Carolyn M. Crockett

Conservation Biology of the Genus Alouatta

As assessed by the IUCN Mace–Lande system, seven (35%) of the 20 Alouatta species and subspecies with adequate data are classified as “threatened,” i.e., critically endangered, endangered, or vulnerable (Rylands et al., 1995). This percentage is much lower than the 75 to 100% threatened taxa for the other large-bodied genera: Ateles, Lagothrix, and Brachyteles. Only 5 of the 16 Neotropical genera have lower percentages of threatened taxa than that of Alouatta: Cebuella, Pithecia, Saguinus, Saimiri, and Cebus. The threatened howler taxa occupy small distributions in areas of forest fragmentation. In general, populations are most affected by major habitat disturbance, such as total deforestation and flooding from dam construction, and by human hunters. Facilitated by their ability to exploit folivorous diets in small home ranges, howlers can tolerate considerable habitat fragmentation but not the increased exposure to hunting that may accompany it. Howlers seem particularly vulnerable to yellow fever and bot fly parasitism. Although the former threat may decrease by increasing fragmentation of the habitat, other sorts of parasitism may increase in disturbed habitats. The low genetic variability of the Central American howlers suggests a resistance to inbreeding depression potentially experienced during population bottlenecks. Greater between-population variability may still exist. Although howlers are not readily bred in captivity, they respond well to translocation. Translocation has been successfully achieved for ≥4 howler species and is a viable option for introducing new genetic variability into population fragments and repopulating areas from which howlers are extinct. Their pattern of bisexual dispersal facilitates colonization of regenerating habitats, and in suitable, protected habitats they have shown the capacity for strong population recovery.

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. Am. J. Primatol. 52:63–80, 2000.

The Relation between Red Howler Monkey (Alouatta seniculus) Troop Size and Population Growth in Two Habitats

No consensus yet exists to explain the diversity of primate social organization. Although ecological and social factors are both involved in the evolution and expression of social organization, they do not necessarily act together and may differ for the two sexes (Wrangham, 1987). Differing social factors usually are rooted in a species mating system— the degree of monopolization of mates by each sex—resulting from the effects of local ecology on the dispersion of the sex investing more in the production of offspring (Emlen and Oring, 1977; Vehrencamp and Bradbury, 1984). However, some features of primate social organization are phylogenetically conservative and resist change in response to varying ecological situations (Di Fiore and Rendall, 1994). At any given point in time, the particular social organization exhibited by a population also reflects recent demographic events (Altmann and Altmann, 1979; Dunbar, 1979). Among these life history variables are birth rates, which may vary directly in response to environmental variation, and sex ratios, which may vary randomly at birth but are affected thereafter by differential mortality (Dunbar, 1987). Social organization, then, is the result of a complex interplay of behavioral responses to ecological conditions, tempered by recent demographic events and constrained by phylogeny (Strier, 1994).

Differences in stress reactivity of laboratory macaques measured by heart period and respiratory sinus arrhythmia.

Some laboratory primates are more likely than others to react to anxiety‐provoking stressors. Individuals that overreact to stressors may experience diminished psychological well‐being and would be inappropriate for some experiments. The differences between reactive and nonreactive individuals may be reflected in heart period and respiratory sinus arrhythmia (RSA). Using surface electrodes and radio telemetry, we measured these two cardiac variables in seven male and ten female singly caged longtailed macaques (Macaca fascicularis) when they were exposed to two stressors, a sudden noise (whistle test) and an unfamiliar technician wearing capture gloves (glove test). Behavior was videotaped during both tests. For the whistle test, cardiac data were recorded before, during, and after two 1 min whistle blasts separated by 90 min. For the glove test, data were recorded in 1 min blocks every 8 min over 96 min before, during, and after 1 min exposure to the gloved technician. Heart period was decreased and RSA was suppressed during both the whistle and glove exposures. After the whistle test, the cardiac activity of most subjects returned to baseline levels within 10 min. The glove test produced more extended suppression, with greater individual differences, than the whistle test. There were greater individual differences in RSA than in heart period. These enhanced individual differences were used to define stress reactors that differed from nonreactors in their cardiac data profiles. Of 16 subjects that completed the glove test, five were identified as reactors. Am. J. Primatol. 45:245–261, 1998.

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.

Behavioral Management, Enrichment, and Psychological Well-being of Laboratory Nonhuman Primates

Animal care in biomedical facilities housing nonhuman primates has undergone a dramatic transformation in the past two decades, with increasing emphasis on behavioral management, psychological well-being, and animal welfare. Today, providing for the psychological well-being of nonhuman primates is an integral part of animal care. Behavioral management is a comprehensive management strategy that includes enrichment, positive reinforcement training, facilities and enclosure design, positive staff–animal interactions, and behavioral monitoring in an effort to promote psychological well-being and animal welfare. Successful behavioral management strategies are tailored to the natural behavior of the species and include both social and nonsocial forms of enrichment. An increasing number of behavioral management programs include positive reinforcement training, a significant refinement to animal care practices. Appropriate behavioral management strategies can help reduce stress for nonhuman primates and prevent behavioral problems from occurring, which ultimately enhances the utility of the primate model in biomedical research. This chapter briefly summarizes several concepts that are integral to the appropriate behavioral management of laboratory primates and to the promotion of their psychological well-being and welfare.

