2. Basic Issues

2,1. How to Refer to an Animal—Using the Proper Pronoun

It is a custom in biomedical research to use the pronoun "it" rather than "he" or "she" when referring to an animal, even if the animal is assigned to a project in which gender-related phenomena—e.g., reproductive physiology/behavior—are studied. I want to question whether it is really appropriate to use the pronoun "it" for an intact animal.

I once referred to individual study animals as he/she. The principal investigator asked me to use "the animal" instead and lectured me that it is not scientifically appropriate to personalize an animal.

Perhaps you do "personalize" an animal, but this does not change the fact that using the gender-appropriate pronoun "he" or "she" is more accurate than using the pronoun "it," as if the subject had no gender. Why would it not be scientifically appropriate to refer to intact animals with the proper pronouns "he" or "she?" I have always called animals, whether research subjects or not, he or she. To refer to an animal as "it" is to remove oneself from a living creature and regard and treat this animal like a thing. I think animals deserve some respect, and calling them "he" or "she" is the least we can do. "Personalizing" the animals provides them basic assurance that you are considerate of the fact that they are living creatures who do feel pain, discomfort and distress in a similar manner as you do, and that their well-being is impaired when you expose them to discomfort, pain and distress. You will probably do your best to promote their well-being, which will also benefit scientific methodology. Not referring to an intact animal as "he" or "she" but as "it" is scientifically less appropriate than the reverse. After all, a "female" is not a neuter, and a "male" is also not a neuter. No scientist can, for example, study reproductive phenomena in an animal who is neither a "she/female" nor a "he/male." Why pretend that animals have no reproductive organs and label them with the pronoun that we use for dead things, i.e., objects? We usually treat "things" differently than animals, because we know that they are not sentient, and hence do not suffer. Once we label an animal as a thing, the risk arises that we will treat the subject accordingly, for example, as a "standardized biological research tool" (Hummer, 1965) and no longer as a living creature.

The animals who serve us for experimental purposes should be treated with respect. They do deserve to be seen and treated accordingly as sentient beings who are, at the very least, referred to by their biological gender. At our facility we try to use the correct pronouns "he" or "she" for all our animals. Perhaps not surprisingly, the worst offenders for labeling an animal "it" are our surgeons! We do discourage our personnel from using the pronoun "it," since we do not want to encourage them to regard animals as mobile test tubes.

I am not convinced that using the correct pronouns "he" and "she" will change the attitude of people who regard animals as sophisticated versions of "test tubes."

As a clinical veterinarian, I suspect that animals assigned to biomedical research have traditionally been labeled as quasi-objects in an attempt to protect the researcher from ethical concerns about the fact that he or she inflicts pain, distress, and probably also suffering on conscious creatures. The way we refer to animals in our language does reflect our attitude toward them, and the way we attend to their basic needs
for well-being and safety. I guess the research laboratory is a place in which this kind of respect for life is not in high regard, because the research itself often implies the mutilation and killing of animals who are, after all, living beings just like scientists themselves.

As caregivers, we do not use the pronoun "it" when referring to an animal. An animal is not an object! We do not think that calling an animal "he" or "she" encourages anthropomorphism, but that it does acknowledge the fact that we are dealing with an individual sentient being who can feel discomfort, pain and distress in very similar ways as we do. Calling individual animals "he" or "she" helps us deal with something that deep down, we are not really comfortable with—namely the fact that these animals have no choice about deciding whether they want to be used in research and then killed.

Referring to an animal as "it" is neither correct nor scientific, because it overlooks the fact that animals, just like humans, have a biological gender. Therefore, they should be referred to accordingly with the correct pronouns "he" or "she." When we label an animal with the incorrect pronoun "it," we risk treating the animal like an inanimate object incapable of feeling discomfort, pain and distress.

2,2. Higher- versus Lower-Order Species

It seems that "refinement" in the use of animals for research includes choosing lower-order species rather than higher-order species, presumably due to the assumption that the lower-order animals suffer less and that their use in experiments poses fewer ethical problems. Where do we draw the line?

To me, nonhuman primates seem to be sufficiently different from other mammals—in having a sense of self and of the future—to deserve particular consideration, but what about dogs versus mice? There is a great cultural difference, in that humans tend to view dogs as beloved pets, and mice as abominable pests. But does that mean that the mouse is of a lower order, and therefore suffers less from research than a dog? As scientists, using animals for "our" research, we should be in the position to go beyond this weird idea of animals being of a lower or higher order. We are at a great risk of not treating our research subjects very well when we consider them of "lower" order, and by doing so, jeopardize the quality of our research methodology. When colleagues tell me that mice are lower mammals who cannot suffer from anything akin to human mental disorders, I ask them:

If mice are so different from us that they cannot suffer from mental disorders, then what is the point of developing drugs in mice to cure mental disorders of humans?

For people who are using these terms, "lower" simply means "less like humans," and "higher" means "more like humans." This terminology is tied in with the incorrect view of evolution as a ladder of progress toward especially evolved beings, such as humans. How would animals, used by humans for biomedical research, classify the human species? Of a high order? Crown of creation? Very unlikely!

An animal species cannot be considered of a relatively "higher" or "lower" order on any scientific ground, because the idea of "lower" and "higher" is just a concept that does not reflect reality. We classify different animal species into a higher or lower order, depending on our personal, hence subjective relationship with these species. This view puts all animals commonly regarded as vermin or pests into the lowest order—e.g., mice and rats—and those animals who have a charismatic appeal, because we know them as companion animals—e.g., dogs, cats, rabbits, hamsters and guinea pigs—nto a higher order. Finally, we put animals who look and behave in ways that are similar to humans—e.g., monkeys and apes—into the highest order. The fallacy in this categorization is that it does not help us determine whether one species suffers more during a certain experimental procedure (and hence deserves more of our concern) than another species. Unfortunately, even professional animal care guides use these unscientific terms of "lower" versus "higher" order animal species. I did a "Google search" on the exact wording "higher species," and my first hit was the Canadian Council of Animal Care (1997), one of the most renowned resources on laboratory animal science. Here is the statement:

The creation of transgenic animals is resulting in a shift from the use of higher order species to lower order species, and is also affecting the numbers of animals used....An example of the replacement of higher species by lower species is the possibility to develop disease models in mice rather than using dogs or non-human primates.

This document does not elaborate on what scientific ground mice are categorized as a "lower" species that implicitly deserves less animal welfare concern than the "higher" species of dogs or non-human primates. The fact that rats and mice are commonly considered of lowest order has probably allowed US legislators to explicitly exclude rats and mice in the legal definition of the term "animal," thereby negating the two most commonly used research animals' legal protection of their basic welfare requirements (United States Department of Agriculture, 2002). This begs the question:

What is the point of having animal welfare legislation if it does not protect the great majority (>90 percent) of research animals?

I think all animals deserve the same consideration, whether they are a rat or mouse—of presumed low order-or a dog or monkey—of presumed higher order. It seems strange to me to categorize animals into different orders and then treat them accordingly.

Do those of you who work on a daily basis with different species in the research lab, feel that the degree of discomfort and distress experienced in the artificial living quarters and during standard procedures differ significantly between species of alleged higher versus lower order?

In my daily work with rabbits, rats, mice, hamsters and guinea pigs, I do not see species differences in the animals' reaction to discomfort and distress. When you ask if it is less distressing for a mouse than for a dog or for a monkey to be killed, I think there is no difference. If there is a difference, it is probably due to the person who does the killing.

Working with quite a number of different species, I have found that the prey species—such as rodents and rabbits—tend to be more distressed during enforced handling and restraint than predator species—such as dogs and cats. All rodents are distressed when they are kept alone, perhaps not to the same degree as dogs or monkeys, but they are distressed nonetheless. To this very day, I feel for every rat, mouse and guinea pig who had to live in our facility without contact with another companion. Frogs do not give the impression of being distressed in their living quarters, but they seem to be just as distressed as warm-blooded animals are when they are handled by people.

Many years ago, I worked with macaques and rats who were kept alone in barren cages. Both the single-caged rat and the single-caged monkey, were miserable—depressed and bored—and I must admit, I could not tell a difference in the degree of distress that they experienced. I have the feeling that even though we may categorize them as animals of "lower order" versus "higher order," rats and monkeys do not differ in their observable distress response to being permanently housed alone in boring living quarters. These animals were often restrained by humans for procedures. While the monkeys always resisted and gave the impression of being scared whenever they were restrained, the rats seemed to tolerate the procedure. The observer got the impression that being restrained was a much more distressing experience for monkeys than for rats. However, there is no reason to believe that this particular difference is somehow related to monkeys being more evolved than rats. The fact that rats do not show their distress during restraint is probably a biological trick that increases their chances of not being killed by a predator who has caught them. Being forcibly restrained is probably equally distressing for all animal species, but some show it while others don't—for biologically sound reasons.

How useful is the concept of genetic relatedness in terms of animal care and welfare? Does the genetic relatedness of animals with us, the human species, affect our concern for their well-being and our willingness to care for their welfare while they are used for research, and when they are no longer used for research?

It can be a little dangerous to suggest that a particular species deserves better care than another—for whatever conceptual reasons—because it implies that this species (for example, chimpanzees) is more capable of suffering than another species (for example, rats). This belief reinforces the misconceptions of those who might wish to protect nonhuman primates, cats and dogs, but not mice and rats. Genetic relatedness should have nothing to do with our welfare concerns for animals. Suffering is a subjective experience, and it is therefore impossible for us to know how another organism is suffering. It might be easier for us to appreciate that an animal is suffering in more genetically related species—e.g., monkeys—because they behave similarly to us, but it does not necessarily mean that a genetically less related species, such as rats, cannot suffer similarly as we do, or as monkeys do. We just don't know, and as long as this is the case, we must assume that suffering is a universal phenomenon that may vary from species to species and between individuals of the same species, but which is experienced as unpleasant by all animals—including humans—independent of their genetic relatedness.

