4. Environmental Enrichment

4,1. Definition

To my knowledge, the term "environmental enrichment" was originally introduced in 1991 by the US Department of Agriculture in its Animal Welfare Regulations pertaining to nonhuman primates (US Department of Agriculture, 1991). These regulations do not provide an explicit definition, but stipulate under the section "environmental enrichment" that "means of expressing non-injurious species-typical activities" must be provided.

As a technician, I like the following definition, which I found on the title page of the Database on Environmental Enrichment and Refinement of Husbandry for Nonhuman Primates:

As a veterinarian, I like the definition from the organization Shape of Enrichment:

As a researcher, I would define environmental enrichment as:

Irrespective of its definition, I will argue that "environmental enrichment" is not a very good term for the following reasons:

  1. It implies that something is added to the environment in which the animals are kept, rather than describing the environment itself.
  1. In the everyday use of language, "enrichment" is understood as "making richer." I could agree that, if you have primates in large enclosures with lots of climbing opportunities, different foods and nice caretakers, you may in fact be providing environmental "enrichment," if you give them puzzle feeders in addition. But when primates are kept in barren cages and are given puzzle feeders, that is not enriching their environment in the everyday sense of the word: it is making it less poor.

If we provide animals in otherwise boring living quarters the opportunity to engage in behaviors that occupy a major portion of their lives in the natural setting, we do not "enrich" their unnaturally barren environment, but rather provide them with basic "necessities" required for the active expression of these behaviors also in the laboratory setting. I am sure the lay person has a different understanding of the nice term "enrichment" than most of us do:

  1. Do we really "enrich" a monkey cage by installing a perch and adding a social partner?
  2. Do we really "enrich" a mouse cage by adding suitable nesting material (Figure 10a,b)?
  3. Do we really "enrich" a cage of a rat by adding a shelter and one or several other rats?
  4. Do we really "enrich" the animals' primary enclosures by allowing them to engage in foraging activities other than eating the freely available daily dry-food pellets or biscuits or chow?

I think the answer is always "no." What we do is not an act of generosity, we simply address very basic behavioral needs—and that is the very minimum that the animals deserve.

 

Figure 10a,b The addition of species-appropriate nesting material (a) to the standard cage of mice (b) does not really enrich the animals' environment; it merely makes it less poor. Photo 10a by Animal Welfare Institute; Photo 10b by Maureen Hargaden.

Regardless of how we define the term "environmental enrichment," it will always distract from the fact that we do not "enrich" the environment of captive animals, but provide them, at best, with opportunities to express basic behavioral needs.

4,2. Criteria of Effectiveness

How do you evaluate the effectiveness of environmental enrichment?

The National Research Council (1998) makes it quite clear:

This sounds very reasonable, but it is a given, albeit sad, reality that time, personnel and budget are limiting factors that make it very difficult, if not impossible for us to evaluate all so-called enrichment items that we give our primates and rodents.

It may not be necessary to actually evaluate all enrichment items when we differentiate between (1) biologically relevant environmental enrichment—which should be mandatory—versus (2) biologically irrelevant environmental enrichmentwhich could be optional:

 

Figure 11 Toys have little "enrichment" value because they cannot sustain the animals' interest beyond a short-lived novelty effect. Photo by Natasha Down.

  1. Biologically irrelevant environmental enrichment triggers a response that has no survival value for the subject, e.g., pushing a ball, manipulating or gnawing a plastic toy, looking into a mirror or TV screen, listening to radio sound. The effect of this type of enrichment needs to be evaluated by means of behavioral observations, because the animals tend to get bored by it over time. Its effectiveness is dependent on its novelty and, hence, requires regular exchange or rotation with new enrichment (Figure 11).
  2. Biologically relevant environmental enrichment triggers a response that has survival value for the subject, e.g., hiding in shelter, interacting with a compatible social partner [including humans], searching for and processing food and nesting material. The effect of this type of enrichment is predetermined by its intrinsic survival value and, hence, does not lose its distracting or enriching value over time.
  3. Biologically relevant enrichment is, by its very nature, effective. For example:

 

Figure 12 Animals are not likely to lose interest in biologically relevant environmental enrichment, such as nesting material for mice. Photo by Pascalle van Loo.

Biologically relevant enrichment options have been described in the literature, so there is no need to spend extra time in evaluating their effectiveness.

Biologically irrelevant enrichment is usually not cost effective when managing large populations of animals. This is particularly true for toys or gadgets for which the animals quickly lose interest, hence several sets of such enrichment objects are then needed to rotate them—and sanitize them at that time—on a regular basis. Therefore, taking the cost benefit ratio into account, I feel it is prudent that we put our resources and manpower into enrichment options that are relevant, producing long-term behavioral benefits to the animals.

