Veterinary Sciences

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18 pages, 925 KiB

Open AccessArticle

Investigating Stress and Coping Behaviors in African Green Monkeys (Chlorocebus aethiops sabaeus) Through Machine Learning and Multivariate Generalized Linear Mixed Models

by Brittany Roman, Christa Gallagher, Amy Beierschmitt and Sarah Hooper

Vet. Sci. 2025, 12(3), 209; https://doi.org/10.3390/vetsci12030209 - 1 Mar 2025

Viewed by 914

Abstract

Integrating behavioral and physiological assessment is critical to improve our ability to assess animal welfare in biomedical settings. Hair, blood, and saliva samples were collected from 40 recently acquired male African green monkeys (AGMs) to analyze concentrations of hair cortisol, plasma β-endorphin, and [...] Read more.

Integrating behavioral and physiological assessment is critical to improve our ability to assess animal welfare in biomedical settings. Hair, blood, and saliva samples were collected from 40 recently acquired male African green monkeys (AGMs) to analyze concentrations of hair cortisol, plasma β-endorphin, and lysozyme alongside focal behavioral observations. The statistical methodology utilized machine learning and multivariate generalized linear mixed models to find associations between behaviors and fluctuations of cortisol, lysozyme, and β-endorphin concentrations. The study population was divided into two groups to assess the effectiveness of an enrichment intervention, though the hair cortisol results revealed no difference between the groups. The principal component analysis (PCA) with a Bayesian mixed model analysis reveals several significant patterns in specific behaviors and physiological responses, highlighting the need for further research to deepen our understanding of how behaviors correlate with animal welfare. This study’s methodology demonstrates a more refined approach to interpreting these behaviors that can help improve animal welfare and inform the development of better management practices. Full article

(This article belongs to the Special Issue The Interface between Veterinary Management and Behavioral Management for Captive Nonhuman Primates)

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22 pages, 3258 KiB

Open AccessArticle

Factors That Determine Successful Social Housing of African Green Monkeys (Chlorocebus sabaeus) in Same-Sex Pairs and Trios

by Amanda M. Murti, Clive C. Wilson, Antonio F. Pemberton, Tatiana M. Corey, Loveness N. Dzikiti, John D. Elsworth and Calvin B. Carpenter

Vet. Sci. 2024, 11(12), 667; https://doi.org/10.3390/vetsci11120667 - 20 Dec 2024

Viewed by 1247

Abstract

Social housing provides a high level of enrichment for captive non-human primates, but providing this in research situations can be challenging. We have developed a multifactorial animal selection and introduction process coordinated by veterinary and animal care behavioral teams. This process sought to [...] Read more.

Social housing provides a high level of enrichment for captive non-human primates, but providing this in research situations can be challenging. We have developed a multifactorial animal selection and introduction process coordinated by veterinary and animal care behavioral teams. This process sought to successfully establish lasting same-sex pairs and trios for African green monkeys (Chlorocebus sabaeus) in studies lasting from three months to over a year. The selection and introduction process addresses variables that impact a successful grouping, including age, animal weight difference, cage size and configuration. Evaluation and consideration of these initial matchmaking parameters has favorably enhanced pairing/trio bonding. Social housing with females has been typically more successful than with males, with 90–100% of females successfully pair- or trio-housed. Successful pairs and trios exhibit multiple affiliative behaviors and demonstrate better overall health while under study, ensuring benefits both to animal welfare and study data. Full article

(This article belongs to the Special Issue The Interface between Veterinary Management and Behavioral Management for Captive Nonhuman Primates)

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12 pages, 2683 KiB

Open AccessCommunication

Collaborating for the Successful Retirement and End-of-Life Care of Non-Human Primates in Biomedical Research

by Amanda R. Maxwell, Eric K. Hutchinson, Jaclyn V. Allen, Melissa C. Painter and Lydia M. Hopper

Vet. Sci. 2024, 11(11), 560; https://doi.org/10.3390/vetsci11110560 - 12 Nov 2024

Cited by 1 | Viewed by 1369

Abstract

Research facilities have established animal adoption programs for laboratory animals. However, adoption to private owners is not an option for non-human primates (NHPs), so their post-research life presents a unique challenge. Here, we describe a collaborative effort between laboratory animal veterinarians and behavioral [...] Read more.

