Enhancing nonhuman primate care and welfare through the use of positive reinforcement training

Nonhuman primates are excellent subjects for the enhancement of care and welfare through training. The broad range of species offers tremendous behavioral diversity, and individual primates show varying abilities to cope with the stressors of captivity, which differ depending on the venue. Biomedical facilities include small single cages, pair housing, and breeding corrals with large social groups. Zoos have social groupings of differing sizes, emphasizing public display and breeding. Sanctuaries have nonbreeding groups of varying sizes and often of mixed species. In every venue, the primary objective is to provide good quality care, with minimal stress. Positive reinforcement training improves care and reduces stress by enlisting a primate's voluntary cooperation with targeted activities, including both husbandry and medical procedures. It can also improve socialization, reduce abnormal behaviors, and increase species-typical behaviors. This article reviews the results already achieved with positive reinforcement training and suggests further possibilities for enhancing primate care and welfare.     

The development of an operant conditioning training program for new world primates at the Bronx Zoo

This article describes the development of an operant conditioning training program for 17 species of New World primates at the Bronx Zoo. To apply less invasive techniques to husbandry protocols, the study introduced behaviors-hand feeding, syringe feeding, targeting, scale and crate training, and transponder reading-for formal training to 86 callitrichids and small-bodied cebids housed in 26 social groups. Individual responses to training varied greatly, but general patterns were noted among species. With the exception of lion tamarins, tamarins responded more rapidly than marmosets, Bolivian gray titi monkeys, and pale-headed saki monkeys in approaching trainers and learning behaviors. Marmosets, in comparison to most tamarins, had longer attention spans. This meant that fewer, lengthier sessions were productive whereas shorter, more frequent sessions were most successful for tamarins. Among the cebids, pale-headed saki monkeys needed relatively few sessions to perform basic and advanced behaviors whereas Bolivian gray titi monkeys were less responsive and progressed at a deliberate pace. Marked changes in the animals' behavior during daily husbandry procedures, their voluntary participation in training activities, and the disappearance of aggressive threats toward care staff indicated that training reduced stress and improved the welfare of the animals. During daily training displays, zoo visitors experienced interactive animals while learning the importance of low-stress animal husbandry.     

Life-Long Well Being: Applying Animal Welfare Science to Nonhuman Primates in Sanctuaries

Nonhuman primates have become common in sanctuaries, and a few such facilities even specialize in their care. Sanctuaries can improve the well being of many unwanted primates, especially in terms of housing and socialization. However, diverse facilities call themselves sanctuaries, and they have varying conditions, care programs, and restrictions. In addition, a general lack of regulation of sanctuaries for nonhuman animals creates problems in enforcing even minimal standards. The application of animal welfare science in the sanctuary setting can help foster high standards and empirically based decision making. Sanctuaries offer excellent environments for studying primates without the limitations inherent in breeding, exhibition, and medical research facilities. However, some sanctuaries avoid scientific study. Many sanctuaries have little opportunity to study animal welfare in a systematic manner due to financial considerations or a lack of specific expertise among staff and volunteers. Most published sanctuary research involves reintroduction procedures at sanctuaries in source countries. Nevertheless, one chimpanzee sanctuary's successes in performing long-term studies and using simple evaluation methods, such as check sheets, have demonstrated the benefits of applying animal welfare science to sanctuary-housed nonhuman primates.     

Life-long well being: applying animal welfare science to nonhuman primates in sanctuaries

Nonhuman primates have become common in sanctuaries, and a few such facilities even specialize in their care. Sanctuaries can improve the well being of many unwanted primates, especially in terms of housing and socialization. However, diverse facilities call themselves sanctuaries, and they have varying conditions, care programs, and restrictions. In addition, a general lack of regulation of sanctuaries for nonhuman animals creates problems in enforcing even minimal standards. The application of animal welfare science in the sanctuary setting can help foster high standards and empirically based decision making. Sanctuaries offer excellent environments for studying primates without the limitations inherent in breeding, exhibition, and medical research facilities. However, some sanctuaries avoid scientific study. Many sanctuaries have little opportunity to study animal welfare in a systematic manner due to financial considerations or a lack of specific expertise among staff and volunteers. Most published sanctuary research involves reintroduction procedures at sanctuaries in source countries. Nevertheless, one chimpanzee sanctuary's successes in performing long-term studies and using simple evaluation methods, such as check sheets, have demonstrated the benefits of applying animal welfare science to sanctuary-housed nonhuman primates.     