  Figure 13 A high perch provides biologically relevant environmental enrichment of which monkeys do not get bored. Photo by Viktor Reinhardt.

Biologically relevant enrichment is intrinsically effective in promoting species-adequate, non-injurious behaviors, hence it does not require extra evaluation. The effectiveness of biologically irrelevant enrichment is not intrinsic and therefore has to be evaluated and reevaluated through repeated behavioral observations to assure that it promotes appropriate behavioral responses.

4,3. Feeding Enrichment

Animals in research labs usually get their daily food ration presented in a free-to-take manner, allowing little or no expression of foraging behavior, i.e., food searching, retrieving and processing. Do you try to promote more foraging behavior in the animals in your charge?

I would assume that very few animals would prefer to "forage" over sitting in front of a bowl and eating.

You may be right, but many animals will want to work for their food nonetheless. When you place a monkey, rat, chicken or pigeon—who have not been starving—into a cage where they have simultaneous access to a bowl with freely accessible food and a foraging device loaded with the same food, but requiring skillful manipulation to retrieve it, chances are high that the animal will move back and forth, eat the freely accessible food and then work for food, eat freely accessible food and then work again for food etc., spending altogether more time working for food than simply collecting and eating it (monkey: Washburn and Rumbaugh, 1992; Reinhardt, 1994a; De Rosa et al., 2003; rat: Carder and Berkowitz, 1970; Hothersall et al., 1973; chicken: Duncan and Hughes, 1972; pigeon: Neuringer, 1969). This kind of experiment demonstrates that the animals are inherently motivated to "forage," even if it implies some effort. A good compromise would perhaps be to offer them daily the opportunity to work for their standard food ration for some time, e.g., 1 hour daily feeding enrichment, then give them the bowl with freely accessible food to make sure that they get and eat enough of their ration.

The more time we can get our animals to perform species-adequate behaviors—such as retrieving their food—in boring living quarters, the less time they will spend engaged in behavioral pathologies.

4,3,1. Primates

I have given whole watermelons to group-housed rhesus, cynos, bonnet and stump-tailed macaques for several years without noticeable adverse effects. It would be a waste of time to cut the melons into small pieces. The monkeys first gnaw a hole into the rind and then "dig" into the soft and juicy part (Figure 14). They really like this and are kept busy until the last morsel has been eaten. They usually discard the rind, but before they do so they thoroughly remove any soft material and eat it. This usually creates quite a mess, but I don't mind cleaning it up, because the animals enjoy this type of feeding enrichment so much.

 

Figure 14 Rhesus macaques love watermelons! Photo by Viktor Reinhardt.

We give whole pumpkins to rhesus and cynos in both single- and group-housed environments. I would say that this is one of the most effective foraging "devices" we have ever given our animals. All of them spent hours processing their pumpkin!

 Figure 15a,b It would be a waste of time to cut apples into small pieces for rhesus macaques. The animals have all the time needed to retrieve whole apples from the food basket in which they receive their daily biscuit ration. Photos by Viktor Reinhardt.

All our group-housed rhesus receive whole apples on a daily basis. In order to make it more interesting for them, I place the apples into troughs that are attached to the chain-link wall of the pen 1.2 m off the floor. The animals have to climb up to the trough, reach into it and get hold of an apple, maneuver the apple up to the chain-link, press the apple towards their mouth while nibbling off pieces until it fits through the mesh of the chain-link barrier. In this way, the monkeys spend a considerable amount of time retrieving/processing apples every day (Figure 15a,b). Whole apples provide an excellent source of daily feeding enrichment also for animals who live in cages (Figure 16).

 

Figure 16 Whole apples provide optimal feeding enrichment for macaques. Photo by Viktor Reinhardt.

As Thanksgiving approaches, I want to give my rhesus monkeys some cranberries, but I wonder, do I have to worry about possible side effects for the animals?

I have fed cranberries to monkeys of several species, including rhesus macaques. They all seem to like them, and I have never noticed any negative effects.

In summer, we give our rhesus macaques raspberries as a special treat. They cannot get enough of them, but the juice of the berries leaves stains on the cage walls that are very difficult to remove.

I give thoroughly cleaned sugar cane, cut into 10 cm long segments, to our group-housed baboons. They love it! Surprisingly and fortunately, they do not leave much of a mess.

Our group-housed chimpanzees also love sugar cane, which we cut into 20-cm sections. Each subject gets about four pieces per day. The chimps chew the wedge for a long time and, doing so, give the impression that they enjoy it. Finally, the wedges are scattered all around the enclosure, which requires a bit of extra time for clean up. Sugar cane can mold easily, so it is a good idea to store it in a cool place, preferably in a refrigerator.

It would probably be fun for our macaques to get corn on the cob, but I am not sure if that would be a safe feeding enrichment option. I would be concerned if they ingested the cob.

