By James A. Love, BVMS, PhD, MRCVS, and Kim Hammond
Laboratory animal facilities have traditionally held rabbits in individual cages, regardless of the type of experiment that the animals are involved in. For many investigations, group-housing would not interfere with the study goals; since wild European rabbits live in groups, group-housing systems may have distinct welfare advantages.
Facilities usually singly house rabbits to aid identification, minimize disease spread, to make the control and observation of food and water intake easier, and to expedite cleaning and handling.But these reasons are related primarily to the care of the animals, not their needs. The space allotted to singly housed rabbits is minimal in both area and height. Guidelines for cage dimensions are based on animal size and do not take into account any behavioral traits. For example, rabbits frequently sit up on their hindlegs–an impossible maneuver in most cages.
Isolating "gregarious" animals, like nonhuman primates, has attracted wide-spread criticism. Attempts to group-house rabbits1,2,3 have been few in number and short- lived. Taking the step to group-house rabbits is neither simple nor trouble-free. Difficulties may stem from animal behavior, the management or housing systems, or diseases. Additionally, the requisites of each study must come into play to avoid introducing uncontrollable variables.
Here, we describe behavioral activities occurring in group-housed New Zealand White (NZW) rabbits. Other researchers have described these activities in wild rabbits5,6. Single-rabbits cages do not accommodate some of these activities. Over a three-year period (1988-1990), we found that group-housing rabbits generated some management problems, which we identified and solved. We also documented the disease problems that occurred.
Materials and Methods
The rabbit wing consisted of 28 indoor/outdoor pens that were formerly dog kennels. The inside pens, which measured 1.68 m x 1.52 m, were constructed of epoxy-painted cement blocks to a height of 1.1 m; chain-link fencing at the top of the blocks increased the height to 2.5 m. There was a small swing-out trough, an easily removable polyurethane resting board, and an automatic waterer in each cage. The floors were epoxy painted. There was a drainage trough, 15 cm wide and 23 cm deep, on the outside of the front of each cage. A hatch, 70 cm x 40 cm, provided access to the outside run for each pen. The indoor pens had thermostatically controlled heat.
The outside runs, which measured 1.68 m x 3.56 m, were separated from each other by galvanized metal panels to a height of 1.1 m and the separation continued to 2.5 m with chain-link fence. There was a partial roof covering to the outside pen for about one-third of its length. The floor was smooth concrete, and there was a drain outside the run.
Eight- to nine-week-old primarily female NZW rabbits came from a commercial supplier, and were slated for antibody production. The ultimate use of the animals figured largely in group assignments, to avoid making new groups necessary. Each pen held six to eight animals, and the animal census ranged from 100 to 180 rabbits per day. Over three years, the number of rabbits was 141,000. The rabbits got their food ad libitum in hoppers located at the front of the pens. Each hopper provided approximately 20 cm of trough space. The rabbits had access to a continuous, fresh supply of water, located in dishes inside and out.
Sawdust covered the floors of the inside pens. A squeegee served to remove feces around the hopper; this freed the inside pens of 60- 70% of all feces. A high- pressure, high-volume hose facilitated pen cleaning every second day, and served to clean the outside runs daily. Applying descaling solutions on a weekly basis (particularly where the rabbits had urinated), and washing with a quaternary ammonium compound also helped to keep the pens clean. Feed hoppers and water tubs got a cleaning in the cage washer on a weekly basis. New animals were greeted with thoroughly cleaned pens.
Rabbits arriving at the facility underwent a thorough check-up for external signs of disease–particularly pasteurellosis–ear mites, and evidence of gastrointestinal disease. Staff members checked fecal samples from new arrivals for coccidia; new arrivals did not receive routine treatment.
Each pen underwent daily observations to assess the animals' demeanor and note any injuries. A small amount of leafy alfalfa hay placed in the pen helped assess if animals were eating normally–the rabbits usually gathered around the alfalfa and started to eat immediately. Staff members observed the nature of the animals' fecal droppings, urine, etc., and the amount of food and water the rabbits consumed. The rabbits had weekly weighings and examinations of their teeth, ears, and hocks. The staff checked fecal samples from some of the pens for coccidia.
Any health problems warranted a sick animal and treatment report. A veterinarian examined rabbits when necessary and initiated treatment, including separation from the group. Conditions like malocclusion got appropriate treatment. Clinical examinations, supported by laboratory tests and autopsy examination when appropriate, were the basis of infectious disease diagnoses. The facility practiced limited virology and histopathology. A total of 124 treatment records were available for analysis. Some common conditions–snuffles, for instance–were underrepresented. Snuffles, in the form of intermittent sneezing, did not significantly interfere with the animals, activities, and did not require treatment.
