Social management of laboratory rhesus macaques housed in large groups using a network approach: A review

Abstract

Biomedical facilities across the nation and worldwide aim to develop cost-effective methods for the reproductive management of macaque breeding groups, typically by housing macaques in large, multi-male multi-female social groups that provide monkey subjects for research as well as appropriate socialization for their psychological well-being. One of the most difficult problems in managing socially housed macaques is their propensity for deleterious aggression. From a management perspective, deleterious aggression (as opposed to less intense aggression that serves to regulate social relationships) is undoubtedly the most problematic behavior observed in group-housed macaques, which can readily escalate to the degree that it causes social instability, increases serious physical trauma leading to group dissolution, and reduces psychological well-being. Thus for both welfare and other management reasons, aggression among rhesus macaques at primate centers and facilities needs to be addressed with a more proactive approach. Management strategies need to be instituted that maximize social housing while also reducing problematic social aggression due to instability using efficacious methods for detection and prevention in the most cost effective manner. Herein we review a new proactive approach using social network analysis to assess and predict deleterious aggression in macaque groups. We discovered three major pathways leading to instability, such as unusually high rates and severity of trauma and social relocations. These pathways are linked either directly or indirectly to network structure in rhesus macaque societies. We define these pathways according to the key intrinsic and extrinsic variables (e.g., demographic, genetic or social factors) that influence network and behavioral measures of stability (see Fig. 1). They are: (1) presence of natal males, (2) matrilineal genetic fragmentation, and (3) the power structure and conflict policing behavior supported by this power structure. We discuss how these three major pathways leading to greater understanding and predictability of deleterious aggression in macaque social groups.

Interactions with humans impose time constraints on urban-dwelling rhesus macaques (Macaca mulatta)

“…Thus, female-female grooming among macaques is key for the maintenance of group social stability and cohesion (Cords, 2012), which can explain why females engaged in higher rates of grooming interactions than males despite the human-induced time constraints on this social behaviour. Indeed, previous work on captive rhesus macaques has shown that a low genetic relatedness might result in more fragmentation and/or subgrouping in grooming networks, which can result in higher social instability and wounding McCowan et al, 2018). Interestingly high-ranking females seemed to experience more time constraints on social grooming than subordinate females.…”

Factors determining male introduction success and long-term stability in captive rhesus macaques

“…Female primates within a matriline form close social bonds [67,68]. These bonds may buffer stress during introductions [22], and increase stability within a group [48]. Increased stability is, in its turn, associated with lower aggression levels from females to males [25], which may increase introduction success.…”

“…Groups with a large number of families (i.e. matrilines) may be more unstable, which is increased even further through introductions [11,46,48]. This indicates that introductions into groups with few females and few matrilines may be more successful.…”

Increased produce enrichment reduces trauma in socially‐housed captive rhesus macaques (Macaca mulatta)

“…While high levels of aggression are a normal reflection of hierarchical maintenance, in a captive setting, victims sometimes cannot escape their aggressors, resulting in significant traumas. For example, in some national primate research centers, up to 60% of a breeding group (ranging in size from 100 to 200 individuals) may be hospitalized within a given year (McCowan, Beisner, & Hannibal, ), with costs ranging from $150 to 3,000 per hospitalization (unpublished raw data). Aside from the financial cost, individual primates may also be temporarily or permanently removed from their social group, which has the potential to perturb social stability (Beisner, Jin, Fushing, & McCowan, ; Oates‐O'Brien, Farver, Anderson‐Vicino, McCowan, & Lerche, ; Wooddell, Kaburu, Suomi & Dettmer, ).…”

“…Aside from the financial cost, individual primates may also be temporarily or permanently removed from their social group, which has the potential to perturb social stability (Beisner, Jin, Fushing, & McCowan, ; Oates‐O'Brien, Farver, Anderson‐Vicino, McCowan, & Lerche, ; Wooddell, Kaburu, Suomi & Dettmer, ). Due to these financial and animal welfare concerns, greater scrutiny is being aimed toward reducing aggression and trauma in captive groups of macaques (Hannibal et al, ; McCowan, Anderson, Heagerty, & Cameron, ; McCowan et al, ).…”