Sudden death caused by Aeromonas hydrophila in a Crab-eating Macaque (Macaca fascicularis) associated with captivity stress.

Aeromonas hydrophila is a facultative anaerobic gram-negative bacterium regarded as an opportunistic pathogen in animals. A 17-year-old female crab-eating macaque (Macaca fascicularis) died after experiencing anorexia and depression for several days. The carcass was severely emaciated, and the sternum was exposed under subcutaneous lesions in the thorax. Many abnormal pathological lesions were found, including tracheal inflammation, pulmonary inflammatory emphysema, yellowish discoloration of the liver, enlargement of the gall bladder, necrosis of the heart, congested bilateral kidneys, and enlargement of the adrenal glands. The stomach was empty, mucosal ulcerations were found, and the duodenum was congested. Giemsa staining revealed rod-shaped organisms in the whole blood smear and major organs, which were identified as A. hydrophila. The animal had experienced stress, and decreased immune system function possibly contributed to the infection.

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'.

Does rank rule? Rank-related grooming patterns in Nicobar long-tailed macaques Macaca fascicularis umbrosus.

Primates maintain social bonds with specific individuals in the group by directing grooming toward them. Social grooming is often targeted toward individuals with whom the most benefits can be exchanged, which are usually the high-ranking individuals. We used the Seyfarth model to investigate whether dominance rank alters the distribution of grooming in a group of Macaca fascicularis umbrosus at Great Nicobar Island. We investigated whether dominance rank predicted grooming rate in both males and females. We used social network analysis to examine whether high-ranking animals maintain a central position in the grooming network. We also investigated whether adult individuals exchange grooming for social tolerance, as indicated by physical proximity. We found that more social grooming was directed toward high-ranking females, but not high-ranking males. Social network analysis suggested that high-ranking animals are not central individuals in the distribution of grooming; rather, middle-ranking animals were major contributors to the distribution of grooming. There was no relation between the grooming rate and proximity in both males and females. Overall, our findings suggest that females prefer to direct grooming toward high-ranking partners, although the dominance hierarchy is less steep than expected for Macaca fascicularis. Thus rank-related grooming patterns may be a relatively conserved trait in this isolated island population.

Do males bond? A study of male-male relationships in Nicobar long-tailed macaques Macaca fascicularis umbrosus.

In primates, males compete for a mate, which is a non-sharable resource. This makes the conditions less conducive for males to have stable relationships. One such special kind of relationship is a bond where the interactions are reciprocated, equitable and differentiated. Bonds in macaque societies are based on the degree of within-group contest competition for mates which is dependent on the synchronization of female fertile phase and reliability of fertility signals. Species of the Fascicularis group, including Nicobar subspecies, show intermediate reliability in the signals with mild peaks, and studies have shown reciprocity but no differentiation. We conducted a study on a group of wild Nicobar long-tailed macaques Macaca fascicularis umbrosus to understand the existing patterns of male-male relationships. We examined whether there is reciprocity in affiliation among the individuals and whether the rate of affiliation is balanced. We also measured the dominance linearity and steepness in the group to understand the monopolizability of females. We used social network analysis to understand whether the relations are differentiated based on hierarchical position and whether the high-ranking individuals are the most central individuals in the distribution of grooming in the group. We found that there is reciprocity among the males although that is not equitable. There was no rankrelated differentiation of affiliation among the males of the group. Instead, the identities of individuals influenced affiliation patterns. Our results correspond to the existent strong relationships but lack of social bond otherwise found in the Fascicularis group of macaques.

Atypical behaviour and connectivity in SHANK3-mutant macaques.

Mutation or disruption of the SH3 and ankyrin repeat domains 3 (SHANK3) gene represents a highly penetrant, monogenic risk factor for autism spectrum disorder, and is a cause of Phelan-McDermid syndrome. Recent advances in gene editing have enabled the creation of genetically engineered non-human-primate models, which might better approximate the behavioural and neural phenotypes of autism spectrum disorder than do rodent models, and may lead to more effective treatments. Here we report CRISPR-Cas9-mediated generation of germline-transmissible mutations of SHANK3 in cynomolgus macaques (Macaca fascicularis) and their F1 offspring. Genotyping of somatic cells as well as brain biopsies confirmed mutations in the SHANK3 gene and reduced levels of SHANK3 protein in these macaques. Analysis of data from functional magnetic resonance imaging revealed altered local and global connectivity patterns that were indicative of circuit abnormalities. The founder mutants exhibited sleep disturbances, motor deficits and increased repetitive behaviours, as well as social and learning impairments. Together, these results parallel some aspects of the dysfunctions in the SHANK3 gene and circuits, as well as the behavioural phenotypes, that characterize autism spectrum disorder and Phelan-McDermid syndrome.