Complexities of Using Wild versus Captive Activity Budget Comparisons for Assessing Captive Primate Welfare

Activity budget comparisons between groups or individuals in the wild and those in captivity are commonly used to determine the range of wild-type behaviors that nonhuman animals in captivity perform. These comparisons are conducted with the view that individuals displaying a greater range of wild-type behaviors have enhanced welfare. Such comparisons have a greater appeal when it comes to primates because increased levels of anthropomorphism toward primates lead to welfare concerns. However, the validity of such comparisons has not been assessed. From the reviewed literature, some of the main complexities identified when defining “good welfare” using activity budgets were the ideas of behavioral motivation and adaptation, obstacles when using the wild as a benchmark for good welfare, study methods causing possible variances in behavior, and social and environmental factors. It is proposed that such influencing factors would be controlled for adequately in future studies with the use of multiple indices to measure welfare and methods that infer positive emotional states. It is hoped we can then build evidence of an animal’s emotional state and allow welfare to be inferred to a higher degree.     

Convergent evolution in social swallows (Aves: Hirundinidae)

Behavioral shifts can initiate morphological evolution by pushing lineages into new adaptive zones. This has primarily been examined in ecological behaviors, such as foraging, but social behaviors may also alter morphology. Swallows and martins (Hirundinidae) are aerial insectivores that exhibit a range of social behaviors, from solitary to colonial breeding and foraging. Using a well‐resolved phylogenetic tree, a database of social behaviors, and morphological measurements, we ask how shifts from solitary to social breeding and foraging have affected morphological evolution in the Hirundinidae. Using a threshold model of discrete state evolution, we find that shifts in both breeding and foraging social behavior are common across the phylogeny of swallows. Solitary swallows have highly variable morphology, while social swallows show much less absolute variance in all morphological traits. Metrics of convergence based on both the trajectory of social lineages through morphospace and the overall morphological distance between social species scaled by their phylogenetic distance indicate strong convergence in social swallows, especially socially foraging swallows. Smaller physical traits generally observed in social species suggest that social species benefit from a distinctive flight style, likely increasing maneuverability and foraging success and reducing in‐flight collisions within large flocks. These results highlight the importance of sociality in species evolution, a link that had previously been examined only in eusocial insects and primates.     

Social organization, reproduction and rearing strategies of Callimico goeldii: new clues from the wild

The callitrichines are a specialized radiation of primates that are characterized in part by variable social systems and cooperative infant care. Callimico goeldii, unlike the other callitrichines, have single rather than twin offspring, reducing the need for allocare and permitting synchronous breeding within groups. Low mortality rates among offspring and unstable social groups are suggested to be possible factors that have led to single births among C. goeldii. Single offspring may benefit from greater maternal investment and more frequent food sharing than twin offspring, factors that may help to explain why C. goeldii reaches sexual maturity more rapidly than other callitrichines. In addition, increased breeding opportunities for young C. goeldii females may have selected for rapid maturation rates among this species. Postpartum ovulation and aseasonal resource availability appear to permit females to have biannual birth seasons, further increasing the potential reproductive output.     

