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Husbandry of Non-Human Primates in Breeding and Research: Latest Insights...
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Husbandry of Non-Human Primates in Breeding and Research: Latest Insights and Developments

A special issue of Biology (ISSN 2079-7737). This special issue belongs to the section "Zoology".

Deadline for manuscript submissions: closed (31 March 2022) | Viewed by 14087

Special Issue Editor

Prof. Dr. Jan A.M. Langermans

E-Mail Website1 Website2
Guest Editor
1. Chairman Animal Science Department & Deputy Director, P.O. Box 3306, 2280 GH Rijswijk, The Netherlands
2. Department Population Health Sciences, Veterinary Faculty, Utrecht University, 8, 3584 CS Utrecht, The Netherlands
Interests: stress responses in NHP, e.g., stereotypic behavior and how to prevent this; enrichment and assessment of optimal enrichment programs; training programs for NHP to cooperate with procedures; breeding activities, e.g., F2 generation (Europe) and weaning procedures; breeding of transgenic NHP: requirements and ethics

Special Issue Information

Dear Colleagues,

The use of NHP in scientific research is a sensitive issue and an important topic on the EU political agenda. In EU Directive 2010/63 on the Protection of Animals used for Scientific Purposes, specific restrictions for the use of non-human primates (NHP) for biomedical research purposes were introduced. Although the ultimate aim is to phase out the use of these highly sentient and social animals, it is recognized that a ban on their use is not feasible in the foreseeable future. Non-human primates are still important for the promotion of human health, as also demonstrated by the current SARS-CoV-2 research programs, and play a critical role in the advancement of various areas in the biomedical field. They also contribute to our general knowledge of processes underlying normal situations and disease processes. Captive NHP are also regularly used in (non-invasive) behavioral research. With their use for the advancement of science also comes our obligation to treat them in the best way possible. This includes optimal housing and care procedures, as well as implementation and consequences of technological advancements and the latest scientific insights and developments. Optimal housing and care are not only important for ethical and moral reasons but also have scientific merit.

This Special Issue will focus on the optimization of primate husbandry, care, and technology and discuss the current insights and developments. This includes a variety of topics, including training, breeding, and housing procedures (including genetically-altered NHP), veterinary care, and animal training to cooperate with procedures.

Prof. Dr. Jan A.M. Langermans
Guest Editor

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Biology is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • enrichment
  • weaning
  • housing facilities: new insights
  • breeding concepts
  • stress and stereotypic behavior prevention
  • ethics
  • transgenic NHP

Published Papers (6 papers)