Depressed female cynomolgus monkeys (Macaca fascicularis) display a higher second-to-fourth (2D:4D) digit ratio.

This research aimed to provide evidence of a relationship between digit ratio and depression status in the cynomolgus monkey (Macaca fascicularis). In stable cynomolgus monkey social groups, we selected 15 depressed monkeys based on depressive-like behavioral criteria and 16 normal control monkeys. All animals were video recorded for two weeks, with the duration and frequency of the core depressive behaviors and 58 other behaviors in 12 behavioral categories then evaluated via behavioral analysis. Finger lengths from the right and left forelimb hands of both groups were measured by X-ray imaging. Finger length and digit ratio comparisons between the two groups were conducted using Student's t-test. In terms of the duration of each behavior, significant differences emerged in "Huddling" and five other behavioral categories, including Ingestive, Amicable, Parental, Locomotive, and Resting. In addition to the above five behavioral categories, we found that depressed monkeys spent less time in parental and rubbing back and forth behaviors than the control group. Furthermore, the 4th fingers were significantly longer in the left and right hands in the control group relative to the depressed monkeys. The second-to-fourth (2D:4D) digit ratio in the left and right forelimb hands was significantly lower in the control group than that in the depressed group. Our findings revealed significant differences in finger lengths and digit ratios between depressed monkeys and healthy controls, which concords with our view that relatively high fetal testosterone exposure may be a protective factor against developing depressive symptoms (or that low fetal testosterone exposure is a risk factor).

Tool-use training temporarily enhances cognitive performance in long-tailed macaques (Macaca fascicularis).

Tool use relies on numerous cognitive functions, including sustained attention and understanding of causality. In this study, we investigated the effects of tool-use training on cognitive performance in primates. Specifically, we applied the Primate Cognition Test Battery to three long-tailed macaques (Macaca fascicularis) at different stages of a training procedure that consisted of using a rake to retrieve out-of-reach food items. In addition, we evaluated a control group (n = 3) performing a grasping task, in order to account for possible effects related to a simple motor act. Our results showed that tool-use training enhances mean performance in the physical cognition domain, i.e. the understanding of spatial relations, numerosity and causality. In particular, causal cognition (evaluating noise- and shape-related causality and understanding of tool properties) showed significant improvement after training, whereas spatial cognition (evaluating spatial memory, object permanence, rotation and transposition) showed a trend to improvement. Despite these findings, none of our trained monkeys succeeded in the tool-use task of the Primate Cognition Test Battery, which involved an unfamiliar tool. Some training-related effects did not persist after a 35-day resting period, suggesting that continuous practice may be necessary, or that a longer training period before resting may be needed to better maintain cognitive performance. In contrast with the training group, the control group did not display any change in cognitive performance. This finding paves the way to further investigation into the link between tool-use behaviour and the evolution of primate cognition.

Resource depletion through primate stone technology.

Tool use has allowed humans to become one of the most successful species. However, tool-assisted foraging has also pushed many of our prey species to extinction or endangerment, a technology-driven process thought to be uniquely human. Here, we demonstrate that tool-assisted foraging on shellfish by long-tailed macaques (Macaca fascicularis) in Khao Sam Roi Yot National Park, Thailand, reduces prey size and prey abundance, with more pronounced effects where the macaque population size is larger. We compared availability, sizes and maturation stages of shellfish between two adjacent islands inhabited by different-sized macaque populations and demonstrate potential effects on the prey reproductive biology. We provide evidence that once technological macaques reach a large enough group size, they enter a feedback loop - driving shellfish prey size down with attendant changes in the tool sizes used by the monkeys. If this pattern continues, prey populations could be reduced to a point where tool-assisted foraging is no longer beneficial to the macaques, which in return may lessen or extinguish the remarkable foraging technology employed by these primates.

Tailored Enrichment Strategies and Stereotypic Behavior in Captive Individually Housed Macaques (Macaca spp.).

The welfare of nonhuman animals in captivity is widely dependent on the natural psychological, physical, and behavioral needs of the animals and how adequately these needs are met. Inability to engage in natural behaviors can lead to chronic stress and expression of stereotypic behavior. The majority of research on decreasing stereotypic behavior in captivity addresses problems at the group level and does not account for individual variability in each animal's needs, history, and preferences. This study combined physiological and behavioral measures of well being to comprehensively assess the unique needs of individually housed captive macaques (Macaca spp.) with the aim of developing tailored welfare strategies. Behavioral and hormonal data were collected under 2 conditions: baseline and individualized enrichment. The results showed a significant decrease in stereotypic behavior under the enrichment condition. Additionally, 7 out of 9 individuals showed a decrease in fecal glucocorticoid (stress hormone) levels, indicating a reduction in hypothalamic-pituitary-adrenal activity. Addressing welfare on an individual, rather than group, level allows for a better overall characterization of well being and maximizes the probability of improving the welfare of each animal.