I believe that humans, other mammals and all vertebrates are capable of suffering, but what about invertebrates? Some are probably suffering, but I cannot imagine an amoeba does. So, where do we draw the line and stop worrying about suffering?

There are questions that are out of our reach, yet this does not imply that I disregard the fact that invertebrates are life forms and, when I observe them a little bit closer, I will quickly find out that all, including the amoeba, avoid "dangerous" situations, and that none of them wants to be killed. So, I try not to kill them consciously and without a "good" reason, e.g., ending the incurable suffering of an animal.
I do not believe we should be using something as vague as genetic similarity to determine how an animal should be cared for. I care for all animals with the same concern for their well-being. Whether they are rats or primates, they all deserve optimal care. Humans share about 40 percent of their genome with bananas, and 85 percent with mice. If this is the case, do we give 98 percent of our welfare concerns to chimps, with whom we share 98 percent of our genome, 85 percent of our welfare concerns to mice and 40 percent to bananas? Are we twice as worried about the welfare of mice as we are about bananas?

It seems absurd to use a human mind-created concept—such as genetic relatedness—as a guide for one's degree of compassion for an animal of another species, yet it seems that we tend to be more casual, focusing more on human concerns than the concern of the animal subject when we design living quarters and develop handling techniques for mice versus monkeys. Why?

I have the uneasy feeling that genetic relatedness with the human species is just a pretext, while money is the actual cause for our relatively discriminating treatment of mice. After all, it is much more expensive to care for one monkey than for 100 mice, and it is much more expensive to replace one monkey than 100 mice. Perhaps this is the main reason why we tend to be more responsible when doing research with monkeys versus mice, i.e., animals who are genetically related to us, versus animals who are less related to us.

To classify animals into those of higher versus lower order, or to classify animals according to their genetic relatedness to the human species may have theoretical value, but it would be unscientific to use these concepts to determine the relative importance of the respective animals' welfare needs.

2,3. Human-Animal Relationship

2,3.1. Affection for Animals

Should animal care personnel be encouraged to establish and foster affectionate rather than neutral relationships with the animals in their charge?

Animal care personnel and researchers should be encouraged to develop affectionate relationships with their animals. Having such a relationship assures that you regard the animals as living beings, rather than biological test tubes. As such, you will be more careful and more patient. You will think more about what the experimental procedure implies to the animals. You will get more creative in refining procedures that are normally stressful or distressing to the animals. You will thus enhance their well-being and, by doing so, you will increase the scientific validity of the research results.

I became a vet tech because of my love for animals. I chose this job because the animals here are in need of someone who cares about them, and not so much because of the research data they provide. If I can make the life of just one of the animals under my care more comfortable and possibly more enjoyable, it is worth all the effort to me. We all grapple with this same issue:

Many of us will rejoice when animals are no longer required for research purposes and will gladly seek another profession at that time. Until then, the animals need us!

When asked how she deals with attachment to animals in her care, a veterinary technician gave the following answer for the journal Lab Animal (Anonymous, 2006):

Even the American Association for Laboratory Animal Science (2001) concedes that:

And Herzog (2002) elaborates that:

I agree wholeheartedly that developing a close bond with research animals can only be a good thing. It seems to me that we can easily get hung up on trying to divorce our emotions from objectivity. I don't think that any normally functioning human being in the world does anything for any reason other than emotional. Is it not the premise of all biomedical and ethological research to make human and animal lives better? If you want to make lives better, it's because of emotion, not because you are logically attached to life. I feel empathy for my animals, and I am genuinely concerned about their well-being, otherwise I would probably not notice when an animal is not behaving and responding normally because of a developing health problem.

For some people, it may be defense mechanism not to get too attached to animals who are intended to be killed within a short time. Wouldn't it be unbearable for technicians to euthanize hundreds or thousands of mice—sometimes after having had to make these animals ill and suffer—during a work year, if they were emotionally attached to each and everyone of these mice? As a researcher, I do take the animals' welfare very seriously and get terribly upset if they suffer, even though I don't have an affectionate relation with them. It's perhaps not necessary to develop affectionate relationships, but kindness toward animals should be a professional prerequisite for any person who is hired to care for animals in research labs. We owe this to the animals!

We also owe this to ourselves, because when we are not kind to animals, we are also not kind to ourselves and to other people. How can we ever expect to find happiness when we are not kind?

If you are not kind to your animals, make no attempt to enrich their boring, often depressing living quarters by addressing species-typical behavioral and social needs, and never show any kind of affection toward them (for example, by offering them food treats from time to time), then I really don't think that you should work in an animal research laboratory. Unfortunately, I did and still do find such people in animal quarters, so if anyone is offended, well, you just might be guilty!

Being indifferent, inconsiderate and rude has no place in a lab, zoo, or anywhere, for that matter.

For me, developing affectionate relationships with the monkeys in my charge (Figure 1a,b) is always a spontaneous process. I know that I could develop this sort of rapport with other species, but based on my experience with mice, I do wonder whether there is a size limit.

If you are on good terms with the animals in your chargehere a rhesus macaquethey will show their trust by engaging in affectionate social interactions with you, such as grooming (a) and allowing you to groom them (b). Photos by Robert Dodsworth.

The way we handle mice is not very attractive! It would never cross my mind to lift a larger animal by the tail or scruff, essentially ignoring whether or not he or she is cooperative. I suppose we handle mice the way we do simply because they are so small. I am really wondering as I look at a picture showing a huge human hand grabbing a tiny mouse baby by the scruff! For an animal that small and vulnerable, the evolutionary programming might very well be "Live as if there was always somebody wanting to eat you." Is it still possible to establish a relationship of trust with mice, in which they will come to you and enjoy being with you, and in which you can exchange signs of affection?

Yes, it is entirely possible to establish a close relationship with mice, involving trust, petting, and lots of physical contact. This is done with rats all the time, and the two species are not that different. The problem with mice is that most of the ones we're likely to come into contact with are wild. I have live-trapped hundreds of deer mice in my house and have never been able to turn them or their offspring into pets. You just have too many generations of skittishness bred into them. On the other hand, one of the best pets I ever had was a store-bought mouse. He was pure black and his name was Juarez. He lived in a small cage with a wheel, and he loved to come out every evening for some cuddle time and hand feeding. He was as tame as a dog—very responsive in every way.

We had a wild mouse spending two winters in our home. She would appear in the fall and make her way out again in spring. Each evening, we could watch her from our pillows as she explored the desk in which she had also built her nest. There was no way for us not to get to know this critter very well, and the naming happened automatically. So for us, this tiny little mouse was not just a mouse, but Minette. I am telling this story to make the point that the development of an affectionate relationship with animals does not necessarily depend on their evolutionary relatedness with our own species or on their size, instead, it may well be a function of the amount of time we spend observing individual subjects, and by doing so, discover their uniqueness. Rats and mice are very charismatic when you deal directly with them, rather than with the "idea" of them (Figure 2). My students often say things like, "Oh, they're actually rather cute" when finally coming face to face with these animals.


Figure 2 You just have to watch them closely to realize that "even mice" are charismatic animals, not just disposable test objects. Photo by Larissa Lone.

2,3,2. Giving Animals Names

Do you give names to the animals in your charge?

Do you give names to the animals in your charge?

Naming the animals helps me realize that I am working with sentient beings who deserve my consideration of their well-being. It is probably more difficult to be callous toward a monkey who is called John than to a monkey referred to as ID #79045. As a clinical veterinarian, I observed that nonhuman primate-caregivers became markedly more concerned for and interested in the animals in their charge when the ID number tags on the cages were replaced with name tags. I guess we can all relate much better to names than to numbers, and we tend to treat named versus numbered animals accordingly. The naming of animals in research labs could serve as a safeguard for optimal animal care.

I was encouraged not to assign names to the many rhesus monkeys in my charge. I was admonished that the animals are research subjects, not pets. The concern was that having names for the animals might blur this distinction between a research subject and a pet. It did not seem possible to remain distant —emotionally isolated— from the animals. In fact, the inevitable closeness that resulted from those intimate interactions was precisely what made us capable of doing what we were asked to do. Eventually, we all came to know that F49 was Sam, A12 was Rosie, and Z13 was Curious. Such attachments are the results of compassionate people doing their job right (Wolfle, 2002).

We have an investigator who is against the naming of rabbits assigned to her research protocol. The PI (principal investigator) is afraid that, when bonding with her research subjects, we add a variable that is detrimental to performing research. Our staff feels that this is an antiquated mentality and we are standing strong in our position of naming all animals in our charge!

I have run into that same mentality here, but ended up naming the animals anyway, using their ID numbers only for the records. I name our animals primarily because we have so many of them, and it helps our care staff and me keep

better track of who is who. We have monkeys, cats, rats, rabbits and mice. All of them, except the mice, have their names. We have a high turnover of mice, and this makes the name-giving a bit of a challenge, but we name the mice who stay around for a while.

Giving names can cause methodological problems under certain circumstances. I remember a large breeding group of rhesus macaques who was constantly tyrannized by the beta-female and her female ally. The beta-female was so vicious that I gave her the name Devil—her official ID was t-42. The situation became serious and I finally had to remove Devil and her buddy to restore the group's harmony. If I had assigned Devil to an ethological study and done the observations myself, my perception would have been pre-conditioned, probably not so much by the name Devil but by the experience I had with that particular animal. Knowing that Devil is vicious, I would presumably put my attention first on her before anybody else—for instance, if a group member screamed during a dispute. In this manner, Devil may end up being scored as the most aggressive animal of the group, which she actually was not, because I have unintentionally missed many overt aggressive acts from other animals.

