Skip to content

Environmental Enhancement Plan for Non-Human Primates

In accordance with the Animal Welfare Act (AWA) (see regulation section in references) each animal facility that houses nonhuman primates must have a Plan for Environmental Enhancement to Promote the Psychological Well-Being of Nonhuman Primates. The primary goal of the UW WaNPRC plan is to meet or exceed the AWA regulations and to incorporate the recommendations of the Guide for the Care and Use of Laboratory Animals regarding the implementation of environmental enhancement and enrichment and the promotion of psychological well-being (PWB).

This plan includes the following key components: exemptions and special considerations, social housing, nonsocial environmental enrichment, detection and treatment of atypical and abnormal behaviors, acclimation, primate training, restraint, and personnel training. This plan has been developed by WaNPRC’s Behavioral Management Services (BMS) and Veterinary Services (VS) along with the Attending Veterinarian and the Institutional Animal Care and Use Committee (IACUC) at the University of Washington. It pertains to all NHPs housed at the WaNPRC facilities in both WA and AZ. This plan is in accord with currently accepted professional standards as cited in professional journals and reference guides, and as directed by the Attending Veterinarian.

Throughout this document, the term ’Attending Veterinarian’ includes any veterinarian to whom the Attending Veterinarian of the University of Washington has delegated authority to perform professional judgments required by the plan.

A. Exemptions from the Environmental Enhancement (EE) Plan

Although no animals can be exempted from the entire Environmental Enhancement Plan, some individuals may be exempted from participating in part of the plan.

There are two types of exemptions: veterinary and scientific.

Veterinary: Animals can be exempted by the Attending Veterinarian because of health or condition, or in other considerations of their well-being. These exemptions will be noted in the animal’s record and disseminated by the veterinarians to animal resources staff via approved communication methods.

Scientific: Scientific exemptions from any portion of the EE Plan must be approved by the IACUC. These exemptions must be requested and justified by the Investigator (PI) as a husbandry exception in their research protocol via the Office of Animal Welfare’s (OAW) Hoverboard website. The IACUC must review and approve the protocol before exemptions are implemented and annually thereafter. WaNPRC staff will refer to Hoverboard to determine whether research exemptions are allowed on a protocol.

The IACUC has a policy regarding prolonged physical restraint. If temporary restraint is used to perform a procedure, that is included in the procedure description in the IACUC protocol in Hoverboard. Any prolonged restraint is described in a specific restraint procedure in the protocol and must be scientifically justified and approved by the IACUC.

B. Special Considerations

Animal welfare regulations require special consideration regarding environmental enhancement to be provided to several classifications of animals.

  1. Infants and young juveniles
  2. Those that show signs of being in psychological distress through behavior or appearance
  3. Those used in research for which the Committee-approved protocol requires restricted activity
  4. Individually housed nonhuman primates that are unable to see and hear NHPs of their own or compatible species

Special psychological well-being considerations of infants and young juveniles are outlined in WaNPRC Standard Operating Procedures. When possible, infants will be housed with their dam or a foster. When that is not possible, infants will be socialized with conspecifics. Infants and juveniles are provided with enrichment appropriate for their age and health status.

Extra environmental enrichment for animals that are singly housed or behaviorally sensitive is provided three times per week in addition to standard daily enrichment. (See Section D).

Animals that are assigned to a research protocol requiring restricted activity are provided the enrichment approved in the protocol.

WaNPRC minimizes situations in which NHPs are unable to see and hear nonhuman primates of their own or a compatible species. The AV, BMS and Vet staff will confer about any special circumstances requiring animals to be housed in this condition, and these animals will receive extra enrichment as outlined in relevant SOPs. Animals will not be housed in this condition for more than 24 hours without the official approval of the AV.

C. Social Housing

The importance of social housing has been emphasized in the Guide for The Care and Use of Laboratory Animals, and the Animal Welfare Act regulations state: “The environment enhancement plan must include specific provisions to address the social needs of nonhuman primates of species known to exist in social groups in nature. Such specific provisions must be in accordance with currently accepted professional standards, as cited in appropriate professional journals or reference guides, and as directed by the attending veterinarian.” In the wild, all species of NHPs housed at the WaNPRC typically live in social groups (see social section in references). In these groups they form intricate relationships, and they spend a great deal of time engaged in social behaviors. In captivity, social contact provides the opportunity for animals to express these species-typical behaviors including social grooming and play.

