, even after controlling for group size, presence of a sire, and group stability. Levels of the five aggression categories were found to affect the probability that a pregnancy ended in either a natural birth of a live infant, a clinical intervention producing a live infant, or a nonviable outcome. The predictive value of aggression was significant when clinical interventions were included as possible reproductive outcomes. Behavioral observation of captive groups could identify "risk" conditions affecting pregnancy outcome and the requirement for clinical intervention.

Evaluating paint rollers as an intervention for alopecia in monkeys in the laboratory (Macaca nemestrina).

Adult female macaques (Macaca nemestrina) in the laboratory with alopecia from known or suspected overgrooming were subjects in a study evaluating effectiveness of a grooming device. The intervention evaluated was a paint roller on a metal bar hung on the cage, replaced weekly for 6 weeks. In a within-subjects design, 6 monkeys were randomly assigned to first experience the paint roller (PR) and later the control (C) condition (roller bar only); 6 monkeys were randomly assigned to C followed by PR. Coat condition scores quantifying alopecia were taken cageside weekly. During PR, PR use was scored 3 times a week based on wear. Alopecia scores during PR did not differ significantly from C. Although all the monkeys used the paint rollers, PR use scores did not correlate significantly with improvement in coat condition. Paint rollers do not appear to be an effective intervention for alopecia from overgrooming.

Development of object concepts in macaque monkeys.

One of the most interesting questions in cognitive development is how we acquire and mentally represent knowledge about objects. We investigated the development of object concepts in macaque monkeys. Monkeys viewed trajectory occlusion movies in which a ball followed a linear path that was occluded for some portion of the display while their point of gaze was recorded with a corneal-reflection eye tracker. We analyzed the pattern of eye movements as an indicator of object representation. A majority of eye movements of adult monkeys were anticipatory, implying a functional internal object representation that guided oculomotor behavior. The youngest monkeys lacked this strong internal representation of objects. Longitudinal testing showed that this ability develops over time providing compelling evidence that object concepts develop similarly in monkeys and humans. Therefore, the macaque monkey provides an animal model with which to examine neural mechanisms underlying the development of object representations.

A computer touch screen system and training procedure for use with primate infants: Results from pigtail monkeys (Macaca nemestrina).

Computerized cognitive and perceptual testing has resulted in many advances towards understanding adult brain-behavior relations across a variety of abilities and species. However, there has been little migration of this technology to the assessment of very young primate subjects. We describe a training procedure and software that was developed to teach infant monkeys to interact with a touch screen computer. Eighteen infant pigtail macaques began training at 90-postnatal days and five began at 180-postnatal days. All animals were trained to reliably touch a stimulus presented on a computer screen and no significant differences were found between the two age groups. The results demonstrate the feasibility of using computers to assess cognitive and perceptual abilities early in development.

Communicative contexts of the LEN facial expression of pigtailed macaques (Macaca nemestrina).

We have investigated the contexts of the LEN (lips forward-ears back-neck extended) or pucker, a species-specific facial expression of Macaca nemestrina, in four breeding groups. Using the behavior sampling method we recorded all LENs, associated behavior, and the identities of the individuals involved. Of 401 LENs initiated, 62% were directed to the observer, who never responded to them in any way. Infants and dams directed more LENs to the observer than did sires or other females. The average intraspecific LEN rate was 0.82 per monkey-hour, including LENs given in reciprocation. Excluding LENs given in reciprocation, sires LENned significantly more often to females and dams than to infants, and significantly more than females and dams LENned to them. Of LENs directed to conspecifics, 21% were reciprocated, 34% were followed by distance reduction, and 16% led to both. Reciprocating LEN responses occurred more often to LENs initiated by sires. Although primarily affiliative, some LENs occurred in agonistic contexts, suggesting a possible appeasing function or rejection of a LEN's social invitation. Aggression preceded 8% of conspecific LENs, and 15% of LENs were responded to by visual aggression. No response followed 47% of LENs. Affirming the conclusions of others, LENs are often directed by males to females before mating. LENs directed at cradled infants suggest that maternal LENs serve more than a summoning function. LENs directed to people by M. nemestrina usually seem to be inviting interaction or attention, but LENs by dams seem to reflect concerns over their infants. We speculate that at the most basic level the LEN emphasizes that the sender's gaze is fixed on the receiver. We propose that the LEN may have evolved in this quiet rainforest species to facilitate coordination of social activity when silence or stealth is advantageous.