I give whole corn with the husk to our pair- and group-housed rhesus and baboons. They love it, and I enjoy observing them "peel and eat," leaving a big mess after they have finished. They gnaw the cob into little pieces that finally fall through the grid floor on the pans. I cannot say whether they actually also eat pieces of the cob, but we have never encountered any health-related problem. I don't mind cleaning up the mess; it's worth the treat!

We use corn on the cob for all our caged cynos, rhesus and vervets. The animals give the impression that they love processing and eating the corn (Figure 17). They typically pick the kernels both with their hands and their teeth. When they are done, they proceed "gnawing" on the cob. I don't know if they actually ingest pieces of it. Even if they do, we have never encountered any clinical problems.

 
Figure 17 Corn on the cob allows macaques to engage in species-typical food processing behavior. Photo by Viktor Reinhardt.

For our rhesus macaques we fill small cardboard containers, such as glove and cereal boxes with wood shavings mixed with food treats and then seal them with tape really well. The monkeys have a great time opening the boxes and getting the stuff out. Some manage to get to the content without dealing with the tape. Others take their time, to first get rid of the tape, and then reach for the treats.

We also use empty plastic pop bottles, fill them with woodchips and treats, and twist the lid on tightly. Some monkeys gnaw their way directly to the treats through the plastic wall of the bottle, while others are more patient and first get the lid off. Whichever strategy they apply, they all seem to enjoy this opportunity to work for the treats. It is a little messy and you have to clean up after the feast, but it is a pretty inexpensive yet effective way of feeding enrichment.

Wood shavings in the catch pans provide an ideal substrate to foster foraging activities. On days when we change the pans—three times a week—we sprinkle sunflower seeds on the shavings. Our rhesus and squirrel monkeys then search with their fingers through the litter and pull the seeds through the floor grids, eat them or store them in their cheek pouches. Since we change the pans, rather than dump the bedding, we don't have any drainage problems in the rooms. This feeding enrichment technique doesn't require undue extra work time in our colony of approximately 130 monkeys. I'd say the benefit of being able to provide even a brief period of "natural" foraging behavior for our caged primates is worth the little additional time it takes to put the bedding in the pans and add a handful of seeds.

With Easter upon us, I was thinking it would be fun to give my monkey friends some hard-boiled eggs, but I am not sure if it would be safe to have them perhaps ingest segments of the egg shells.

I have given hard-boiled eggs in shells to rhesus, cynos and baboons. Most of the animals like them, but we have a few picky eaters who refuse them. Those who like the eggs, carefully peel off the shells. I am not sure if they digest bits of them, but even if they do, it does not harm them.

We have commercial foraging boards for our caged rhesus and cynos. I have difficulties keeping the boards clean, especially when they have leftover peanut butter and seeds stuck in the little crevices of the Astroturf. This can be very frustrating and time consuming!

We don't use peanut butter with the foraging board, because—as you have found out yourself—it's too messy and our animals don't seem to like it all that much. We use cracked corn, white millet, whole wheat, sunflower seeds, and sweet feed—a horse feed—on a rotational schedule. As for cleaning, we just bump the boards upside down into a trash can, line them up against the wall and high pressure-hose them. Then they run through the cage washer. I'd say that 98 percent of the leftover forage base is removed this way.

I sprinkle the seeds and other small foraging items on the board, then soak it with water and freeze it. When the foraging surface of the board is frozen, the animals spend a lot more time picking the seeds and crunching on the ice. Our monkeys are having a great time with this kind of feeding enrichment.

Our pair-housed and group-housed rhesus macaques retrieve their daily biscuit ration through the mesh ceiling of their cages and pens (Reinhardt, 1992a; Reinhardt, 1993a). This allows them to engage in skillful foraging activities that keep them quite busy. This kind of feeding enrichment is very effective, although it does not cost anything. You simply throw the biscuits up on the top of the cages or pens rather than distribute them in the feeder-boxes.

I have converted the ordinary feeder-boxes of our caged rhesus and stump-tailed macaques into food puzzles, by remounting them away from the access holes directly onto the front mesh walls of their cages (Reinhardt, 1993b; Reinhardt, 1993c). Rather than collecting freely accessible biscuits, the animals now have to use skillful foraging techniques to retrieve their daily biscuit ration (Figure 18).

Figure 18 Converting ordinary feeder-boxes into food puzzles is an inexpensive way to foster more foraging activities in macaques. Photo by Viktor Reinhardt.


Do your animals keep normal body weights when they have to work for their daily food ration?

Yes, working for food, rather than having free access to it has no noticeable effect on the animals' body weight maintenance (Reinhardt, 1993a,b,c,d).

4,3,2. Mice and Rats

Corncob bedding provides a great foraging enrichment substrate, because it invariably has small pieces of corn hidden in it. Every time we change the cages, the mice scurry around searching for the corn.

