Behavioral contrasts between male cynomolgus and lion-tailed macaques

Evidence indicates that primate species differ not only in social structure and concordant social propensities, but also in their approach toward novel objects, environments, and procedures. These differences in response dispositions have been described as being based on differences in characteristic stances toward the environment, also called temperaments. This report extends previous comparative primate research by describing behavioral contrasts observed among males of two macaque species, liontailed and cynomolgus macaques. The lion-tails demonstrated more interest in other animals, more vigilance and instrumental behavior, and more readily adapted to training to enter a small and unfamilar cage than the cynomolgus. These results suggest temperamental differences between the two species. Lion-tails may be characterized as bold, curious, and instrumental in their approach to the environment, while cynomolgus may be characterized as more passive or “reserved”. These differences may form the basis for the well-developed sensorimotor abilities observed in liontails such as the manufacture and use of tools, and may also be related to their highly omnivorous diet. © 1993 Wiley-Liss, Inc.     

Environmental enrichment of brown capuchins (Cebus apella): Behavioral and plasma and fecal cortisol measures of effectiveness

No consensus exists about the quantity and variety of environmental enrichment needed to achieve an acceptable level of psychological well‐being among singly housed primates. Behavioral and plasma and fecal cortisol measures were used to evaluate the effectiveness of four levels of toy and foraging enrichment provided to eight wild‐caught, singly housed adult male brown capuchins (Cebus apella). The 16‐week‐long study comprised six conditions and began with a 4‐week‐long preexperimental and ended with a 4‐week‐long postexperimental period during which the subjects were maintained at baseline enrichment levels. During the intervening 8 weeks, the subjects were randomly assigned to a sequence of four 2‐week‐long experimental conditions: control (baseline conditions), toy (the addition of two plastic toys to each cage), box (access to a foraging box with food treats hidden within crushed alfalfa), and box & toy (the addition of two plastic toys and access to a foraging box). Behavioral responses to changes in enrichment were rapid and extensive. Within‐subject repeated‐measure ANOVAs with planned post hoc contrasts identified highly significant reductions in abnormal and undesirable behaviors (and increases in normal behaviors) as the level of enrichment increased from control to toy to box to box & toy. No significant behavioral differences were found between the control and pre‐ and postexperimental conditions. Plasma and fecal cortisol measures revealed a different response to changing enrichment levels. Repeated‐measure ANOVA models found significant changes in both these measures across the six conditions. The planned post hoc analyses, however, while finding dramatic increases in cortisol titers in both the pre‐ and postexperimental conditions relative to the control condition, did not distinguish cortisol responses among the four enrichment levels. Linear regressions among weekly group means in behavioral and cortisol measures (n = 16) found that plasma cortisol was significantly predicted by the proportions of both normal and abnormal behaviors; as the proportion of normal behaviors increased, the plasma cortisol measures decreased. Plasma cortisol weekly group means were also significantly and positively predicted by fecal cortisol weekly group means, but no behavioral measure significantly predicted fecal cortisol weekly group means. In sum, these findings argue strongly that access to a variety of toy and foraging enrichment positively affects behavioral and physiological responses to stress and enhances psychological well‐being in singly housed brown capuchins. Am. J. Primatol. 48:49–68, 1999. © 1999 Wiley‐Liss, Inc.     

Comparison of confined mandrill (Mandrillus sphinx) behavior in traditional and “ecologically representative” exhibits

Behavior in a confined group of mandrills (Mandrillus sphinx) was compared before and after their move from a traditional, all indoor exhibit to an indoor/outdoor facility. The outdoor exhibit was designed to represent as well as is possible important features of the mandrills' forest habitat. We predicted that activity budgets in the outdoor exhibit would more closely resemble those of wild African Cercopithecines, specifically that time spent in forage/feed, locomotion, and social behavior would increase and time spent stationary would decrease. Time spent in forage/feed, locomotion, and stationary did change, as expected. However, there was a small significant decrease in some social behaviors. Differences in proximate environmental contingencies may explain the behavioral changes observed: feeding/foraging opportunities throughout the time on exhibit; increased social refuges; modest increase in facility size; and significantly increased environmental complexity and novelty. Our results are discussed within the context of data obtained from mandrills and baboons observed along a theoretical continuum between confined and free‐ranging environments. This analysis supports what others have suggested: that primate well‐being is not so much a function of confinement as of the presence of relevant incentives to engage in species‐appropriate behavior. Zoo Biol 18:163–176, 1999. © 1999 Wiley‐Liss, Inc.     