Research facilities have established animal adoption programs for laboratory animals. However, adoption to private owners is not an option for non-human primates (NHPs), so their post-research life presents a unique challenge. Here, we describe a collaborative effort between laboratory animal veterinarians and behavioral management staff in retiring NHPs in place to ensure their quality of life after the completion of research projects. The success of our retirement program hinges on our collaborative efforts to manage clinical diseases such as arthritis, amyloidosis, and diarrhea; to surgically ex-plant previous research hardware; and to evaluate the animals’ behavior and temperament to ensure each individual is placed in a new group or living situation in which they are likely to be successful and to have good welfare. Implementation of a quality-of-life assessment tool for all retired animals allows all staff involved in the animals’ care to proactively and periodically assess the quality of life of these animals. The successful retirement of NHPs living in social groups is rewarding for all personnel and promotes a culture of caring. Research animal retirement is an important way for us to give back and honor the contributions these animals have made to advancing medicine. Full article

(This article belongs to the Special Issue The Interface between Veterinary Management and Behavioral Management for Captive Nonhuman Primates)

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15 pages, 3037 KiB

Open AccessArticle

Social Housing of Previously Single-Caged Adult Male Cynomolgus Macaques (Macaca fascicularis)

by Fitriya N. Dewi, Permanawati, Suryo Saputro, Adinda D. Azhar, Wahyu Putriyani, Jeffrey D. Wyatt, Irma H. Suparto and Huda S. Darusman

Vet. Sci. 2024, 11(11), 538; https://doi.org/10.3390/vetsci11110538 - 1 Nov 2024

Viewed by 1460

Abstract

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 [...] Read more.

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. Full article

(This article belongs to the Special Issue The Interface between Veterinary Management and Behavioral Management for Captive Nonhuman Primates)

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13 pages, 1339 KiB

Open AccessArticle

The Effects of the Fire Hose Square Knot Browser as a Foraging Enrichment Device on the Behavior of Captive Macaca fascicularis

by Puji Rianti, Tamara M. Anisa and Huda S. Darusman

Vet. Sci. 2024, 11(11), 535; https://doi.org/10.3390/vetsci11110535 - 1 Nov 2024

Viewed by 1618

Abstract

Effective management of captive M. fascicularis (long-tailed macaques) is crucial for maintaining high-quality research models, necessitating strategies to promote their welfare. This study evaluated the impact of a foraging enrichment device, the “fire hose square knot browser”, on the behavior of 32 long-tailed [...] Read more.

Effective management of captive M. fascicularis (long-tailed macaques) is crucial for maintaining high-quality research models, necessitating strategies to promote their welfare. This study evaluated the impact of a foraging enrichment device, the “fire hose square knot browser”, on the behavior of 32 long-tailed macaques at the Primate Research Center of IPB University in Bogor, Indonesia. We observed and analyzed daily behaviors across various food types over 288 h using scan and instantaneous sampling methods. Statistical analyses, including ANOVA and Kruskal–Wallis tests, revealed significant behavioral changes in the presence of the foraging enrichment device. The foraging enrichment device notably increased eating and affiliative behaviors, while reducing resting, agonistic, and stereotypic behaviors. No significant differences in eating, auto-grooming, resting, sexual, agonistic, or stereotypic behaviors were observed between the morning and afternoon. However, mobility and affiliation behaviors varied between these periods. The highest percentage of eating behavior occurred with the enrichment foraging device and a mixture of fruits. Furthermore, a three-way non-parametric analysis suggests a significant effect of food type and treatment on behaviors such as mobility and stereotyping. These findings underscore the positive impact of foraging enrichment devices on promoting active behavior and enhancing animal welfare in captive long-tailed macaques. Full article

(This article belongs to the Special Issue The Interface between Veterinary Management and Behavioral Management for Captive Nonhuman Primates)

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14 pages, 3390 KiB

Open AccessArticle

The Interface Between Veterinary and Behavioral Management of Chimpanzees (Pan troglodytes) in a United States Sanctuary Demonstrated by Two Clinical Cases

by Raven Jackson, Rebekah Lewis and Amy Fultz

Vet. Sci. 2024, 11(11), 523; https://doi.org/10.3390/vetsci11110523 - 28 Oct 2024

Viewed by 1267

Abstract

Chimp Haven is a private, nonprofit organization that serves as the largest chimpanzee sanctuary in the world. The National Institutes of Health supports the federal sanctuary system, which is operated by Chimp Haven, to provide lifetime care for chimpanzees who have retired from [...] Read more.

