Animal social structure is influenced by multiple socioecological factors. Of these, the links between changes to group demography through the arrival of new individuals and residents’ social structure remain unclear. Across seven groups of captive rhesus macaques (Macaca mulatta), we examine how male introductions may be influenced by, and in-turn influence, aspects of female social structure. GLMMs revealed that males integrated more successfully into groups in which females showed more ‘despotic’ social structures, i.e., higher aggression rates, steeper dominance hierarchies, and greater rank-skew in allogrooming network connectedness. Yet during periods that followed males’ social integration, females increased their social tolerance (decreased aggression and shallower hierarchies) and group cohesivity (less clustered allogrooming networks), but retained their tendencies to groom dominants. Our findings, independent of group size and matrilineal relatedness, help better understand how dispersal/immigration may influence social structure, and how assessing changes to social structure may inform macaque welfare and management.
Functional analysis (FA) is a method developed and used by behavior analysts in human clinical settings to identify possible environmental variables that reinforce undesired behavior. FA is increasingly being applied to better understand the behavior of nonhuman animals. When training monkeys in a room with others, disruptive behavior displayed by neighboring monkeys can impede training progress. In the present study, a FA identified possible reinforcers of disruptive behavior (loud shaking of a toy) exhibited frequently (24% duration pre-treatment) by a rhesus macaque (Macaca mulatta) during in-room training sessions. The functional analysis identified that contingent delivery of foods was maintaining the disruptive behavior, with a mean percent duration of 57% in this condition. The implementation of a function-based treatment consisting of continuous access to a preferred food during in-room training sessions successfully decreased disruptive behavior by over 90% as measured during 15 subsequent sessions. This study advances the current literature applying functional analysis to nonhuman primates as a means of determining the reinforcers maintaining aberrant or undesirable behavior and applying effective treatments based on understanding this function.
Migration patterns of wild rhesus macaque males are often mimicked in captivity by introducing unfamiliar males to female groups every few years. This strategy prevents inbreeding and has been shown to encourage group stability once males are fully integrated. The current study focused on female coalitionary aggressive behavior directed toward males during introductions to describe factors that predict its frequency and any relationship with introduction success. Observational data (755 h) were collected during eight introductions of male cohorts (3–7 individuals) to established female groups (14–39 breeding-age females). Female coalitionary aggression (FCA), defined as four or more females simultaneously attacking an individual male, was recorded 114 times and occurred during all introductions. Data showed that male groups with alpha males who aggressed females during the coalitionary events were more likely to be successfully integrated than those with alpha males who did not retaliate against females. Stepwise multiple regression analyses of individual females (N = 183) revealed that females from larger groups and older females were more likely to be involved in coalitionary aggression, while rank, family size and number of matrilines in the group did not play a role. A rating system of the severity of FCA events revealed male groups receiving more severe FCA were less likely to be successfully introduced, and larger male groups received more severe FCA than did smaller groups of males. Based on these data, it is recommended that colony managers expect FCA to occur during introductions, especially with older females and larger groups. Colony managers should monitor the alpha male's response to FCA, as well as the severity of the FCA since those factors may predict introduction success.
In captive populations of rhesus macaques, novel adult males are commonly introduced to female groups every few years to prevent inbreeding, which mimics male dispersal in wild macaque populations. However, introducing adult males is challenging because macaques are aggressive to newcomers, which can result in serious injuries. Efforts to reduce trauma risk during the introduction process and increase the probability of success are needed. Here we investigate the impact of multiple factors, including male attributes (e.g., age, weight, rank, and experience), introduction method (punctuated vs. continual exposure to females), and female behavior, on males' trauma risk and integration success. We studied eight introductions of multimale cohorts (3–7 males each; N = 36 total) into existing female groups of rhesus macaques at the Yerkes National Primate Research Center. Four cohorts were introduced using the punctuated exposure method where adult males were moved each morning from run housing to the females' indoor enclosure and returned to run housing in the afternoon, and four cohorts were introduced using the continual exposure method where adult males were moved to an introduction enclosure attached to the females' outdoor compound, allowing males to live in protected contact next to the female group continuously. Generalized linear mixed models fitted to trauma risk (e.g., latency to first trauma; total trauma count) and success or failure to integrate (i.e., continual residence within the female group for greater than 53% of days within a 28-day window after first overnight stay) showed that continual exposure to females in the introduction enclosure reduced male trauma risk and increased the likelihood of successful integration compared to punctuated exposure. Males received less trauma when they received a higher rate of grooming from females. Male attributes had no effect. These findings highlight the importance of introduction technique and female behavior in the process of males' social integration into female groups.
Introduction:
Although medroxyprogesterone acetate (MPA) is used commonly as a contraceptive in women and female nonhuman primates, its effects on social behavior remain unclear. This study examined whether MPA treatment and introduction of new adult males during the breeding season influence the social behaviors of group-housed adult female rhesus macaques.
Methods:
Subjects were 12 MPA-treated and 12 matched-case control females. Aggressive, affiliative and sexual behaviors were measured.
Results:
MPA-treated females showed less affiliative and sexual behavior compared to matched controls during the breeding season. MPA treatment was associated with decreased aggression emitted towards and received from females during the breeding season.
Conclusion:
MPA treatment is associated with differences in social behavior of female rhesus macaques during the breeding season, when normal hormonal cycles are attenuated by the treatment, but there is no indication that MPA-treated females bring an additional risk for more aggression during the male introduction and breeding season.
