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Social housing of rhesus macaques (Macaca mulatta) is considered to be the cornerstone of behavioral management programs in biomedical facilities. However, it also involves the risk of socially inflicted trauma. The ability to avoid such trauma would contribute to the animals' well-being and alleviate staff's concerns, thus paving the path for more...
Citations
... These hierarchies provide a conflict resolution mechanism, reducing the risk of injury caused by agonistic conflicts over limited resources [3][4][5]. Dominance signals and individual recognition are suggested mechanisms for assessing resource competitors [6], facilitating conflict resolution by avoiding the costs associated with overt aggression and injuries [7][8][9][10]. These mechanisms are integral to the formation and maintenance of dominance hierarchies. ...
Dominance hierarchy is widespread among group-living animals as a conflict resolution strategy to avoid the cost and risk of fights among individuals. Dominance signals are well-known mechanisms that allow individuals to assess their opponent’s fighting ability without physical contact, thereby maintaining dominance relationships. In fission–fusion societies, where group composition is fluid, dominance status can shift depending on the current group members. In such situations, vocal signals may be particularly useful as dominance signals due to their easy modification by the signaller. In this study, we investigated the relationship between rank-dependent behaviours and rank ascending by temporarily removing individuals from captive groups of large-billed crows (Corvus macrorhynchos). We removed either the first-ranked or third-ranked individuals from the group for 1 day and compared the behaviours of the remaining group members before the removal, during the removal and after the removed individuals rejoined the group. We found that the number of sequential ka calls, which is assumed to be a status signal, increased only during the removal of first-ranked individuals and decreased after they rejoined the group. These results suggest that sequential ka calls serve as dominance signals, and the subordinates flexibly adjust their vocalization depending on the presence of high-ranked individuals.
... Social housing of male macaques as a small group will naturally result in the establishment of social ranks, and aggression tends to occur when the hierarchy has not settled [31]. It has been reported that an early onset of submissive behaviors during introduction of pairing is associated with lower wounding [32]. One limitation of our study was the lack of behavior-data quantification associated with social housing attempts, such as data acquired with focal animal sampling or scan sampling. ...
Cynomolgus macaques (Macaca fascicularis; Mf) serve an essential role in the advancement of biomedical research. Aged macaques, in particular, are highly valued as animal models for the study of geriatric diseases. While social housing has become the default for nonhuman primates (NHPs), socially housing sexually mature males poses a unique challenge. Moreover, socially housing aged males that have been previously kept in single housing may pose even greater challenge and risk due to a higher likelihood of aggression. Temperament assessment plays an integral part in determining the success of social housing arrangements of NHPs. In this paper, we report our work at the Primate Research Center of IPB University in integrating behavior observation and veterinary management to socially house adult, male Mf. We describe our experience in successfully housing young-adult, male Mf (n = 8–10, aged 6 years) for over 2.5 years, and the multiple efforts to socially house a small group of previously singly housed aged, male Mf (n = 6, aged >15 years). The temperament of each Mf was considered in the planning and implementation of social housing attempts. While a simplified behavioral observation was performed for the young adults, a more rigorous PAIR-T assessment was performed on the aged Mf. A group formation was initially attempted, aiming to achieve a small group of six aged, male Mf. While this group at first showed promising outcomes, significant incidents of aggression required regrouping as pairs or triads wherein the subject combinations were determined based on temperament and dominance. A total of three attempts were made to house these aged Mf in a small group throughout the course of 17 months, and the results showed that at our facility, aged, male Mf are best housed as triads or pairs, with selections based on their temperament and dominance compatibility. We concluded that behavioral assessments and veterinary management are pivotal in supporting the social housing efforts of adult, male Mf in order to optimize their well-being.
... 18,53 However, dominance ranks are not static and can change if aspects of the social environment change, 1,11,17 such as the loss of keystone individuals 34 or addition of new allies. 17 As many NHPs are housed in pairs or small social groups, substantial research has been aimed at understanding pairing success, 14,31,38 but less is known about factors that contribute to successful formations of large, naturalistic social groups. Because high levels of aggression and trauma can occur even in well-established groups, 8,45 gauging social stability in large group formations of rhesus macaques is difficult, as aggression does not necessarily equate to incompatibility or trauma. ...