Use of positive reinforcement training in the management of species for reproduction

Positive reinforcement training holds great potential for enhancing the management of species for reproduction. This paper reviews a wide range of animal training activities and resultant benefits which could have application to captive reproduction programs. Recognized benefits fall into several categories. Basic animal care can be improved through voluntary cooperation by the animals with veterinary procedures and routine husbandry activities. The quality and quantity of physiological data collected for research can be improved through voluntary cooperation by the animal subjects with sample collection. Positive social interaction and reproductive behavior can be increased and aggressive behavior reduced through employment of a specialized training regime called cooperative feeding. Good success has been reported with special training programs to facilitate introduction of new members into primate social groups, while mixed results have been obtained in efforts to use training to enhance maternal skills. Finally, a discussion of both direct and indirect enhancement of psychological well-being through the use of positive reinforcement training is presented. While positive reinforcement training techniques will not be useful in every situation, information developed to date strongly suggests that these techniques should be given serious consideration when developing comprehensive programs for the management of species for reproduction. © 1994 Wiley-Liss, Inc.     

Care for kin: within-group relatedness and allomaternal care are positively correlated and conserved throughout the mammalian phylogeny

With an increasing amount of data becoming available, comparative analyses have called attention to the associations between cooperative breeding, monogamy and relatedness. We focus here upon the association between allomaternal care and relatedness among females within a social unit. Previous studies found a positive association, but such results date back to before molecular tools were in common use, they considered only a few mammalian orders, neglected phylogenetic clustering and/or did not correct for group sizes. Here, we use molecular data on relatedness from 44 species of mammals to investigate the phylogenetic clustering of, and the association between, allomaternal care and relatedness among females within a social unit. We find (i) a strong phylogenetic signal for allomaternal care and a moderate one for relatedness and group size, and (ii) a positive association between relatedness and allomaternal care, even when correcting for the smaller than average group sizes in species with allomaternal care. We also find that, in species without allomaternal care, adult females often live with unrelated females even when groups are small. We discuss these results in the light of recent evidence for the role of kin selection and the monogamy hypothesis in cooperative breeding.     

Impact of female contraception for population management on behavior and social interactions in a captive troop of Guinea baboons (Papio papio)

As part of a population management strategy for a troop of Guinea baboons (Papio papio) at Yorkshire Wildlife Park, adult females were given a Suprelorin contraceptive implant. There was no information on the effect of contraception on behavior in this species, so behavioral data were collected before and after implant placement to determine any impact on the troops’ welfare. Social interactions, affiliative, agonistic, and self-directed displacement behaviors (SDBs) in all adults were monitored via focal sampling. Preimplant data were collected in August/September 2019 before Suprelorin placement on November 2019, and postimplant data were collected in August/September 2020, allowing for comparison while controlling for seasonal differences in behavior. We found a significant reduction of SDBs after intervention, suggesting that contraception has a positive impact on group welfare, as SDBs are key behavioral indicators of stress and anxiety in nonhuman primates. Additionally, the rate of substate change per hour (i.e., the number of times the baboon changed their behavior), duration of sentry behavior, and the frequency of agonistic bouts were significantly lower postimplant, further suggesting improvements in welfare. There were also no significant decreases in the duration of positive social interactions, such as allogrooming and play. The results show that Suprelorin did not have a detrimental impact on the behavior of adults in the troop and may have even improved welfare. The use of Suprelorin in females could be considered as an effective population management strategy for primates existing in similar social systems.     

Friends with benefits: Social support and its relevance for farm animal welfare

Despite growing interest in promoting positive welfare, rather than just alleviating poor welfare, potential measures of good welfare, and means to provide it, have remained elusive. In humans social support improves stress-coping abilities, health, and promotes positive psychological welfare. Therefore, social support may be a key approach to promote positive physical and psychological welfare in farm animals. However, the roles of positive social behaviors and social support have been overlooked in comparison to negative social behaviors such as agonistic interactions. The benefits of social partners on an animal's stress coping abilities and welfare are yet poorly understood.The purpose of this paper is to review the protective or buffering effects of social support against stressful challenges and its potential implications for farm animal welfare. The biology of social support is first presented with its behavior, endocrine, autonomic and immune components. The major factors modulating the social support process are then synthesized. Research and implications for animal welfare in different farm species are discussed. Lastly, this review identifies research areas that especially deserve further attention in our effort to understand and implement social support in farm animal welfare.Social support could constitute one of the foundations for welfare researchers to leap from the absence of negative welfare to the provision of positive welfare and emotional experiences.     

