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| Figure 5 The traditional small-particle bedding substrate does not allow mice to construct nests which could insulate them from aversive environmental factors. |
Environmental Improvements are changes in traditional housing conditions that can promote the physical and behavioral well-being of the confined subject. Well-being is the subjective state contentment. The well-being of a subject is enhanced when basic needs for physical health, behavioral health and comfort are met.
3.1. Environmental Necessities
Environmental Necessities are husbandry factors that address basic species-specific needs of the confined subject.
3.1.1. Flooring and Bedding Material
Grover-Johnson and Spencer (1981) found, in Sprague-Dawley rats who were kept all their lives on wire mesh flooring, that the distal sciatic/tibial/plantar nerve complex developed striking morphological abnormalities, presumably as a result of the rat-inadequate flooring condition of the cages. Peace and Singer (2001) assessed the clinical records of Sprague-Dawley rats who had been kept for more than one year either in wire-bottom cages or in large solid-bottom cages with woodchip bedding. The incidence of clinically observed foot lesions (callus, ulcer/crust, swelling) was:
2 percent in both females and males kept on a solid floor, compared with
30 percent in females and 92 percent in males kept on a wire mesh.
Bradshaw and Poling (1991) tested Sprague-Dawley rats in divided wire-bottom cages where one half was empty, and the other half was covered with plywood or a layer of woodchips that were prevented from falling through the wire mesh by a pan attached to the cage bottoms. The rats avoided the wire mesh and showed a significant preference for the side of the cage with plywood (72 percent) or with woodchips (71 percent). Manser et al. (1995) showed in Sprague-Dawley rats, raised on wire mesh flooring, that the animals strongly prefer a solid floor when they are given the choice, and that they are prepared to make considerable efforts to reach a solid floor when they want to rest (Manser et al., 1996). They will spend most of the time (81 percent) in such a cage and will stay away from the mesh floor cage to which they were originally habituated (Manser et al., 1996). Blom et al. (1993) confirmed in Wistar rats, that individuals avoid wire mesh flooring.
Krohn et al. (2003) measured telemetrically two cardiovascular stress parameters in pair-housed Sprague-Dawley rats. Blood pressure and heart rate were significantly higher during both day and night when the rats were kept on wire mesh or solid plastic floors compared with a layer of woodchips. This suggests that hard floors are relatively stressful for rats.
Mulder (1974a), Blom et al. (1993) and Ras et al. (2002) found that Sprague-Dawley and Wistar rats have a strong preference for large, fibrous bedding material such as woodchips over corncob litter and sawdust.
Blom et al. (1996) tested the preference of C57BL/6 and BALB/c mice for a cage with wire mesh flooring vs. solid flooring with various beddings. The animals avoided the wire mesh but showed a significant preference for solid flooring with bedding. Shredded filter paper was the most attractive substrate, followed by woodchips. Bedding material of small particles was relatively unattractive, probably because it was unsuitable for nest building and potentially irritating to the eyes (Figure 5). Eskola and Kaliste-Korhonen (1999) also noticed that BALB/c and C57BL/6 mice clearly prefer aspen wood-wool to "conventional bedding" (presumably aspen chips; Eskola et al., 1999), because they can use it both as bedding and convert it into comfortable nests. Paper tissues and paper-based structures that can be shredded provide ideal bedding and nesting material for mice (Figure 6).
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| Figure 5 The traditional small-particle bedding substrate does not allow mice to construct nests which could insulate them from aversive environmental factors. |
Port and Kaltenbach (1969) found in SCH:ARSHa mice a significantly increased preweaning mortality when the animals were kept on corncob when compared with pine sawdust bedding (22 vs.13 percent).
Mulder (1974b, 1975) noticed that female SCH:ARSHa mice invariably prefer woodchips over small particle bedding materials derived from corncob, dehydrated alfalfa or clay.
Smith et al. (2000) furnished the wire-bottom cages of individually housed CD-1 mice each with a 5 x 5-cm rayon/polyester gauze. This pad was changed weekly throughout a test period of 52 weeks. The study confirmed that the mice preferred to rest on the gauze pad rather than on the wire mesh. Whenever they were undisturbed, the mice were in contact with their pads. Usually they pulled at the threads without breaking them, and fluffed them into perfect material for nest construction (Watson, 1993).