... Because high levels of aggression and trauma can occur even in well-established groups, 8,45 gauging social stability in large group formations of rhesus macaques is difficult, as aggression does not necessarily equate to incompatibility or trauma. 8,31,38 Understanding whether individuals maintain their previous hierarchies is critical information for behavioral managers as they form new social groups. ...
Forming groups of captive rhesus macaques (Macaca mulatta) is a common management practice. New formations of unfamiliar macaques can be costly, with high levels of trauma, particularly as intense aggression is used to establish a dominance hierarchy. Combining previous subgroups into one new group may be beneficial, as some individuals already have established dominance relationships. We tested this hypothesis by forming a new mixed-sex group of rhesus macaques that combined an established group of females with an established group of males. Prior to the mixed-sex group formation, both the female and male hierarchies had been stable for 3 y; after mixed-sex group formation these hierarchies were maintained by the females and were initially maintained by the males for 3 wks. However, the temporary hospitalization (due to a laceration caused by aggression) of the alpha male destabilized the male hierarchy. Age and weight then predicted male rank. Temporary hospitalizations resulted in rank changes for the males, evidenced by reversals in subordination signals. Thisstudy indicates that using established groups of familiar individuals may maintain female hierarchical stability in a mixed-sex group formation, but further research is needed to understand how to maintain and predict male hierarchical stability to reduce trauma. Improved knowledge of hierarchical stability would be invaluable to managers of large rhesus macaque groups and would help improve the welfare of captive rhesus macaques.
... Having lived in a group previously, familiar animals will have already established their rank based on matriline membership within that context. Reliance on the display of submissive behaviors to reinforce established rank, shown to be associated with lower risk of wounding after the first 30 days of newly introduced pairs (Pomerantz & Baker, 2017), and engaging in affiliative behaviors (Snyder-Mackler et al., 2016), both of which serve to inhibit aggression (Marler, 1976), may be underlying drivers for why pairs with social familiarity are less likely to be later separated for social reasons. Our findings highlight the importance of prior familiarity in the social stability of established dyads and how it might be used specifically to choose potential partners when pair formation of macaques is required. ...
... When compared with single housing, pair housing of macaques results in more physical activity, a more complete expression of species-typical social behaviors, and a reduction in abnormal behaviors (DiVincenti & Wyatt, 2011). Social introductions carry potential risk to the animals involved because of possible injury or stress, they require specialized housing facilities, and involve considerable effort to arrange and monitor (e.g., Pomerantz & Baker, 2017;Ruhde, Baker, Russell-Lodrigue, Blanchard, & Bohm, 2020;Truelove et al., 2017b;Worlein et al., 2017). Given these costs, one goal of the primate manager is to establish social partnerships that endure. ...
Social housing improves the well-being of monkeys in research settings; however, little is known about factors influencing the long‐term stability of established, full-contact pairs. Archival data were examined to determine whether sex, age, weight, duration pair housed, familiarity, social interruptions, room changes, or sedation events predicted eventual separation of pairs for social incompatibility (n = 80) or for nonsocial reasons (e.g., research or health needs) (n = 1143). Using a logistic regression model (Wald Χ2(8) = 42.325, p < .001), three significant factors were identified. Pairs in which partners had known prior familiarity in group housing were less likely to experience social incompatibility (p = .034). Pairs housed together longer (p < .001) and who staff had temporarily separated through the placement of a cage divider to reduce physical contact were more likely to require permanent separation for social incompatibility (p < .001); additional analysis revealed that dividers were often placed for social reasons, suggesting early signs of social instability. Findings may be useful for primate caregivers when making decisions about managing social partners.
... The current study sought to build on previous research conducted by us and others [30,[36][37][38] that identified predictors of pair success (i.e., can social partners remain together continuously in a shared space without persistent aggression and wounding). In particular, our recent study [36] demonstrated that, for female pair formations, three measures, taken from the California National Primate Research Center's (CNPRC) BioBehavioral Assessment (BBA) Program (see Section 2.4) predicted success in pairings. ...