Social learning in pig-tailed macaques (Macaca nemestrina) and adult humans (Homo sapiens) on a two-action artificial fruit.

An artificial fruit (AF) was used to test for social learning in pig-tailed macaques (Macaca nemestrina) and adult humans (Homo sapiens). A monkey demonstrator opened the AF, showing alternative methods to 2 groups of cage mates. Video films of the monkey demonstrations were presented to adult humans. Compared with chimpanzees and children, the macaques watched the demonstrations significantly less and in a much more sporadic manner. They also produced only very weak and transitory evidence of social learning. In contrast, the adult humans performed as one might expect of optimum imitators, even producing evidence of components of a "ratchet effect."

Animal behaviour: old world monkeys build new world order.

New experimental evidence shows that policing behaviour by dominant monkeys stabilizes and integrates macaque societies.

Policing stabilizes construction of social niches in primates.

All organisms interact with their environment, and in doing so shape it, modifying resource availability. Termed niche construction, this process has been studied primarily at the ecological level with an emphasis on the consequences of construction across generations. We focus on the behavioural process of construction within a single generation, identifying the role a robustness mechanism--conflict management--has in promoting interactions that build social resource networks or social niches. Using 'knockout' experiments on a large, captive group of pigtailed macaques (Macaca nemestrina), we show that a policing function, performed infrequently by a small subset of individuals, significantly contributes to maintaining stable resource networks in the face of chronic perturbations that arise through conflict. When policing is absent, social niches destabilize, with group members building smaller, less diverse, and less integrated grooming, play, proximity and contact-sitting networks. Instability is quantified in terms of reduced mean degree, increased clustering, reduced reach, and increased assortativity. Policing not only controls conflict, we find it significantly influences the structure of networks that constitute essential social resources in gregarious primate societies. The structure of such networks plays a critical role in infant survivorship, emergence and spread of cooperative behaviour, social learning and cultural traditions.

Macaques (Macaca nemestrina) recognize when they are being imitated.

This study investigated whether monkeys recognize when a human experimenter imitates their actions towards an object. Two experimenters faced 10 pigtailed macaques, who were given access to an interesting object. One experimenter imitated the monkeys' object-directed actions, the other performed temporally contingent but structurally different object-directed actions. Results show a significant visual preference for the imitator during manual object manipulations, but not mouthing actions. We argue that the ability to match actions could be based on both visual-visual and kinaesthetic-visual matching skills, and that mirror neurons, which have both visual and motor properties, could serve as a neural basis for recognizing imitation. However, imitation recognition as assessed by visual preference does not necessarily imply the capacity to attribute imitative intentionality to the imitator. The monkeys might implicitly recognize when they are being imitated without deeper insight into the mental processes of others.

Markovian models for the developmental study of social behavior.

Behavioral development involves changes in the probabilities of both social and nonsocial activities and the sequential pattern of activities over time. A number of methods have been offered for the analysis of these patterns of behavioral sequences. However, there continue to be problematic issues, including the analysis of nonstationary data; accommodation of changes in patterns within an observation period, or over repeated observations or age; and identification of differences in pattern changes between individuals or groups, and the factors responsible for these differences. In this work, we analyze data from 15 young monkeys (Macaca nemestrina) using classification and Markovian methods, including a new approach to nonstationary data called the double-chain Markov model (DCCM). These methods allowed us to identify differences in behavior patterns that differentiate between normal subjects and those presenting developmental anomalies.

Between-species variation in the development of hand preference among macaques.

This research examined between-species variation in the development of hand preference among Macaca. Specifically, we examined hand preference using juveniles and adults of three macaque species that differ in social and reactive tendencies in order to examine whether the correlation between temperament and handedness that has been noted within Macaca mulatta occurs between closely related species. Each of the species studied exhibited a different pattern of hand preference development. Both juvenile and adult M. mulatta exhibited group-level left-hand bias. Juvenile Macaca nemestrina were not biased towards either hand at the group-level, whereas adults exhibited a group-level left-hand bias. Neither juvenile nor adult Macaca fascicularis exhibited manual bias at the group-level. Analysis of variance indicated statistically significant main effects of species and age class on hand preference measures. Post-hoc analysis indicated greater use of the left- versus right-hand, and greater hand preference strength independent of direction, among M. mulatta and M. nemestrina than among M. fascicularis, and among adults than among juveniles. These results indicate significant between-species variation in the development of hand preference within the genus Macaca, and are inconsistent with any one single-factor theory yet offered to explain the etiology of primate laterality. We hypothesize that the relationship between handedness and temperament that has been shown within M. mulatta may generalize across closely related primate species.