We were scattering sunflower seeds on the paper-based bedding of our mice until a researcher, who agreed at first, complained that the body weights of the mice were yo-yoing. This was the end of this foraging enrichment attempt. The increased variation in body weight was caused by the fact that the mice anticipated the sunflower seeds eagerly but did not touch their normal food pellets!

Doesn't that tell us something about the palatability of the pellets?!

Yes, but it also tells us something about the animals' strong motivation to forage!

We buy cracked corn and wild birdseed mix, add popcorn, a few sunflower seeds in the shell, and occasionally some dry cereal or fruit-flavored bird treats. Toward the end of the day, I scatter a small scoop of the mix around the cages of our rats, and then add a little portion on top of the pellets in the hopper so that a few treats will trickle down here and there when the animals retrieve the chow. The daily provision of this mix keeps the rats busy for quite a while, and they really seem to enjoy it.

Wrightson and Dickson (1999) designed a feeding arrangement for rats that helped to prevent obesity, by making the animals work for the retrieval of their standard food ration. Unintentionally, these authors came up with a very simple feeding enrichment option: Group-housed rats were induced to work for their food by soldering metal plates over their food hoppers, so that only 3 percent of the original area remained available. The animals fed for longer periods and rested less during the night. No changes were observed in the rats' social hierarchy and there were no increases in fighting with restricted hoppers, as up to three rats could feed at a time. It was felt that this method of food restriction was preferable to giving less food to avoid obesity. Rather than rapidly eating a reduced ration and feeling hungry for long periods, the rats worked harder for their food, which enabled them to burn more calories and eat throughout the day. This reduced the incidence of obesity while encouraging the animals to engage in more food-related activities.

We keep jars of sunflower seeds for mice, and jars of whole peanuts, cereals and dried fruits—especially apples—for rats on the counters in the animal rooms, so that attending personnel can distribute treats whenever they are inclined to do so. These regular visits enriched the daily routine not only of the animals but also of the personnel. At the same time, they foster a positive human-animal relationship.

4,3,3. Guinea Pigs and Rabbits

Our guinea pigs and rabbits get a wide variety of fresh produce—we do not chop the veggies—including dandelion greens and curly kale. The animals seem to enjoy processing and eating this natural food without any adverse effects. There is only one investigator concerned about pesticides, so the food must be scrubbed, peeled or grown organically. Besides that, none of our investigators has a problem with their animals receiving fresh produce as a means of feeding enrichment.

4,3,4. Cats

Our cats receive their pellet diet in simple food puzzles consisting of recycled cardboard rolls of paper towels. A few pieces of cork are glued into each roll, making it more difficult for the cats to retrieve their food. The animals don't get tired of "stalking" their "prey," waiting for the prey to emerge, and retrieving it with dexterous manipulation from the "burrow" (Figure 19).

Figure 19 This is a simple but very effective foraging device loaded with the standard food ration for cats. Photo by Annie Reinhardt

We are using a similar device that consists of a plastic ball with a few holes just large enough so that the cats can maneuver food pellets through them. They not only engage in cat-typical foraging activities, but also play with these balls. It is definitely more fun for the staff to watch the cats playing with these enrichment gadgets instead of sleeping. We have all noticed that our cats have become easier to handle in their enclosure, as well as easier to catch, since we have introduced these balls. My own cat has also had one for three years. She made it clear right from the beginning that she prefers having her daily food ration distributed in the ball rather than in the boring food bowl. Obviously, she likes to "work" for the retrieval of her food, similar to a free cat who probably prefers to spend time hunting for a live mouse rather than pick up a dead mouse.

4,3,5. Sheep

Busterballs filled with grain work well as feeding enrichment gadgets for our post-surgical sheep. They spend lots of time head-butting and kicking the balls around the pen in order to retrieve the grain (Figure 20).

 

Figure 20 Busterballs filled with grain keep sheep quite busy retrieving the food treat. Photo by Tamara Godbey.

4,3,6. Objections by Investigators

Do investigators accept the feeding of supplemental fresh produce or treats as part of your environmental enrichment program?

Investigators regularly object to the introduction of enrichment—whether it is food or toys—because they fear for the comparability of their studies with previous work or with the work of others who do not provide enrichment. They insist on keeping their animals under "standardized," albeit species-inadequate environments under the pretext that environmental variables need to be controlled to make the study a truly "scientifically valid" study, yet they tacitly overlook basic variables such as the investigator himself, new caging design, cage location, new or renovated animal holding facility, etc. Using a double standard when it comes to extraneous variables may be convenient, but it is not at all scientific.