Survey of environmental enhancement programs for laboratory primates

Animal welfare regulations in the United States require that nonhuman primate environmental enhancement plans be made in accordance with currently accepted professional standards; however, little information is available for quantifying common practice. Here we report the results of a 2003 survey that was sent to individuals overseeing enrichment programs at a variety of primate research institutions. The surveys requested information on program administration and management, implementation standards, procedures, and constraints pertaining to major categories of environmental enrichment, as well as intervention plans for animals exhibiting behavioral pathologies. Data were obtained on the management of 35,863 primates in 22 facilities. Behavioral scientists performed program oversight at the majority of facilities. Most programs reported recent changes, most commonly due to external site visits, and least commonly resulting from internal review. Most facilities' institutional animal care and use committees (IACUCs) included of individuals with behavioral expertise, and about two-thirds reported that enrichment issues could influence research protocol design. While most primates were reported to be housed socially (73%), social housing for indoor-housed primates appears to have changed little over the past 10 years. Research protocol issues and social incompatibility were commonly cited constraints. Implementation of feeding, manipulanda, and structural enrichment was relatively unconstrained, and contributions to these aspects of behavioral management generally included individuals in a wide variety of positions within a facility. In contrast, enrichment devices were used on a less widespread basis within facilities, and positive reinforcement programs that involved dedicated trainers were rare. We suggest that altering the role of the IACUC would be a productive avenue for increasing the implementation of social housing, and that an emphasis on prevention rather than intervention against behavioral pathology is warranted. The data from this survey may be useful for anticipating future program evaluations, establishing more effective internal evaluations, and assessing program progress and resource allocation.     

Obesity and Physical and Emotional Well‐Being: Associations between Body Mass Index,Chronic Illness,and the Physical and Mental Components of the SF‐36 Questionnaire

Objective: To clarify the associations between obesity and health‐related quality of life by exploring the associations between physical and emotional well‐being in relation to obesity and the presence of other chronic illness. Research Methods and Procedures: The study data were collected as part of a postal‐survey within the old Oxford Regional Health Authority of England in 1997. Completed questionnaires were returned by 8889 of 13,800 randomly selected adults aged 18 to 64 years. The main outcome measures were body mass index in five categories (underweight, normal weight, overweight, moderately obese, morbidly obese); chronic illness status (any vs. none and number of such illnesses 0, 1 to 2, 3+); and mean SF‐36 questionnaire score in two summary component measures reflecting physical and emotional well‐being. Results: Of the subjects, 31% were overweight and an additional 11% were obese. Body mass index was significantly associated with health status, but the pattern varied according to whether the measure reflected physical or emotional well‐being. Physical, but not emotional, well‐being deteriorated markedly with increasing degree of overweight and was limited in subjects who were obese but had no other chronic condition; subjects with chronic illnesses other than obesity were compromised in both dimensions. In terms of the number of chronic illnesses reported, the additional presence of obesity was associated with a significant deterioration in physical but not emotional well‐being. Discussion: Overweight and obesity are associated with poor levels of subjective health status, particularly in terms of physical well‐being. The limitations in emotional well‐being that are reported here and in other studies may be a result of confounding by the presence of accompanying chronic illness.     

Styles of male social behavior and their endocrine correlates among high-ranking wild baboons

We have previously studied the relationship between dominance rank and physiology among male olive baboons (Papio anubis) living freely in a national park in Africa. In stable hierarchies, such males have distinctive secretory profiles of glucocorticoids and of testosterone. We find that these endocrine features are not, in fact, purely markers of social dominance; instead, they are found only among dominant males with particular stylistic traits of social behavior. One intercorrelated stylistic cluster revolved around the intensity with which the male is involved in sexual consortships (e.g., frequency of copulation, of grooming, degree to which feeding is suppressed by being in consortship). Males most involved in such consortships had the lowest basal cortisol concentrations and smaller cortisol stress-responses. A second stylistic cluster revolved around the degree of social affiliation (e.g., rate of grooming and interacting positively with non-estrus females and infants). Males who were highly affiliated had low basal cortisol concentrations and an attenuated cortisol stress-response. A third cluster revolved around the degree to which males could distinguish between highly threatening interactions with rivals and neutral or mildly threatening ones. Males most adept at this had lower basal cortisol concentrations. These behavioral/endocrine clusters were independent of each other. This suggests that the same adaptive physiological feature (e.g., low basal cortisol concentrations) may arise from different and independent personality styles. © 1992 Wiley-Liss, Inc.     