A comparison of food preferences and nutrient composition in captive squirrel monkeys, Saimiri sciureus, and pigtail macaques, Macaca nemestrina.

I assessed the occurrence of food preferences in captive squirrel monkeys and pigtail macaques and analyzed whether their preferences correlate with nutrient composition. Using a two-alternative choice test, I repeatedly presented six Saimiri sciureus and six Macaca nemestrina with all possible binary combinations of 12 types of food that are part of their diet in captivity. The two species exhibited significantly different rank orders of preference. Correlational analyses revealed that the preference ranking of the squirrel monkeys was significantly positively correlated with total energy content, irrespective of the source of energy as neither total carbohydrate content nor protein or lipid content was significantly correlated with food preference. In contrast, the preference ranking of the pigtail macaques showed a significant positive correlation with total carbohydrate content and with fructose content but not with total energy content of the food items. These results suggest that squirrel monkeys are opportunistic feeders with regard to maximizing net gain of energy, whereas pigtail macaques are not but rather seek to meet their requirements of metabolic energy by preferring foods that are high in carbohydrates.

Behavior, appetite, and urinary cortisol responses by adult female pigtailed macaques to cage size, cage level, room change, and ketamine sedation.

Pigtailed macaques (Macaca nemestrina) and longtailed macaques (M. fascicularis) show behavioral, ecological, and possible temperament differences, and their responses to the laboratory environment might therefore be quite different. We tested pigtailed macaques under the same conditions that were investigated in a previous study with longtailed macaques, using the same comprehensive set of physiological and behavioral measures of stress. First, eight adult females' adaptation to a new room in regulation-size cages was monitored, and in the third week their responses to ketamine sedation were measured. Then they spent two weeks singly housed in each of four cage sizes (USDA regulation size, one size larger, one size smaller, and a very small cage). Half of the subjects were in upper-level cages and the remainder in lower-level cages for the entire study. Cage size, ranging from 20% to 148% of USDA regulation floor area, was not significantly related to abnormal behavior, self-grooming, manipulating the environment, eating/drinking, activity cycle, cortisol excretion, or biscuit consumption. Locomotion and frequency of behavior change were significantly reduced in the smallest cage, but did not differ in cage sizes ranging from 77% to 148% of regulation size. The only manipulation to produce an unequivocal stress response, as measured by cortisol elevation and appetite suppression, was ketamine sedation. Room change and cage changes were associated with minimal cortisol elevation and appetite suppression. Wild-born females showed more appetite suppression after room change than captive-born females. No differences were related to cage level. Pigtailed macaques strongly resembled longtailed macaques except they showed weaker responses to the new room and cage change, probably because the pigtails had spent more time in captivity. These findings support the conclusion that increasing cage size to the next regulation size category would not have measurable positive effects on the psychological well-being of two species of laboratory macaques.

Demographic analysis of the washington regional primate research center pigtailed macaque colony, 1967-1996.

This work presents the results of a demographic analysis of 30 years of breeding records from the University of Washington's recently closed Primate Field Station at Medical Lake, Washington. Summaries of population growth, age-specific fertility and mortality rates, first-year survival, and seasonality of reproduction are presented, as well as an analysis of survival by decade. In addition, we present data on interbirth intervals in this population. In general, pigtailed macaques represent a typical Old World monkey pattern of age-specific fertility and mortality, with a few minor exceptions. We suggest that pigtailed macaques are most similar to rhesus and Barbary macaques, and that Japanese and bonnet macaques differ somewhat in their demographics.

Infant monkeys' visual responses to drawings of normal and distorted faces.

Face-like patterns attract attention from both human and nonhuman primates. The present study explored the facial preferences in infant pigtailed macaques (Macaca nemestrina). Twenty-five subjects looked at 20 paired drawings of adult conspecific monkey faces, and their looking time was recorded. The facial features in the drawings were arranged in positions ranging from a normal to a scrambled face. The subjects looked at the normal face more than expected by chance (P < .02), suggesting a preference, whereas the distorted faces were observed randomly. The normal face may have been preferred because the eyes were in a normal position within the facial outline.