Animal welfare regulations, guidelines, and published research studies therefore concur that social housing of nonhuman primates improves their psychological well-being. The presence of chronic psychological distress adversely impacts animal welfare and may result in inaccurate research data and increase the number of animals required for biomedical research. Many nonhuman primates used in biomedical research can be socially housed without compromising the validity of these studies. For projects requiring social housing restrictions due to study design, scientific exemptions must be approved by the IACUC. The WaNPRC has adopted the best practices that all NHPs that are not officially exempted should be housed socially and that every effort will be made by animal resources staff to provide social contact to non-exempt animals. The definition of social housing used in this document is two or more animals housed in the same space including in an enclosure or in fully connected housing units. WaNPRC does not consider a lack of caging sufficient reason to singly house an animal.

BMS staff will implement the WaNPRC Socialization Program. Socialized animals will be regularly assessed by BMS staff during standardized behavioral and social monitoring as well as hierarchy rankings for breeding groups. Whenever possible, social pairs/groups will be kept together when moved within the WaNPRC and/or assigned to projects. BMS staff provide input prior to project assignment to facilitate this process.

Compatibility: Social aggression or other potential compatibility concerns will be reported to BMS for assessment. Whenever possible, strategies for ameliorating social incompatibility will be employed by BMS, including but not limited to: cooperative feed training, managing social hierarchies to minimize aggression, and with the collaboration of veterinary staff and the PI, birth control to allow mixed- sex pairings. Birth control options may include injectable birth control, vasectomy, castration, tubal ligation, or hysterectomy. Protected contact may be used to initially assess social compatibility. Protected contact used in lieu of full-contact requires an exemption but may be pursued on a case-by-case basis for animals that have otherwise limited social options or a history of incompatibility in full contact. In some cases, animals who have been previously compatible may be deemed incompatible after assessment, and thus require new social partners as outlined in relevant SOPs.

Exemptions: Exemptions from social housing may be granted for scientific and/or veterinary reasons as previously mentioned. Exemptions for scientific reasons must be for the shortest period possible given the research protocol and can only be obtained through justification and approval by the IACUC. Research restrictions are not considered veterinary exemptions and thus must go through the IACUC approval process. All research exemptions are reviewed by a veterinarian, BMS, and the IACUC prior to the start of a project, when amendments are submitted, or when EE exceptions are reviewed.

Veterinary exemptions can be authorized by the Attending Veterinarian (AV), or a veterinarian designated by the AV, for reasons such as repeated incompatibility, extreme age, debilitation, or a clinical concern. The Associate Director of Animal Resources and BMS staff meet monthly to review social exemptions and the socialization action plans for singly housed animals. This information is then submitted to the AV each month. Veterinary exemptions are reviewed by the Attending Veterinarian at least every 30 days in ARMS and are recorded in a monthly report. A complete description of social housing exemptions is contained in relevant SOPs.

Exemptions may not be implemented outside the formal scientific or veterinary approval process. It is the expectation of WaNPRC that if an animal is not exempt from socialization that socialization attempts will proceed.

Animals officially exempt from social housing will receive extra nonsocial environmental enrichment as outlined in relevant SOPs and section D below

D. Nonsocial Environmental Enrichment

Manipulanda, Devices, and Structural enrichment: A variety of items can be used to provide environmental enrichment for nonhuman primates (see enrichment section in references). The housing unit of each NHP is enriched with a perch, toy, and an external enrichment device. Perches allow for the use of vertical space and allow animals to have various levels of view. They are positioned at an appropriate height to allow the animal to attain an upright posture while sitting on the perch. Toys allow for manipulation and play and may be used in species typical display behavior. External enrichment is used to provide stimulation and prolong engagement. Such devices include foraging devices (standard), and other manipulable devices such as mirrors, computer tablets, etc. Singly housed or behaviorally sensitive animals receive an extra enrichment device. It is the responsibility of husbandry staff to ensure these minimums are met unless otherwise officially exempted for veterinary or scientific reasons. Enrichment is rotated every two weeks when the housing units are cleaned and changed unless more frequent rotation is prescribed by BMS for behavioral reasons.

Animals that are housed in pens or compounds will be provided with perches and/or large structures for climbing and perching, as well as floor barrels or other visual barriers that provide animals the opportunity for respite from conspecifics. At least one toy for every two animals is also provided. Climbing ropes and other structures are regularly inspected and replaced as needed. Since primates spend a considerable proportion of time foraging in the wild, animals in the indoor group pens are provided with foraging opportunities such as a floor substrate (hay, straw, sawdust, wood wool, wood shavings, alfalfa etc.) through which they may forage.

Daily Enrichment: All animals will be given daily enrichment in the form of food treats, foraging opportunities, or other destructible enrichment such as paper.