Do monkeys compare themselves to others?

Social comparisons are a fundamental characteristic of human behaviour, yet relatively little is known about their evolutionary foundations. Adapting the co-acting paradigm from human research (Seta in J Pers Soc Psychol 42:281-291, 1982. doi: 10.1037//0022-3514.42.2.281), we examined how the performance of a partner influenced subjects' performance in long-tailed macaques (Macaca fascicularis). Using parallel testing in touch screen setups in which subjects had to discriminate familiar and novel photographs of men and women, we investigated whether accuracy and reaction time were influenced by partner performance and relationship quality (affiliate vs. non-affiliate). Auditory feedback about the alleged performance of the co-actor was provided via playback; partner performance was either moderately or extremely better or worse than subject performance. We predicted that subjects would assimilate to moderately different comparison standards as well as to affiliates and contrast away from extreme standards and non-affiliates. Subjects instantly generalized to novel pictures. While accuracy was not affected by any of the factors, long reaction times occurred more frequently when subjects were tested with a non-affiliate who was performing worse, compared to one who was doing better than them (80% quantile worse: 5.1, better: 4.3 s). For affiliate co-actors, there was no marked effect (worse: 4.4, better: 4.6 s). In a control condition with no auditory feedback, subjects performed somewhat better in the presence of affiliates (M = 77.8% correct) compared to non-affiliates (M = 71.1%), while reaction time was not affected. Apparently, subjects were sensitive to partner identity and performance, yet variation in motivation rather than assimilation and contrast effects may account for the observed effects.

Stress-relevant social behaviors of middle-class male cynomolgus monkeys (Macaca fascicularis).

Stress from dominance ranks in human societies, or that of other social animals, especially nonhuman primates, can have negative influences on health. Individuals holding different social status may be burdened with various stress levels. The middle class experiences a special stress situation within the dominance hierarchy due to its position between the higher and lower classes. Behaviorally, questions about where middle-class stress comes from and how individuals adapt to middle-class stress remain poorly understood in nonhuman primates. In the present study, social interactions, including aggression, avoidance, grooming and mounting behaviors, between beta males, as well as among group members holding higher or lower social status, were analyzed in captive male-only cynomolgus monkey groups. We found that aggressive tension from the higher hierarchy members was the main origin of stress for middle-class individuals. However, behaviors such as attacking lower hierarchy members immediately after being the recipient of aggression, as well as increased avoidance, grooming and mounting toward both higher and lower hierarchy members helped alleviate middle-class stress and were particular adaptations to middle-class social status.

Effect of new training technique on affinity of cynomolgus monkeys for animal care personnel.

To confirm our hypothesis that the sex and age of cynomolgus monkeys influences the effect of training, we employed a new training technique designed to increase the animal's affinity for animal care personnel. During 151 days of training, monkeys aged 2 to 10 years accepted each 3 raisins/3 times/day, and communicated with animal care personnel (5 times/day). Behavior was scored using integers between -1 and 5. Before training, 35 of the 61 monkeys refused raisins offered directly by animal care personnel (Score -1, 0 and 1). After training, 28 of these 35 monkeys (80%) accepted raisins offered directly by animal care personnel (>Score 2). The mean score of monkeys increased from 1.2 ± 0.1 to 4.3 ± 0.2. The minimum training period required for monkeys to reach Score 2 was longer for females than for males. After 151 days, 6 of the 31 females and 1 of the 30 males still refused raisins offered directly by animal care personnel. Beneficial effects of training were obtained in both young and adult monkeys. These results indicate that our new training technique markedly improves the affinity of monkeys for animal care personnel, and that these effects tend to vary by sex but not age. In addition, abnormal behavior and symptoms of monkeys were improved by this training.

No costly prosociality among related long-tailed macaques (Macaca fascicularis).