4,3,7. Conclusions

Feeding enrichment is a practical option for animals kept in research laboratories. The regular provision of thoroughly cleaned, whole fruits and vegetables and of seeds scattered on woodchips or corncob bedding is probably the easiest yet most effective way to promote species-typical food searching and food processing activities in primates, rodents and rabbits. For cats, standard dry food can easily be presented in such a way that the animals can engage in cat-typical hunting-related behaviors.

4,4. Coconuts

Do coconuts provide suitable and safe environmental enrichment?

I am involved in a project in which we are examining various enrichments for mice. One of these is coconut shells that the mice seem to enjoy immensely. They climb on them, use them as olfactory look-outs—rear on their hind legs and sniff the air—use them as shelters, and chew, chew, chew, chew on them! Often, the mice chew the coconuts from the inside, so when we pick the shell up a week later, it is paper-thin!

Rhesus don't care much about coconuts, but stump-tailed macaques are fascinated by them and do not get tired "working" on them until the last morsel has disappeared in the drop pan. It never occurred that one of the monkeys somehow became injured while processing a nut.

I give whole coconuts to our individually caged cynos. More than anything, they like them for grooming purposes. It gives them something else to do besides bite themselves. I also had a female who carried her coconut around as if it was a baby, constantly clutching it to her chest, and lip smacking to it, grooming it, etc. She was a chronic alopecia case. The coconut alleviated some—unfortunately not all—of her stereotypical hair pulling behavior.

Whole coconuts seem to provide effective and safe environmental enrichment for macaques and mice, and presumably for other rodents as well.

4,5. Mirrors

Can anyone share first-hand experiences on the usefulness of mirrors as enrichment objects?

All of our single-housed long-tailed macaques have mirrors mounted on swivels that are attached to the outside of their cages, low enough so that an animal can chose to either bend down and intentionally look into the mirror or to make no extra effort, hence not be confronted—bothered?—by the mirror reflection. Our monkeys use their mirrors frequently.

We hang stainless steel mirrors right into the cages of our macaques. Some monkeys will cling to them and look at them for long periods ot time, often lip smacking or making other facial gestures, while others will threaten their own reflection and bang the mirror onto the side of the cage. There are a few animals who "attack" their own reflection in the bottom of the stainless steel cup when it is empty. It's quite hilarious!

Most monkeys use their mirrors to look around the room at other monkeys or at people, whom they could not normally see. I assume that the animals feel more at ease when they can avoid direct eye contact with personnel and other monkeys, yet can observe them without being noticed. It's fascinating to watch them moving the mirror in the right position so that they can look at a person, who is not in their field of vision (Figure 21).

 

Figure 21 A cyno male uses a mirror to watch a person who is not in his direct field of vision. Photo by Richard Lynch

Our rhesus love mirrors too. They like to check us out by looking at us through the mirror. I guess they don't feel so threatened when they can look at us without being seen. They also like to check out the room, by looking at the reflections in the mirror. We have one male who never looks at people directly, but holds up a polished stainless steel mirror to watch people who have just entered the room. Of course, we named him Mirror Man.

We have found an acrylic sheet mirror that we can cut into different-sized pieces. Some get hung on the walls, using double sided tape, while other pieces get hung right inside the enclosures, using zip ties. We also cut small pieces and give these directly to the primates. Our rhesus macaques often combine the wall and hand mirrors to get extra viewing advantage! It's really fun to watch them. The acrylic leaves no sharp edges when it breaks; this means it is safe for the animals. We never encountered a problem.

It has been shown in rhesus macaques that mirrors serve not only as enrichment gadgets, but that they can also promote social facilitation, with the mirror reflection of another animal playing with a toy triggering the interest to do the same (Baker, 2000). This is an elegant way of enhancing the novelty effect of enrichment objects, at least in primates.

Our singly housed baboons get the most enjoyment from their mirrors, while pair- and group-housed animals show little interest in them. We place the mirrors on the outside of the cages of our single-caged baboons, leave the mirrors only for a few hours at a time and replace them after a few days. This seems to work nicely: The animals' interest in the "new" mirror is always very strong, gradually declines and is hardly noticeable at the end of the day, when we take the "old" mirror away. Often the baboons will lip smack the mirrors or use them to look around the room. One boy was recently seen presenting to the mirror! I think that mirrors offer great enrichment to the animals.

I have a male olive baboon in my charge who regularly sits for long periods at a time looking at himself in a mirror. He is housed with two females but appears to prefer looking at his own mirror reflection versus the nice tumescent females hovering around him! He also uses his mirror to see reflections of what is going on behind him, sitting diagonally with his back facing the main traffic area for techs, as if he was spying on us! I do believe he is entertaining himself quite a bit with the mirror.

We use stainless steel mirrors for our vervets who, just like the macaques, use them to look at either themselves or at other monkeys. Harris and Edwards (2004) studied singly housed animals and found that individuals contacted mirrors, hung on one side of their cages with a 18 cm long chain, about 5 percent of the time. Habituation did not appear to occur even a year after the mirrors were introduced.