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| Figure 6 Mice need large, fibrous material for the construction of their nests. (Photo by Maureen Hargaden, Hoffmann-La Roche Inc., Nutley, NJ, USA. ©Roche Laboratories Inc., 2005) |
Pettijohn and Barkes (1978) observed gerbils who were given the choice of entering equally-sized compartments offering plastic flooring, woodchips, sand, a sheet of newspaper, or a terrycloth towel. Both sexes had a significant preference for sand and a secondary preference for woodchips. The sand was particularly attractive, eliciting digging and gerbil-typical sand bathing, which serves to remove excess body oils from the fur.
Arnold and Estep (1994) tested golden hamsters in an apparatus that gave them simultaneous access to a wire-floored 510-cm2 standard cage and to a solid-floored 450- cm2 cage with corncob litter. Subjects spent significantly more time (70 percent) on the solid floor with litter, even though this implied a reduction in floor space.
Fullerton and Gilliatt (1965) examined guinea pigs housed singly in 1000-cm2 cages and noticed pressure neuropathies in the plantar nerves in:
94 percent of 16 animals kept on wire mesh floors, in contrast to
19 percent of 16 animals kept on solid floors covered with a deep layer of sawdust.
Turner et al. (1992) observed Dutch x French Lop rabbits in a test cage offering a choice of two different substrates. The rabbits avoided sawdust, woodchips and bare concrete floor but showed a significant and equal preference for both straw and shredded paper. Straw was specially favored, and the animals spent more time nibbling and manipulating it than they did paper (Figure 7).
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| Figure 7 Straw is a particularly attractive bedding and foraging material for rabbits. Cardboard boxes provide look-out posts and shelters (Gunn-Dore, 1997). |
3.1.2. Shelter, Burrows, Nest Boxes and Nesting Material
Bradshaw and Poling (1991) tested the preference of Sprague-Dawley rats for equally-sized living quarters that were either barren or furnished with a PCV tube 7.6 cm in diameter, or with paper towels. The rats showed little interest in the plastic tube but a strong preference for paper towels, which they immediately used to construct comfortable nests.
Patterson-Kane et al. (2001) gave Hooded Norway rats the choice of spending time in a barren cage versus identical cages provisioned either with four sheets of tissue paper (sic), one handful of shredded paper, a PVC tube (8-cm diameter), a plastic cylinder (15-cm diameter) or a coffee tin with an 8-cm-diameter entrance hole. Female and male rats showed significant preferences over the barren cage only for shredded paper and the tin box. The other enrichment options elicited negligible attention.
Nolen and Alexander (1966) compared two different nesting materials and noticed that Sprague-Dawley rats weaned significantly more pups per litter (10.8) when they were kept in cages furnished with shredded paper vs. woodchips (7.0). Access to shredded paper decreased infant mortality from 45 to three percent. Females with woodchips simply "dried up". Those with shredded paper built nests and had full milk glands, as reflected in substantially higher lactation indices. The paper nests allowed them to burrow and insulate themselves from disturbing environmental factors and also to create an optimal microclimate for their pups (Figure 8). Norris and Adams (1976) found in CFHB rats, that wood-wool may be an even more appropriate nesting material. Females with access to wood-wool reared a much higher proportion of their young (82 percent of 1182) than females with paper tissues (40 percent of 791). Rats with wood-wool constructed more elaborate, and probably more species-typical, nests than rats with paper tissues. Animals who had access to wood-wool for a long period of time (500 days), however, were susceptible to subcutaneous tumors and nasal scabbing.
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Figure 8 Appropriate nesting material here shredded paper is a necessity for rats to build relatively comfortable nests for themselves and for their offspring (Lawlor, 1997). |
Galef and Sorge (2000) examined the usefulness of 7.5-cm-diameter PCV tubes as shelters for singly caged Long-Evan rats. While males were seen inside the tubes only rarely, females used the tubes approximately 36 percent of the time during the night and 20 percent of the time during the day.