The pole-and-collar method is one of several techniques that enable the safe transfer of a nonhuman primate from its home environment into a restraint chair without the need for sedation. It has been used within the scientific community for decades. Traditional methods to train animals for pole-and-collar use rely primarily on aspects of negative reinforcement, with very little incorporation of positive-reinforcement techniques. With increasing emphasis on animal training and welfare, research facilities are incorporating positive-reinforcement training into husbandry and experimental procedures. Here we demonstrate the feasibility of training rhesus macaques (Macaca mulatta; n = 8) to cooperate for pole-and-collar transfer to a primate restraint chair. By using predominantly positive-reinforcement techniques, with supplemental elements of negative reinforcement, macaques were trained in a mean of 85 training sessions (a mean of 1085 min of training time). We also provide tools for investigators using the pole-and-collar method to help them successfully incorporate positive-reinforcement training into their procedures. This refinement has the potential to improve animal welfare and enhance the value of nonhuman primate models in research.
The separate influences of spatial density and housing quality on the behavior of captive animals are difficult to measure because the two factors are often intrinsically linked. Here, we recorded affiliative and agonistic behavior in adult sooty mangabeys in various housing situations, testing spatial density and housing quality changes separately (N=26 experienced spatial density changes; N=12 experienced housing quality changes). We varied spatial density by 50% while holding housing quality constant and we varied housing quality while holding spatial density constant (achieved by comparing two types of run-housing that varied in the amount of visual privacy and outdoor access). Each housing condition was one month in duration. Prior to collecting data in each housing condition, we evaluated the subjects’ initial responses to the change in housing environment during two-week novelty periods. Affiliative behavior did not change during the novelty periods. Agonistic behavior initially increased slightly when spatial density increased and it decreased significantly when spatial density decreased; it also decreased when subjects moved to housing that offered more visual privacy and outdoor space, indicating that the mangabeys were sensitive to these housing changes. After the novelty periods, affiliative behavior increased under higher spatial density, but remained unchanged across housing quality conditions; agonistic behavior remained unchanged across all conditions. Results suggest that a prolonged increase in spatial density led the mangabeys to adopt a tension-reduction coping strategy, in which the increase in affiliative behavior alleviates a presumed increase in social tension. Reducing visual privacy and choice did not affect the mangabeys’ behavior, post-novelty period. Thus, like many other primates, the mangabeys managed tension by flexibly adapting to changes in their housing environment in ways that reduce the risk of severe aggression. This study highlights the importance of controlled behavioral studies in facilitating data-driven management decisions that promote animal welfare.
The use of systematic preference assessments can enhance positive reinforcement training with captive animals. We found that the multiple stimulus without replacement (MSWO) technique identified food preferences in laboratory housed rhesus macaques, with raisins and grapes being ranked higher on average than dried apricot, pasta, and green beans (Friedman Test, χ2 (4) = 35.52, p < .001). Agreement between individuals (N = 21) was moderate (Kendall’s W = .42), and consistency across time varied among individuals (W = .03 to .90). Highly preferred items identified by the MSWO assessment were subsequently found to increase subjects’ engagement in a husbandry task on which they were being trained (Mann-Whitney U = 6.00, p = .002) and to improve performance on a progressive ratio schedule (Wilcoxon signed-rank test, Z = −2.17, p = .03) when compared with low preference items. The progressive ratio technique supplements other preference assessment techniques by measuring the amount of work a subject will do to gain access to an item. The use of more effective reinforcers identified through systematic assessment has the potential to increase animal performance on husbandry and research tasks and to improve animal welfare in the laboratory setting.
Pair housing of macaques has become a widely implemented compromise between meeting the social needs of the monkeys and allowing for their use in biomedical research. While beneficial to the animals, pair housing can provide challenges for those caring for them. Drawing from both scientific literature and direct experience, this paper provides a review of practical aspects of pair housing including partner selection, pairing methodologies, staff education, and equipment considerations. Recommendations include selecting a pairing method appropriate to the facility and the individual animals being paired, educating staff on social behavior, and establishing a pair monitoring program to facilitate long-term pair maintenance. Assessment of behavior is essential in determining the compatibility of new pairs and in identifying established pairs that may need interventions to enhance their long-term compatibility. The pair housing program at the Yerkes National Primate Research Center is described as one model of a successful program.
For decades, animal welfare standards and practices have been advanced by evidence from research conducted in agricultural, biomedical, and zoological settings (Broom, 1988; Broom, 2011). These standards and practices are generally aimed at defining minimum rather than optimal criteria for welfare. One outcome of this is that regulated animals whose care and housing meets the minimum standards may be able to cope but may not thrive. The welfare continuum of suffering, to coping, to thriving has been proposed as a useful lens through which to view animal welfare, and is based on the study of human well-being (Maple and Bocian, 2013). Indeed, coping has been characterized by some investigators as an indicator of animal welfare. The American Veterinary Medical Association (AVMA) website, for example, defines animal welfare as “how an animal is coping with conditions in which it lives.” If an animal is judged to be “healthy, comfortable, well nourished, safe, able to express innate behavior, and it if is not suffering from unpleasant states such as pain, fear, and distress” it is said to be living in a “good” state of animal welfare (AVMA). Animal welfare science developed out of concern for animal suffering in captive settings. Suffering has been dramatically reduced due to improvements in physical and social environments (Maple, 2016), but thriving is still a distant goal. Elsewhere, we have argued that we are aiming too low if we accept coping as a good outcome (Maple and Perdue, 2013). In fact, all of the welfare attributes advocated by AVMA and other organizations are characteristics of animals that thrive. Thriving goes beyond what most minimal regulatory standards require. It is the difference between good and optimal welfare.