Wake Forest University

1. Wake Forest University Information Regarding Nonhuman Primate Natural History, Behavior, Reproduction, Environmental Enrichment, Special Cases

2. Introduction Greetings! This presentation contains custom animation for instructional purposes. To activate the text, simply left click on the mouse or use the Page Down key, located to the left of the #7 on the number pad, to scroll through the information. After each click of the mouse or use of the Page Down key, pause to give the animation a moment to run its course. It is estimated that this presentation should take 25-30 minutes to review. A test follows the presentation. If you experience any difficulties during this training, please contact the EH&S Information & Education Coordinator at 716-6084 for help. Press the Page Down key or left click on your mouse to continue.

3. Objectives Why is this training important? • It serves to increase awareness of monkey behaviors, both threatening and non-threatening. • It provides non-human primate handlers with a detailed look at the Wake Forest University Plan for Nonhuman Primate Environmental Enrichment.

4. Let’s begin with some background. . . Important Note: No images contained herein were taken at Wake Forest University School of Medicine unless otherwise indicated.

5. Background Wake Forest University School of Medicine’s conducts research with four Old World species of monkeys. The terms “Old World” and “New World” refer to the species’ place of origin “Old World” monkeys are native to Africa and Asia “New World” monkeys are native to southern Mexico, Central America and South America.

6. Habitat

7. Species at WFUSM African Green monkeys (Chlorocebusethiops) • Also known as Vervet monkeys

8. Species at WFUSM Rhesus monkey (Macaca mulatta)

9. Species at WFUSM Cynomolgus monkey(Macaca fascicularis) • Also called crab-eating macaque, long-tailed macaque, and Java monkey

10. Species at WFUSM Bonnet monkey (Macaca radiata)

11. Common Physical Features Old World monkeys share several common physical features: Quadrapedal – walk on all fours Cheek pouches for food storage in the mouth Opposable thumb – enables grasping Large canine teeth and sharp fingernails Non-prehensile tail – used for balance rather than grasping objects or substrates Ischial callosities - hairless, callused areas on either side of the rump used for sitting (also called butt pads) Sexual dimorphism – males are bigger in size than females

12. Diet Macaques and Vervet monkeys are omnivorous—they consume both plant and animal material. In fact, Vervet monkeys are the most omnivorous of all primate species. Their diet may consist of the following: • leaves • acacia tree gum • seeds • nuts • grasses • fungi • fruit • berries • flowers • buds • shoots • invertebrates • birds • bird eggs • lizards • rodents • other vertebrate prey

13. Mating and Reproduction Females typically begin cycling around 2.5 yrs of age, but may begin as early as 1.5 yrs. Early weaning can result in psychological problems and inadequate development of social and maternal skills. Juveniles become sexually mature at 3 to 4 years of age. Females have sex skin – genital areas (also sometimes face and arms) turn red and swollen around ovulation; signals males to their receptiveness to mating. (Note: Vervet and bonnet monkeys do not have sex skin.) Gestation lasts between 5 – 6 months. Infants are nursed between 10 and 12 months, and weaning occurs around 12 months old.

14. Question/Answer: Which of the following species ARE NOT housed at WFUSM? A. African Green monkeysB. ChimpanzeesC. Rhesus monkeysD. Cynomolgus monkeys

15. Monkey Behaviors

16. Behavior • Macaques and vervet monkeys are both arboreal and terrestrial. • Macaques and vervet monkeys are social animals and live in groups of multiple males and females.

17. Behavior • Within groups, individuals are ranked according to dominance status. • Dominance is often determined by the rank of the mother, which creates what is called a matrilineal dominance hierarchy.

18. Behavior • Dominant animals benefit from having first access to and control over food, higher rates of successful breeding, social exchanges such as grooming, and control of other desirable resources (preferred perches, objects). • Young males leave the group and form bachelor troops before reaching sexual maturity, while the females stay with their family group, often for life.

19. Behavior Most of their communication is done through facial signals and vocalizations. There are several types of facial signals for communication.