Chimp Haven is a private, nonprofit organization that serves as the largest chimpanzee sanctuary in the world. The National Institutes of Health supports the federal sanctuary system, which is operated by Chimp Haven, to provide lifetime care for chimpanzees who have retired from biomedical research. Chimp Haven is home to over 300 chimpanzees, with a wide variety of individual health needs including infectious diseases. The chimpanzees live in large, mixed-sex social groups within corrals, multi-dimensional enclosures, and naturally forested habitats, which presents challenges for monitoring and balancing individual versus group needs. Primate veterinarians and animal behavior directors have an obligation to collaborate for the best possible health and welfare outcomes for the species in their care. This manuscript details how veterinarians and behavioral staff at Chimp Haven interface to enhance clinical management and improve chimpanzee welfare using two clinical cases to illustrate this relationship. This is accomplished through the development of individual care plans that include the utilization of welfare assessment metrics and positive reinforcement training programs collaboratively developed between the veterinarians and behaviorists to facilitate voluntary medical procedures without the need for social isolation. Specifically, welfare metrics such as monitoring chimpanzee wounding levels and severity, as well as targeted assessments, involve the input of both the veterinarians and behaviorists. Positive reinforcement training initiatives such as weight loss, heart health, and wound care also require the interface between the two disciplines. The authors aim to demonstrate that working together provides optimal levels of expert care for both the physical and mental health of the chimpanzees in our care. Full article

(This article belongs to the Special Issue The Interface between Veterinary Management and Behavioral Management for Captive Nonhuman Primates)

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16 pages, 3676 KiB

Open AccessArticle

Shared Accountability Shaping the Destinies of Individual and Groups of Nonhuman Primates

by Ori Pomerantz and Gregory Brion Timmel

Vet. Sci. 2024, 11(10), 486; https://doi.org/10.3390/vetsci11100486 - 9 Oct 2024

Viewed by 1258

Abstract

At the California National Primate Research Center (CNPRC), the preferred housing for rhesus macaques involves maintaining them in complex social groups outdoors, primarily for breeding purposes. This functionally appropriate environment promotes effective coping through the expression of species-typical behaviors and important aspects of [...] Read more.

At the California National Primate Research Center (CNPRC), the preferred housing for rhesus macaques involves maintaining them in complex social groups outdoors, primarily for breeding purposes. This functionally appropriate environment promotes effective coping through the expression of species-typical behaviors and important aspects of species-typical social structure, thus enabling normal animal development, higher reproductive success, and the production of high-quality biological models. Despite the benefits, social housing introduces challenges like trauma from aggressive interactions. These challenges necessitate a delicate balance between tolerating some aggression and preventing repeated targeting of individuals. Therefore, the CNPRC has established a multidisciplinary working group of behavioral management experts, veterinarians, animal care, and researchers that meets regularly to review cases of animals that may need to be removed from their social group. We discuss the criteria and decision-making processes employed to manage and mitigate aggression. We describe the systematic approach to identifying at-risk individuals and the comprehensive evaluation process that guides whether to relocate an animal from their groups or not. Considerations include the welfare of the individual and the group’s social stability. This paper provides case studies demonstrating how the working group applies these criteria and processes in practical scenarios, highlighting the complexities and challenges of such decisions. Full article

(This article belongs to the Special Issue The Interface between Veterinary Management and Behavioral Management for Captive Nonhuman Primates)

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14 pages, 3546 KiB

Open AccessCommunication

The Integration of Veterinary Medicine and Behavioral Management in the Care of Captive Pigtail Macaques (Macaca nemestrina)

by Jessica E. Toscano, Sarah A. Hart and Carolyn M. Malinowski

Vet. Sci. 2024, 11(10), 465; https://doi.org/10.3390/vetsci11100465 - 1 Oct 2024

Cited by 1 | Viewed by 1237

Abstract

The Washington National Primate Research Center (WaNPRC) maintains the largest domestic breeding colony of pigtail macaques (Macaca nemestrina) in the United States, with animals housed in small to medium-sized social groups. As part of the animal care plan, a programmatic framework [...] Read more.