Habituation and desensitization as methods for reducing fearful behavior in singly housed rhesus macaques

Operant conditioning using positive reinforcement techniques has been used extensively in the management of nonhuman primates in both zoological and laboratory settings. This research project was intended to test the usefulness of counter-conditioning techniques in reducing the fear-responses of singly housed male rhesus macaques living in the laboratory environment. A total of 18 male rhesus macaques (Macaca mulatta) were selected for this project and randomly assigned to one of three groups: a desensitization training group, a husbandry training group, or a control group. Behavioral data were collected before and after a 6 weeks training and/or habituation period during which the first two groups received a total of 125 min of positive reinforcement training (and also were assumed to undergo habituation to the environment) and the control group experienced only simple habituation to the environment. Based on a Wilcoxon Matched-Pairs Sign Test, we found that a significant proportion of animals exposed to desensitization training showed a reduction in the rate at which they engaged in cringing toward humans (exact significance=0.016, one-tailed, N-ties=6), cringing in general (exact significance=0.016, one-tailed, N-ties=6), and in stress-related behaviors (exact significance=0.016, one-tailed, N-ties=6). This was not the case for animals exposed to basic husbandry training or animals in the control group. A significant proportion of desensitization-exposed animals also showed a reduction in the duration of time spent cringing toward humans (exact significance=0.016, one-tailed, N-ties=6), but not in cringing behaviors in general or in stress-related behaviors. There were not a significant proportion of animals in either the husbandry training group or the control group that showed a decrease in duration of these behaviors. Results of this study could enhance both laboratory animal welfare and laboratory animal research, and could be a first step in developing techniques for reducing fearful behavior in rhesus monkeys in the laboratory environment.     

Training of laboratory-housed non-human primates in the UK

Abstract

Laboratory-housed non-human primates may experience a range of potential stressors, including physical and chemical restraint, venepuncture, injection, catching and cage-change. Training them to co-operate, using positive reinforcement techniques, is one means of significantly reducing the adverse impact of such procedures upon them and, therefore, is a refinement. Furthermore, the additional time that staff spend with the primates, and the need for individual recognition and close observation of animal behavior, mean that the trainer develops a relationship with each individual animal which can be beneficial for animal welfare (e.g., by reducing the occurrence of abnormal behavior and fear of humans). We surveyed use of training in thirteen UK establishments using and breeding primates, utilizing a mixed-mode questionnaire. The survey demonstrated that there is widespread awareness of training as a refinement and appreciation of its diverse benefits, but training is not used as widely or as fully as it might be. This is largely due to real constraints (principally staff and time and a lack of confidence in ability to train), and perceived constraints (such as a supposed lack of information on how to train and assessment of the benefits, and an overestimation of the time investment needed). There is also considerable variation between establishments in the purposes of training and techniques used, with a reliance on negative reinforcement in three. We conclude that there is considerable scope for refinement of common scientific, veterinary and husbandry procedures, and refer to some resources designed to help establishments take action (e.g., Prescott and Buchanan-Smith 2003).     

Re-Evaluating Primate Monogamy

Researchers propose hypotheses for the occurrence of monogamy as a social system in primates based on the assumption that there are a group of primates, including humans, which live exclusively in "nuclear families" and share a similar set of social behaviors. Examining the primates purported to be "monogamous" reveals that they cover a wide range of grouping types, mating patterns, taxonomic groups, and evolutionary grades. While there are a few primate species that do live in small, two-adult groups and share a similar set of social behaviors, the vast majority of the supposed "monogamous" primates, including humans, do not. [monogamy, social systems, evolution, variability in social organization]     

Social organization of the Alaotran gentle lemur (Hapalemur griseus alaotrensis)