I think that it is not really the name Devil that would have influenced your attention but the actual experience you had with this animal. You cannot avoid such experiences, so your focus of perception is bound to be pre-determined by memory. This is unavoidable regardless of whether we give the animal names or go by their IDs.

2,3,3. Touching Animals

When you work with animals on a regular basis, you may develop an attachment to certain individuals and then want to touch, stroke or groom them. This is a very nice experience, but it can be dangerous if you misunderstand the subject's feelings and motivations. How do you know for sure—and you must be sure for your own safety!—that an animal wants to be touched, stroked or groomed by you? Rodents

If a rat enjoys being groomed by me, she will respond with a relaxed stance and closed eyes, and then she will also start grooming my hand.

A few years ago, we had a small litter of mice who lost their mother when they were only 12 to 15 days old. They were without a mother for almost two days. I was successful in caring for three of them to the point that they thrived. Because of the stressful event of losing their mother before weaning, they were not suitable for research purposes. They became my "sentinels," really my pets kept at work! I would handle them a little more during cage changing than the other mice, but not usually between cage changing. Over time, the male mouse came to accept my petting. He no longer moved away but seemed to be completely at ease with the situation. His two sisters were different. They did not like the gentle head rubs and always tried to get away the moment I touched them.

I often had the chance to hold guinea pigs in my hands but never got the feedback from the animals that being gently stroked was appreciated. The animals would remain still and would never contact-vocalize in the typical guinea pig fashion; they showed no reaction to being petted. Adult guinea pigs never groom each other, so it is probably not such a great experience for them to be petted by a human.

Hamsters and rabbits demonstrate very clearly that they do not enjoy being touched: they try to get away from my hand.

2,3,3,2. Monkeys

In our aotus monkey colony, we have a few animals who will back up to the front of their cages to get a good back-scratch. If you stand in front of their cages, stick your fingers up and do the scratching motion, they will back up, and you can see on their faces that they enjoy it when you groom them. When they have had enough, they just leave.

When a rhesus monkey approaches me and does a rump or chest present, I can tell the animal wants attention. Typically, a monkey will press his or her body up against the cage, allowing me to gently tug at the fur from the outside of the cage, as if I were grooming. I am sure the animals enjoy this as much as I do.

I have one girl, Meera, who loves to have her bum rubbed and her face groomed. She actually asks for it by presenting herself. This is a very clear signal that the animal is not afraid of you and wants you to come closer and, as in this case, start a grooming session. We had another monk [monkey], Kiwi, who absolutely loved human contact. She would pretend to be asleep after a procedure, so that I would hold her longer before placing her in the recovery cage. I used to watch her squint her eyes slightly open to see what was going on, only to quickly close them if someone was looking at her!

The key signal that tells me that an animal likes to be touched is when she or he "presents," i.e., entices me to do so. A chair-restrained rhesus monkey, for example, will twist her body in an attempt to present her rear, thereby letting me know that she wants to be groomed. Under such a condition, the monkey will show no fear or aggressive-defense reactions, but rather be relaxed and calm.

I know quite a number of rhesus macaques who will present their chests, only to get very mad when you touch them. Maybe presentation is not always a reliable sign that an animal wants to be scratched?

What you describe is a quite common scene in primate labs. I believe that, what the animals are doing is nothing less than teasing us. These guys are bored in their cages—who wouldn't be?!—and they are looking for some action. They present their chests or rear ends to the naïve caretaker or visitor, knowing beforehand what the reaction and the outcome of this little game will be. You have hardly touched them, and they will turn around, bang against the cage wall like a devil and/or threat-yawning like a lion. You may be shocked and react accordingly, and that's what they are after: your reaction to their display. Your reaction will reinforce the teasing. Once you no longer participate in this game, you will no longer be invited to groom, but you can pass those animals without being harassed.

A human-animal relationship that involves contact is very rewarding for both human and animal, and it helps to instill and foster trust. As such, developing such a relationship with macaques seems worthwhile as long as it is done carefully. It is usually fairly evident which animals are soliciting grooming simply to tease you and which ones really want to be groomed.

2,3,3,3. Cats

Cats are a bit tricky when it comes to trust. They can easily give you the wrong impression of enjoying being touched. Their time span for direct continuous social contact is usually very short when compared, for example, with dogs and monkeys. When you have reached this time limit, you may be in for a hiss or even a scratch. These critters can switch from "I am in bliss while you groom me!" to "Let me alone!" in a blink of an eye. I have had encounters with cats during which they allowed me to touch them, and then all at once, without any warning, turned around and gave me a swat. In some cases, the animal will solicit to be touched again right after swatting.

This exact situation happened to me just yesterday. I was at a friend's house and her cat entered he room. The cat knows me well and jumped straight on to my lap. He settled down, began purring and kneading, and seemed very comfortable with my stroking him. After a couple of minutes, my attention was distracted and I looked away, and at that very moment my hand was suddenly attacked, quite viciously! I think cats might be a special case, because they are generally solitary but live in groups when there is plenty of food available. Perhaps they have not lived socially long enough to have evolved a gesture to say "Thanks for the strokes, but I've had enough," other than by hissing.

2,3,3,4. Farm Animals

One of the bull calves in my charge looks forward to a daily "sponge bath." When I approach his stall, he gets up, sticks his head out and watches me until I come over. He constantly rubs on me while I am wiping him down with a damp cloth. I have no doubt that he likes it very much. If you gangbust calves and go to them for petting, they are usually fearful and combative, but if you give them the space to make their own decision when to approach you, then you can scratch them. They seem to truly enjoy this and often end up being quite affectionate (Figure 3).

Figure 3 Most social animals like to be touched, provided they trust you and can initiate and terminate the interaction at their own wills. Photo by Viktor Reinhardt.

I have worked many years with pigs and can affirm that they do enjoy human touch very much, but it must be their idea, and they will of course let you know when it should end, usually by moving away or vocalizing if they feel trapped. I purchased a toilet brush for scratching the pigs in my charge. Most of them cannot resist, once they realize what it is for and how good it feels. They seem to like being scratched just about anywhere. When I need to obtain a rectal temperature, I scratch them around their tails. They like this and stand still, allowing me to get their temperature without any ado.

2,3,3,5. Cold-Blooded Animals

When we had tree frogs in our home, I would often gently "tickle" one of those little guys under the chin. The frog would be transfixed—as they often seem to be—but I couldn't figure out if the animal was blissed- or stressed-out.

My daughter has a leopard gecko who is very responsive to human interaction, and it is obvious that he prefers her to anyone else. If I am holding him and she comes near, he literally jumps to her. He tracks her voice and likes to crawl up on her shoulder. As for touching, he will tolerate his chin being rubbed, but other than that he doesn't like to be "petted."

I have had a female green iguana as a pet for seven years. It is my impression that she loves it when I rub her neck or gently scratch her back; she closes her eyes and leans into my hand, almost like a dog.

I had an Oscar fish who loved to be rubbed on his stomach/ventral area. Oscar was trained to jump, roll over and move from point A to point B. He was used for training/teaching purposes only, but became very attached to certain caregivers, i.e., would only eat if fed by them and would even allow them to rub his stomach. He was great with the students because he opened their eyes to the idea that fish have more cognitive abilities than most people give them credit for. I don't know if Oscar was an anomaly, but I am willing to bet he wasn't.

When I was a boy, I used to touch trout in our river. I would reach under one of those typical overhanging rocks and very carefully find my way to a trout. Gently stroking her belly with my fingers would inevitably make her stay still.

2,3,4. Alleviating Fear of Humans

Does gentle, regular interaction with humans help animal subjects overcome their fear of humans when they are handled during experimental procedures?

I firmly believe that regular interaction helps animals overcome their fear of humans and procedures. Several years ago, I worked on studies with rhesus, in which we were told that the animals would become very ill and require great care from all the techs in order to keep them comfortable. Because we were doing terminal studies, we generally received "recycled" animals. Many of them were quite afraid of humans when they arrived in our lab, but we were instructed to spend time with them so that they would become used to our presence and develop a bit of trust in all these hairless apes. We would sit by their cages, give them treats, and try to desensitize them to human contact. The time we spent proved to be very beneficial when we would have to care for these animals later during the actual study. I will admit that we didn't have a 100 percent success rate, but quite a number of animals would would seek our attention and affection after a while. I vividly remember an adult male cyno who would raise his arms up, much like a small child, to be lifted from his cage to the examination table for treatment. Following treatment he would cry if placed into his cage immediately, because he wanted to spend a little more time outside, being held or groomed by one of the techs.

I have fostered a relationship with some of the rhesus macaques in my charge, strong enough for reciprocal grooming (Figure 1a,b). Animals with whom you have this kind of affiliation are more apt to cooperate under routine husbandry circumstances such as catching, weighing and TB testing. Having such a close bond with one of our rhesus girls helped me tremendously when it came to "doing business" with her. Kia was a very friendly monkey and liked pretty much everyone. Because I worked with her every day and was the one feeding and playing with her, I like to think that she had a particularly strong bond with me. On a few occasions, she escaped, and I was able to walk into the room, scoop her up and place her back in her cage. During chair training, she would snuggle into me—like a child hugging her mother—and we would sit in front of the chair. I would put treats all over the chair and she would retrieve them without leaving my side. She was a doll when I had to give her injections. There was no need to squeeze her, I only had to show her the syringe and she would back up close to the front of the cage and allow me to proceed with the injection. I had not trained her to cooperate: she just did it spontaneously. I visited Kia several times a day and we would often groom each other.