Standard daily food enrichment includes a wide variety of dry goods and produce. Composition and distribution of food enrichment is governed by the WaNPRC SOPs. BMS is responsible for ordering for enrichment and husbandry staff are responsible for disbursement unless the approved research protocol specifies that PI staff will provide the enrichment. Foraging enrichment provides opportunities for extra manipulation and prolonged consumption time thus providing additional mental stimulation.

Foraging enrichment includes, but is not limited to complex produce or browse, frozen items, food frozen inside of toys or paper products, and the provisioning of foraging devices.

Other destructible enrichment may include wood, pinecones, paint rollers, or paper items such as shredded paper, paper tubes, souffle cups, lunch sacks, etc.

Sensory Enrichment: Sensory enrichment is provided at least weekly through use of music, TVs, browse, scents, and other multi-sensory options outlined in relevant SOPs.

Extra Enrichment: For singly housed animals and/or those that are flagged by BMS for behavioral sensitivity, extra enrichment is provided three times per week in addition to enrichment provided daily. If possible, additional cage space or activity cage rotation may be provided. BMS staff will be responsible for scheduling rotations through activity cages and will work with husbandry staff on ensuring that extra enrichment is distributed.

Daily, Sensory, and Extra Enrichment is provided according to the schedules created and posted by BMS. Alterations to the schedule must be approved by BMS. Documentation of daily enrichment and extra enrichment is recorded on the Enrichment Calendars which are created and posted outside every animal room by BMS. This documentation will be scanned and retained by BMS per standard WaNPRC retention schedules. If an approved research protocol dictates that researchers are to provide their own enrichment, it is their responsibility to document enrichment for each research animal and to provide these documents for inspection by regulatory agencies.

Additional Enrichment as therapeutic intervention: Specific enrichment items may be designated as a therapeutic intervention (see section E).

Novel Enrichment: Novel enrichment requires approval before being ordered, implemented, and tested for safety and efficacy. For novel food, Vet Staff (and if applicable, the PI) are consulted. For novel toys, structural enrichment, sensory enrichment or enrichment devices, approval is required from senior leadership and the WaNPRC Caging and Enrichment Committee. The Caging and Enrichment Committee consists of animal resources (including husbandry, BMS and veterinary members), and facilities staff, with PI participation as needed. Novel enrichment may be approved for testing as is or may require modifications. Novel items, once approved, are initially tested with a subset of animals while BMS conducts safety and efficacy observations. Any concerns observed by other animal resources or PI staff are to be reported immediately to BMS and veterinary staff so appropriate action can be taken to address those concerns.

Exemptions: As with social exemptions, exemptions from enrichment may be granted for scientific and/or veterinary reasons. BMS staff oversee the implementation of the EE Plan and will work with PIs on options that may suit their needs while maintaining the goals of the enrichment plan. Exemptions may not be implemented outside the formal scientific or veterinary approval processes. All research exemptions are reviewed by a veterinarian, BMS, and the IACUC prior to the start of a project, when amendments are submitted, or when EE exceptions are reviewed.

E. Detection and Treatment of Atypical and Abnormal Behaviors

All animals at the WaNPRC are monitored by BMS through standardized quantitative and qualitative methods. Standardized monitoring occurs monthly and biannually, and includes species-typical behaviors, social behaviors as well as atypical or abnormal behaviors. Other personnel working with the animals are trained by BMS to identify and report atypical and/or abnormal behaviors as well. BMS staff review these referrals, conduct behavioral assessments and if necessary, implement an individualized therapeutic treatment plan, consulting PI staff and veterinarians as needed.

Therapeutic treatment plans may involve socialization, movement to another room or within the room, changes in group composition, extra housing space, positive reinforcement training, extra enrichment, or other options. For behavior cases requiring pharmaceutical intervention, BMS will collaborate on a treatment plan with the facility veterinarian and the PI staff. In addition, veterinary staff may prescribe additional treatment plans.

Prophylactic medications will be requested by BMS on a case-by-case basis for behaviorally sensitive animals prior to exposure to a known stressor such as relocation. Such requests require approval by the facility veterinarian and the PI. If prophylactic medication for behaviorally sensitive animals is initiated by the facility veterinarian or the PI, BMS will be kept informed.

During biannual monitoring (or during biannual tb testing and clinical exams), animals will be scored for the presence and extent of alopecia. If significant alopecia (defined in our alopecia scoring methods) is present, BMS will assess and if necessary, implement a therapeutic treatment plan and/or refer to vet staff for an additional clinical evaluation. Additional alopecia scoring may be conducted as needed.

