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Open Access Publications from the University of California

Scholarly Works (67 results)

  • Article
  • Peer Reviewed
UC Davis Previously Published Works (2014)
The signaling context has been found to change the meaning of the silent bared-teeth display (SBT) in pigtail macaques (Macaca nemestrina) such that the SBT in apparently peaceful contexts communicates subordination, a long-term pattern of behavior, whereas in conflict contexts it communicates immediate submission (PNAS, 104: 1581-1586). However, the context dependent nature of the SBT has not yet been explored in other species. We investigated SBT usage with respect to grooming, severe aggression, and signaler-receiver sex, rank difference, and body size in seven captive groups of rhesus macaques. Peaceful SBTs were given most often to male receivers by male and female signalers whereas conflict SBTs were given to both male and female receivers primarily by female signalers. Male signalers rarely gave SBTs (peaceful or conflict) to female receivers. Unlike pigtail macaques, peaceful SBTs in rhesus were often accompanied by withdrawal behavior (referred to as peaceful SBT-leave), which influenced grooming, but not aggression, at the dyadic level. Severe aggression was less frequent among dyads using peaceful SBTs (regardless of withdrawal behavior) than those using conflict SBTs. In contrast, grooming was more frequent among dyads using peaceful SBT-stay signals than those using peaceful SBT-leave signals or conflict SBTs. In total, our results indicate that peaceful SBTs are a functionally different signal from conflict SBTs in rhesus macaques.
    Cover page: Signaling context modulates social function of silent bared‐teeth displays in rhesus macaques (Macaca mulatta)
    • Thesis
    • Peer Reviewed
    UC Davis Electronic Theses and Dissertations (2023)

    This dissertation addresses the escalating threat of anthropozoonosis at human-wildlife interfaces by investigating the social dynamics of disease transmission among wildlife populations, focusing particularly on long-tailed macaques (Macaca fascicularis) inhabiting human-wildlife interface areas. Tuberculosis (TB) serves as the model infectious disease due to its high prevalence in Southeast Asia, air-borne transmission and its zoonosis nature. Although concerns about disease risks to these macaques have been raised, the role of individual variation, encompassing social network attributes and human exposures, has remained unexplored. To address these questions, this project utilizes non-invasive techniques for sample collection from a population of free-ranging macaques in Thailand. I adopt a network approach to examine the intricate relationship between social attributes and TB infection status. Furthermore, an epidemiological model, Susceptible-Exposed-Infectious-Recovered-Susceptible (SEIRS), is integrated to monitor changes in individuals' disease states and explore hypothetical scenarios of disease spread within social networks, with parameters tailored to each individual.Chapter One investigates the factors driving pathogen infection by identifying infected animals and examining how sociodemographic attributes, combined with interactions with conspecifics, humans, and responses to stress and sickness, influence TB infection patterns within social groups. Notably, it reveals that the likelihood of TB infection increases among individuals with high human interaction and those engaging in less grooming activity. Chapter Two explores the influence of social network positions on TB transmission. By implementing a social network approach to locate infected individuals, this chapter explores the interplay between contact-transmission and social buffering. It highlights the significance of individual macaques' social network positions in their infection status, emphasizing that monkeys with fewer grooming interactions and living periphery are more likely to have TB. Chapter Three employs mathematical modeling within the network to investigate transmission dynamics and the persistence of TB, taking into account variations in transmissibility and latency periods. SEIRS models reveal that over half of the population remains in the latent stage of TB infection. It elucidates that social buffering, specifically the adjustment of the latency period from latency to active TB, plays a pivotal role in explaining the presence of infected individuals in the social network periphery. In contrast, adjusting transmissibility fails to accurately represent observed relationships in this population. Overall, this dissertation aims to uncover the social and demographic factors that influence the acquisition and transmission of TB among free-ranging long-tailed macaques inhabiting human-wildlife interface areas. Understanding the attributes of social network components in wildlife populations at the human-wildlife interface contributes to mitigating infectious disease transmission, reducing zoonotic risks, and promoting the well-being of both humans and wildlife. These insights play a crucial role in clarifying steps to prevent potential future pandemics.