... A mean of this novelty preference measure was taken for the seven problems. Overall, rhesus macaques (and humans) prefer to look at the novel stimuli in such a test, and we found that on our particular test, animals that showed the novelty preference at 3-4 months of age demonstrated high social functioning in their living cages at 1-4 years of age, while animals that did not show this preference did not [38]. This test, then, tells us something about social information processing, and we hypothesized that it might be influential in pairing success. ...
... Beisner and McCowan [60] reported that in social groups of captive rhesus macaques, animals employ silent bared-teeth display (also known as fear-grimacing) to communicate subordination and submission (depending on the context). Similarly, Pomerantz and Baker [38] found that higher levels of submissive behaviors expressed at the early stages of the introduction process were associated with reduced likelihood of altercations (resulting in wounding) between rhesus macaque social partners. We emphasize that the pairs in the current study did exhibit such behaviors during the introduction. ...
Simple Summary
Rhesus macaques are highly social animals that are used extensively in research. Providing them with a supportive social environment by pairing individuals with compatible partners improves their life quality and also their use as research animals. Therefore, identifying suitable social partners will benefit both the animals and the science. Previous work showed that female rhesus macaques were more likely to form successful pairs that exhibit little aggression if they showed similarities in certain personality traits measured in infancy. In the current study, we assessed the relationships between the same personality traits and the quality of social interactions between partners. This is important since by ensuring that animals benefit the most from being paired to a compatible partner, we are more likely to expose the animals to positive experiences instead of simply avoiding negative ones. We found that pairs with similar emotionality scores showed more positive social interactions, and pairs with similar nervous temperament used fewer behavioral signals to communicate their dominance relationship. Moreover, pairs that paid more attention to unfamiliar monkey faces were more anxious. These results highlight the importance of taking the animals’ personalities into consideration when attempting to match social partners and provide them with an environment that fits their needs.
Abstract
Previous reports suggest that female macaques with greater similarity in emotionality and nervous temperament, as evaluated in a well-established BioBehavioral Assessment (BBA) at the California National Primate Research Center, were more likely to form successful pairs. We tested whether the same measures can also predict the quality of social interactions among 20 female rhesus macaque pairs. We correlated the pairs’ emotionality and nervous temperament scores obtained in infancy and the levels of behaviors recorded systematically during the pairing process years later. Supporting previous findings, partners with similar emotionality scores were more affiliative, and pairs with similar nervous temperament expressed less dominance/submissive behavior. Exploratorily, we found that pairs that were better at processing social information (part of BBA) were also more anxious. Such animals should be prioritized to be introduced in rooms that house calmer, less aggressive animals and provide opportunities for hiding to alleviate their anxiety. Indeed, positive social experiences not only promote animal welfare, but also reduce stress related confounds and unexplained data variability. Therefore, by incorporating the animals’ temperament into the pair configuration process we increase the likelihood of forming high-quality pairs, both in terms of welfare and the research of which they are a part.
... Taking pictures might be associated with lower odds of experiencing aggression at Sepilok because the tourists are looking at their phone or through their camera, rather than making prolonged eye contact, which was associated with significantly increased odds of experiencing aggression. Eye contact or staring between conspecifics has been associated with aggression in a number of macaque species, including long-tailed macaques (Cannon et al. 2016;Chance et al. 1977), pig-tailed macaques (Oettinger et al. 2007), and rhesus macaques (Macaca Mulatta: Pomerantz and Baker 2017;Symons 1974). Research that demonstrated that macaques are aware of and sensitive to human gaze dates back to the 1960s (e.g., Wada 1961), and previous work on macaques and tourism listed eye contact as a potential cause of human-directed aggression (Beisner et al. 2015;Fuentes and Gamerl 2005). ...