Styles of male social behavior and their endocrine correlates among low-ranking baboons

We have previously studied the relationship between social subordinance (by approach-avoidance criteria) and physiology among male olive baboons (Papio anubis) living freely in a national park in Africa. In stable hierarchies, subordinate individuals have elevated basal glucocorticoid concentrations and a blunted glucocorticoid response to stress, as well as a prompt suppression of testosterone concentrations during stress. These facets have been interpreted as reflecting the chronic stress of social subordinance. In the present report, we find that these endocrine features do not mark all subordinate individuals. Instead, endocrine profiles differed among subordinate males as a function of particular stylistic traits of social behavior. A subset of subordinate males was identified who had significantly high rates of consortships, a behavior usually shown only by high-ranking males. Such behavior predicted the beginning transition to dominance, as these males were significantly more likely than other subordinates to have moved to the dominant half of the hierarchy over the subsequent 3 years. In keeping with this theme of emerging from subordinance, these individuals also had significantly larger glucocorticoid stress-responses, another feature typical of dominant males. However, these subordinate males also had significantly elevated basal glucocorticoid concentrations; it is suggested that this reflects that stressfulness of their overt and precocious strategy of reproductive competition. In support of this, subordinate males with high rates of covert “stolen copulations” did not show elevated basal glucocorticoid concentrations. A second subset of subordinate males were the most likely to initiate fights or to displace aggression onto a third party after losing a fight. These males had significantly or near-significantly elevated testosterone concentrations, compared to the remaining subordinate cohort. Moreover, these males had significantly lower basal glucocorticoid concentrations; this echoes an extensive literature showing that the availability of a displacement behavior (whether aggressive or otherwise) after a stressor decreases glucocorticoid secretion. In support of this interpretation suggesting that it was the initiation of these aggressive acts which attenuated glucocorticoid secretion, there was no association between glucocorticoid concentrations and participation (independent of initiation) in aggressive interactions. Thus, these findings suggest that variables other than rank alone may be associated with distinctive endocrine profiles, and that even in the face of a social stressor (such as subordinance), particular behavioral styles may attenuate the endocrine indices of stress. Am. J. Primatol. 42:25–39, 1997. © 1997 Wiley-Liss, Inc.     

Dopamine D4 receptor and serotonin transporter gene effects on the longitudinal development of infant temperament

Existing studies of the effect on infant temperament of the 48 base pair variable number of tandem repeats polymorphism in exon 3 of the dopamine D4 receptor gene, DRD4 VNTR, and the serotonin transporter-linked polymorphic region, 5-HTTLPR, have provided contradictory results, and age seems to be an important factor. The present study investigated the effect of these two polymorphisms on the stability of infant temperament between 4 and 9 months of age. Furthermore, the effect of a recently discovered single nucleotide polymorphism which modulates the 5-HTTLPR (rs25531) was investigated in relation to infant temperament. The study sample consisted of 90 infants, who were assessed by parental report at the two ages under consideration using the Revised Infant Behavior Questionnaire. It was found that infants carrying the 7-repeat allele of the DRD4 VNTR had higher levels of Negative Affect. Furthermore, there was an interaction between DRD4 VNTR and 5-HTTLPR genotype such that infants with the DRD4 VNTR 7-repeat allele and the highest expressing 5-HTTLPR genotype (L(A) L(A) ) had the highest level of Negative Affect. These effects were largely driven by scores on the Falling Reactivity scale. Genetic effects were stable across age. The results emphasize the need for developmental studies of genetic effects on temperament.     

Factors affecting wounding aggression in a colony of captive chimpanzees (Pan troglodytes)

Previous research has suggested that chimpanzees (Pan troglodytes) display higher levels of aggression in captivity than in the wild. One of the challenges of captive management, therefore, is to balance the chimpanzees' need for social interaction with managements' desire to minimize wounding and aggression. Various captive studies have examined the effects of individual and social variables on the frequency of wounding aggression, but none have examined these variables simultaneously. We collected retrospective wounding data for severe wounds from 83 captive chimpanzees (36 males, 47 females) from January 1993 to December 2003. The context of the wounding event, including individual age and sex, group age and sex composition, group duration, and portion of the week (weekday vs. weekend) were collected. Logistic regression analysis was performed to determine which variables had a significant effect on the probability of a severe wounding event. The sex and age composition of the group, group duration, and portion of the week had a statistically significant association with wounding. All‐male groups (Odds Ratio (OR)=6.738) had the highest risk of wounding aggression, with uni‐male groups (OR=3.311) having the next largest. Compared to individuals in all sub‐adult groups, individuals in either all‐adult (OR=4.516) or mixed‐age (OR=3.587) groups had a higher risk of wounding. There was an inverse association between group duration and wounding (OR=0.821). Finally, there was an increased risk of wounding during the work week (OR=1.653). These results suggest that captive management should pay close attention to group composition, as well as levels of human activity, when devising strategies to reduce captive chimpanzee aggression. Zoo Biol 29:351–364, 2010. © 2009 Wiley‐Liss, Inc.     