The Washington National Primate Research Center (WaNPRC) maintains the largest domestic breeding colony of pigtail macaques (Macaca nemestrina) in the United States, with animals housed in small to medium-sized social groups. As part of the animal care plan, a programmatic framework is utilized, which integrates clinical care with socialization considerations for nonhuman primates (NHPs). This framework encompasses the following areas: (1) socialization in the clinical setting; (2) positive reinforcement training (PRT); (3) measures to ensure proper identification and medication distribution; and (4) in-group treatments. The success of this framework is demonstrated by the high socialization rate for hospitalized animals (99.5% social pairing success), with the majority of clinical cases (95%) being treated in social groups. Ultimately, this framework seeks to buffer stressors when animals require clinical care or husbandry manipulations. Taken together, the above components foster an environment that provides a comprehensive approach to NHP medical and behavioral management. Full article

(This article belongs to the Special Issue The Interface between Veterinary Management and Behavioral Management for Captive Nonhuman Primates)

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22 pages, 1508 KiB

Open AccessArticle

Longitudinal Baboon (Papio anubis) Neutrophil to Lymphocyte Ratio (NLR), and Correlations with Monthly Sedation Rate and Within-Group Sedation Order

by Sarah J. Neal, Steven J. Schapiro and Elizabeth R. Magden

Vet. Sci. 2024, 11(9), 423; https://doi.org/10.3390/vetsci11090423 - 11 Sep 2024

Cited by 2 | Viewed by 1063

Abstract

Neutrophil to lymphocyte ratio (NLR) is a simple marker of stress and inflammation, but there is limited research regarding NLR in nonhuman primates (NHPs), with studies showing associations with longevity, certain medical conditions, and stressful circumstances. Here, we examined baboon NLR longitudinally, and [...] Read more.

Neutrophil to lymphocyte ratio (NLR) is a simple marker of stress and inflammation, but there is limited research regarding NLR in nonhuman primates (NHPs), with studies showing associations with longevity, certain medical conditions, and stressful circumstances. Here, we examined baboon NLR longitudinally, and as a function of health parameters. We also examined whether NLR was affected by sedation rate, as well as the order of sedation within a group, given that sedation events during clinical and research practices can induce stress in NHPs. While older adult and geriatric baboon NLR did not differ longitudinally, juvenile and young adult NLR tended to increase, primarily driven by increases in females. Additionally, baboons sedated later within a group showed significantly higher NLRs than those sedated earlier in the process. However, baboons with higher sedation rates per month showed lower NLRs. These data indicate that NLR may be dysregulated in different ways as a function of different types of stress, with sedation order (i.e., acute stress) causing pathological increases in NLR, and sedation rate over time (i.e., chronic stress) causing decreases. Importantly, we propose that NLR, a routinely obtained veterinary measure, has potential utility as a welfare indicator of stress resulting from clinical and research practices, as well as a measure that can inform behavioral management practices and interventions. Full article

(This article belongs to the Special Issue The Interface between Veterinary Management and Behavioral Management for Captive Nonhuman Primates)

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12 pages, 789 KiB

Open AccessArticle

Nursery- vs. Mother-Reared Baboons: Reproductive Success and Health Parameters

by Sarah J. Neal, Steven J. Schapiro, Susan P. Lambeth and Elizabeth R. Magden

Vet. Sci. 2024, 11(9), 416; https://doi.org/10.3390/vetsci11090416 - 7 Sep 2024

Cited by 2 | Viewed by 1378

Abstract

There is a plethora of data demonstrating the deleterious consequences of nursery rearing in nonhuman primates (NHPs). However, baboon studies report varying consequences of nursery rearing, from no differences in reproduction and sociality to moderate differences in social cognition and abnormal behavior. We [...] Read more.

There is a plethora of data demonstrating the deleterious consequences of nursery rearing in nonhuman primates (NHPs). However, baboon studies report varying consequences of nursery rearing, from no differences in reproduction and sociality to moderate differences in social cognition and abnormal behavior. We compared health and reproductive parameters in a large sample (N= 231) of mother-reared (MR) and nursery-reared (NR) captive olive baboons housed at the Keeling Center for Comparative Medicine and Research, Texas. MR baboons had higher neutrophil-to-lymphocyte ratios and heart rates than NR baboons. Rearing was not a significant predictor of body condition score or body weight (p > 0.20), and MR and NR individuals did not differ in the level of wounding observed (p > 0.70). The proportion of successful births across NR and MR females was also not significantly different (p > 0.70), nor were rates of maternal neglect and infant death. These data suggest minimal differences in health and reproductive parameters across rearing statuses in baboons housed at this facility. In conjunction with previous research that also seems to show minimal differences as a function of rearing in baboons, but directly contrast with data in other NHP species, these data suggest that baboons may be more robust against deleterious effects of abnormal rearing conditions than other NHP species. Full article