Some of the marmosets I deal with will groom the back of my hand if I "present" it to them, or they will jump onto my shoulder and groom my hair or neck. One particular marmoset even tries to pry my lips open to "groom" my teeth—but, yes, there are limits! The marmosets with whom I have a grooming relationship don't have to be physically restrained during common procedures, probably because they don't see my hand moving in their direction as a "threat."

Caged macaques often freak out when a person dressed in professional protection garb is entering their room. When such a person wears heavy leather gloves, things get really wild! What can we do to help the animals deal with their negative experience-conditioned fear of people?

Several things seem to help our monks:

  1. The animal care staff and the researchers are in and out of the rooms frequently, at least once every two hours. Our researchers are very good about just visiting their monkeys (Figure 4).
  2. We try to make each visit not a frightening experience for the animals. We remain quiet and avoid sudden, jerky movements that could alarm the monkeys.
  3. Low-level background music is played all day long in the monkey rooms.
  4. If one monkey is being sedated via intramuscular injection and taken out of the room, we give a food treat to each of the other animals of this room.

Our monks are pretty good about not freaking out when someone enters the room.

Figure 4 Animals who are visited regularly by research personnel gradually lose their fear of people. Photo by Viktor Reinhardt.

It is great that your researchers are taking the time to visit the monkeys. If more investigators would be inspired to do this, less negative conditioning would probably occur, because the animals would learn through experience that the researcher is usually harmless, not a life-threatening enemy.

2,3,5. Summary and Conclusions

Relationships that develop between facility personnel and laboratory animals may result in an overall reduction in stress for the animals, and they may serve to buffer the potential stress of certain experimental situations. Administrators of animal research, testing, and teaching programs should look for opportunities to encourage the development and maintenance of bonds between personnel and laboratory animals, beginning with the initial employee interview (Bayne, 2002). Researchers must continue to question the barriers that have traditionally been erected against forming human-animal bonds in the name of objectivity and to investigate seriously the ways in which fostering the formation of such close relationships can promote animal welfare without compromising the scientific respectability of research (Russow, 2002). Naming animals helps to correctly and quickly recognize individuals. An affectionate relationship based on mutual trust often makes it possible to touch or groom an animal. Certain postures and gestures indicate whether an animal likes to be touched. The fear of humans can be alleviated by visiting animals with good intentions on a regular basis.

2,4. Emotionality—Is it Unprofessional to Cry?

Working with animals for researchers can sometimes be very stressful, hectic and frustrating. Is it justified to cry at work once in a while?

If I cry due to work-related issues, I just remove myself from everyone. If anyone notices my emotions, it is labeled as unprofessional.

Are you joking? I cry at work all the time! More seriously, crying at work for the animals can mean that your empathic feelings are alert, rather than put to sleep by the routine of the lab work. So, to me, it is a healthy response to an emotionally upsetting situation. I would ask those who are uncomfortable with those of us who cry to just let us be, especially if it is not interfering with our work. Crying is an important safety valve that some of us need. I do the termination of my macaques, because I want them to have the feeling that this day is not different from those when they are normally anesthetized. Some of these animals I have worked with weekly, if not daily, for up to five years. That loss deserves some tears! I believe in the research that is done with the animals, but this does not hinder me from offering them the best possible care, and I will cry when they are gone.

I have also cried at work on occasions when an animal suffered unnecessarily, or when I was involved in putting down an animal I had worked with for a long time. Expressing one's sadness is only unprofessional if it prevents me from doing a job in a way that is best for the animal. Otherwise it is simply an indication that I have compassion. One of the most horrible times I ever had at work was when we traded out one dog for another, who would be used for a terminal study. We had received a group of dogs from a class B dealer, and a huge beautiful golden retriever pup who we named Anton was one of them. It was decided that if we could find a trade with the dogs we already had, we would save Anton. When my supervisor brought the little female terrier mix over for the trade, we just broke down. We used her because she would never be able to be adopted out due to the tick-borne disease research she had been used for. She was so sweet! I sat there for a good 30 minutes crying and talking to her and hoping someday she would forgive us. On the positive side, Anton is running on the prairie with a loving family!

Whenever an animal had to be put down, be it mouse or dog, my supervisor was very strict about respecting the animals' dignity. If anyone joked or kidded about it, she was like a cobra to correct them as to why it's no laughing matter. She is still my dear friend! We do such a tough job, especially, since I think all of us are animal lovers. If we didn't cry, we would probably also not care, and wouldn't feel bad about what we are doing. If I didn't cry in the face of the animals' suffering, I wouldn't be in this profession. I, too, have hid in order to be alone, because crying is looked down upon here. I do support the research, but I am also sad that there isn't yet another way besides using animals to accomplish the goals of this research.

I am glad—as hard as it is on a daily basis—to work as an animal technician, because I feel that I can offer the animals a special gift. Every day, I do whatever I can to foster their well-being and make sure that while they are here, they are getting the best care possible—and the best toys, of course! After working with a group of beagles for several weeks, I was asked to assist in the euthanasia of my favorite one, whom we had nicknamed Cico; he was a porker but so cute! I did assist, but I cried like a baby. My co-workers' solution was that I should not be around for future euthanasia. But this was not the point. Even if I wasn't there for the euthanasia, I still would have been upset; it's hard not to be. I did and can do the euthanasia; that's part of my job. I have not had to say goodbye to any of our monkeys yet, and I honestly don't know how I'll deal with this situation.

Yes, I think it's absolutely normal to be sad and cry sometimes with our line of work. To bottle up feelings of sadness, frustration or anger doesn't change the unacceptable situation but drains your energy and enthusiasm and makes you bitter. Walking through animals rooms, with row after row of cages from which lonely monkeys were sadly looking at me, made me often cry because of my limited power to change the situation. It's hard to be exposed to these realities. Crying is certainly a more healthy response than angrily arguing with investigators or administrators who are responsible for the situation. The first response gives you some relief, the second makes you even more frustrated, tense and angry—because you are usually talking to deaf ears.

People often make the mistake of assuming that we must not be animal lovers, because we work in biomedical facilities. I think it's just the opposite. Most of the animal technicians and animal caregivers I know truly do love animals, and I think this is the main reason why we chose to work for the animals in research labs: we can make life easier for the animals in our charge. Yes, there are some days that are almost unbearable, but I know that I do make a difference for the animals, and this is what keeps me from running away. The animals need me!

I work with guinea pigs, and we euthanize quite often in order to collect tissues. I haven't cried yet, maybe because I don't spend much time with individual animals. Although I don't cry, each euthanasia hurts! I'm not a crier normally, but I do go through times of depression. I can't tell you about my experiences of loss and sorrow both for personal and professional reasons, but I can say that the feelings we have for the animals are an important part of what makes us the best candidates for our field. Imagine if we had no feelings for the animals we work with. Things would be horribly different. Try to keep in mind what you give them and why you are important to them. It is the nature of this field that makes it difficult, but through love and commitment, we are able to lessen the burden on the animals.

We too had to let some of our guys [macaques] go off to a better place. Although no one would express any tears, there would definitely be a different feel in the air. Some became quiet, others a little snappy, and others would choose to just not be around for the terminal procedure. As for myself, the day before, I would sit with "my young man" or "little girl" and talk to them. I'd let them know that I was happy for them to move on, and thank them and apologize for the sacrifice they have done for us. It is embarrassing to cry at work. Therefore I don't, but I've come close! I will always think of the monkeys I have had the privilege to work with, and I will always talk about them and tell stories about them for a long time.

A month ago, we had a young monkey experience a seizure after she was used for an experiment. After the seizure had stopped, she was paralyzed completely on her left side. She was awake, alert and hungry. Every time I tried to give her some food, she made an earnest attempt to sit up, but invariably would flop all over the place. It was heartbreaking to witness this, and I couldn't help but cry. Here was this perfectly healthy animal, and we did this to her! Because I work with the girls on a daily basis, I can't help but become attached to them. I can't work any other way. I know what I'm in for, what they're here for and what will eventually happen to them. I'm fortunate to have an understanding boss. When the time comes to sacrifice an animal, I will inject the anesthetic and that's the last I see of the animal: a sleeping peaceful monkey. It is comforting to know that I am not the only one who gets upset with much of what we do and that there are other people with whom I can share my feelings.

In conclusion, it is not unprofessional to cry when you face situations in which animals have to be killed or endure unnecessary discomfort, pain or distress while you are helpless to interfere on their behalf. The expression of sadness in such situations is a reflection of your sincere concern for the well-being of animals.

2,5. Humane—What Does this Term Mean?

How would you define the word "humane" in the context of animals in research institutions?

I think the term "humane" should be defined as "to treat animals the same way you would treat a human being," that is to say, with respect and concern for their well-being.

If only you were right! Humans very often treat humans even worse than they treat animals. Those who have obtained a certain power position—be it social, economical, political or sheer muscle strength—often misuse their power and treat other humans in ways they would not like to be treated themselves. It is a very sad reality. I think the term "humane" implies an idealistic vision, yet we do need a working definition because it is used in legal animal welfare texts such as the US Department of Agriculture's Specifications for the "Humane" Handling, Care, Treatment and Transportation of selected animal species (United States Department of Agriculture, 2002). The term "humane" is not defined in these regulations, leaving it up to the research industry to interpret it as deemed practicable. The National Research Council claims that the goal of its Guide for the Care and Use of Laboratory Animals is to promote the "humane" care of animals used in research, but fails to explain what this quasi-noble term actually means (National Research Council, 1996). Not being defined, the term "humane" has no value and lends itself to subtle and gross misinterpretation when used in animal welfare legislation and guidelines.