Knowledge of the social organization of lemurs is still limited for most species. Where there is sufficient information, it has been shown that lemur social organization differs in essential points from that of other primates. In the field study reported here, demographic structure and life-history processes were investigated in order to characterize the social organization of the Alaotran gentle lemur (Hapalemur griseus alaotrensis). Data were obtained through captures and observations. Alaotran gentle lemurs were found in small groups of up to nine individuals. Although most groups contained just one breeding female, a substantial proportion of groups (35%) had two breeding females. Therefore, Alaotran gentle lemurs cannot be classed as being organized in monogamous family groups. An extended birth season was found, and groups with two breeding females had significantly higher breeding output per adult than groups with a single adult female. Limited data suggest that females emigrate from their natal group while still subadult, whereas males can stay in the natal group until they are fully grown and disperse as adults. Variability in group composition, significantly higher reproductive output per adult in groups with two breeding females, and delayed dispersal of males suggest that Alaotran gentle lemurs pursue a resource-defense mating strategy, rather than a female-defense mating strategy. The suggestion that extant social lemurs may have evolved from a monogamous system, could explain the differences between lemur social systems and those of other primates.     

Different Responses to Reward Comparisons by Three Primate Species

Background

Recently, much attention has been paid to the role of cooperative breeding in the evolution of behavior. In many measures, cooperative breeders are more prosocial than non-cooperatively breeding species, including being more likely to actively share food. This is hypothesized to be due to selective pressures specific to the interdependency characteristic of cooperatively breeding species. Given the high costs of finding a new mate, it has been proposed that cooperative breeders, unlike primates that cooperate in other contexts, should not respond negatively to unequal outcomes between themselves and their partner. However, in this context such pressures may extend beyond cooperative breeders to other species with pair-bonding and bi-parental care.

Methods

Here we test the response of two New World primate species with different parental strategies to unequal outcomes in both individual and social contrast conditions. One species tested was a cooperative breeder (Callithrix spp.) and the second practiced bi-parental care (Aotus spp.). Additionally, to verify our procedure, we tested a third confamilial species that shows no such interdependence but does respond to individual (but not social) contrast (Saimiri spp.). We tested all three genera using an established inequity paradigm in which individuals in a pair took turns to gain rewards that sometimes differed from those of their partners.

Conclusions

None of the three species tested responded negatively to inequitable outcomes in this experimental context. Importantly, the Saimiri spp responded to individual contrast, as in earlier studies, validating our procedure. When these data are considered in relation to previous studies investigating responses to inequity in primates, they indicate that one aspect of cooperative breeding, pair-bonding or bi-parental care, may influence the evolution of these behaviors. These results emphasize the need to study a variety of species to gain insight in to how decision-making may vary across social structures.     

Positive reinforcement training as a technique to alter nonhuman primate behavior: quantitative assessments of effectiveness

Many suggest that operant conditioning techniques can be applied successfully to improve the behavioral management of nonhuman primates in research settings. However, relatively little empirical data exist to support this claim. This article is a review of several studies that discussed applied positive reinforcement training techniques (PRT) on breeding/research colonies of rhesus macaques (Macaca mulatta) and chimpanzees (Pan troglodytes) at The University of Texas M. D. Anderson Cancer Center and measured their effectiveness. Empirical analyses quantified the amount of time required to train rhesus monkeys to come up, station, target, and stay. Additionally, a study found that time spent affiliating by female rhesus was changed as a function of training low affiliators to affiliate more and high affiliators to affiliate less. Another study successfully trained chimpanzees to feed without fighting and to come inside on command. PRT is an important behavioral management tool that can improve the care and welfare of primates in captivity. Published empirical findings are essential for managers to assess objectively the utility of positive reinforcement training techniques in enhancing captive management and research procedures.     