F. Primate Training Program

The BMS Primate Training Program was established to help promote the well-being and safety of nonhuman primates, reduce the need for chemical restraint, and enhance the safety of staff. Positive reinforcement training (PRT) is the expectation for all staff at WaNPRC. Participation in the Primate Training Program is included in staff job descriptions and is part of the WaNPRC standards of animal handling and interactions.

In addition to the published stress-reducing benefit of cooperative participation, animal training bolsters enrichment programs by providing positive human-animal interactions, increasing mental stimulation, expanding behavioral repertoires, and increasing activity (see training section in references).

The BMS Primate Trainers teach PRT techniques to research and animal resources staff in order to help them train NHPs to cooperate in research, clinical, husbandry and behavioral management processes. Training requests may be submitted via an online form that is available to all personnel within WaNPRC.

Staff must be deemed proficient in individual PRT techniques/tasks by BMS before proceeding to train primates or other staff members. Once affirmed, proficient staff will be responsible for tracking the training proficiency of the animals or staff they are directly teaching.

G. Acclimation

Social separation and relocation can affect both psychological well-being and research results. Wherever possible, animals will be provided with a minimum of 1 week acclimation time to a new housing environment before any new invasive research procedures will be implemented. This allows them time to acclimate to the new environment. Because unstressed animals provide better data, this benefits the research as well. This policy is further outlined in the relevant SOPs. Veterinarians can grant exceptions for reduced acclimation time.

H. Restraint

If physical restraint must be used it should be for the shortest period necessary. Restraint devices should not be used simply as a convenience, and alternatives to restraint must be considered. The use of restraint must be justified and approved by the IACUC. Animals new to restraint devices will receive positive reinforcement training per the BMS Primate Training Program to adapt to the equipment and personnel. Animals who fail to adapt will be removed from the study. Personnel who are involved in the study will be trained regarding the purpose of the restraint and its duration as outlined in the approved research protocol and any relevant WaNPRC SOPs.

For frequent but minor non-painful procedures (as deemed by IACUC), short term restraint may be less stressful than repeated sedation. In these situations, restraint devices such as a tabletop restraint device (TTRD) or procedure cage may be utilized. Procedures may be done in the home cage only if the animal is trained to voluntarily participate in the procedure. Animals will be acclimated to a restraint device through positive reinforcement methods as taught by the Primate Trainers, other qualified BMS staff or staff that have met the proficiency criteria designated by BMS.

I. Personnel Training

All personnel who will be entering an animal housing or testing room unescorted will receive training from BMS personnel. Training will include the Environmental Enhancement plan, appropriate interaction with NHPs, environmental enrichment implementation, how to identify and report abnormal or atypical behaviors, positive reinforcement training techniques and expectations, as well as the behavioral ecology of the species housed at the WaNPRC.

J. References

References

  • USDA/APHIS. Animal Welfare Regulations. 2010. CFR 9, Chapter 1, Part 3, Subpart D, Section 3.81. Animal Welfare Act.
  • National Research Council (U.S.) 2011. Committee for the Update of the Guide for the Care and Use of Laboratory Animals. & Institute for Laboratory Animal Research (U.S.). Guide for the Care and Use of Laboratory Animals, xxv, 220 p. National Academies Press, Washington, D.C.