I am not sure I can tell you what the "humane" treatment of research animals means to me. Our chosen field of practice tends to skew our view of the plight of research animals. We amputate their toes for identification, we cut their tails for genetic analysis, we burn them to study healing, and we subject them to chemicals to see how these harm them. We have many, many ways of causing them harm to study abnormal occurrences in humans, and then we "sacrifice" them at the end of a study. This does not sound very "humane" to me, but who am I to judge.

If we do all these "inhumane" things to animals, don't we have to "judge," i.e., make an ethical assessment so that we can live at ease with ourselves? If this ethical assessment puts us at dis-ease with ourselves, we will do something—for example alleviate or avoid the pain or distress of other creatures—to come back to a state of mental and emotional ease.

2,6. Euphemism—Do We Really "Sacrifice" Animals?

How appropriate is it not to use the verb "killing" when we euthanize an animal at the termination of a study or because the animal is no longer of use for biomedical research?

Many times, I got in trouble for writing in a protocol or report that the animals will be "killed" at the end of the study. In the interest of clarity and honesty, I always put "killed" in the first draft, but it is inevitably changed by someone higher up the chain to "euthanized" or "culled." It seems to me that it would be more honest to stick with the facts. When it comes to terminating an animal's life, euphemism is a cheap way of beating around the bush. The word "sacrifice" implies that the act of killing is "sacred" [justified] and performed by a "priest" [the scientist], and that the subject is "offered to a deity" [science]. This euphemism is a gross distortion of reality. Things are much more "down to earth" than this: we "kill" the animals!

The principal investigator who kills animals—or has others do the killing on his or her behalf—to achieve the goal of his or her scientific endeavor probably feels more at ease when he or she can hide behind the elegant phrase: "I have sacrificed animals for an important scientific project." This kind of wording is not "scientific," because it has nothing to do with the reality as experienced by the animal who, de facto, is killed.

To me, the word "killing" paints a picture of violence, so I prefer to use the verb "euthanizing," because it makes me feel somehow better about the death and loss that I face daily. It can at times be overwhelming! "Terminating" is also accurate but carries the same coldness as "killing." When I have to euthanize an animal, I am not callous, but do it in the most humane way possible.

I agree, "to euthanize" seems to be the most appropriate verb, however, it may be misleading in regards to animals who are "killed" because they are surplus. When watching hundreds of "surplus rats" being killed or gassed in big tanks, because they are "spent," have the "wrong sex," have the "wrong phenotype," or have reached the "end of research," I don't feel the word "euthanasia" is appropriate. I am not so certain that rodents killed with gas as a way of "inducing death without pain" do not experience distress—either in theory or in practice. I believe the majority of them are in panic and feel considerable pain before they get unconscious, particularly in "bulk killing" settings.

If we use the terms "sacrificing" or "euthanizing" with full awareness of what they actually imply to animals in research, we are honest to ourselves and we will do our very best to minimize the discomfort, pain and distress that the animals may experience during this life-terminating procedure. If, however, we use these polite terms to give the impression that what we are doing is justified and humane, we are dishonest to ourselves and to the lay public.

2,7. Self-Awareness—Do Animals Recognize Themselves?

Some species we are working with respond to the reflection they perceive in a mirror. They may use a mirror to see objects that they could otherwise not see, and they may respond to the reflection of other conspecifics and of themselves differently. Do they recognize their own reflection as themselves?

It's funny that you have brought this up, because just the other day I was telling the story of such a case. In my first job, we had a cyno (long-tailed macaque, Macaca fascicularis) who, we firmly believed, was conscious of himself. He would use his small cage mirror to check areas of his face for grooming and to send facial expressions across the room at other animals. Our attending vet found this so delightful that he bought a large wall mirror and hung it across from the monkey's cage. We then all got a kick out of this animal using the mirror to examine and groom the fur of his back and to check his teeth very thoroughly. He must have recognized the reflection in the mirror as himself. If he had thought the reflection was another monkey, wouldn't he try to groom the mirror monkey rather than himself? He was a real character!

I worked with two rhesus females who would very attentively look into mirrors while grooming their own faces, especially around the eyes. To me it seems logical to conclude that these two monkeys made the connection between the reflection in the mirror and the sensation that went along with seeing their own faces being groomed: they saw themselves being groomed.

One of my cynos seems to recognize herself in the mirror. A few months ago, I first noticed Annie looking into the mirror and examining her own teeth. She used her fingers to pull her lip down to get a better look, with her face close to the mirror. She noticed a small raisin stuck to a tooth, used the mirror to direct her fingers to the raisin, picked at the raisin and finally removed it (Schultz, 2006). Recently I put a red dot on Annie's forehead while she was anesthetized for a medical procedure. After she had recovered, I took her to the mirror. Annie put her face very close to the mirror and looked at the dot for some time. Then she reached up to the dot on her forehead—not in the mirror image!—while looking into the mirror and tried to touch the dot on her forehead. On another occasion, I put a small piece of white sticky paper on top of Annie's head. At the mirror once again, she noticed the white dot in her mirror image and removed it promptly. Later in the day, I saw Annie searching the top of her head with the help of the mirror. She appeared to be "checking herself out," looking for another dot!

I don't want to stretch this discussion too much beyond the mirror but would like to make this, perhaps provocative, statement that the members of any animal species that develops a social hierarchy, must be self-aware, otherwise no stable relationships, predictable for each group member, could ever evolve. Cattle, for example, establish dominance-subordinance relationships that are respected by the individual social partners for many years. I have no doubt that these animals have self-awareness, but this does not imply that individuals recognize themselves in a mirror as humans do. Different species have different perceptions, but they may nevertheless share the same mental faculty of self-awareness.

Would you include invertebrates such as bees and ants?

Yes, I would include bees and ants and any other creatures who do establish stable social one-on-one relationships. Just considering the highly sophisticated inter-individual relationships and communication skills of bees and ants, I have no doubts that individual members of such colonies do possess self-awareness, perhaps not the ego-dominated self-awareness of humans, but the pure self-awareness that is not linked to a memory-based personal story.

Empirical evidence and ethological considerations make it plausible that animals are capable of self-recognition.

2,8. Pound Dogs—How to Work with Them in the Research Laboratory

Is it emotionally more challenging to work with pound dogs than with dogs who have been bred specifically for biomedical research?

It is a lot more difficult for me to work with pound dogs, such as a golden retriever or a Labrador, than with the dogs who have been bred for research purposes. I know that the dogs from the pound were companion animals at some point. They exhibit many signs of a companion animal: knowing how to sit and give paw, wanting to play fetch with a toy, or just craving human attention (Figure 5). I can offer these pound animals, who have abruptly been turned into "research animals," some comfort by trying to recreate a home environment as much as I can while they are here. Because of my experience as a dog owner, it's easier for me to provide enrichment to ex-companion dogs than to purpose-bred dogs who are more aloof, although some do play.

Figure 5 Dogs from the pound often behave like companion animals and crave human affection. It can be an emotional challenge to work with them in a research lab setting.Photo by Marvin Ehlin.

I remember the time when we worked with dogs who were ex-pets. It was emotionally very disturbing, and all the techs and the majority of the researchers I worked with found this circumstance extremely difficult to tolerate, even though we knew that the owners had willingly sold their pets to our supplier. We were lucky in that the researchers used to turn a "blind" eye to our re-homing schemes and entered into the records that the animals for whom we found new homes had died from "natural" causes.

Since our facility has a fairly strong adoption program, I would rather that we use pound animals, as it gives these dogs a chance to be adopted into a good home. In addition, most pounds in the US hold animals for possible adoption only for about 5-7 days and then euthanize them. At my prior facility, we actually removed dogs from the pound's euthanasia area just prior to them being killed—literally minutes before. In the two years that I worked there, we were able to return four dogs to their owners. While that's not a big number, you have no idea how good it felt to bring these animals back to their original homes!

If research laboratories could purchase pound animals scheduled to be euthanized because no new home could be found for them in time, pounds would make enough money to allow for a longer stay of ex-companion animals, thereby increasing their chances to finally get adopted. I would rather see dogs used for research purposes than killed in pounds. The hard part is convincing the "general public" that those animals to be used for research would be sold just prior to euthanasia and not at the whim of the people running the pound.

Animal lives could be saved if pound dogs who have not been adopted in time, were given to research labs rather than killed and another healthy purpose-bred dog used for research instead. Working with pound dogs can be very challenging because the animals often show typical pet-behaviors, thereby eliciting strong emotional attachment.

2,9. Adoption of Animals After Research Completion

2,9,1. Adoption by Private Homes

I was wondering if I could get some feedback regarding adoption of animals after research completion. We were able to get one dog adopted by an employee after the dog had chewed at an implanted probe. Our institution had to get lawyers involved and go through a bunch of red tape, but the dog is now finally "outside," living a normal life with a caring family. This ultimately positive experience made us ask ourselves, "Why can't we do this for more animals?" We currently have an investigator who would like to adopt one of his canine patients once the study is over. The dog could live a normal life. Can anybody share experiences on successful adoption programs?

In the Netherlands, there is an organization for re-homing animals that is also specialized in re-homing dogs and cats who have been research subjects. This organization has contact with biomedical institutions, and I believe uses standard ownership transfer contracts. The dog or cat who is no longer used for research is placed with a foster family for an observation period. If the animal readjusts to normal life, bonds with the new family and is healthy, he or she can be adopted permanently in the new home.