Townsend (1997) demonstrated that male Wistar rats have a strong preference for living quarters that contain an upturned mouse cage (33 x 15 x 13 cm). The animals used such a structure as shelter, an object to sit on, gnaw and move around. The mouse cage also increased the wall surface, thereby fostering the animals' urge to move close to walls (thigmotaxis, "wall-hugging") rather than on unprotected terrain.
Patterson-Kane (2003) tested female Wistar rats in a T-maze for preference of a barren cage versus a cage of the same size, furnished with one of seven different shelters the size of a mouse cage. The rats had a consistent (73-95 percent) preference for the cage containing the shelter. They preferred:
- shelters made from plastic or tin to cardboard,
- opaque shelters to translucent shelters and
- enclosed shelters with one 8-cm2 entrance hole to those open on one side.
When their cages are furnished with appropriate shelters, rats will spend about 85 percent of the time in them during the day when the animals rest and 25 percent of the time during the night when the animals are active (Collier et al., 1990; Townsend, 1997; Eskola et al., 1999; Saad et al., 2004).
Manser et al. (1998a) tested the suitability of 20 x 12.5 x 12-cm plastic boxes of different transparencies and design, and various nest materials, in male Sprague-Dawley rats. All three boxes were used for resting throughout most the day and part of the night. The rats favored an opaque nest box over a transparent one, and a nest box with enclosed corners (one 9 x 10-cm entrance) over one without front and back walls. They strongly preferred soft paper strips (0.5-1.0 cm wide and 40 cm long) over coarse paper strips, woodchips, and nestlets. They did not build nests with the paper strips but spent an average of 93 percent of the time manipulating and gnawing them during the day and 77 percent of the time during the night.
Jegstrup et al. (2005) demonstrated, in three inbred strains (BN, BDIX, LEW) of pair-housed male rats, that naïve animals who have never had access to any kind of nesting material do build nests if the correct stimuli are provided. The animals were housed in 48 x 38 x 20-cm cages with aspen chips bedding, each furnished with a roofed wooden nest box measuring 28.5 x 20.5 x 12.5 cm. The box had entrance holes on two sides, each of 6-cm diameter. Wood-wool and autoclaved straw the material of choice for nest-building in wild rats (Calhoun, 1962) were placed outside the box. Every two weeks the nest was removed and the box, along with the two rats, transferred to a new cage. Additional fresh bedding material and straw were added twice a week, and wood-wool once a week. The nest box was machine-washed every two months. All animals built a new nest in the box during the two-week period between cage changing procedures. They would begin with the removal of all aspen chips from the nest box, continue with the collection of straw and wood-wool and finally form a mat inside the empty nest box. This mat could be several centimeters thick and was then arranged into a cup-shape nest. The nest consisted of both straw and wood-wool fibers, with straw making up the major part of the structure. Constructing their own nests not only allowed the rats to engage in a species-typical behavior, which presumably enhanced their feeling of security, but also reduced the incidence of aggressive interactions (Jegstrup and Ritskes-Hoitinga, 2004).
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| Figures 9a&b When they are provisioned with a rat-adequate shelter and rat-adequate nesting material (a) male rats will move all the substrate into the shelter and build a well-formed nest (b) even when they have never before been exposed to nesting material nor shelter. (Photos by I. Jegstrup; reproduced with the permission of the publishers of the Proceedings of the 8th FELASA Symposium, 2002) | |
Van de Weerd et al. (1998a, 1998b) assessed in choice tests the preference of C57BL/6 and BALB/c mice for barren versus same-sized cages furnished with (a) a rectangular, 8 x 10 x 6-cm nest box of various qualities or (b) different types of nesting material. Pilot studies by Buhot-Averseng (1981) have shown that outbred mice have a preference for rectangular, narrow, roofless frames with perforated walls. In Van de Weerd's studies, both strains and both sexes showed significant preferences for a cage containing a nest box or nest material over an empty cage. Heinzmann et al. (1998) made a similar observation in group-housed female Him:OF1 mice. Van de Weerd's mice strongly preferred nest boxes made of materials that allowed olfactory and visual cues to pass, e.g., grid metal or perforated metal. They stayed away from dark nest boxes, made of sheet metal or gray PVC. Paper tissue was preferred over paper towel as nesting material. When given the choice the mice spent an average of more than 69 percent of the 24-hour day in the cage with the paper tissue, compared with less than 25 percent in the cage with the most preferred nest box.