  • Albers PCH, De Vries H. 2001. Elo-rating as a tool in the sequential estimation of dominance strength. Animal Behaviour, 61(2): 489-495.
  • Baker KC, Bloomsmith MA, Oettinger B, Neu K, Griffis C, Schoof V, Maloney M. 2012. Benefits of pair housing are consistent across a diverse population of rhesus macaques. Appl Anim Behav Sci. 137(3-4): 148-156.
  • Baker KC, Crockett CM, Lee GH, Oettinger BC, Schoof V, Thom JP. 2012. Pair housing for female longtailed and rhesus macaques in the laboratory: behavior in protected contact versus full contact. J Appl Anim Welf Sci. 15: 126-43.
  • Baker KC, Bloomsmith MA, Oettinger B, Neu K, Griffis C, Schoof V. 2014. Comparing options for pair housing rhesus macaques using behavioral welfare measures. Am J Primatol. 76(1): 30-42.
  • Baker K, Bloomsmith M, Coleman K, Crockett C, Lutz C, McCowan B, Pierre P, Weed J, Worlein J. 2017. The Behavioral Management Consortium: A partnership in promoting consensus and best practices. Pp 9-23 in the Handbook of Primate Behavioral Management, CRC Press, New York, Steve Schapiro (Ed).
  • Bellanca RU, Crockett CM. 2002. Factors predicting increased incidence of abnormal behavior in male pigtailed macaques. Am J Primatol. 58(2): 57-69.
  • Bellanca RU, Koberstein DR, Delio PJ, Kelley ST, Crockett CM. 2006. Successful introduction of Macaca nemestrina infants to their mothers after cesarean delivery. J Am Assoc Lab Anim Sci. 45(3): 27-32.
  • Briffa M, Hardy IC, Gammell MP, Jennings DJ, Clarke DD, Goubault M. 2013. Analysis of animal contest data. Pp. 47-85 in Animal Contests. Cambridge University Press. Hardy ICW, Briffa M, (Eds).
  • Buchanan-Smith HM. 1997. Considerations for the housing and handling of New World primates in the laboratory. Pp 75-84 in Comfortable Quarters for Laboratory Animals, Animal Welfare Institute, WA DC. Reinhardt V (Ed).
  • Capitanio JP & Lerche NW. 1998. Social separation, housing relocation, and survival in simian AIDS: A retrospective analysis. Psychosomatic Med. 60: 235-244.
  • Crockett CM, Bowers CL, Bowden DM, Sackett GP. 1994. Sex differences in compatibility of pair-housed adult longtailed macaques. Am J Primatol. 32: 73-94.
  • Crockett CM, Bellanca RU, Bowers CL, Bowden DM. 1997. Grooming-contact bars provide social contact for individually caged laboratory macaques. Contemp Top Lab Anim Sci. 36: 53-60.
  • De Vries H. 1998. Finding a dominance order most consistent with a linear hierarchy: a new procedure and review. Animal Behaviour. 55(4): 827-843.
  • DiVincenti, L, Jr, Wyatt, JD. 2011. Pair housing of macaques in research facilities: a science-based review of benefits and risks. J Am Assoc Lab Anim Sci. 50: 856-63.
  • Doyle LA, Baker KC, Cox LD. 2008. Physiological and behavioral effects of social introduction on adult male rhesus macaques. Am J Primatol. 70: 542-50.
  • Fa JE, Lindburg DG. 1996. Evolution and Ecology of Macaque Societies, Cambridge University Press.
  • Gilbert MH, Baker KC. 2011. Social buffering in adult male rhesus macaques (Macaca mulatta): Effects of stressful events in single vs. pair housing. J Med Primatol. 40: 71-80.
  • Gust DA, Gordon TP, Brodie AR & McClure HM. 1994. Effect of a preferred companion in modulating stress in adult female rhesus monkeys. Physiol Behav. 55: 681-684.
  • Kezar SM, Baker KC, Russell-Lodrigue KE, Bohm RP. 2022. Single-dose diazepam administration improves pairing success of unfamiliar adult male rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci. 61(2): 173-180.
  • Kikusui T, Winslow JT, Mori Y. 2006. Social buffering: relief from stress and anxiety. Philos Trans R Soc Lond B Biol Sci. 361(1476): 2215-2228.
  • Lee GH, Thom JP, Chu KL & Crockett CM. 2012. Comparing the relative benefits of grooming-contact and full-contact pairing for laboratory-housed adult female Macaca fascicularis. Appl Anim Behav Sci. 137: 157-165.
  • McCowan B, Beisner B, Hannibal D. 2018. Social management of laboratory rhesus macaques housed in large groups using a network approach: A review. Behav Proc. 156: 77–82. doi:10.1016/j.beproc.2017.11.014.
  • Pomerantz O, Baker KC. 2017. Higher levels of submissinve behaviors at the onset of the pairing process of rhesus macaques (Macaca mulatta) are associated with lower risk of wounding following introduction. Am J Primatol. 79: e22671.
  • Pomerantz O, Baker KC, Bellanca RU, Bloomsmith MA, Coleman K, Hutchinson EK, Pierre PJ, Weed JL, National Primate Research Centers’ Behavioral Management Consortium. 2022. Improving transparency- a call to include social housing information in biomedical research articles involving nonhuman primates. Am J. Primatol. 84(6): 1-5. DOI: 10.1002/ajp.23378
  • Schapiro SJ, Bloomsmith MA, Porter LM, Suarez SA. 1996. Enrichment effects on rhesus monkeys successively housed singly, in pairs, and in groups. Appl Anim Behav Sci. 48(3-4): 159- 171.
  • Schapiro SJ. 2002. Effects of social manipulations and environmental enrichment on behavior and cell-mediated immune responses in rhesus macaques. Pharm, Biochem, and Behav. 73: 271-278.
  • Sosa S, Zhang P, Cabanes G. 2017. Social networks dynamics revealed by temporal analysis: an example in a non-human primate (Macaca Sylvanus) in La Foret des Singes. Am J Primatol. 79: e22662. doi.org/10.1002/ajp.22662.
  • Truelove MA, Martin AL, Perlman JE, Wood JS, Bloomsmith MA. 2017. Pair Housing of Macaques: A review of partner selection, introduction techniques, monitoring for compatibility, and methods for long-term maintenance of pairs. Am J Primatol. 79: e22485
  • Williams LE, Bernstein IS. 1995. Study of primate social behavior. Pp 77-100. In: Bennett BT, Abee CR, Henrickson R, editors. Nonhuman Primates in Biomedical Research: Biology and Management. San Diego: Academic Press.
  • Worlein JM, Kroeker R, Lee GH, Thom JP, Bellanca RU, Crockett CM. 2016. Socialization in pigtailed macaques (Macaca nemestrina). Am J Primatol. 79(1): 1-12. doi:10.1002/ajp.22556. PMID: 27109591, PMCID: PMC5994344.