A Correction to this paper has been published: https://doi.org/10.1007/s10764-021-00225-3
... Taking pictures might be associated with lower odds of experiencing aggression at Sepilok because the tourists are looking at their phone or through their camera, rather than making prolonged eye contact, which was associated with significantly increased odds of experiencing aggression. Eye contact or staring between conspecifics has been associated with aggression in a number of macaque species, including long-tailed macaques (Cannon et al. 2016;Chance et al. 1977), pig-tailed macaques (Oettinger et al. 2007), and rhesus macaques (Macaca Mulatta: Pomerantz and Baker 2017;Symons 1974). Research that demonstrated that macaques are aware of and sensitive to human gaze dates back to the 1960s (e.g., Wada 1961), and previous work on macaques and tourism listed eye contact as a potential cause of human-directed aggression (Beisner et al. 2015;Fuentes and Gamerl 2005). ...
Conservationists continue to grapple with the practical risks that accompany ecotourism initiatives, where access to threatened ecosystems is exchanged for financial support for both protected areas and local communities. One of the most practical ways to mitigate the potentially harmful effects of an increasing number of visitors is to identify problematic human behaviors and attempt to limit them through education or staff intervention. We observed the behavior of both visitors and macaques in a hybrid group (Macaca fascicularis × M. nemestrina) at Sepilok Orang-utan Rehabilitation Center in Sabah, Malaysia over a period of 10 months to better understand patterns in tourist-directed aggression. We witnessed 307 encounters between macaques and tourists but intense aggression was absent. Overall rates of minor visitor-directed aggression were low, with only 0.71 bouts observed per hour. Eye contact between tourists and macaques was associated with significantly higher odds of experiencing minor human-directed aggression, such as an open mouth threat. Taking a picture, however, was associated with reduced odds of experiencing aggression from the macaques. Tourists were not able to provision the animals, which may help explain the lower rates of intense aggression compared to those at other tourist sites. Although improved education signs and staff supervision could further reduce visitor-directed aggression at Sepilok, these results are promising because they highlight the role that relatively simple policies (such as those that forbid provisioning by tourists) can play in reducing unwanted behavior by both humans and nonhuman primates at ecotourism locations.
... Despite the importance of knowing this information, there are few published studies that have empirically examined whether early behaviors can predict pair success for monkeys. In one study of rhesus macaques, Pomerantz and Baker (2017) found that high levels of submissive behavior (e.g., fear grimace, eye avert, and crouch) exhibited by partners early in the protected contact phase of the introduction were associated with a reduced likelihood of wounding within the first month of full contact. While wounding is clearly an undesired outcome in socialization attempts, pairs may be separated for nonaggressive signs of incompatibility as well, such as the subordinate animal being overly fearful of the dominant. ...
... Because the presence of affiliative behavior is often used as an indicator of pair compatibility (DiVincenti & Wyatt, 2011;Doyle et al., 2008), we hypothesized that social grooming would predict pair success, such that pairs that engaged in a great deal of grooming would be more likely to remain cohoused compared with those that showed little grooming. Based on the findings of Pomerantz and Baker (2017), we also hypothesized that pairs in which one partner exhibited high levels of submissive behaviors would be more likely to be successful than pairs that displayed few submissive behaviors. ...
... Contrary to our hypothesis, submissive behaviors (crouching, cowering, or extended grimacing) were very rare in our dataset and not predictive of pair success for either male or female pairs. These results were surprising, given that these behaviors had been previously found to negatively correlate with wounding (Pomerantz & Baker, 2017). However, in that study, animals were in protected contact for ∼12 days on average before full contact pairing, and were assessed within the first 15 min of protected contact. ...