非人灵长类的亲缘选择

亲缘选择是动物进化的重要研究领域之一,非人灵长类因具有丰富的社会网络,是亲缘选择研究领域的重要类群。动物进行亲缘选择的前提是亲缘识别,并常通过社会行为的亲缘偏向表现。因此,本文从非人灵长类的亲缘识别机制和亲缘关系对其社会行为的影响两方面进行了综述:熟悉性和表现型匹配是目前普遍认同的非人灵长类亲缘识别机制,同时这两种机制并不相互排斥,它们可能共同在灵长类的亲缘识别中起作用;在非人灵长类中,亲缘关系是影响社会行为模式的主导因子,它影响着多种灵长类个体的友好行为、攻击行为和性行为的选择,同时亲缘偏向行为在不同物种中表现不尽相同,说明亲缘选择理论可以部分解释灵长类的行为,但存在一定的局限性。本文分析了两种亲缘识别机制的异同以及在实际研究中利用亲缘选择理论解释非人灵长
类社会行为的局限及可能原因。目前,对非人灵长类社会中的亲缘选择研究正逐步深入,其中分子遗传学技术的应用是重要的推动力量。同时,依然存在诸如汉密尔顿规则参数估计和新大陆猴的亲缘选择研究案例的难点,有待研究者进一步探究。     

Hormones associated with non-maternal infant care: a review of mammalian and avian studies

Hormonal changes during non-maternal infant care have been demonstrated in many cooperatively breeding bird species, some monogamous rodents and two species of New World primates. Coevolution of hormones and social traits may have provided for the different breeding systems that occur today. Several hormones have been shown to covary with the breeding systems of vertebrates. Elevated levels of the hormone prolactin with male parenting behaviours are common to many birds, rodents and the callitrichid monkeys Callithrix jacchus and Saguinus oedipus. In birds, prolactin may be elevated in both male and female breeders during various stages of nest building, egg laying, incubating and feeding of young. Testosterone levels appear to have an inverse relationship to prolactin levels during infant care in birds and rodents, but this relationship has not been examined for primates. In cooperatively breeding birds, helpers who remain at the nest also have elevated levels of prolactin when displaying parental care behaviours. Prolactin levels are elevated in helper callitrichid monkeys during the postpartum period. Monogamous male rodents demonstrate elevated prolactin levels with parental care behaviour but, in contrast to the birds, the mechanisms mediating prolactin increase appear to differ for male and female rodents. Two factors may influence male parental behaviours and hormonal changes: stimuli from the pregnant female and stimuli from the newborn pups; whereas maternal behaviours are influenced by the maternal hormones of the female and the pup stimuli. An experiential factor may also influence male parental behaviours. Neuropeptides such as oxytocin and vasopressin appear to be involved in male rodent parental care and there may be an interaction between a series of hormones and neurosecretions and stimuli from mates and pups. Studies of Saguinus oedipus, the cotton-top tamarin, suggest that prolactin levels are responsive to stimuli from contact with infants and the level of infant care experience influences the levels of prolactin with male infant care. Father tamarins also have elevated levels of prolactin before the birth of infants suggesting that cues from the pregnant female are important. Prolactin's role in parental care may have evolved from prolactin's role in other reproductive functions. Hormonal regulation of non-maternal care may occur due to a complex interaction of many hormones and neurotransmitters. Studies described here should provide the impetus for further work on parental care hormones in a wide variety of primates.     

Population genetics meets behavioral ecology

Populations are often composed of more than just randomly mating subpopulations - many organisms from social groups with distinct patterns of mating and dispersal. Such patterns have recieved much attention in behavioral ecology, yet theories of population genetics rarely take social structures into account. Consequently, population geneticists often report high levels of apparent in breeding and concomitantly low efective sizes, even for species that avoid mating between close kin. Recently, a view of gene dynamics has been introduced that takes dispersal and social structure into account. Accounting for social structure in population genetics leads to a different perspective on how genetic variation is partitoned and the rate at which genic diversity is lost in natural populations - a view that is more consistent with observed behaviors for the minimization of inbreeding.