20. Threatening Behaviors Open mouth threat: mouth opens and forms the shape of an “O” Threat yawn:tilting head back while opening mouth wide, exposing the teeth Threat displays:

21. Threatening Behaviors A direct stare—to Old World monkeys, such as macaques and vervets, direct eye contact is a sign of aggression Shaking an object in the environment, such as the cage door Other Threatening Displays: Charging with the intent to fight Raising eyebrows quickly and repeatedly Piloerection: hair stands on end A jerkyhead-bob Slapping the ground Flapping the ears

22. Friendly/Submissive Behaviors • Grooming not only reduces fur parasite load, but it’s also important for forming and maintaining social bonds. • Studies have shown that a monkey’s heart rate is significantly lower when being groomed by another than when self-grooming or while displaying any other behaviors.

23. Friendly/Submissive Behaviors • Embracing • Sitting in close proximity • Lip Smacking – bringing the lips together repeatedly and rapidly without showing the teeth, making a slight smacking sound

24. Friendly/Submissive Behaviors • Coo calls can be used as food calls (made upon discovery of a low quality food) or used to make auditory contact with group members. • Food sharing has often been used as an indicator of a socially compatible pair of monkeys.

25. Friendly/Submissive Behaviors • Fear grimacing: pulling back the lips to reveal the teeth while the mouth is closed • Resembles a human smile • Indicates fear, submission, and no intent to attack

26. Auditory Communication • Monkeys also rely on vocalizations to communicate with other monkeys. • Vocalizations can be used to contact members of the group, alert others to a predator, beg for food, and convey emotions (aggression, fear, excitement). • Vervet monkeys have evolved specific “alarm call” vocalizations to alert their group to the presence of different predators. Examples: • leopard alarm call • snake alarm call • eagle alarm call • Vervet monkeys recognize the different alarm calls and will respond accordingly after hearing them. For example, if the snake alarm call is given, Vervets have been observed looking down in the grass to detect the predator.

27. Vocalizations Please click on the links to listen to samples and to view videos: • Samples of different Rhesus vocalizations http://www.wjh.harvard.edu/%7Emnkylab/media/rhesuscalls.html • Samples of different Vervet vocalizations http://www.wjh.harvard.edu/%7Emnkylab/media/vervetcalls.html

28. Question/Answer: Which of the following is NOT a threatening behavior? A. StaringB. YawningC. Lip smackingD. Piloerection

29. Human-Monkey Interactions

30. Interactions with Laboratory Primates Laboratory primates are not pets. They are wild animals and should be respected. Because eye contact is interpreted by monkeys as a sign of aggression, avoid staring directly into a monkey’s face. Respect the physical space of monkeys by not putting your hands into their caging or standing too close to their caging. Like humans, monkeys have comfort zones for proximity to others. Unsolicited touching or attempts at petting may be interpreted as aggression and the monkey may respond aggressively in return.

31. Interactions with Laboratory Primates If a monkey is acting fearfully or aggressively towards a human by displaying threats, vocalizations, or making physical contact, the proper way to respond is to avert your gaze, step out of reach, and IGNORE the undesirable behaviors. If your job requires working closely with a monkey who is acting aggressively, ask for help from your supervisor. It is NEVER acceptable to attempt to punish a monkey’s inappropriate behavior by staring, returning threats, becoming physical, or using other measures of punishment such as the squeeze bar or water hose. Any overt aggression or punishment will be subject to disciplinary action.

32. Interactions with Laboratory Primates If you ever witness inappropriate treatment of a monkey or questionable research procedures: 1. Report it to your supervisor immediately. OR 2. Make an anonymous report to the Animal Care and Concern Hotline at 716-5899. OR 3. Make an anonymous report to the Research Concern Hotline at 716-0338.

33. Question/Answer: The best way to respond to a monkey who is acting aggressively is to: A. Stare them downB. Yell at them and slap the cageC. Ignore the behavior and take a time-outD. Distract them with treats

34. Environmental Enrichment

35. Environmental Enrichment Question: What is Environmental Enrichment? Environmental Enrichment is defined as changes made to the environment and husbandry practices that provide the opportunity for choice and the expression of species-typical behavior. Question: Why is Environmental Enrichment important? Congress responded to public concern for animals used in research by passing the Animal Welfare Act of 1966 and 1978. When the U.S. Department of Agriculture (USDA) adopted the act as regulations in 1991, it required that “dealers, exhibitors, and research facilities must develop, document, and follow an appropriate plan for environmental enhancement adequate to promote the psychological well-being of nonhuman primates”.