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Research

19 pages, 929 KiB  
Article
The Older the Better: Infanticide Is Age-Related for Both Victims and Perpetrators in Captive Long-Tailed Macaques
by Karlijn Gielen, Annet L. Louwerse and Elisabeth H. M. Sterck
Biology 2022, 11(7), 1008; https://doi.org/10.3390/biology11071008 - 4 Jul 2022
Viewed by 2338
Abstract
In wild primates, infanticide is a risk that is especially prevalent when a new male takes over the alpha position. Insight into risk factors related to infanticide may decrease the incidence of infanticide in captivity during male introductions. We investigated several risk factors [...] Read more.
In wild primates, infanticide is a risk that is especially prevalent when a new male takes over the alpha position. Insight into risk factors related to infanticide may decrease the incidence of infanticide in captivity during male introductions. We investigated several risk factors of infanticide derived from hypotheses explaining infanticide in the wild and tested this in captive long-tailed macaques (Macaca fascicularis) using demographic data spanning a 25.5-year period. Factors that are related to infanticide in the wild explained a large proportion, but not all incidences, of infanticide in captivity. Consistent with the wild data, infants young enough to decrease the interbirth interval (<215 days) were at risk of being killed. In contrast to studies from the wild, infanticidal males were more than 2.5 years younger than non-infanticidal males. This indicates that captive settings can lead to new risks since relatively young males may gain the alpha position, promoting infanticide. Therefore, we propose the adolescent male risk hypothesis as a captive risk factor in which subadult males pose a risk of infanticide. In conclusion, the ages of both males and infants are related to infanticide in captivity and have to be taken into account during male introductions. Full article
(This article belongs to the Special Issue Husbandry of Non-Human Primates in Breeding and Research: Latest Insights and Developments)
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18 pages, 10127 KiB  
Article
Factors Associated with Injury Rate and Pregnancy Success in Rhesus Macaques
by David A. Massey, Faye Peters, Jim Willshire and Claire L. Witham
Biology 2022, 11(7), 979; https://doi.org/10.3390/biology11070979 - 28 Jun 2022
Viewed by 1413
Abstract
Fight injuries are a major welfare concern in group-housed rhesus macaques. This is particularly a problem in breeding groups. We investigated which factors might affect the injury rate in group-housed macaques and also looked at how the same factors might affect productivity. We [...] Read more.
Fight injuries are a major welfare concern in group-housed rhesus macaques. This is particularly a problem in breeding groups. We investigated which factors might affect the injury rate in group-housed macaques and also looked at how the same factors might affect productivity. We analysed 10 years of health records at a breeding colony in which monkeys were kept in small breeding groups consisting of a single adult male and 2–13 females and their offspring or single-sex juvenile groups. We found that females over the age of 2.5 years in breeding groups were the most likely to be injured. We focused on these females and used generalised mixed-effect models to examine which factors affected the injury rate and their productivity (probability of getting pregnant). The biggest risk factor for injury was the introduction of a new adult male to a breeding group. However, this also produced a large increase in the proportion of females that became pregnant, suggesting that there may be a trade-off between the risk of injury and the productivity. We also found that females in large groups with a young breeding male had a very high risk of injury. We recommend keeping young breeding males (<7 years) in smaller groups. Full article
(This article belongs to the Special Issue Husbandry of Non-Human Primates in Breeding and Research: Latest Insights and Developments)
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12 pages, 1052 KiB  
Article
Multigenerational Social Housing and Group-Rearing Enhance Female Reproductive Success in Captive Rhesus Macaques (Macaca mulatta)
by Astrid Rox, Sophie Waasdorp, Elisabeth H. M. Sterck, Jan A. M. Langermans and Annet L. Louwerse
Biology 2022, 11(7), 970; https://doi.org/10.3390/biology11070970 - 27 Jun 2022
Cited by 2 | Viewed by 1661
Abstract
To optimize costs and reproductive success, rhesus macaques in biomedical primate research facilities are often peer-reared. Older, dependent infants are typically removed from their natal group to enhance female reproduction. The minimal husbandry age-norm of infant removal is ten months. These practices deviate [...] Read more.
To optimize costs and reproductive success, rhesus macaques in biomedical primate research facilities are often peer-reared. Older, dependent infants are typically removed from their natal group to enhance female reproduction. The minimal husbandry age-norm of infant removal is ten months. These practices deviate from species-specific behavior and may reduce welfare, suggesting a trade-off between female reproduction and welfare. However, the effect of breeding group type and rearing history on female reproductive success (i.e., birth rate; inter-birth interval (IBI); offspring survival) is unclear. This retrospective study investigated whether group type (i.e., peer groups versus multigenerational groups) and rearing history (i.e., peer- or hand-reared; group-reared with peer- or hand-reared mother; group-reared) affected female reproductive success in captive rhesus macaques. Data on female reproduction between 1996 and 2019 were collected at the Biomedical Primate Research Centre, Rijswijk. Birth rates were higher in multigenerational breeding groups than in peer groups. Moreover, group-reared females had higher offspring survival than peer- or hand-reared females. IBI was not affected by breeding group type or female rearing history. However, females in both peer and multigenerational breeding groups typically conceived earlier after giving birth than the husbandry infant removal age-norm of ten months. Thus, infant removal at an age of ten months does not enhance a female’s reproduction. Altogether, female reproduction and non-human primate welfare can simultaneously be optimized through multigenerational breeding groups and group-rearing. Full article
(This article belongs to the Special Issue Husbandry of Non-Human Primates in Breeding and Research: Latest Insights and Developments)
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19 pages, 9208 KiB  
Article
Behavioral Management as a Coping Strategy for Managing Stressors in Primates: The Influence of Temperament and Species
by Sierra Palmer, Scott Hunter Oppler and Melanie L. Graham
Biology 2022, 11(3), 423; https://doi.org/10.3390/biology11030423 - 10 Mar 2022