We have an adoption policy that was drafted with the advice of our lawyers. We primarily adopt out cats, but occasionally also rats, frogs and rabbits. We have adopters sign a release/waiver of liability before the animal goes out. All potential adopters are screened as carefully as possible. The cats and rabbits are spayed or neutered and deemed healthy by the veterinarian before they leave our facility. We haven't—knock on wood—had any major problems with these adoption procedures. I think there's a good publicity potential in running adoption programs: (a) The facility shows people that it is concerned about the animals, and (b) gives evidence that there is research that doesn't harm the animals but leaves them fit enough to carry on a normal life as pets outside the laboratory.

For more than a decade, the University of Florida College of Veterinary Medicine has allowed investigators to arrange for the adoption of animals who are no longer used in research. Di Gangi et al. (2006) surveyed 458 cats adopted over a period of six years and found that 91 percent of the animals were still in their original adoption homes, and 80 percent were highly valued family members.

At my institution pigs, sheep, chickens, ponies, dogs, cats, rats, mice and guinea pigs have been successfully adopted out after completion of research projects. I have adopted several rats myself. They are very cute! Watching some of your favorite animals go to good homes after their hard work is quite rewarding. We have adoption forms that are almost identical to what one would fill out when adopting an animal from the humane society. I remember one instance where all 39 beagles of a study got homes after working for 2 to 3 years. It was a very, very positive experience for our entire staff!

2,9,2. Adoption by Schools

Mice are used in large numbers and are not much in demand as companion animals. But what about science classes in schools? I'm not thinking of dissections, but of "classroom pets."

Outbred rats may be a better choice than mice. They are easier to handle, respond as individuals with humans, and can readily be kept in pairs.

I agree, rats would be a much better choice for small children than mice. We have adopted Wistar rats several times now at home. They are friendly, very easy to handle—even for small children—easy to keep, and much fun to watch and interact with. I recently have kept three females together outdoors in a large rabbit enclosure. I got them as weanlings in the summer, and housed them outside when it was still warm, so they could slowly get used to colder weather. You just have to make sure that they have a warm nest. The oldest rat was with us for three years before dying in her sleep last summer. Two of the animals were once caught by a cat when my daughters forgot to close the door of the rat enclosure. It was amazing to see how these two rats survived. We found them after a few hours with bite marks and scratches, sitting in the garden of a neighbor. They were surrounded by three cats and did not try to run away. I think this strategy saved them, because the cats got bored and no longer had the incentive to attack these two unmoving critters. I treated the two survivors with antibiotics, and they recovered in no time.

My experience is also in favor of rats. They are friendlier and more robust than mice, and kids seem to bond with them better. They do learn their names and come when called. They are larger than mice and, therefore, easier to handle with little risk of being accidentally dropped. They are much less likely to bite, and they can be group-housed nicely.

Animals who have been adopted by schools often live under housing conditions that are worse than in the research lab. Many instructors/teachers have insufficient background knowledge of the behavioral and physical needs of the animals. When ex-research animals are "adopted" by schools, it is very advisable to discuss environmental enrichment options or necessities (e.g., shelter, nesting material) with the person in charge. This will also help the children to get a better feeling for the fact that animals/pets have species-specific needs that must be met in order to keep them healthy and "happy."

2,9,3. Conclusions

Rather than killing animals who are no longer useful for research, many laboratories have started releasing animals for adoption by personnel and by private homes. Some of these adoption programs have proven to be very successful.

2,10. Individual Housing—Justifications

When is individual housing of social animals called for?

Studies in which I feel single-housing of rodents and rabbits is justified are those involving:

All single-caged animals must be housed within smell/sound of companions and, if possible, also in sight of conspecifics.

In socially housed primates, it sometimes happens that individual animals do not get along with others. It would be unrealistic to force a persistently incompatible animal to live in a social-housing situation. It is my experience with rhesus macaques that some sub-adult, 3.5-5 years old males can go through a very difficult developmental phase during which they are highly aggressive towards other males. Such animals should be caged alone, but always in visual or auditory contact with other conspecifics until they settle down, usually when they reach full sexual maturity. If there are surplus infants from breeding troops, pair-housing otherwise incompatible sub-adult males with such infants is a good alternative to single-housing. I have experienced it many times that a young male who seemingly is a monster with other males turns into a gentle, caring fellow when he gets a naturally weaned infant as a cage companion. It's amazing to witness the abrupt shift in such a male's demeanor.

Primates assigned to food intake studies are often removed from their social partners and kept alone in single-cages. This is not necessary. The daily food ration is usually distributed in the morning and mid-afternoon, and the cages are cleaned with water in the late afternoon; on this occasion, all food leftovers of the day are removed. Since the animals have no food during the night phase, there is no good reason why compatible companions cannot live together during the night. They can then be separated prior to the morning food distribution with a grated/transparent panel, allowing them to keep social contact with each other during the hours when their food intake is monitored. In the evening, the panel is again removed, etc. This system helps to minimize, or perhaps even eliminate altogether, the extraneous variable stress resulting from social deprivation.

Yes, there is no good reason why paired animals cannot be put together after the last cage cleaning of the day and then separated again in the morning as you suggest. The trickier part of this schedule is to get the husbandry folks to cooperate during the weekends and take the extra time to separate and reunite the animals.

2,11. Legal Space Requirement Stipulations

Is it indicated to push for larger than minimum-size standard cages?

Individually caged animals have little or no use for extra space beyond the space required for free postural adjustments and a few normal steps/hops. Rather than "exploring" empty space, primates will climb up to a "safe" high corner of the enclosure and stay there, while rodents will show thigmotactic behavior, i.e., shunning the "unprotected" center but staying close to the walls of a barren enclosure, even if it is relatively large (Figure 6). The classical open field test (Hall and Ballachey, 1932) is based on this phenomenon: being exposed to an enclosed open area evokes anxiety. If I had to stay in a room for a long time, I certainly would prefer objects with which I can do something versus having access to another room that is completely empty. I assume that a monkey or a rat would show a similar preference to objects over more empty cage space.

Figure 6 Unstructured space has little value for prey animals, such as this mouse, but is likely to induce anxiety and the urge to stay close to the peripheral wall. Original photo by Chris Sherwin; re-designed by Annie Reinhardt.

The current legal minimum space and exercise stipulations of the US Animal Welfare Regulations (United States Department of Agriculture, 2002) do not make it clear that the prescribed space must be structured in a species-appropriate manner so that the confined animals are encouraged to make use of it. It is easy to demonstrate "scientifically" that animals do not exercise or play, or benefit in any manner in a relatively large but empty enclosure (Hite et al., 1977; Bayne and McCully, 1989; Hughes et al., 1989; Line et al., 1989; Line et al., 1990a; Bebak and Beck, 1993; Crockett et al., 1993; Galef and Durlach, 1993; Crockett et al., 2000). To conclude from such findings that the animals do not need more than the minimum space required for free postural adjustment would be quite misleading. Legal space requirement specifications are insufficient as long as they only prescribe quantity of space—usually based on body weight—and fail to define quality of space.

Yes, this is a crucial point. To concentrate too much on minimum space distracts from the real question, which is: What can the animal do with the space in the enclosure? More space, if not structured, will not do much to the welfare of animals in captivity. Any discussion on quantity of space needs be accompanied by a discussion on quality of space in order to be meaningful. Once you get beyond the minimum space needed by the animal for free movement and postural adjustments, the quality of space becomes much more important than the quantity of space. However, I have trouble when it comes to legislating quality of space. It would be rather impossible to write a legal document that could address each of the different species that are kept in research laboratories. I am not sure what the answer might be.

Perhaps, experts of the various species can agree on basic space quality provisions that should be legally mandatory, for example:

A good number of people do not need the law, telling them how to furnish the cages of the animals in their charge. I see the real problem in the fact that these people usually do not have the administrative power to implement their experience-based, often excellent ideas. Legal requirements are very important for them to give them some backing. Then there are other people who do not have the proper knowledge or do not really care. Here, professional guidelines and basic legal stipulations, defining the quality of cage space, would probably be helpful.

I am sympathetic to the difficulties of adapting inflexible regulations to current circumstances. Unfortunately, however, animal welfare often takes a back seat to other concerns, and we are left with little option for refining traditional housing practices until the inspector shows up and says we have to.

It would be a lot easier for us to improve the housing conditions for our animals if we had some legal regulations prescribing the quality of the enclosure space rather than just its minimum size.

2,12. Impaired Well-Being, Pain and Suffering

2,12,1. Signs of Impaired Well-Being and Pain

When you check your animals, what signs—behaviors, gestures, reactions, vocalizations—tell you that the well-being of an individual animal is impaired? We often make use of these signs spontaneously, yet they seem to be very reliable.

For most animals, the coat changes when they do not feel well. It may only be slightly "off-color," dull and "staring," rough looking with the hair clumping rather than lying sleek and glossy. Goats get a rounded face and a ridge along their backs due to the hair standing on end. Haven't observed any coat changes in sheep, but pigs will get a "fluffy" appearance when they are not okay.

Rodents, pigs, goats and sheep will take on a characteristic hunched posture when they are in pain, with their backs becoming arched and their abdomens tucked up toward their spines. I haven't observed this in rabbits. Sheep and goats will continually shift their weight from one leg to another when they are in pain, especially if the gut/abdomen is involved.

A change in idiosyncratic behaviors usually indicates that the individual animal does not feel well. For example, there may be one particular mouse who is always the first to emerge from the nest, or a certain cat who is particularly playful. When the mouse doesn't show up first or the cat is not at all playful, chances are that something is wrong with the animal.