Pair housing is one of the most important components of behavioral management for caged macaques; however, it can result in aggression and injury if partners are incompatible. Knowing when to proceed and when to stop social introductions can be challenging, and can have consequences for the partners. We examined whether behavior early in social introductions predicted success (i.e., partners remained cohoused with full contact for at least 28 days) in 724 female–female and 477 male–male rhesus macaque pairs. We took cage side one–zero focal observations on pairs during the first 2 days of full contact, recording social and aggressive behaviors. The majority of pairs (79.6% of female and 83.0% of male) were successful. The most common behaviors exhibited by pairs during these observations were maintaining proximity, tandem threats, and anxiety. Mounting was also relatively common in male pairs. Grooming and close social contact (e.g., touching) were not common in our study. Several behaviors observed on Day 1 significantly predicted pairing success. For females, these included proximity, tandem threat, rump present, mount, and groom. Day 1 predictors of success for male pairs included proximity, tandem threat, rump present, mount, and social contact. Fewer behaviors predicted success on Day 2. Maintaining proximity on Day 2 predicted success for both sexes, but tandem threat predicted success only for females. Behaviors that predicted incompatibility for females on Day 1 included displace, grimace, threat, bite, and other aggressive contacts. Day 1 predictors of separation for male pairs were displaced, grimace, and abnormal behavior. The only Day 2 behavior that correlated with incompatibility was grimace, which was predictive for males. Interestingly, aggression did not predict incompatibility for male pairs. Identifying behaviors exhibited by monkeys early in the pair introduction that are predictive of long‐term compatibility can shape pairing decisions, reducing later stress and potential injury.
Research Highlights
• Several behaviors, including maintaining proximity (i.e., staying close without touching) and tandem or cothreat, exhibited by rhesus macaques on the first day of full contact predicted pair success for isosexual male and female pairs.
• Behaviors on Day 1, such as displace and grimace, predicted incompatibility.
• Successful pairs displayed some aggression towards each other, suggesting that a degree of aggression early on does not necessarily mean the pair is incompatible.
... While the benefits of pair-housing are now well established, pairing laboratory macaques with compatible companions is challenging and requires knowledge of and experience with species-specific social behavior (Truelove, Martin, Perlman, Wood, & Bloomsmith, 2017). Thus, research on laboratory macaque pair-housing has shifted focus to refining pairing practices to improve partner compatibility, welfare, and pairing success (e.g., Capitanio et al., 2017;Pomerantz & Baker, 2017;Truelove et al., 2017). Relatively little progress has been made, however, to improve our understanding of how frequent changes to pair-housing affect NHP physiology, despite the implications for biomedical research (reviewed in Hannibal et al., 2017). ...
... First, and as a bare minimum, the absence of serious aggression or injury demonstrates that pair-mates at least tolerate each other, and is a baseline feature of determining pair compatibility in most pairing programs at research facilities across the United States. Second, clear directionality in dominance signals between pair-mates indicates a certain and well established relationship (Pomerantz & Baker, 2017). Strongly compatible pair-mates will display these first two traits, as well as high levels of affiliative interaction, and score low on Tense as a pair when evaluated by staff with species-specific behavioral knowledge. ...
Laboratory rhesus macaques are often housed in pairs and may be temporarily or permanently separated for research, health, or management reasons. While both long‐term social separations and introductions can stimulate a stress response that impacts inflammation and immune function, the effects of short‐term overnight separations and whether qualities of the pair relationship mediate these effects are unknown. In this study, we investigated the effects of overnight separations on the urinary cortisol concentration of 20 differentially paired adult female rhesus macaques (Macaca mulatta) at the California National Primate Research Center. These females were initially kept in either continuous (no overnight separation) or intermittent (with overnight separation) pair‐housing and then switched to the alternate pair‐housing condition part way through the study. Each study subject was observed for 5 weeks, during which we collected measures of affiliative, aggressive, anxious, abnormal, and activity‐state behaviors in both pair‐housing conditions. Additionally, up to three urine samples were collected from each subject per week and assayed for urinary free cortisol and creatinine. Lastly, the behavioral observer scored each pair on four relationship quality attributes (“Anxious,” “Tense,” “Well‐meshed,” and “Friendly”) using a seven‐point scale. Data were analyzed using a generalized linear model with gamma distribution and an information theoretic approach to determine the best model set. An interaction between the intermittent pairing condition and tense pair adjective rating was in the top three models of the best model set. Dominance and rates of affiliation were also important for explaining urinary cortisol variation. Our results suggest that to prevent significant changes in HPA‐axis activation in rhesus macaque females, which could have unintended effects on research outcomes, pairs with “Tense” relationships and overnight separations preventing tactile contact should be avoided.