Altruism, benefiting another at a cost to the donor, may be achieved through prosocial behavior. Studies of nonhuman animals typically investigate prosocial behavior with paradigms in which the donor can choose to give a recipient a food item, and the choice does not affect the donor's reward (which is either present or absent). In such tasks, long-tailed macaques (Macaca fascicularis) show prosocial behavior, especially toward kin. Here, we tested captive long-tailed macaques with related recipients in an alternative task, in which the donor had to give up a preferred reward to benefit the recipient; that is, they had to choose a lower valued reward for themselves to provide food to their kin. Overall, the macaques did not provide their kin with food. The task forced the donor to balance its prosocial behavior with its selfish choice for a higher value reward, a balance that turned out to favor selfish motives. Consequently, our study shows that a prosocial tendency is not sufficient to elicit costly prosocial behavior in long-tailed macaques. Subsequently, we feel that tasks in which the donor must choose a lower value reward to benefit another individual may allow the titration of the strength of prosocial behavior, and thus provides interesting possibilities for future comparative studies.

There Is More than One Way to Crack an Oyster: Identifying Variation in Burmese Long-Tailed Macaque (Macaca fascicularis aurea) Stone-Tool Use.

We explored variation in patterns of percussive stone-tool use on coastal foods by Burmese long-tailed macaques (Macaca fascicularis aurea) from two islands in Laem Son National Park, Ranong, Thailand. We catalogued variation into three hammering classes and 17 action patterns, after examining 638 tool-use bouts across 90 individuals. Hammering class was based on the stone surface used for striking food, being face, point, and edge hammering. Action patterns were discriminated by tool material, hand use, posture, and striking motion. Hammering class was analyzed for associations with material and behavioural elements of tool use. Action patterns were not, owing to insufficient instances of most patterns. We collected 3077 scan samples from 109 macaques on Piak Nam Yai Island's coasts, to determine the proportion of individuals using each hammering class and action pattern. Point hammering was significantly more associated with sessile foods, smaller tools, faster striking rates, smoother recoil, unimanual use, and more varied striking direction, than were face and edge hammering, while both point and edge hammering were significantly more associated with precision gripping than face hammering. Edge hammering also showed distinct differences depending on whether such hammering was applied to sessile or unattached foods, resembling point hammering for sessile foods and face hammering for unattached foods. Point hammering and sessile edge hammering compared to prior descriptions of axe hammering, while face and unattached edge hammering compared to pound hammering. Analysis of scans showed that 80% of individuals used tools, each employing one to four different action patterns. The most common patterns were unimanual point hammering (58%), symmetrical-bimanual face hammering (47%) and unimanual face hammering (37%). Unimanual edge hammering was relatively frequent (13%), compared to the other thirteen rare action patterns (<5%). We compare our study to other stone-using primates, and discuss implications for further research.

Differential behavior patterns in cynomolgus monkey Macaca fascicularis in home cage in response to human gaze.

BACKGROUND: Non-human primates, when encountering human beings, show wariness and alertness. These behaviors differ when there is direct human gaze vs. when human averts his gaze. METHODS: We observed cynomolgus monkey in their home cage and studied their behaviors in response to human gaze. Four behaviors were analyzed: opening mouth, staring at observer, agitated activity, and approaching observer. RESULTS: Three behaviors appeared to be sensitive to human gaze between when the human observer gazed at the monkey and when the human observer looked away. Individual animals also displayed subpatterns of responses to human gaze. CONCLUSIONS: These results indicate that, even in their home cage, monkeys display a heightened level of awareness when gazed upon by a human observer, suggesting that human gaze may elicit emotional reactions. Further, under the human gaze, distinct behavioral subpatterns were apparent within the monkey cohort in our study, indicative of subgroups within the cohort.

Costs of mate-guarding in wild male long-tailed macaques (Macaca fascicularis): physiological stress and aggression.

Mate-guarding is an important determinant of male reproductive success in a number of species. However, it is known to potentially incur costs. The aim of the present study was to assess the effect of mate-guarding on male physiological stress and aggression in long-tailed macaques, a species in which males mate-guard females to a lesser extent than predicted by the Priority of Access model (PoA). The study was carried out during two mating periods on three groups of wild long-tailed macaques in Indonesia by combining behavioral observations with non-invasive measurements of fecal glucocorticoid (fGC) levels. Mate-guarding was associated with a general rise in male stress hormone levels but, from a certain threshold of mate-guarding onwards, increased vigilance time was associated with a decrease in stress hormone output. Mate-guarding also increased male-male aggression rate and male vigilance time. Overall, alpha males were more physiologically stressed than other males independently of mating competition. Increased glucocorticoid levels during mate-guarding are most likely adaptive since it may help males to mobilize extra-energy required for mate-guarding and ultimately maintain a balanced energetic status. However, repeated exposure to high levels of stress over an extended period is potentially deleterious to the immune system and thus may carry costs. This potential physiological cost together with the cost of increased aggression mate-guarding male face may limit the male's ability to mate-guard females, explaining the deviance from the PoA model observed in long-tailed macaques. Comparing our results to previous findings we discuss how ecological factors, reproductive seasonality and rank achievement may modulate the extent to which costs of mate-guarding limit male monopolization abilities.