Assessing chimpanzee personality and subjective well‐being in Japan

We tested whether the cultural background of raters influenced ratings of chimpanzee personality. Our study involved comparing personality and subjective well‐being ratings of 146 chimpanzees in Japan that were housed in zoos, research institutes, and a retirement sanctuary to ratings of chimpanzees in US and Australian zoos. Personality ratings were made on a translated and expanded version of a questionnaire used to rate chimpanzees in the US and Australia. Subjective well‐being ratings were made on a translated version of a questionnaire used to rate chimpanzees in the US and Australia. The mean interrater reliabilities of the 43 original adjectives did not markedly differ between the present sample and the original sample of 100 zoo chimpanzees in the US. Interrater reliabilities of these samples were highly correlated, suggesting that their rank order was preserved. Comparison of the factor structures for the Japanese sample and for the original sample of chimpanzees in US zoos indicated that the overall structure was replicated and that the Dominance, Extraversion, Conscientiousness, and Agreeableness domains clearly generalized. Consistent with earlier studies, older chimpanzees had higher Dominance and lower Extraversion and Openness scores. Correlations between the six domain scores and subjective well‐being were comparable to those for chimpanzees housed in the US and Australia. These findings suggest that chimpanzee personality ratings are not affected by the culture of the raters. Am. J. Primatol. 71:283–292, 2009. © 2009 Wiley‐Liss, Inc.     

Variables influencing the origins of diverse abnormal behaviors in a large sample of captive chimpanzees (Pan troglodytes)

The developmental origin of abnormal behaviors is generally associated with early rearing environments that lack sufficient physical and sensory stimulation. However, other factors should also be considered. A large sample of captive chimpanzees (128 males and 140 females) was surveyed for the presence or absence of 18 abnormal behaviors. Origin variables included the subject's source (zoo, pet, performer, or laboratory), rearing (mother‐ or hand‐reared), and sex. Animals were assessed while held at the Primate Foundation of Arizona, University of Texas M. D. Anderson Cancer Center, or White Sands Research Center. There was a confound among origin variables; more hand‐reared animals than expected were from laboratories. Logistic regression tested the relationship of rearing and source, with sex as a secondary predictor variable, to each of the abnormal behaviors. There was no clear association between any abnormal behavior and source. However, for coprophagy, relative to animals from the laboratory, zoo animals tended to show a higher prevalence, while performers tended to show a lower prevalence (when rearing and sex were controlled). Rocking and self‐sucking were significantly more likely in hand‐reared animals. Coprophagy and depilation of self were significantly more likely in mother‐reared animals. When rearing and source were statistically controlled, the only significant sex difference was a higher prevalence of coprophagy in females and a higher prevalence of rocking in males. In a second, smaller sample of 25 males and 33 females from Southwest Foundation for Biomedical Research, no significant sex association was found for coprophagy, urophagy, rocking, or self‐depilation. In this second sample, coprophagy was also significantly more likely in mother‐reared than hand‐reared subjects. The association of some abnormal behaviors with mother‐rearing suggests that some form of social learning may be involved in the origin of some of these behavior patterns. This indicates that some abnormal behaviors may not be always be indicative of reduced psychological well‐being in captive chimpanzees. Am. J. Primatol. 48:15–29, 1999. © 1999 Wiley‐Liss, Inc.     

Terrestrial predator alarm vocalizations are a valid monitor of stress in captive brown capuchins (Cebus apella)