Eating and Drinking: Rabbits ate at all times of the day, but only ate together when they received hay. The food hoppers did not provide enough linear space for the rabbits in each pen to feed simultaneously. Seemingly, no disputes over trough space occurred. The rabbits lapped water up from the dishes with their tongues; frequently, more than one rabbit drank simultaneously.
Urination and Defecation: Though the rabbits urinated and defecated throughout both the inside and outside of each pen, they seemed to hold to a pattern. During cold or wet weather, the rabbits spent more time inside and mostly urinated and defecated there. But in warm or dry weather, the animals spent more time outside, leading to an increase in urination and defecation outside. The rabbits usually urinated in the corners or along the sides of the pen. Defecation occurred throughout the pen, but there was always a large concentration of feces around the food hopper.
Marking Behavior: The rabbits appeared to mark the pens by rubbing their chins on the edges of various structures. Casual, general observations did not reveal the purpose of this marking behavior. Occasionally, one rabbit would chin-rub another, usually between the ears.
Grooming: Rabbits spent considerable portions of each day self-grooming. Additionally, the animals often participated in mutual grooming, particularly when the group was resting and lying together. One rabbit groomed another, and occasionally the grooming was reciprocated, although only one rabbit groomed at a time.
Aggressive Behavior: There were few incidences of aggressive behavior leading to disruption of the group. Fighting among females caused eyelid injuries, but not corneal injuries. Males often suffered scrotal injuries (which required at least unilateral castration), as well as eyelid injuries. The incidents leading to these injuries did not occur during observations, and initiators were unidentified. Rabbits did chase each other, and even pulled out fur, during observations. These episodes erupted in what appeared to be a tranquil setting, and the aggressor often attacked several animals in the group. Introducing a strange animal to an established group usually lead to a period of aggressive chasing; if the incident did not conclude peacefully, it was necessary remove the stranger to avoid injury. Yellow stains on the animals' white coats signified that they were urinating on one another. Again, this activity occurred when a stranger joined an established group. Access to food and water did not seem to cause aggressive behavior, and, since the sexes were separated, there was no apparent aggression associated with sexual behavior. There was no territorial aggression, and no animals were forced by the others to live in the outside part of the pen.
Exploratory Behavior: The rabbits explored the pens each day, checking out the corners, the side walls, the resting board, etc. The rabbits participated in "digging," usually in the corners or along the sides of the pen. They explored the resting board, and quickly learned to hop up on it–they often slept on it. Rabbits often sat up on their hind-legs –sometimes in response to extraneous stimulus (like a loud noise).
The animals investigated any new objects in, or close to, the pen. Buckets, ramps, and even the appearance of a technician aroused the rabbits' interest. The animals seemed to have a real "people interest" that wasn't restricted to the technician who brought their food. The animals did quickly learn the sound of the hay bag, and the noise evoked an immediate response.
Groups: The rabbits formed small, labile groups within the pen–whether they were resting or engaged in feeding or exploration. Several groups coexisted, and each group had a different activity. When at rest, the rabbits laid tight against each other, sometimes laying on top of each other. Only occasionally did a rabbit lay by itself.
Alarm Behavior: After the first week or so, the rabbits became used to their surroundings, and so there were few alarm reactions. If startled, they did dive for cover under the resting board, or rushed outside. This response in one pen, and the noise it produced, created a similar reaction amongst animals in other pens even when they had not experienced the original stimulus. Back leg thumping was rare, and the rabbits used it to alert other pen members. In neighboring pens, the response to thumping ranged from ear movement to no response.
Play Behavior: The rabbits engaged in what seemed to be play. They primarily "gamboled," much like lambs. While running slowly, they would kick out the hind legs and give a flick of the head. On some occasions, a rabbit would spring in the air and turn 180-360 degrees. The rabbits spent some time running quickly from one end of the pen to the other. They also tossed small pieces of wood around.
Sexual Activity: Although the groups were primarily female-only, there was some mounting. In the spring, some females pulled out fur and built nests. Usually just one female in a group indulged in this activity.
Diseases and Injuries
Our information about the incidence of disease in the group-housed rabbits came from the sick animal and treatment reports. Therefore, the reports only represented animals whose conditions warranted treatment. The incidence of some conditions, like snuffles, was higher than the treatment reports indicated. Table 1 summarizes the disease incidence.
TABLE 1. Summary of Conditions Requiring Treatment 1988-1990.
|Middle ear disease||1||1||1||3|
Severe disease problems were minimal, and usually occurred when the animals arrived at the facility. The supplier was known to have endemic pasteurellosis and coccidosis. Coccidosis outbreaks did not occur more than one week after the animals' arrival.