The role of anthropic, ecological, and social factors in sleeping site choice by long-tailed macaques (Macaca fascicularis).

When choosing their sleeping sites, primates make adaptive trade-offs between various biotic and abiotic constraints. In human-modified environments, anthropic factors may play a role. We assessed the influence of ecological (predation), social (intergroup competition), and anthropic (proximity to human settlements) factors in sleeping site choice by long-tailed macaques (Macaca fascicularis) occupying a habitat at the interface of natural forests and human-modified zones in Bali Barat National Park, Indonesia. Over the course of 56 nights, we collected data relating to physical features of sleeping trees, patterns of the use of sleeping sites within the home range, pre-sleep behavior, diurnal ranging patterns and availability of natural and human food. Overall, the macaques used 17 sleeping sites with 37 sleeping trees. When the monkeys slept in forest zones, they selected sleeping trees that had larger trunks but were not significantly taller than surrounding trees. Though the macaques rarely re-used sleeping sites on consecutive nights, they frequently re-used four sites over the study period. The group favored sleeping within the core area of its home range, despite the occurrence of frequent agonistic intergroup encounters there. Macaques preferentially selected sleeping trees located within or near human-modified zones, especially when human food was abundant and natural food was scarce. These results partially support the hypothesis that long-tailed macaques choose their sleeping sites to avoid predation; proximity to human settlements appears to be the primary factor influencing sleeping site choice in this primate species. Our results reflect the strong influence that anthropic factors have on primates, which subsist in increasingly human-dominated landscapes.

The mutual influences between depressed Macaca fascicularis mothers and their infants.

OBJECTIVE: To assess the influence of infant rearing on the behavior of depressed adult female Macaca fascicularis and the influence of depressed infant-rearing adult female Macaca fascicularis on their infants in a free enclosure environment. METHODS: Here, 20 depressed subjects and then 20 healthy subjects were randomly selected from a total population of 1007 adult female Macaca fascicularis subjects. Four depressed subjects and eight healthy subjects were rearing infants. By focal observation, three trained observers video-recorded the selected subjects over a total observational period of 560 hours. The video footage was analyzed by qualified blinded analysts that coded the raw footage into quantitative behavioral data (i.e., durations of 53 pre-defined behavioral items across 12 behavioral categories) for statistical analysis. RESULTS: Between infant-rearing and non-rearing healthy subjects, ten differential behaviors distributed across five behavioral categories were identified. Between infant-rearing and non-rearing depressed subjects, nine behaviors distributed across five behavioral categories were identified. Between infant-rearing healthy and infant-rearing depressed subjects, fifteen behaviors distributed across six behavioral categories were identified. CONCLUSION: Infant-rearing depressed adult female Macaca fascicularis subjects may have a worse psychological status as compared to non-rearing depressed counterparts. Infant rearing may negatively influence depressed Macaca fascicularis mothers. Infant-rearing depressed subjects were less adequate at raising infants as compared to infant-rearing healthy subjects. Thus, maternal depression in this macaque species may negatively impact infatile development, which is consistent with previous findings in humans.

Seeing the experimenter influences the response to pointing cues in long-tailed macaques.

Methodological variations in experimental conditions can strongly influence animals' performances in cognitive tests. Specifically, the procedure of the so-called object-choice task has been controversially discussed; here, a human experimenter indicates the location of hidden food by pointing or gazing at one of two or more containers. Whereas dogs usually succeed, results for nonhuman primates are ambiguous. In the standard version of the task the majority of subjects do not respond appropriately to human pointing. However, modifying the task setup, such as placing the containers further apart, seems to improve subjects' performances, suggesting that cue salience may be an important variable. Here we investigated whether the visibility of the experimenter inhibits long-tailed macaques' (Macaca fascicularis) usage of the pointing cue. In our baseline condition, with the experimenter fully visible, the monkeys chose the correct container in 61% of the trials. The performance increased significantly, however, when the experimenter was hidden behind a curtain and only the arm of the experimenter, a doll's arm, or a stick was visible. Furthermore, the monkeys performed significantly better when the tip of the pointing finger or device was close to the target compared to the more distant condition. Intriguingly, after these experiments the monkeys' performance was also significantly improved in the baseline condition (70%). Apparently, the monkeys were first distracted by the presence of the experimenter, but then learned to use the cue. These findings highlight the importance of the test conditions, and question some of the assumptions about species-specific differences in the object-choice task.