    • 1 supplemental PDF
    Cover page: Tuberculosis Infection in Free-Ranging Long-Tailed Macaques through Social Network and Modeling
    • Thesis
    • Peer Reviewed
    UC Davis Electronic Theses and Dissertations (2023)

    Cognitive ecology investigates how interactions with the environment shape the cognitive abilities of organisms. Studies on humans have emphasized that cognition is selected for under specific environmental conditions to extract information efficiently. More recently this approach has been applied to animals and focuses on how variation within the environment shapes the evolution of cognitive systems. Animals may use certain behavioral styles or cognitive traits to adapt to the amount of variability and predictability in their environment. Variation in resources and environmental complexity are two major factors that drive the diversity of cognitive adaptations seen across animals, as these are often beneficial for specific conditions or allow for adjusting to novel or changing conditions. For example, animals who experience displacement due to rapid urbanization may benefit from enhanced cognitive abilities and/or behavioral flexibility to adjust to those environmental changes quickly.Combining cognitive and urban ecology is particularly interesting because animals often need to consider both predictable and unpredictable elements of human behavior to survive. While many animals can capitalize on the predictable elements of human behavior in the urban environment by avoiding direct interactions with humans, those who can capitalize on more unpredictable sources of variation, such as opportunistic provisioning, may gain an advantage in environments where this type of variation exists in substantial quantities. One way that animals may capitalize on these benefits is by exhibiting traits such as reduced neophobia, enhanced problem-solving abilities, and behavioral flexibility. These traits would allow them to access a wider variety of food resources available in urban spaces and may provide significant fitness advantages. This dissertation explores several aspects of behavioral flexibility ranging from specific, technical quantifications of an individual’s flexibility to solve foraging problems to more holistic or general strategies that individuals may adopt in foraging contexts. Combining experiments from the field and captivity, I explore how individuals innovate (i.e. solve a new problem or apply an old solution to a new problem) and whether they are flexible in their problem-solving behavior. For both the cognitive experiments and behavioral observations, I focused on two closely related species of macaques, rhesus (Macaca mulatta) and long-tailed (Macaca fascicularis). By combining these approaches, I explore both the proximate mechanisms of behavioral flexibility through induced innovation as well as the natural manifestations of flexibility in female foraging behavior. Together, these projects quantify inter-individual differences in foraging behavior and extractive foraging abilities, as well as the role of individual traits in those abilities. Further, these studies provide important insights on the differences in foraging strategies for individuals living in complex and uncertain environments. These insights may be important for understanding the effects of rapid human-induced environmental change and how animals cope with those changes through behavioral diversity and problem-solving.

    • 10 supplemental ZIPs
    Cover page: Behavioral Flexibility and Cognitive Performance in Macaques
    • Article
    • Peer Reviewed
    UC Davis Previously Published Works (2011)
    We address two largely overlooked, fundamental issues in computing a ranking hierarchy within a society: which information in the network is relevant, and what effect chance has on the hierarchy. To properly account for uncertainty from limited data, we construct a random field in a matrix form having entry-wise posterior Beta distributions based on a graph of pairwise conflict outcomes. To evaluate relevant network information using information transitivity, another random matrix of synthesized transitive dominance odds is computed collectively along observed dominance paths. These two matrices are coupled together to fuse both direct and indirect dominance information. An ensemble of realizations of this fused random matrix facilitates an ensemble of optimal ranking networks by means of simulated annealing. Conditional statistical inferences regarding network features are derived, manifesting the effect of uncertainty. Our computational approach is suitable for large graphs of pairwise conflict outcomes, and can accommodate tremendous data heterogeneity-a typical feature in such studies. We also demonstrate the infeasibility of the classical maximum-likelihood approach, and expose the mechanistic flaws that stem from completely ignoring relevant information residing in the graph. We analyse two real datasets of decisive conflict outcomes, the first involving college football teams, and the second involving an adult rhesus macaque society in captivity.