Cited by 7 | Viewed by 2860
Abstract
Primates involved in biomedical research experience stressors related to captivity, close contact with caregivers, and may be exposed to various medical procedures while modeling clinical disease or interventions under study. Behavioral management is used to promote behavioral flexibility in less complex captive environments [...] Read more.
Primates involved in biomedical research experience stressors related to captivity, close contact with caregivers, and may be exposed to various medical procedures while modeling clinical disease or interventions under study. Behavioral management is used to promote behavioral flexibility in less complex captive environments and train coping skills to reduce stress. How animals perceive their environment and interactions is the basis of subjective experience and has a major impact on welfare. Certain traits, such as temperament and species, can affect behavioral plasticity and learning. This study investigated the relationship between these traits and acquisition of coping skills in 83 macaques trained for cooperation with potentially aversive medical procedures using a mixed-reinforcement training paradigm. All primates successfully completed training with no significant differences between inhibited and exploratory animals, suggesting that while temperament profoundly influences behavior, training serves as an important equalizer. Species-specific differences in learning and motivation manifested in statistically significant faster skill acquisition in rhesus compared with cynomolgus macaques, but this difference was not clinically relevant. Despite unique traits, primates were equally successful in learning complex tasks and displayed effective coping. When animals engage in coping behaviors, their distress decreases, improving welfare and reducing inter- and intra- subject variability to enhance scientific validity. Full article
(This article belongs to the Special Issue Husbandry of Non-Human Primates in Breeding and Research: Latest Insights and Developments)
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20 pages, 4057 KiB  
Article
Quantitative Rapid Test for Detection and Monitoring of Active Pulmonary Tuberculosis in Nonhuman Primates
by Zijie Zhou, Anouk van Hooij, Richard Vervenne, Claudia C. Sombroek, Elisa M. Tjon Kon Fat, Tom H. M. Ottenhoff, Paul L. A. M. Corstjens, Frank Verreck and Annemieke Geluk
Biology 2021, 10(12), 1260; https://doi.org/10.3390/biology10121260 - 2 Dec 2021
Cited by 2 | Viewed by 2052
Abstract
Nonhuman primates (NHPs) are relevant models to study the pathogenesis of tuberculosis (TB) and evaluate the potential of TB therapies, but rapid tools allowing diagnosis of active pulmonary TB in NHPs are lacking. This study investigates whether low complexity lateral flow assays utilizing [...] Read more.
Nonhuman primates (NHPs) are relevant models to study the pathogenesis of tuberculosis (TB) and evaluate the potential of TB therapies, but rapid tools allowing diagnosis of active pulmonary TB in NHPs are lacking. This study investigates whether low complexity lateral flow assays utilizing upconverting reporter particles (UCP-LFAs) developed for rapid detection of human serum proteins can be applied to detect and monitor active pulmonary TB in NHPs. UCP-LFAs were used to assess serum proteins levels and changes in relation to the MTB challenge dosage, lung pathology, treatment, and disease outcome in experimentally MTB-infected macaques. Serum levels of SAA1, IP-10, and IL-6 showed a significant increase after MTB infection in rhesus macaques and correlated with disease severity as determined by pathology scoring. Moreover, these biomarkers could sensitively detect the reduction of bacterial levels in the lungs of macaques due to BCG vaccination or drug treatment. Quantitative measurements by rapid UCP-LFAs specific for SAA1, IP-10, and IL-6 in serum can be utilized to detect active progressive pulmonary TB in macaques. The UCP-LFAs thus offer a low-cost, convenient, and minimally invasive diagnostic tool that can be applied in studies on TB vaccine and drug development involving macaques. Full article
(This article belongs to the Special Issue Husbandry of Non-Human Primates in Breeding and Research: Latest Insights and Developments)
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15 pages, 1975 KiB  
Article
Effect of Housing Conditions on Cortisol and Body Fat Levels in Female Rhesus Macaques
by Dian G. M. Zijlmans, Lisette Meijer, Marit K. Vernes, Jacqueline A. M. Wubben, Linda Hofman, Annet L. Louwerse, Elisabeth H. M. Sterck, Jan A. M. Langermans and Marieke A. Stammes
Biology 2021, 10(8), 744; https://doi.org/10.3390/biology10080744 - 3 Aug 2021
Cited by 2 | Viewed by 2579
Abstract
Macaques are among the most commonly used non-human primates in biomedical research. They are highly social animals, yet biomedical studies often require group-living animals to be pair-housed in a controlled environment. A change in environment causes only short-term stress in adapting individuals, while [...] Read more.
Macaques are among the most commonly used non-human primates in biomedical research. They are highly social animals, yet biomedical studies often require group-living animals to be pair-housed in a controlled environment. A change in environment causes only short-term stress in adapting individuals, while non-adapting animals may experience long-term stress that can adversely affect study results. Individuals likely differ in their ability to adapt depending on individual characteristics. Changes in cortisol and body fat levels may reflect these different individual responses. Here, we investigate the long-term effect of a change from group- to pair-housing on cortisol and body fat levels in 32 female rhesus macaques, exploring whether age, dominance rank, original cortisol, and body fat levels are related to long-term stress in pair-housing. Hair samples were analyzed for cortisol levels, while anthropometric measurements and computed tomography were performed to quantify body fat. Monkeys served as their own control with a 7.5-month period between the measurements. Cortisol levels increased, while average body fat levels did not differ when individuals were moved from group- to pair-housing. Cortisol and body fat levels were not significantly correlated. Changes in cortisol were independent of age and dominance rank, whereas individual variation in body fat alterations was related to the group-housed body fat level and dominance rank. Although this study did not identify individual characteristics related to long-term stress in pair-housing, the individual variation confirms that some individuals are more resilient to change than others and provides possibilities for future refinement studies. Full article
(This article belongs to the Special Issue Husbandry of Non-Human Primates in Breeding and Research: Latest Insights and Developments)
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