The guinea pigs, rats, rabbits, rhesus monkeys and dogs in my charge show typical positive responses when I enter the room and approach their cages. When one of them does not move but stays quietly in a shelter or in the back of the cage, I know for sure that this animal is not feeling well and needs to be checked more thoroughly. The response to my presence is probably the most reliable indicator of an animal's state of well-being, be it a dog, a monkey, a rat, a guinea pig, a chicken or any other animal who is in my charge. This leads us back to our discussions on the human-animal relationship. It would be impossible for me to take the subject's unusual response to my entering the room and approaching the cage as a sign of impaired well-being if the animal would not have a good relationship with me, but would be scared and always hide when I approach the cage. This scenario often happens with investigators who, therefore, are dependent on animal care personnel to check the health status of the animals assigned to their projects.

Rats are very good at conceiling pain and health problems. However, if one of my guys is really "ouchy" he or she may show:

As for monkeys, I find the following signs useful indicators of an animal's impaired well-being:

2,12,2. Pain and Suffering

What is the difference between pain and suffering?

What is the difference between pain and suffering?

The whole issue of whether animals feel pain is one of logic. Pain is a subjective experience. Therefore, I can never have "proof" that you, or a monkey, mouse, cat or dog is in pain.

If we are willing to relieve discomfort only when we have "proof" that the subject—be it an animal or a human—is actually experiencing pain, we negate compassion. If you accept this inherent "feeling for another creature" you will do your best to alleviate the pain or suffering of an animal or another human being. This response is spontaneous, not a result of logical consideration.

Pain per se is a physiological, measurable, hence objective phenomenon. Pain is impersonal, but how it is interpreted by the subject is a subjective phenomenon that depends on the subject's relationship with the pain. Based on my own experience I would say that animals usually do not take a painful experience personally; it's not "their" pain, just pain that needs to be alleviated and avoided. They do not resist the pain, thereby making the sensation even more intense, but respond to it in the most appropriate way possible. Humans, however, have the tendency of identifying with "their" pain, thereby turning the impersonal perception of a neutral phenomenon into a subjectively interpreted experience. The pain is now a personal problem, quasi an enemy that may trigger emotional reactions such as helplessness, self-pity, frustration, despair and worry. These emotional reactions often transform pain into suffering. Pain is unavoidable for animals and humans alike, but suffering is a choice that humans make probably much more often than animals. So it may then well be that animals usually suffer less during painful situations than we do.

This is an interesting way of looking at pain. It seems to suggest that dwelling upon pain makes the pain even more painful. It could also suggest that captive animals, unlike wild animals, have nothing that could distract them from pain, so they are at a greater risk of dwelling upon "their" pain, which would then make them suffer. Gentle and Corr's (1995) study of chickens supports this hypothesis: When chickens were placed in pairs into pens containing a deep layer of wood shavings, they showed significantly less pain-related behavioral reactions to a joint inflammation than chickens placed alone in barren pens. When tested in the barren cage, the whole of a bird's attention was occupied in trying to reduce the pain as far as possible [one-legged standing, limping, sitting]. In the more stimulating pen, the bird's attention was shifted from the pain to the social partner and the wood shavings, thereby reducing the intensity of pain that was actually experienced.

How can we define the term "suffering?"

Quite a number of authors—Balls (1994), Cockram (2004), Dawkins (1980), Fraser et al. (2000), Morton (1995), Mroczek (1994), Pollo et al. (2004), Reilly (1998), Richmond (1999), Sherwin (1998), Wemelsfelder (1993), Zimmermann (1987)—have used this term in scientific animal welfare related publications, which suggests that it does have practical value in the context of animal welfare in the research laboratory.

The lay person doesn't know what distress means, has a vague idea what stress means, but "knows" what is meant by "scientists inflict unnecessary `suffering' on animals," because "suffering" is a term most people are very familiar with, even though they have not thought much about its actual meaning.

We cannot "objectively" measure the "subjective" experience of suffering, but this should be no hindrance for defining the term so that those who want to alleviate suffering can reason with those who inflict the suffering. Without such a definition, the animals are at the mercy of professional judgment, which is often influenced by personal interests.

  1. As a researcher, I believe that "suffering" occurs when an animal experiences depression, frustration, boredom or anxiety of great intensity or of long duration.
  2. As a clinical veterinarian, I would define "suffering" as an involuntary exposure to a painful or injurious situation over which the subject has no control and which the subject is hindered to alleviate.
  3. As an ethologist, I define suffering as the internal subjective state experienced when:
  4. As moderator of this forum I summarize that suffering is the experience of:

Even if we cannot find a consensus on the definition of "suffering," it should be possible to come up with agreeable case-by-case decisions on conditions that do or do not inflict suffering on animals in research labs. In this way, animal advocates and animal research personnel could develop common ground and dispel the myth that "biomedical research inflicts suffering on animals" but also the assertion that "biomedical research does not inflict suffering on animals." This approach is certainly better than sweeping the "unscientific" term "suffering" under the carpet, thereby making a constructive dialogue on behalf of the animals impossible. For example, if primates kept alone in barren cages, engage in stereotypical self-biting, will we not agree with animal advocates that these animals "suffer" from loneliness and boredom, even though we cannot prove it scientifically? On the other hand, animal advocates will have no good reason to argue that primates suffer when we keep them with compatible companions in cages that are equipped with high perches onto which the animals can retreat.

2,12,3. Conclusions

There are general signs—reduced alertness, lack of interest in food and enrichment gadgets, unusual coat condition, unusual response to human presence—and species-specific signs that tell you that an animal does not feel well. The response of an animal to you is probably the most reliable indicator of his or her well-being.

Not surprisingly, we were not able to reach a consensus on the definition of the term "suffering." Here is an elegant way of circumventing this dilemma:

I think this is a very reasonable assumption in most cases. It could certainly be treated as a starting point with any deviations requiring evidence.

2,13. Stress and Distress

The terms "stress" and "distress" are often used in the scientific literature but usually without a definition. If you use these terms, how do you define them? Are there signs that tell you that an animal is stressed or distressed?

Stress and distress are physiological and emotional responses to events:

  1. An external situation (stressor) leads to stress, which implies an alteration of the subject's physiological and behavioral equilibrium (e.g., increased heart rate and fear). This kind of stress—"eustress" would probably be a more appropriate term—is not necessarily harmful, but it disturbs the subject's equilibrium, hence has the effect of a potentially data-biasing variable that needs to be accounted for in the research context. Being approached by unfamiliar personnel is a typical stress situation.
  2. If the subject cannot adapt to the stressor, i.e., return to physiological and behavioral equilibrium, stress becomes "distress." Pathophysiological processes (e.g., chronic diseases, generalized alopecia), emotional disturbances (e.g., anxiety, frustration, depression) and/or maladaptive behaviors (e.g., self-injurious biting, hair pulling, stereotypical movements and gestures) often develop as a result of distress. Being permanently confined in a barren cage is a typical distress situation.

Although both "stress" and "distress" have negative connotations, distress is always bad, but stress can be both good or bad. A certain amount of stress is part of life and some mild stressors can make life a little more interesting. Introducing a new cage-mate probably causes some stress for nonhuman primates—similar to how human primates might feel when going on a first date—but, assuming the companions are compatible, this is a good stress, as it breaks up the monotony and allows the animals to express their need for social contact and social interaction. However, when stress gets out of hand, because of its intensity, frequency, or harmful nature, then that is when I say the animal is distressed. In practice, I think distress requires action to alleviate, but stress usually does not.

I consider some level of stress as normal, and, depending on the study, research conducted on animals experiencing normal levels of stress may be more biologically relevant than research conducted on animals shielded from stressors. However, it is important to be aware when stress is present, since it could affect research data, and it could develop into distress.

Stress as such is not harmful, even though it challenges the subject's physiological equilibrium. Severe stress or prolonged stress both develop into distress, when the subject can no longer cope with the stressor and shows maladaptive responses. A stressed animal needs to be monitored carefully, while a distressed animal requires immediate assistance.

3. Maladaptive Behaviors

3,1. Stereotypical Behavior

Are stereotypical behaviors "abnormal?"

Animals kept in legal minimum-sized, unstructured enclosures very often exhibit stereotypical behaviors. Traditionally, these repetitive movement patterns without obvious goals or functions are categorized as "abnormal." A healthy animal kept in a small, barren enclosure has little choice of expressing his or her biologically inherent drive to engage in species-typical behaviors, other than pacing back and forth, running in circles, somersaulting, rocking, self-biting, bar-biting, wood-gnawing, ear-pulling, hair-pulling, eye-poking and other bizarre activity patterns (Figure 7). There is nothing really "abnormal" except the abnormally restrictive and abnormally boring housing conditions that induce the stereotyped expression of these activities. The majority of macaques who are kept in conventional barren cages exhibit stereotypical activities (Erwin and Deni, 1979; Lutz et al., 2003). These behavioral patterns thus become "normative" under the given circumstance. In caged mice, barbering is another example of a stereotypy that has become a normative behavior within the context of inadequate living conditions.

Figure 7 Sheep often engage in stereotypical gnawing when they are kept singly in a barren environment that is not appropriate for their species. Photo by Viktor Reinhardt.

We tend to project abnormality onto animals rather than the people who create deficient living quarters for them. It would be fair to first focus on the husbandry conditions, study the environmental factors that lead to the development of behavioral pathologies, and then correct these factors in order to prevent behavioral pathologies in the future.

The label "abnormal" would be more befitting of the inadequate confinement condition, rather the subject's frustrated attempt to adjust.

3,2. Hair Pulling-and-Eating and Alopecia (Hair Loss)

3,2,1. Primates

Some of the cyno ladies started to lose hair shortly after arriving at our facility. There are three groups living in the same room in relatively spacious quarters that are provisioned with windows, climbing structures, visual barriers and toys. Ethological observations indicate that the groups are compatible. The ladies seem to be just fine, except for the new hair fashion they have created. Does anybody have some ideas about what to think and do regarding this phenomenon?