Pasteurellosis, manifested as snuffles, occurred throughout the year, particularly in the spring. Most of the time, the condition was mild and went unreported. A small number of animals developed severe involvement of the nares with crusting. In some cases, it was necessary to clean the nostrils daily. Animals autopsied at the time of terminal exsanguination occasionally showed extensive involvement of the lungs, in spite of an absence of clinical signs. Other clinical manifestations of pasteurellosis included pneumonia and otitis media.
Two rabbits developed abscesses of the lower jaw that were so extensive that there was invasion of the mandible. The source or site of infection was unknown. Abscesses occurring at immunization sites were probably the result of the Freund's adjuvant leaking back along the needle track (intradermal injections with Freund's complete or incomplete adjuvant were not permitted). There were five cases of sore hocks that responded to bandaging of the feet for a few days with antibiotic application to the injured areas. There was one case of dewlap dermatitis which occurred on a rabbit with a particularly large dewlap; the lesion site was right under the chin. Animal care technicians clipped the lesion site and treated it with silver sulfadiazine 1% (Flamazine, Smith and Nephew, Lachine, Quebec, Canada). Eight animals had malocclusions with overgrowth of the incisors. Treatment involved clipping these animals' teeth and checking them for this problem subsequently.
Of the incidents that required treatment, fighting injuries represented 41% over the three-year period. A higher number of males got injured than females. Generally, there were no injuries among the males until they weighed 2.7-3.0 kg. Once they reached this size, the males could not stay in groups because they inflicted scrotal and eyelid injuries on each other. Seven of the 51 reported fighting injuries occurred at sites other than the scrotum or eyelid; of these, four were tail injuries.
Other diseases occurred sporadically (Table 1).
Several problems, including catching rabbits, identifying them, and establishing new groups, needed solving.
Catching: Technicians shepherded the rabbits into the inside pen, and closed the door to the outside. Usually, this task required only one person, since the animals spent most of their time indoors during the working day. The technician entered each pen quietly: most rabbits went under the resting board, while some investigated the technician. By partially lifting the board, technicians could identify the required animal, and pick it up in the usual manner. Quietness and avoiding sudden movements were key to this catching method .
Identification: Whenever possible, only one investigator's animals were together in a pen. Identification cards gave information about the occupants of each pen. When an investigator started to use the animals, they got marked in one of two ways: if the investigator initially wanted to inject the animals to initiate antibody production, colored marking pens served to mark the ears; when bleeding the animals, technicians tattooed the animals.
Technicians took blood samples after mildly sedating the rabbits with fentanyl and droperidol (Innovar-vet; Janssen Pharmaceutica, Ontario, Canada, 0.05 mg/kg). This had several benefits–the vessels in the ears were dilated, the rabbit sat quietly (so no restrainer was required) and the analgesia permitted tattooing. Large letters and numbers made it easy to identify the animals at a distance.
Regrouping: When the number of rabbits in a pen fell to two or three, it was necessary to regroup them. It was necessary to sedate the animals with fentanyl and droperidol (8.0 mi/kg) and place them together in a small holding cage, making sure that pen-mates were not next to each other. As they recovered from sedation, the rabbits rubbed each other in the close confines of the cage. Staff members then placed them in a pen which had not been previously to any of the animals. Some chasing occurred, but generally the group settled down within 24 hours, usually without any injuries. Attempts to regroup mature rabbits without going through this process have uniformly failed.
In an attempt to improve the quality of life for laboratory rabbits, several investigators have looked at group-housing as an alternative to single caging1,2,3. On the surface, the behavior of the wild European rabbit suggests that laboratory rabbits will live together in groups4, this does not imply that group-housing will automatically succeed. The two major threats to successful group housing are the behavior of the animals and the potential for disease spread.
Many of the behavioral patterns seen in the wild rabbit also occur in the domesticated rabbit, when it has the opportunity5,6. Most important among these activities are those which involve more than one animal–mutual grooming and sexual activities, for example. It is almost always necessary, though, to restrict sexual activity for the female laboratory rabbit, since pregnancy may exert profound effects on many experiments, including antibody production. Generally, the groups in this study were comprised of female rabbits–not typical of the wild situation. Furthermore, there is some evidence to suggest that under certain conditions, even in the wild, females remain relatively isolated from each other within what could be qualified as a warren7
It is important, therefore, to recognize how group-housing will genuinely improve laboratory rabbits' well-being before implementing such a system. The major benefits of group-housing will be the increased space available to each animal, and the increased opportunity for social interactions. The major detriments include the potential for social exclusion, fighting injuries, and infectious disease spread.