  • Baker KC, Bloomsmith MA, Coleman K, Crockett CM, Worlein JM, Lutz CK, McCowan B, Pierre P, Weed J. 2017. The Behavioral Management Consortium: A Partnership for Promoting Consensus and Best Practice. Pp 9-24 in: Handbook of Primate Behavioral Management. CRC Press. Schapiro SJ (Ed).
  • Behavioral Management Consortium website
  • Bellanca RU & Crockett CM. 2002. Factors predicting increased incidence of abnormal behavior in male pigtailed macaques. Am J Primatol. 58: 57-69.
  • Bellanca RU, Lee GH, Vogel K, Ahrens J, Kroeker R, Thom JP, Worlein JM. 2014. A simple alopecia scoring system for use in colony management of laboratory-housed primates. J Med Primatol. 43(3): 153-161. PMID: 24571509; PMCID: PMC4438708
  • Bloomsmith MA, Perlman JE, Hutchinson E, Sharpless M. 2018. Behavioral Management Programs to promote laboratory animal welfare. Pp 63-82 in Management of Animal Care and Use Programs in Research, Education and Testing, second edition. CRC Press/ Taylor & Francis. Weichbrod RH, Thompson GAH, Norton JN (Eds).
  • Coleman K, Pierre PJ. 2014. Assessing anxiety in nonhuman primates. ILAR Journal. 55(2): 333- 346. DOI: 10.1093/ilar/ilu019
  • Davenport MD, Lutz CK, Tiefenbacher S, Novak MA, Meyer JS. 2007. A rhesus monkey model of self-injury: effects of relocation stress on behavior and neuroendocrine function. Biol Psychiatry. DOI: 10.1016/j.biopsych.2007.10.025
  • Hamel AF, Lutz CK, Coleman K, Worlein JM, Peterson EJ, Rosenberg KL, Novak MA, Meyer JS. 2016. Responses to the human intruder test are related to hair cortisol phenotype and sex in rhesus macaques (Macaca mulatta). Am J Primatol. 79(1): 1-10. DOI: 10.1002/ajp.22526. PMCID: PMC5108684.
  • Kroeker R, Bellanca RU, Lee GH, Thom JP, Worlein JM. 2014. Alopecia in three macaque species housed in a laboratory environment. Am J Primatol. 76(4): 325-334. PMID: 24243351; PMCID: PMC4066655
  • Kroeker R, Lee GH, Bellanca RU, Thom JP, Worlein JM. 2016. Prior facility affects alopecia in adulthood for rhesus macaques. Am J Primatol. 79(1): 1-9. DOI: 10.1002/ajp.22551. PMCID: PMC7364428.
  • Lutz C, Well A, Novak M. 2003. Stereotypic and self-injurious behavior in rhesus macaques: A survey and retrospective analysis of environment and early experience. Am J Primatol. 60: 1-15.
  • Lutz CK, Coleman K, Worlein JM, Novak MA. 2013. Hair loss and hair-pulling in rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci. 52(4): 454–457.
  • Lutz CK, Coleman K, Worlein JM, Kroeker R, Menard MT, Rosenberg K, Meyer JS, Novak MA. 2016. Factors influencing alopecia and hair cortisol in rhesus macaques (Macaca mulatta). J Med Primatol. 45(4): 180-188. doi:10.1111/jmp.12220. PMCID: PMC5029426
  • Lutz CK, Coleman K, Hopper LM, Novak MA, Perlman JE, Pomerantz O. 2022. Nonhuman primate abnormal behavior: etiology, assessment, and treatment. Am J Primatol. 84(6): 1-21. DOI: 10.1002/ajp.23380
  • Novak MA and Meyer JS. 2009. Alopecia: Possible Causes and Treatments, Particularly in Captive Nonhuman Primates. Comp Med. 59(1): 18-26.
  • Novak MA, Hamel AF, Coleman K, Lutz CK, Worlein J, Menard M, Ryan A, Rosenberg K, Meyer JS. 2014. Hair loss and hypothalamic-pituitary-adrenocortical axis activity in captive rhesus macaques (Macaca mulatta): A cautionary tale. J Am Assoc Lab Anim Sci. 53(3): 261-266. PMID: 24827567; PMCID: PMC4128563
  • Novak MA, Hamel AF, Kelly BJ, Dettmer AM, Meyer JS. 2014. Stress, the HPA axis, and nonhuman primate well-being: A review. Appl Anim Behav Sci. 143(2-4): 135-149.
  • Novak MA, Menard MT, El-Mallah SN, Rosenberg K, Lutz CK, Worlein J, Coleman K, Meyer JS. 2016. Assessing significant (>30%) alopecia as a possible biomarker for stress in captive rhesus monkeys. Am J Primatol. 79(1):1-8. DOI: 10.1002/ajp.22547. PMCID: PMC5055463.
  • Novak MA. 2020. Self-injurious behavior in rhesus macaques: issues and challenges. Am J Primatol. 83(6): 1-15. DOI: 10.1002/ajp.23222
  • Rommeck I, Anderson K, Heagerty A, Cameron A, McCowan B. 2009. Risk factors and remediation of self-injurious and self-abuse behavior in rhesus macaques. J Am Assoc Lab Anim Sci. 12: 61-72.
  • Schapiro SJ, ed. 2017. Handbook of Primate Behavioral Management. CRC Press.
  • Shively CA, Willard SL. 2012. Behavioral and neurobiological characteristics of social stress versus depression in nonhuman primates. Exp. Neuro. 233: 87-94.
  • Weed JL, Wagner PO, Byrum R, Parrish S, Knezevich M, Powell DA. 2003. Treatment of persistent self-injurious behavior in rhesus monkeys through socialization: a preliminary report. Contemp Top Lab Anim Sci. 42(5): 21-23.