36. Assessing Psychological Well-Being To assess psychological well-being, we need to address the following criteria: • The animal’s ability to cope with day-to-day changes in its social and physical environment • The animal’s ability to engage in beneficial species-typical activities • The absence of maladaptive behaviors that result in self-injury or negative consequences • The presence of a balanced temperament (balance of aggression and passivity) and absence of chronic signs of distress (distress vocalizations, depressed postures, labored breathing, excessive cardiac response, lack of appetite, abnormal hormone concentrations)

37. Environmental Enrichment Plan The Wake Forest University Plan for Nonhuman Primate Environmental Enrichment seeks to facilitate psychological well-being by implementing five major types of enrichment: • Structuralenrichment • Food enrichment • Sensory enrichment • Object enrichment • Socialenrichment

38. Structural Enrichment • Housing design should allow the expression of species-typical postures and movement. • Cage furnishings such as perches, climbing structures, shelves, barrels, and tunnels have been used to allow monkeys to assume a variety of movements and postures, have access to vertical space, and to have some form of privacy when socially housed. • Monkeys prefer to sit and sleep on perches and will seek out the highest point in the environment when threatened. • All cages at WFU are required to be equipped with perches. Examples follow . . .

39. Structural Enrichment Milk crates and surgical tubing serve as swings, perches, and food puzzles. Various swings made from fire hose and PVC tubing; the barrel serves as a swing, shelter, and hiding place.

40. Structural Enrichment Wooden cable spools offer shelter, a hiding place, and area for climbing; monkeys also enjoy gnawing wood. WFUSM image

41. Structural Enrichment To reduce and manage social conflict, each cage must be equipped so that monkeys can escape the aggressive displays of others. In a social setting, barrels make very good hiding places. Monkeys who are housed individually in cages must also have a way to avoid eye contact with other monkeys housed in the same room. Visual barriers offer individually housed monkeys the option of privacy. Visual barriers attach to the front of the cage, where the monkey can choose to sit behind it.

42. Food Enrichment • Monkeys in the wild typically spend about 70% of their time foraging for food. • Offering primates the opportunity to engage in this behavior is one of the simplest and most important tools in ensuring psychological well-being and preventing abnormal behaviors. • In the research setting, our goal is to increase manipulation and exploration, the time required to procure food items, and the time required to ingest food items. • There are many commercial devices designed to enable foraging behavior. Examples follow . . .

43. Food Enrichment Some examples of foraging devices that can be loaded with food: Challenger ball Kong toy Primate Choo PVC food puzzle Holee Molee ball Foraging turf board

44. Food Enrichment In addition to devices, natural food itemscan provide the opportunity for foraging. Examples: • corn on the cob • bird seed • food and flavored liquids frozen in ice cube trays • pomegranate • whole coconut

45. Food Enrichment Like human primates, monkeys enjoy a wide variety of foods and novel treats. There are several online nonhuman primate recipe resources, such as The Cattarhine Café Cookbook, created by Washington National Primate Research Center. This recipe collection can be found online at http://www.wanprc.org/wanprc/cookbook-forExternal.pdf

46. Question/Answer: In the wild, monkeys spend a majority of their time engaged in which behavior: A. ReproductionB. Fighting C. GroomingD. Foraging for food

47. Sensory Enrichment In some cases, monkeys may participate in daily experimental sessions. This may involve manipulating joysticks, response levers, or making operant responses to obtain food pellets. After initial training, it is clear that such rewarded responses contribute to psychological well-being. Other types of sensory enrichment include: • Music and television • Training through positive reinforcement • Novel scents – the ARP provides novel scent enrichment with liquid potpourri one day each week. • Swimming

48. Sensory Enrichment Macaques are skillful swimmers. Here are pictures of macaques enjoying a swimming pool. Plastic Sand Box Livestock Water Tank

49. Object Enrichment Object enrichment includes durable, manipulable objects such as mirrors, plastic balls, cone-shaped rubber toys, and gnawing sticks that are safe to be used by monkeys. Objects should be rotated at least every two weeks to maintain novelty and should be replaced when worn or damaged.

50. Social Enrichment Monkeys are social animals. As such, living with an animate, responsive mate is the best form of environmental enrichment. Group and pair housing reduces boredom and anxiety and facilitates expression of a wider range of species-typical behaviors. Monkeys who are socially housed develop better coping skills and are less likely to display abnormal and self-injurious behaviors. Individually housed monkeys should be provided increased environmental enrichment, and visual, auditory, and olfactory contact with other monkeys via close caging, a mesh cage divider, or grooming panel.