I have videotaped singly caged rabbits who had constant access to a mirror mounted on the inside of their cage. Neither does nor bucks were attracted by their mirrors, even though they seemed to perceive their own reflection in the mirror as a social counterpart (Figure 22). Jones and Phillips (2005) found that single-caged rabbits do show initial interest in mirrors, but that this novelty effect wears off very quickly.

Figure 22 Rabbits do respond to mirrors at first, but they quickly lose interest in them. Photo by Joanne Edgar.

Sherwin (2004) concluded from a preference test study that a mirror can be aversive to singly housed mice, especially during feeding. It might be that for mice—who use olfaction as their primary sensory modality—the "confusion" of seeing another mouse with no smell is frightening. Obviously, a mirror is not a suitable enrichment gadget for them.

Sheep, who are housed individually for research-related reasons, typically become extremely skittish and vocal for long periods of time. McLean and Swanson (2004) mounted a large mirror on one wall of single-housing units. Isolated sheep stood close to and nudged the mirror image without showing any signs of agitation. The risk of injury was eliminated, as the sheep no longer tried to jump or escape the enclosure. Parrott et al. (1988) also emphasize that isolated animals show considerable interest in their mirror reflection, and that physiological stress reactions to social isolation are lower in sheep with a mirror versus without a mirror. Piller et al. (1999) made a similar observation in cattle and concluded that the mirror-image reflection seems to buffer isolation stress.

Mirrors provide useful environmental enrichment for primates. The literature suggests that mirrors may help to buffer isolation stress in some species.

4,6. Music

Does sound or music have any environmental enrichment value for animals in research labs, other than keeping the attending personnel in a good mood?

Several people at our facility request to have radios in their rodent colony rooms to act as a sound buffer. If that's a good reason, my preference would be to have the radio set to static or have an actual white noise generator. I've found that some technicians and care staff play the radios so loudly, you can hear them outside the animal rooms, sometimes even in adjoining rooms. I am lucky and can just leave when the noise gets too much on my nerves. The animals have no choice but listening to this cacophony, probably not a situation that is animal welfare-conducive.

We have had an ongoing problem with people playing radios in the animal rooms at excessive volumes, which could drive me—and probably also the caged monkeys—crazy! There was no way to get people to change their habits voluntarily, so we had to make it a rule that no radios are allowed in the animal rooms and in the corridors. What a difference it made!

We found a compromise: Rather than playing radios, we play CDs with classical music at a background volume that cannot be changed by the attending personnel.

It's probably not only the volume but also the quality of music that can affect animals differently. Our monkeys used to be exposed to rock music. We then switched to classical music, and I have the impression that the animals are now calmer and much easier to work with. Brent and Weaver (1996) noted a decrease in heart rate in baboons, Howell et al. (2002) an increase in social grooming and fewer aggressive interactions in chimpanzees when the animals were exposed to classical music.

Primates, being diurnal animals, may enjoy listening to certain types of music during the daylight hours, but rabbits and rodents are nocturnal animals who want to sleep during the day. I would not think music is beneficial for them, even if they don't show any specific reactions to the music. I don't have any experience with music in rabbit rooms here at work, but I do have a pet rabbit who very clearly prefers not to be in the same room as loud or fast-tempo music. He will simply leave the room.

We have a radio playing in all our rooms including those of the rabbits. The radios are left on round the clock with the aim of providing a constant noise environment that may help the animals to better cope with disturbances for example, not to be startled if someone enters their room. The radio-created noise in the animal rooms is kept so low that you cannot hear it in the corridors.

Background music can have a calming effect on caged primates. We do not really know if being forced to listen to loud music of the personnel's liking is also to the animals' liking. If it is not to their liking, chances are that they feel distressed. This probably holds true, for rodents and rabbits, who are biologically adapted to sleep during the day.

4,7. Windows

How useful are windows for environmental enrichment?

Windows are particularly attractive for cats who, biologically, are intensely motivated to keep visual control of their immediate living environment. On the basis of caregivers' perception, most cats look out of windows for at least five hours a day (Figure 23; Shyan-Norwalt, 2002).

 
Figure 23 An exterior window provides optimal environmental enrichment for cats. Photo by Geoff Loveridge.

We expose our squirrel monkeys to natural daylight via big windows during the summer. This is supplemented with artificial light in late fall and early spring, when the days are short, and throughout the winter. Some of our squirrel monkeys will lie as close to the window as possible and let the sun rays dance on their belly.

I've seen the same behavior in our marmosets. As soon as the sunlight hits the window, the animals stop what they are doing, run over to the window ledge, and start stretching out and basking in the sunrays. There is no doubt in my mind that exposure to natural light, especially sunlight, is highly appreciated by the animals.