  • Baker K. 2007. Enrichment and primate centers: closing the gap between research and practice. J Appl Anim Welf Sci. 10: 49-54.
  • Baker KC, Weed JL, Crockett CM, Bloomsmith MA. 2007. Survey of environmental enhancement programs for laboratory primates. Am J Primatol. 69: 377-94.\
  • Bayne K, Wurbel H. 2014. The impact of environmental enrichment on the outcome variability and scientific validity of laboratory animal studies. Rev sci tech. 33(1): 273-280.\
  • Bennett AJ, Corcoran CA, Hardy VA, Miller LR, Pierre PJ. 2010. Multidimensional cost-benefit analysis to guide evidence-based environmental enrichment: providing bedding and foraging substrate to pen-housed monkeys. J Am Assoc Lab Anim Sci. 49(5): 571-577.
  • Bloomsmith MA, Brent LY, Schapiro SJ. 1991. Guidelines for developing and managing an environmental enrichment program for nonhuman primates. Lab Animal Sci. 41(4): 372-377.
  • Buchanan-Smith HM. 2010. Environmental enrichment for primates in laboratories. Adv Sci Res. 5: 41-56.
  • Coleman K, Novak MA. 2017. Environmental Enrichment in the 21st Centure. ILAR Journal. DOI: 10.1093/ilar/ilx008.
  • Crockett CM, Bielitzki J, Carey A,Velez, A. 1989. Kong toys as enrichment devices for singly-caged macaques. Lab Primate News. 28: 21-22.
  • Crockett CM, Bellanca RU, Heffernan KS, Ronan D.A. & Bonn W.F. 2001. Puzzle ball foraging device for laboratory monkeys. Lab Primate News. 40: 4-7.
  • Doane CJ, Andrews K, Schaefer LJ, Morelli N, McAllister S, Coleman K. 2013. Dry bedding provides cost-effective enrichment for group-housed rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci. 52(3): 274-252.
  • Gottlieb DH, O’Connor JR, Coleman K. 2014. Using porches to decrease feces painting in rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci. 53(6): 653-656.
  • Lloyd CR, Lee GH & Crockett,CM. 2005. Puzzle-ball foraging by laboratory monkeys improves with experience. Lab Primate News. 44: 1-3.
  • Lutz CK & Novak MA. 2005. Environmental enrichment for nonhuman primates: theory and application. ILAR J. 46: 178-91.
  • Lutz CK and Brown TA. 2018. Porches as enrichment for singly housed cynomolgus macaques (Macaca fascicularis). J Am Assoc Lab Anim Sci. 57(2): 134-137.
  • Wells DL. 2009. Sensory stimulation as environmental enrichment for captive animals: a review. Appl Anim Behav Sci. 118: 1-11.