The vocal behavior of captive animals is increasingly exploited as an index of well‐being. Here we show that the terrestrial predator alarm (TPA) vocalization, a robust and acoustically distinctive anti‐predation vocal response present in many mammal and bird species, offers useful information on the relative well‐being and stress levels of captive animals. In a 16‐week experiment evaluating the effects of varying levels of physical environmental enrichment (control < toys < foraging box < foraging box and toys) in the cages of eight singly housed adult male brown capuchins, we quantified the 1) emission rate of TPAs, 2) proportions of normal and abnormal behavior sample intervals, and 3) fecal and plasma cortisol levels. Variation in TPA emission across the experimental conditions was significant. We found significant reductions in the mean TPA production rate by the group in the enriched (toys, foraging box, and foraging box and toys) compared to the control condition; pre‐ and post‐experimental conditions, however, did not differ from the control condition. Mean TPA production by the group was also significantly positively correlated to mean group levels of fecal cortisol and proportion of abnormal behavior sample intervals, and significantly negatively correlated to the average proportion of normal behavior sample intervals in the group. Based on group means, plasma cortisol levels were positively, but not significantly, related to increasing TPA rate. At the level of the responses of an individual subject, however, the covariation between the vocal and non‐vocal behavioral measures and the cortisol assays seldom attained significance. Nevertheless, the direction of the relationships among these parameters within individual subjects typically mirrored those correlations based on group means. At both the group mean and individual levels, our results are consistent with the interpretation that in conditions of low environmental enrichment the study subjects were more stressed, and therefore more reactive to the presence of a threatening terrestrial stimulus (human observer), than when in more enriched conditions. We suggest that protocols to evaluate the effectiveness of enrichment for captive species other than brown capuchins could also profitably exploit TPAs as a first‐line monitor or as corroboratory evidence of current well‐being. Zoo Biol 18:295–312, 1999. © 1999 Wiley‐Liss, Inc.     

Assessing the effectiveness of environmental enrichment in bottlenose dolphins (Tursiops truncatus)

Environmental enrichment is often used to improve well-being and reduce stereotyped behaviors in animals under human care. However, the use of objects to enrich animal environments should not be considered to be effective until its success has been scientifically demonstrated. This study was conducted at Asterix Park in France in April 2009. The study investigated the use of 21 familiar objects with a group of six bottlenose dolphins (Tursiops truncatus). The dolphin trainers introduced four different objects into the dolphin pool every day on a rotating basis. Using a focal-object sampling method, we collected and analyzed data from twenty-one 15 min sessions. The results revealed a positive correlation between interest behaviors and interactive behaviors. Some dolphins had "favorite toys". However, only 50% of objects elicited manipulative behaviors. These findings demonstrate that dolphins do not treat all objects provided to them as "toys". Behavioral changes in the animals subsequent to the introduction of objects do not necessarily indicate an enrichment effect of the objects; rather, the motivation for the dolphins' behaviors toward the objects must be investigated. The animals' behavior must be considered in light of the social context and of the animals' individual behavioral profiles. The relevance of a constructivist approach to evaluating the effectiveness of enrichment programs is discussed.     

Consistent inter‐individual differences in common marmosets (Callithrix jacchus) in Boldness‐Shyness,Stress‐Activity,and Exploration‐Avoidance

The study of animal personality, defined as consistent inter‐individual differences in correlated behavioral traits stable throughout time and/or contexts, has recently become one of the fastest growing areas in animal biology, with study species ranging from insects to non‐human primates. The latter have, however, only occasionally been tested with standardized experiments. Instead their personality has usually been assessed using questionnaires. Therefore, this study aimed to test 21 common marmosets (Callithrix jacchus) living in three family groups, in five different experiments, and their corresponding controls. We found that behavioral differences between our animals were not only consistent over time, but also across different contexts. Moreover, the consistent behaviors formed a construct of four major non‐social personality components: Boldness‐Shyness in Foraging, Boldness‐Shyness in Predation, Stress‐Activity, and Exploration‐Avoidance. We found no sex or age differences in these components, but our results did reveal differences in Exploration‐Avoidance between the three family groups. As social environment can have a large influence on behavior of individuals, our results may suggest group‐level similarity in personality (i.e., “group personality”) in common marmosets, a species living in highly cohesive social groups. Am. J. Primatol. 78:961–973, 2016. © 2016 The Authors. American Journal of Primatology published by Wiley Periodicals, Inc.     

Postdispersal nepotism in male long‐tailed macaques (Macaca fascicularis)

Cooperative behaviors are promoted by kin selection if the costs to the actor are smaller than the fitness benefits to the recipient, weighted by the coefficient of relatedness. In primates, cooperation occurs primarily among female dyads. Due to male dispersal before sexual maturity in many primate species, however, it is unknown whether there are sufficient opportunities for selective tolerance and occasional coalitionary support for kin selection to favor male nepotistic support. We studied the effect of the presence of male kin on correlates of male reproductive success (residence time, duration of high dominance rank) in non‐natal male long‐tailed macaques (Macaca fascicularis). We found that “related” (i.e., related at the half‐sibling level or higher) males in a group have a significantly higher probability to remain in the non‐natal group compared to males without relatives. Moreover, males stayed longer in a group when a relative was present at group entry or joined the same group within 3 months upon arrival. Males with co‐residing relatives also maintained a high rank for longer than those without. To our knowledge, this is the first demonstration of a potential nepotistic effect on residence and rank maintenance among non‐natal males in a social system without long‐term alliances.