All our rhesus macaques have access to one-way glass exterior windows mounted high above ground level. I very often see the animals gather up, attentively gazing out of the windows towards the source of some noise, at caretakers, activities in the garden and birds. One would think that exposure to daylight and the natural diurnal rhythm couldn't be anything else but a good thing for these animals.

I remember visiting a facility that had constructed a playroom for male cynos with a window facing outside. The attending personnel told me that the animals spend more than half of the day, during which they are released in this room once a week, on the shelf looking out of the window, ignoring all the other environmental enrichment gadgets, including toys and mirrors, most of the time (Figure 24; Lynch and Baker, 2000).

Figure 24  Exterior windows can provide macaques with species-adequate distraction in which they do not lose interest over time. Photo by Richard Lynch.

 

This playroom with a window is a great idea! Our facility is in a basement with no windows, just artificial light, which I think is a bummer. Our monkeys never experience natural light or a vista of something more natural beyond the walls. I am sure they would also love an outdoor view. To me it always seems a depressing ambiance in which our animals are forced to exist behind bars. My office is in the animal quarters and consequently has no window, but I have the freedom to leave that "cell." I am sure that lack of natural light does affect nonhuman primates in a similar manner as it does human primates, who can get SAD (seasonal affective disorder) during the winter when the possible exposure to sunlight is decreased by many hours. The great majority of caged nonhuman primates are never exposed to natural light, let alone sunlight.

I have often also thought about this, wondering how nice it would be for our monkeys, if we could put some skylights in their room. I am sure my facility would not go for it!

External windows provide optimal environmental enrichment for diurnal animals.

4,8. Toys

Blankets, stuffed dolls and teddy bears are items that are highly valued by human toddlers, and I would guess also by macaques.

Many of our rhesus and cynos either shred blankets or "stuffies," or they are deathly afraid of them. We had a male rhesus who was donated to us for retirement. Ozzie came with a "blankie" that he loved dearly. He groomed it and carried it around. He was extremely protective of Blankie and only gave it up after he was successfully integrated into a group.

There is a rhesus male in our facility, who is very attached to a "purple stuffed monkey." He grooms his buddy daily, becomes fiercely protective when the stuffed monkey is removed for cleaning, and even tries to take it along to the restraint chair. Patch never attempts to rip the stuffed animal apart, but acts as if it is his social partner. It's so funny! The technician responsible for his care has to hunt for other "purple stuffed animals" in order to replace them when Patch has worn them out. Brown and yellow stuffies will not do, they have to be purple!

We use an assortment of kong toys for our pair-housed rhesus macaques.

I find that they do not pay much attention to them, unless I have stuffed them with some food treats or filled them with frozen juice. Once the contents have been consumed, the toys are pretty much ignored. The little interest they show in

plain kong toys does not differ with the little interest they have for their other commercial toys. Crockett et al. (1989) made a similar observation in single-caged long-tailed macaques.

It is my experience with macaques that the animals show no habituation to destructible, yet biologically irrelevant enrichment such as cardboard boxes, telephone directories and gnawing sticks, but quickly lose interest in indestructible enrichment such as hard rubber toys and nylon balls.

Some very simple toys may become quite attractive, depending on how the animals may actually use of them. When I worked with baboons, we had several males who never tired of their metal cans. Part of the appeal was that, without fail, they would bang the cans very loudly right when you least expected it. You'd be working and the room would be very quiet with just the occasional "coo/whistle" and then suddenly "bang, bang, bang." We'd always jump, and I think it was our reaction—not the cans—that brought the most entertainment.

Dogs quickly lose interest in any toys, unless a human caregiver entices them to play (Figure 25). There are a few dogs who enjoy chewing on them for a while, but the majority don't. I have also suspended a few nylabones on chains. Some dogs chew on them quite a bit, but most are not interested, and after a few days ignore them.

 

Figure 25 Dogs tend to lose interest in commercial toys, unless a person entices them to play. Photo by Animal Welfare Institute.

It is sometimes recommended to exchange toys on a regular basis (rotation) to recreate novelty effects. How practical is this recommendation in your situation?

I am working with several hundred rats, and I rotate their toys. Novelty "returns" after an item has been taken away for a few weeks. Rotating toys to provide novelty effects isn't really that much of an effort. Storing and sorting them is the harder part for us.

Rotating toys for our caged rabbits is actually very easy. If it's noticed that a rabbit is not interested or has lost interest in a particular toy, we simply exchange it with another toy during the morning health check. Otherwise, all enrichment objects are rotated on a routine basis when racks are changed.

We have approximately 500 caged macaques. Their toys are rotated every two weeks. This is practicable.