  • Baker KC. 2004. Benefits of positive human interaction for socially housed chimpanzees. Anim. Welfare 13: 239-45.
  • Baker KC, Bloomsmith MA, Neu K, Griffis C, Maloney M, Oettinger B, Schoof V, Martinez M. 2009. Positive reinforcement training moderates only high levels of abnormal behavior in singly housed rhesus macaques. J. Appl. Anim. Welf. Sci. 12: 236-252.
  • Baker KC, Bloomsmith, MA, Neu, K, Griffis, C & Maloney, M. 2010. Positive reinforcement training as enrichment for singly housed rhesus macaques (Macaca mulatta). Animal Welfare. 19: 307-313.
  • Bliss-Moreau E, Moadab G. 2016. Variation in behavioral reactivity is associated with cooperative restraint training efficiency. J Am Assoc Lab Anim Sci. 55(1): 41-49.
  • Buchanan-Smith HM. 2003. The benefits of positive reinforcement training and its effects on human non-human animal interactions. Proceedings of the Fifth Annual Symposium on Zoo Research. 21-26.
  • Coleman K, Maier, A. 2010. The use of positive reinforcement training to reduce stereotypic behavior in rhesus macaques. J. Appl. Beh. Sci. 124: 142-148.
  • Graham ML, Rieke EF, Mutch LA, Zolondek EK, Faig AW, DuFour TA, Munson JW, Kittredge JA, Schuurman H-J. 2012. Successful implementation of cooperative handling eliminates the need for restraint in a complex non-human primate disease model. J Med Primatol. 41(2): 89-106. doi:10.1111/j.1600-0684.2011.00525.x
  • Laule GE, Bloomsmith MA, Schapiro, SJ. 2003. The use of positive reinforcement training techniques to enhance the care, management, and welfare of primates in the laboratory. J Appl Anim Welf Sci. 6: 163-73.
  • Laule G, Whittaker M. 2007. Enhancing nonhuman primate care and welfare through the use of positive reinforcement training. J Appl Anim Welf Sci. 10: 31-38.
  • Mason S, Premereur E, Pelekanos V, Emberton A, Honess P, Mitchell AS. 2019. Effective chair training methods for neuroscience research involving rhesus macaques. J Neuro Methods. 317: 82-93.
  • McMillan JL, Bloomsmith MA, Prescott MJ. 2017. An international survey of approaches to chair restraint of nonhuman primates. Comp Med. 67(5): 442-451.
  • Minier DE, Tatum L, Gottlieb DH, Cameron A, Snarr J, Elliot R, Cook A, Elliot K, Banta K, Heagerty A, McCowan B. 2011. Human-directed contra-aggression training using positive reinforcement with single and multiple trainers for indoor-housed rhesus macaques. Appl Anim Behav Sci. 132(3): 178-186. doi:10.1016/j.applanim.2011.04.009
  • O’Brien JK, Heffernan S., Thomson PC, McGreevy PD. 2008. Effect of positive reinforcement training on physiological and behavioural stress responses in the hamadryas baboon (Papio hamadryas). Animal Welfare. 17: 125-138.
  • Perlman JE, Bloomsmith MA, Whittaker MA, McMillan JL, Minier DE, McCowan, B. 2012. Implementing positive reinforcement animal training programs at primate laboratories. Appl Anim Behav Sci. 137(3-4): 114-126.
  • Shirasaki Y, Yoshioka N, Kanazawa K, Maekawa T, Horikawa T, Hayashi T. 2013. Effect of physical restraint on glucose tolerance in cynomolgus monkeys. J Med Primatol. 42(3): 165-168. doi:10.1111/jmp.12039
  • Schapiro SJ, Bloomsmith MA, Laule GE. 2003. Positive reinforcement training as a technique to alter nonhuman primate behavior: quantitative assessments of effectiveness. J Appl Anim Welf Sci. 6(3): 175-187.
  • Schapiro SJ and Lambeth SP. 2007. Control, choice and assessments of the value of behavioral management to nonhuman primates in captivity. J Appl Anim Welf Sci. 10(1): 39-47

K. Approval/Review Dates

Last Reviewed/Revised by the IACUC: 04/20/2023

 

Skip to toolbar