      Cover page: Computing a ranking network with confidence bounds from a graph-based Beta random field
      • Article
      • Peer Reviewed
      UC Davis Previously Published Works (2013)
      Studies of prosocial policing in nonhuman societies traditionally focus on impartial interventions because of an underlying assumption that partial support implies a direct benefit to the intervener, thereby negating the potential for being prosocial in maintaining social stability for the benefit of the group. However, certain types of partial interventions have significant potential to be prosocial in controlling conflict, e.g. support of non-kin subordinates. Here, we propose a policing support hypothesis that some types of agonistic support serve a prosocial policing function that maintains group stability. Using seven large captive groups of rhesus macaques, we investigated the relationship between intervention type and group-level costs and benefits (rates of trauma, severe aggression, social relocation) and individual level costs and benefits (preferential sex-dyad targeting, dominance ambiguity reduction, access to mates, and return aggression). Our results show that impartial interventions and support of subordinate non-kin represent prosocial policing as both (1) were negatively associated with group-level rates of trauma and severe aggression, respectively, (2) showed no potential to confer individual dominance benefits, (3) when performed outside the mating season, they did not increase chances of mating with the beneficiary, and (4) were low-cost for the highest-ranking interveners. We recommend expanding the definition of 'policing' in nonhumans to include these 'policing support interventions'.
        Cover page: Policing in Nonhuman Primates: Partial Interventions Serve a Prosocial Conflict Management Function in Rhesus Macaques
        • Article
        • Peer Reviewed
        UC Davis Previously Published Works (2018)
        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.
          Cover page: Social management of laboratory rhesus macaques housed in large groups using a network approach: A review
          • Article
          • Peer Reviewed
          UC Davis Previously Published Works (2024)
          For nonhuman primates living in anthropogenic areas, predation by larger predators is relatively rare. However, smaller predators, such as free-ranging as well as domesticated dogs, can shape the socioecology of urban nonhuman primates, either directly by attacking and killing them or indirectly by modifying their activity patterns. Here, we describe three (two probably fatal) cases of dog attacks on adult rhesus macaques inhabiting an anthropogenic landscape in Northern India and the circumstances surrounding these incidents. We discuss the importance of considering human presence and intervention in dog-nonhuman primate relationships while studying nonhuman primate populations across anthropogenic gradients, and its potential influences on group social dynamics and transmission of zoonotic agents.
            Cover page: Lethal dog attacks on adult rhesus macaques (Macaca mulatta) in an anthropogenic landscape.
            • Article
            • Peer Reviewed
            UC Davis Previously Published Works (2020)
            Limiting opportunities for captive nonhuman primates (NHPs) to express species-specific social behaviors may disrupt the adaptive drive for social companionship and may lead to increases in coping behaviors and inactivity. While captive NHPs show improved welfare when moving to pair-housing from single-housing, the impact of daily separation of pair-mates, as is implemented in intermittent pair-housing, is not fully understood. We compared behavioral indices of welfare exhibited by adult female rhesus macaques (Macaca mulatta) in two conditions: (1) intermittent pair-housing, involving daily overnight separation of pair-mates, and (2) continuous pair-housing, involving little separation of pair-mates. A within-subjects study design tested two groups of females experiencing both pairing conditions in an alternate order, switching either from continuous to intermittent pair-housing, or from intermittent to continuous pair-housing. Behavioral observations, recording activity state, self-directed, abnormal, and social behaviors, were conducted at midday when all females were paired, and in the afternoon when intermittent pairs were separated. Females exhibited higher levels of inactivity and self-directed behavior when separated due to intermittent pair-housing in comparison to continuous pair-housing. In addition, intermittently paired females showed higher levels of grooming and other types of affiliation when paired, than during the same time frame when they were continuously paired. These results suggest that females in the continuous presence of a social partner experience improved levels of activity and do not need to elevate levels of behavioral coping mechanisms (e.g., self-scratching, increased affiliation) as they receive the benefits associated with social companionship consistently throughout the day. Overall, this study provides the first evidence that continuous pair-housing affords better welfare than intermittent pair-housing in adult female rhesus macaques. Pair-housing options, such as continuous pairing, that reduce reliance on behavioral coping mechanisms and promote adaptive social behavior throughout the entirety of the day should be prioritized over husbandry care scheduled for convenience.