Compulsive hair pulling-and-eating is a common problem in single-caged and in group-housed macaques. This behavioral pathology is typically associated with localized—not generalized!—hair loss. I did ethological studies in group-housed rhesus and noticed that it was almost exclusively (378/388) partner directed and performed in 96 percent of observations by a dominant, only in 4 percent of observations by a subordinate monkey (Reinhardt et al., 1986). Based on my observations of the agonistic and affiliative interactions between group members, I came to the conclusion that hair pulling-and-eating is an ethopathology, reflecting adjustment problems to permanent confinement. It is a great challenge for social animals—including humans—to adjust to living under the same roof without possibility of taking a "vacation" from each other. Many of our group-housed rhesus and stump-tailed monkeys were almost bald. Some of them lived in a zoo, and we got many complaints from the public. I remember one particularly bad case of alopecia, George the ß-male of a breeding troop (Figure 8a). This gentleman showed no obvious signs of stress or distress, but we received so many complaints that we finally decided to remove him and pair him up with a juvenile male in a double cage. His hair grew back almost visibly. It was really amazing (Figure 8b). I am sure that George was distressed in his group, given the fact that he had to cope with being the second ranking animal, a position that is known to be quite demanding.


Figure 8a,b George, the ß-male of a rhesus breeding troop has lost almost all his hair (a). George's fur grew back within a few weeks after he was taken out of his original group and paired up with a juvenile companion (b). Photos by Viktor Reinhardt.

I have a young male rhesus who has just started to engage in pulling and eating his own hair. I also assume it is stress-related. This monkey has been at our facility for about six months. He has not yet been used in a research project. He is very healthy, but also feisty and very nervous. I nicknamed him Tarzan because of his wild look and behavior. He shares a room with eight mature females and has visual, olfactory and auditory contact with them. Being prevented from engaging in direct sexual contact with these females must be very frustrating, and I think this is the reason why he resorts to pulling out his own hair.

I have been working with several hundred macaques over a number of years, and I have offered them all types of natural foraging and occupational enrichments, but I did not have much success in reducing, let alone eradicating, hair pulling behavior. At best, enrichment may provide a short-term distraction to deep-seated psychological maladjustment problems. Some of these problems may have their origin in a lack of basic environmental stimuli during early infant development, such as social deprivation or barren living quarters. This lack of appropriate external feedback may cause the animals to resort to self-directed strategies to get some relief of their tension. Once these critters are hard-wired it is almost impossible to change a well-entrenched behavioral pathology such as hair pulling.

That hair pulling-and-eating is a sign of distress in nonhuman primates is supported by the fact that this behavior (trichotillomania) is associated with clinically significant distress—especially social distress—in human primates, who typically show this "mental disorder" (American Psychiatric Association, 1987) in the context of depression, frustration and boredom (Christenson and Mansueto, 1999).

3,2,2. Mice

We have some mice who are going crazy barbering and overgrooming. They have hair on their faces, but are bald from their necks to their butts with a thin strip of hair left on their abdomens. The investigator would like to try offering enrichment in an attempt to fix the problem. Currently, the animals are kept on corncob bedding with a handful of aspen bedding and a nestlet. I was thinking of adding a commercial mouse house or igloo, and maybe something additional to chew on, i.e., cardboard rolls.

Your idea of cardboard rolls is a very good one, especially in conjunction with a mouse house and shredded paper. You might also consider a more varied diet, e.g., pet mouse food, as this requires more handling and chewing.

We give our mice mini-igloos, PVC (polyvinyl chloride) tubes, egg cartons, paper towel rolls, nestlets, shredded paper towels, wood blocks, hanging plastic tubes, Kleenex boxes and running wheels, but they still barber each other! We also removed the barber in some cages. This brought some initial reduction of hair pulling, but the problem started soon again when another mouse took over the role of the barber. A "therapy" for this behavioral pathology seems to be elusive not only in primates but also in mice.

3,2,3. Rabbits and Guinea Pigs

There are hardly any published records on hair pulling-and-eating in rabbits, even though it seems that intestinal obstruction resulting from fur balls is not an uncommon cause of death in individually caged animals (Jackson, 1991; Kraus et al., 1994). How can you prevent, alleviate or eliminate this behavioral pathology?

Brummer (1975) showed many years ago that the provision of straw not only prevents the development of hair pulling-and-eating (trichophagia) in young rabbits, but also eradicates this behavior in breeding females. Rabbits are biologically adapted to process and eat fibrous food stuff, so it may well be that they resort to trichophagia as a substitute to normal food processing behavior when their diet, such as pelleted food, does not have a high enough fiber content.

Hay is probably as effective as straw in preventing this maladaptive behavior: All our single- and group-housed rabbits receive autoclaved hay on a daily basis; none of the animals was ever observed pulling-and-eating hair. Access to hay gives them no reason to engage in this activity. This probably also applies to guinea pigs, who show a substantial reduction in hair pulling-and-eating when they are provisioned with hay ad libitum (Gerold et al., 1997).

In guinea pigs, hair pulling can also serve as a dominance gesture to make another animal move out of the way (Harper, 1976). When we used water bottles for our group-housed animals, hair pulling was a real problem, despite the fact that the animals had plenty of hay. With a bit of observation, it was discovered that this behavior occurred specifically at the water bottles, where dominant animals displaced others by pulling their hair. We consequently changed to open water dishes, and the problem disappeared.

3,2,4. Conclusions

Hair pulling-and-eating reflects maladjustment to a distressing condition in primates and mice. The inherent constraints of permanent confinement makes it very difficult to cure affected animals from this behavioral pathology. In rabbits and guinea pigs, hair pulling-and-eating is associated with a lack of fibrous foodstuff. A generous daily provision of hay or straw is probably the easiest way to prevent this behavioral disorder from developing in these two species.

3,3. Self-Injurious Biting

Self-injurious biting is a serious behavioral pathology in primates. I have videotaped rhesus macaques with the resulting impression that self-injurious biting occurs more often in singly housed than socially housed animals. Among pair-housed individuals, unfortunately, the primary trigger for self-injurious biting appears to be the mild aggressive behavior from cage mates who occasionally supplant or swat subordinate partners. In this context, self-biting does not result in visible injuries, so I will accept it for the sake of keeping pairs together. Also, there is no telling how much worse it could get if such animals were separated from their partners and transferred to single-housing.

I would argue that the development of self-injurious biting, which occurs in more than 10 percent of singly caged macaques (Jorgensen et al., 1998; Alexander and Fontenot, 2003; Novak, 2003), can be prevented if the animals are raised and naturally weaned by their mothers in compatible group settings. I was able to eradicate this behavioral pathology in seven single-caged rhesus macaques by transferring them to compatible social-housing arrangements. Some animals responded promptly to the housing modification, while others gradually stopped engaging in this stereotypy (Reinhardt, 1999). Fritz (1989) made a similar finding in chimpanzees, and subsequent studies by Alexander and Fontenot (2003) and Line et al. (1990b) confirm them again in rhesus and long-tailed macaques, respectively.

At our facility are three adult male rhesus who had a history of SIB (self-injurious biting). The animals were treated with various drugs—diazepam, fluoxetine, guanfacine—which did alleviate but not eradicate the self-biting. Once the treatments were discontinued, the animals resorted to SIB as before. All three males self inflicted repeatedly serious laceration that required surgical care. When it was considered to euthanize these males, because the SIB could not be stopped with pharmacological therapy, we were finally given permission to pair them with other compatible companions. This "treatment" brought the self-biting to an end in all three cases. Carl, however, had a relapse when his companion was removed for research-assignment reasons after 14 months. Fortunately, the PI was considerate enough to drop the companion from the research protocol and allowed us to re-unite him with Carl, who promptly stopped again self-biting himself.

What does self-biting actually look like?

In my own experience with rhesus and stump-tailed macaques, self-biting occurs in the following two sequences of events and circumstances:

  1. The subject is extremely bored, shows no signs of excitation, and repeats the same movement patterns over and over again—for example, circling, pacing or somersaulting—interjected by sham biting of specific body parts (Figure 9). This behavior often goes unnoticed because there is no visible abrasion or laceration, plus the subject usually does not show the behavior when there is a distraction, for example when personnel is present.
  2. The subject is extremely frustrated—with high emotional arousal, e.g., shaking, intense staring, piloerection—for example, when fear-inducing personnel approach the cage, with the subject having no option of escape or attack. The animal will predictably attack specific sites of arms or legs, perhaps always the right wrist or always the left upper thigh. This typically leads to noticeable abrasion over time—first local alopecia, followed by mild inflammation—but may also result in serious wounds. Typically an animal self-inflicts lacerations of the same body part several times on different occasions, often necessitating the amputation of the repeatedly injured limb.


Figure 9 A single-caged male rhesus macaque self-bites without actually injuring himself. Photo by Matt Rossell.

I remember seeing a video of a dog who would suddenly behave towards his left rear leg as if it was another dog trying to steal his food. He would growl, snarl and eventually bite one of his own legs very hard. He was an abnormal dog for sure and only one example, but I don't think self-injurious behavior is limited to primates.

When I worked in small animal veterinary practices, I saw several dogs biting their feet repeatedly. Large dogs who do not get enough exercise, can end up chewing on their hind extremities to such an extent as to expose the bone. Cats who are kept strictly indoors also engage in self-injurious biting. They attack their tails. I remember several cases that required tail amputation.

Self-injurious biting is a serious behavioral pathology that reflects gross insufficiencies in the rearing, housing and care of an animal.

4. Environmental Enrichment

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