Destructible toys are usually more attractive and of longer lasting interest for animals in research labs than indestructible toys. For dogs, toys become interesting when personnel entice them to play. Rotation of toys every two weeks is practicable even when this involves a large number of animals.

4,9. Paper-Based Items

Does anyone offer paper or cardboard boxes as enrichment to the animals in their charge?

I use brown paper bags as "foraging bags" for our rhesus macaques. I mix a bunch of cut up fruits, seeds, veggies, and peanuts and wrap them up in a bag. The monkeys rip the bag open and dive in! They seem to enjoy it. Most of them will just eat what's inside, and some will also go for strips of the paper bag. I had a couple of husbandry complaints because the paper would sometimes stick to the cage walls and had to be removed by hand during the hose-cleaning of the cages.

You can avoid this problem by replacing the bags with cardboard boxes. I use empty glove boxes, fill them with shavings mixed with dried fruit and other treats. The monkeys absolutely love them! When they see me coming into the room with treat boxes, they get all excited. Within seconds of receiving the boxes, the monkeys have pulled everything out and proceed eating the treats, leaving the boxes alone for a while. By the next morning, the boxes are completely shredded. Cleaning up the mess is not a big deal for me; it's worth it since the animals have such a great time with these enrichment gadgets.

My rhesus and cynos get paper towel rolls and old phone books. While the cynos will often chew the paper material, the rhesus typically shred it. Animal care staff don't really like this kind of environmental enrichment, because the paper gets stuck to the bottom of the pans. Since the animals really like it, we struck a compromise, offering them paper enrichment not daily, but at least two times a month.

I gave group-housed rhesus macaques (16 animals) one cardboard box once a week and made observations after a habituation period of eight weeks. During the first 120 minutes after cardboard distribution, individuals spent on average 78 minutes tearing the box apart and chewing pieces of it (Figure 26; Beirise and Reinhardt, 1992). At the end of the 2-hour observation sessions, the cardboard box was shredded into pieces that were so small that they did not cause problems with the routine cleaning; no clogged drains! The cardboard box then became a standard enrichment item for group-housed animals.

Figure 26  Recycled cardboard boxes do not cost anything, but rhesus macaques appreciate them as a source of entertainment. Photo by Viktor Reinhardt.

We recycle cardboard boxes and big paper bags in our rabbit playpen. Most animals use the boxes as a look-out post, but some will scratch at them, tip them over and use them as an alcove. Typically, the cardboard boxes are vigorously batted around the cage, so they don't last long enough to get too dirty. The bags make great "tunnels" that the rabbits will run in and out of. Some animals chew on the outer part of the bags, but for the most part leave them intact but well-stomped. The great thing is that when the rabbits are done with a box or a bag, you simply throw it out and replace it with a new one! It's a very inexpensive way of giving rabbits something to do in an otherwise boring environment.

We also have tried shredded paper, but our rabbits don't seem to enjoy it as much as the cardboard boxes and the paper bags. The rabbits turn shredded paper quickly into a stomped, wet soggy mass. This is not a good idea for enrichment!

I often observe some of my techs "feeding" strips of soft paper towels through the cage fronts to our rats, who then enthusiastically chase whoever is in possession of the strip and try to grab bits of it. The one who has the strip tries to sit on it or wrap it around her body, and you finally end up with a pile of rats and lots of smaller pieces of paper. Once the paper is torn up, the game is over. We have not seen any injuries during these games nor any signs of overt aggression. I am not sure who enjoys it more—humans or rats!

Cardboard boxes offer inexpensive and practical yet effective environmental enrichment for primates and rabbits. Rats enjoy playing with paper strips.

4,10. Wooden Objects

I give our single-caged baboons 20 cm long gnawing sticks made of pecan branches. They love them! It takes one to two weeks for a stick to be whittled down to about half of its size.

Gnawing sticks cut from dead red oak branches provide inexpensive enrichment for macaques (Figure 27a,b). The animals do not get bored by these sticks which, due to gradual wear and progressive dehydration, keep changing their texture and configuration, thereby retaining novelty (Reinhardt, 1997).

 

 

Figure 27a,b Rhesus macaques do not lose interest in their gnawing sticks. They like to gnaw at the sticks (a), manipulate them (b) and drag them around. Photos by Viktor Reinhardt.

We use aspen sticks for all our rodents and rabbits. They are soft enough for a good "bite." These sticks are used heavily, which suggests that the animals like them. The sticks can be sterilized for use behind barriers. Normally, they are changed every two or more weeks, depending on how soiled they are and how much is left of them. From my experience, gnawing sticks do not lose their attractiveness over time, probably because they allow rodents to fulfill their inherent drive to engage in gnawing.

Properly sized and properly cleaned/replaced wooden objects provide inexpensive but effective environmental enrichment for rodents, rabbits and macaques.

4,11. Running Wheels


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