Our experiences showed that in a group-housing situation, rabbits behaved very much like their wild counterparts5,6. There were some differences; for example, the animals fed all day, not just at dawn and dusk. Activities–like feeding, grooming, lying down–involving more than one rabbit were common. The area of the inside pen was adequate for five large singly housed rabbits (0.46 m2 for a rabbit > 4 kg, Canadian Council on Animal Care Guidelines). When the rabbits in the pen gained access to the entire space, there was enough room for them to indulge in activities not possible in a single cage. The outdoor run was a bonus.
On the negative side, there were fight injuries which would not have occurred if the animals were in isolation. The problem was most severe in males larger than 2.7 kg. Castrating males before they reached puberty resolved this problem (Love, unpublished), but castration is not always an option. The levels of fighting injuries was low, and considered acceptable.
There was no evidence that infectious disease spread was a problem among the group-housed rabbits. Although the common infectious diseases of rabbits were present, there were no disease outbreaks, and cases were confined to single animals in a pen. Direct contact, common feed, and drinking utensils are possible routes for the spread of disease. If a facility takes care to identify problem animals when they arrive, and ensures that feed and drinking utensils and the pens themselves are properly and constantly cleaned, the problems of infectious diseases are minimized.
Identifying heavily infected animals early on and following a regular cleaning routine to keep the rabbits from reinfecting themselves helped to control coccidosis. Sporulation of oocysts does not usually occur for two to three days after a rabbit excretes them9. Thus, cleaning every second day made it unlikely that the rabbits would be exposed to large numbers of infective oocysts.
There were no clinical cases of trichobezoars in the group-housed rabbits. Several factors–lack of exercise, lack of roughage, pathologic grooming due to isolation–are implicated in the formation of trichobezoars, and the group-housing system took these into account. The rabbits did not ingest the sawdust bedding in the pens.
From a management point of view, catching and regrouping rabbits presented challenges. If the rabbits had a hiding place, and if staff members approached them quietly, the catching was simplified; even new rabbits responded well to this technique. It was important that nothing very stressful happened to the rabbits when we caught them. Tattooing and blood sampling occurred while the rabbits were under neroleptanalgesia, without rabbit restrainers.
Using fentanyl and droperidol for sedation during the introductory phase solved the regrouping problem10. The most important effect was to allow the animals to interact and to chin each other while they recovered from sedation, thereby spreading recognizable smells among the group.
Group-housing of rabbits requires the ability to recognize the signs of an unwell animal. Adding treats like hay to the diet helps, as does the weekly health check. These checks become routine every time technicians handle the rabbits, and do not require much time.
1. Hammond, K. Management of group-housed rabbits. Proc. of AALAS Conference. Detroit, MI, 1988.
2. Heath, M., and Stott, E. Housing rabbits the unconventional way. Animal Technology; 41(1):13-25, 1990.
3. Love, J.A. Humane innovations in rabbit housing. Humane Innovations and Alternatives in Animal Experimentation; 2:47-48, 1988.
4. Cowan, D.P., and Bell, D.J. Leporid social behavior and social organization. Mammal Rev.; 16:169-179, 1986.
5. Bell, D.J. The behavior of rabbits: implications for their laboratory management. In: Standards in Laboratory Animal Management; pp.151-162. University Federation for Animal Welfare, Potters Bar, Herts., England, 1984.
6. Podberscek, A.L., Blackshaw, J.K., and Beattie, A.W. The behavior of group-penned and individually caged laboratory rabbits. Appl. Anim. Behav. Sci.; 28:353-363. 1991.
7. Roberts, S. Group-living and consortships in two populations of the European rabbit (Oryctolagus cunniculus). J. Mammology; 69(1):28- 38,1987.
8. Worden, A.N., and Leahy, J.S. The behavior of rabbits. In: E.S.E. Hafez, ed. The Behavior of Domestic Animals; pp.397-414. Williams and Wilkins Co., Baltimore, MD. 1962.
9. Flynn, R.J. In: Parasites of Laboratory Animals. Iowa State University Press, Ames, IA, 1973.
10. Hammond, K., and Love, J.A. The use of fentanyl and droperidol for group formation in adult rabbits. Proc. Canadian Association for Laboratory Animal Science Conference, Ottawa, Ont.. Canada, 1989.
The authors are affiliated with the Animal Care Centre, University of British Columbia. Send reprint requests to J. Love, Animal Care Centre, 6199 South Campus Rd., University of British Columbia, Vancouver, B.C., Canada, V6T 1W5.
Reproduced with permission of the publisher. Published in Lab Animal 1991 20(8).