              Cover page: Improved behavioral indices of welfare in continuous compared to intermittent pair‐housing in adult female rhesus macaques (Macaca mulatta)
              • Article
              • Peer Reviewed
              UC Davis Previously Published Works (2016)
              In social animals, group living may impact the risk of infectious disease acquisition in two ways. On the one hand, social connectedness puts individuals at greater risk or susceptibility for acquiring enteric pathogens via contact-mediated transmission. Yet conversely, in strongly bonded societies like humans and some nonhuman primates, having close connections and strong social ties of support can also socially buffer individuals against susceptibility or transmissibility of infectious agents. Using social network analyses, we assessed the potentially competing roles of contact-mediated transmission and social buffering on the risk of infection from an enteric bacterial pathogen (Shigella flexneri) among captive groups of rhesus macaques (Macaca mulatta). Our results indicate that, within two macaque groups, individuals possessing more direct and especially indirect connections in their grooming and huddling social networks were less susceptible to infection. These results are in sharp contrast to several previous studies that indicate that increased (direct) contact-mediated transmission facilitates infectious disease transmission, including our own findings in a third macaque group in which individuals central in their huddling network and/or which initiated more fights were more likely to be infected. In summary, our findings reveal that an individual's social connections may increase or decrease its chances of acquiring infectious agents. They extend the applicability of the social buffering hypothesis, beyond just stress and immune-function-related health benefits, to the additional health outcome of infectious disease resistance. Finally, we speculate that the circumstances under which social buffering versus contact-mediated transmission may occur could depend on multiple factors, such as living condition, pathogen-specific transmission routes, and/or an overall social context such as a group's social stability.
                Cover page: Social buffering <i>and</i> contact transmission: network connections have beneficial and detrimental effects on <i>Shigella</i> infection risk among captive rhesus macaques.
                • Article
                • Peer Reviewed
                UC Davis Previously Published Works (2016)
                Behavior and health, including the incidence of chronic idiopathic diarrhea, can vary widely among NHP reared indoors. We hypothesized that factors during gestation account for some of the variability in chronic diarrhea risk that cannot be explained by postnatal environment, genes, or known physiologic deficits. We hypothesized that, among macaques reared indoors postnatally, outdoor housing during gestation (when the dam engaged with a large, species-typical social group) would be protective against diarrhea as compared with gestation experienced in an indoor setting. We also hypothesized that exposure to routine husbandry and veterinary care in utero would increase diarrhea rates in offspring. We built models to test the influence of specific events during pregnancy as well as their interactions with anxiety-related genotype as a way of understanding gene×environment interaction on the development of diarrhea in indoor-reared rhesus macaques. Although previous reports have suggested that rearing by the mother in an indoor environment is preferable to nursery rearing, we found that whether gestation occurred indoors (in single or pair housing) or outdoors (in a large social group) better explained the variability in diarrhea rate in our study population of indoor-reared macaques. Furthermore, the diarrhea incidence was associated with nervous temperament and serotonin transporter promoter genotype. Several significant interactions indicated that some of these effects were specific to subsets of animals. Our results demonstrate that the prenatal environment can have unexpected lasting health consequences.
                  Cover page: Effect of Indoor Compared with Outdoor Location during Gestation on the Incidence of Diarrhea in Indoor-Reared Rhesus Macaques (Macaca mulatta).
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