(This article belongs to the Special Issue The Interface between Veterinary Management and Behavioral Management for Captive Nonhuman Primates)

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15 pages, 1845 KiB

Open AccessArticle

The Role of Behavioral Management in Enhancing Clinical Care and Efficiency, Minimizing Social Disruption, and Promoting Welfare in Captive Primates

by Scott H. Oppler, Sierra D. Palmer, Sydney N. Phu and Melanie L. Graham

Vet. Sci. 2024, 11(9), 401; https://doi.org/10.3390/vetsci11090401 - 1 Sep 2024

Cited by 4 | Viewed by 2231

Abstract

Medical procedures necessary for routine care can induce stress in both the veterinary and human clinical situations. In the research environment, nonhuman primates undergo procedures like physical examination, blood sampling, and intravenous drug or fluid administration either as a part of routine veterinary [...] Read more.

Medical procedures necessary for routine care can induce stress in both the veterinary and human clinical situations. In the research environment, nonhuman primates undergo procedures like physical examination, blood sampling, and intravenous drug or fluid administration either as a part of routine veterinary care or during the modeling of clinical disease and interventions under study. Behavioral management techniques, such as training for cooperation, allow caregivers to train primates to voluntarily engage in various medical procedures. This approach reduces stress and anxiety associated with necessary procedures, thereby enhancing efficiency and minimizing the invasiveness of medical care. Consequently, veterinary evaluation and care can be provided without compromise, resulting in enhanced clinical outcomes and overall better health. In this study, we explored the impact of the behavioral management program implemented at our center on a subset of animals undergoing routine veterinary care, focusing on the overall experience, including animal welfare, scientific rigor, and efficiency in terms of economics and time. We investigated its impact on key factors, such as the total procedure and recovery time, incidence of side effects, and welfare indicators, revealing a significant positive influence on animal care. Furthermore, through case studies, we illustrate how behavioral management facilitates timely medical care and monitoring, effectively mitigating stressors that could otherwise impair health and welfare, enabling the provision of care that would have otherwise been unachievable. A thoughtfully designed primate behavioral management program, integrating cooperation and participation with veterinary care, forms the cornerstone of superior animal welfare, enhanced clinical care, and more accurate scientific outcomes. Full article

(This article belongs to the Special Issue The Interface between Veterinary Management and Behavioral Management for Captive Nonhuman Primates)

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Review

Jump to: Research

13 pages, 1956 KiB

Open AccessReview

Refinements in Clinical and Behavioral Management for Macaques on Infectious Disease Protocols

by Lauren Drew Martin, Jaclyn Shelton, Lisa A. Houser, Rhonda MacAllister and Kristine Coleman

Vet. Sci. 2024, 11(10), 460; https://doi.org/10.3390/vetsci11100460 - 1 Oct 2024

Viewed by 1270

Abstract

Providing optimal clinical and behavioral care is a key component of promoting animal welfare for macaques and other nonhuman primates (NHPs) in research. This overlap between critical areas of management is particularly important for NHPs on infectious disease protocols, which often have unique [...] Read more.

Providing optimal clinical and behavioral care is a key component of promoting animal welfare for macaques and other nonhuman primates (NHPs) in research. This overlap between critical areas of management is particularly important for NHPs on infectious disease protocols, which often have unique challenges. For example, traditionally these NHPs were often housed alone, which can have behavioral and clinical consequences. However, in the past decade or so, considerable effort has been directed at modifying procedures in an effort to improve animal welfare for this group of NHPs. In this review, we examine some refinements that can positively impact the clinical and behavioral management of macaques on infectious disease studies, including increased social housing and the use of positive reinforcement techniques to train animals to cooperate with procedures such as daily injections or awake blood draws. We also discuss ways to facilitate the implementation of these refinements, as well as to identify logistical considerations for their implementation. Finally, we look to the future and consider what more we can do to improve the welfare of these animals. Full article

(This article belongs to the Special Issue The Interface between Veterinary Management and Behavioral Management for Captive Nonhuman Primates)

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