Tenure in current captive setting and age predict personality changes in adult pigtailed macaques

Personality change in nonhuman primates is a topic that warrants more research attention. Many studies focus on intraindividual repeatability, but few note population-wide trends in personality change. In part, this results from the large sample size that is required to detect such trends. In the present study, we measured personality in a large sample (N = 293) of adult, mother-reared pigtailed macaques, Macaca nemestrinam, over a period of 3 years. We looked at four personality components (sociability towards humans, cautiousness, aggressiveness and fearfulness) derived from behavioural observations at two to four time points per subject. We found these components to have repeatabilities similar to those reported elsewhere in the literature. We then analysed population-wide changes in personality components over time using a linear mixed effects model with three predictors: entry age at the current primate facility, tenure at the primate facility at the time of the first personality test and time elapsed since the first personality test. We found that adult personality changed with life experiences (here, tenure at the facility where tested) and age. Throughout adulthood, pigtailed macaques became less cautious and more aggressive. At the same time, subjects became less cautious and more sociable with increasing time in individual caging at the current primate research facility. We also found that individuals differed significantly in their personality consistency. Other researchers may benefit by applying similar methodology to that described here as they extrapolate about personality measures over time.

Modeling Managed Monkey Populations: Sustainable Harvest of Longtailed Macaques on a Natural Habitat Island

Computer simulation of population dynamics can be useful in managing harvested populations of monkeys on islands. Between 1988 and 1991, 420 adult female and 58 adult male simian retrovirus‐free Macaca fascicularis were released onto Tinjil Island, Indonesia, to provide the nucleus for a free‐ranging breeding colony. Natural habitat breeding facilities are excellent alternatives to wild trapping and compound breeding, maximizing the health and well‐being of animals destined for essential biomedical research. To avoid a population crash, the number of offspring that can be harvested annually must be based on life table characteristics such as age‐specific natality and mortality. We used a modified Leslie matrix to model changes in female population size over 26 years. First, we assumed that all 420 females were released simultaneously and varied the annual birth rate (50%, 60%, 70%), survival rate, and number of offspring harvested per year. Assuming high survival and birth rates vs. low rates, about four times as many female offspring could be harvested annually from a stable population (87 vs. 20 offspring). Terminal population size after 26 years did not differ much across rates modeled (568–696 females). Second, we modeled the number of females actually released (including the recent addition of 42 new female breeders) and harvested (averaging 49 annually 1991–1994), and projected the population through 2014. This indicated that threshold harvest rates and terminal population sizes increased considerably over the first model, assuming intermediate (78 harvested, 952 females) and high (152 harvested, 1,331 females) rates of survivorship and natality, but were unchanged assuming low rates (20 harvested, 559 females). A review of the literature and field observations on Tinjil suggest that actual birth and survival rates resemble the intermediate values modeled. If so, the present density on the island, projected to be ∼215 males and females per square kilometer, is approaching carrying capacity. The high values are realistic upper limits. If actual survivorship and birth rates are at the high end of those modeled, the islands population may be on the verge of rapid expansion, requiring increased harvest and provisioning.

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.

Floating limb behaviors and self-biting are associated in laboratory monkeys.

Early descriptions of floating limb behaviors in monkeys were associated with isolation rearing, a practice that ended more than two decades ago. The present authors named various forms of behaviors in which a leg is elevated for no apparent reason: “Floating Limb Suite” (FLS). Floating limb behaviors, identified in laboratory monkeys at the Washington National Primate Research Center (WaNPRC), consist of two subcategories distinguished by whether monkeys seem to react to the elevated leg or ignore it. Given the past association of isolation rearing with both self‐biting (SB) and floating limb, the investigators predicted that SB and FLS would be associated in monkeys not reared in isolation. The investigators tracked, over a period of 3 years, the presence of FLS and SB in macaques (Macaca nemestrina, M. fascicularis, M. mulatta) and Papio cynocephalus at WaNPRC. SB and both subcategories of FLS occurred in mother‐reared and surrogate‐peer‐nursery‐reared monkeys. We analyzed presence of FLS, the two subcategories of FLS, and SB in 1,117 macaques monitored for up to 3 years, and 781 macaques observed for 8 min of structured data collection. The Papio sample size was insufficient for statistical analysis. Both sampling methodologies found FLS and FLS subcategories to be associated with SB. Nearly half the monkeys only engaging in seemingly harmless nonreactive forms of FLS also performed the potentially injurious behavior of self‐biting. The positive association between FLS and SB suggests that monkeys exhibiting one of these behaviors are at a heightened risk for developing the other. One impediment to studying floating limb behaviors is lack of consensus on definitions. This study defined seven forms of apparently functionless elevated limb behaviors. Continued research on factors associated with floating limb behaviors across demographic groups and settings may provide insights into the etiology and treatment of self‐biting. Am. J. Primatol. 72:725–733, 2010.