These observations demonstrate the importance for mice to construct their own nests according to their comfort and microclimatic needs. Prefabricated structures have their place as a refuge in the event of an alarming situation, but not as a mouse-adequate sleeping site.
Key and Hewett (2002) observed same-sex trios of BALB/c mice who each had access to a dark triangular plastic shelter with one entrance at the front and a second entrance/exit in the roof. Mice with the shelter showed no difference in general activity, or in agonistic behavior, but they engaged in bar-gnawing significantly more than control mice without shelter. These findings were confirmed in both sexes and they suggest that this particular shelter did not meet mouse-specific comfort requirements.
When appropriate nesting material is put on the cage lid, mice will not hesitate to pull it into the cage and start building a nest (Lynch and Hegmann, 1972). Van de Weerd et al. (1997) inferred from choice tests that C57BL/6 and BALB/c mice of both sexes prefer soft paper over woodchips or wood-wool. They will spend about 15 percent of the 24-hour day dragging the material into the right position and building a nest, in which they will spend about 50 percent of the time sleeping and grooming.
Porter and Lane-Petter (1965) reported that mice had a lower preweaning mortality when they had access to shredded paper to build nests than when they were kept on woodchips. Obviously, a nest provides a quieter rearing environment and a much better regulated microclimate than woodchip bedding.
Hobbs et al. (1997) videotaped male mice kept in groups of four in 260-cm2 cages furnished with nestlets. This cellulose nesting material was contacted by CD-1 mice 89 percent of the time, by DBA/s mice 65 percent of the time and by B6C3F1 mice 72 percent of the time.
Nestlets are attractive for mice, but they can be a health hazard. Bazille et al. (2001) noticed an increased prevalence of conjunctivitis in Hsd:Athymic Nude-nu mice who were provided with nestlets. The conjunctivitis resolved completely when the nestlets were replaced with paper towels as nesting material.
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| Figure 10 Paper-based shelters and soft paper are species-appropriate materials for mice to build nests in which they can retreat and sleep. (Photo by M.K. Meijer, Utrecht University, The Netherlands) |
Van Loo et al. (2005) tested the preference of groups of three or four female BALB/c, C3H/HeNHsd and C57BL/6 mice for an approximately 15 x 9 x 6-cm paper-based, triangular nest box with a 4-cm-wide access hole, or a similarly shaped and sized red transparent plastic nest box with a 5 x 3-cm opening on the long side and another triangular opening in the top of the box (Figures 10 & 11c). All three strains showed a significant preference for the paper box, which had the advantage of being much lighter (20 g) than the plastic box (95 g), allowing the mice to move the whole structure around and change the position of its entrance. The plastic box was too heavy for such maneuvering and hence never changed its place. The mice also gnawed the paper box, occasionally nibbled an extra hole in the side or shredded part of its walls, using the shreds to strengthen the nest. They could not do this with the plastic box. All groups of mice slept inside the paper box, but never in the plastic box. If they chose to sleep in the cage that contained the plastic box, they did so in the sawdust outside the box. When paper tissues were provided, the mice dragged the material into the paper box and built a nest, but they never attempted to build a nest in the plastic box (Figures 6 & 10).
Mice may investigate and climb on plastic shelters but will be reluctant to use them as nests (Figure 11a). They will rather sleep outside than in a plastic shelter (Figure 11b). When given the choice, they will build their own nest and sleep in it rather than make use of a prefabricated, indestructible "mouse house" (Figure 11c).
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Sherwin (1996) concluded, from a series of preference tests with individually caged male TO mice, that the animals were less motivated to use tubes as sleeping sites than to use sawdust. No preference for tubes was found, regardless of their shape, length, openness, opacity and width. A tube can be useful as a refuge when the animals are startled, but it is not a good substitute for a nest.
Sherwin et al. (2004) found that BALB/c mice are more motivated to burrow rather than run through tunnels. They will spend about ten percent of the 24-hour day burrowing if they are provided with a suitable substrate such as compacted dampened peat. Throughout a study period of nine days, the mice did not decrease their burrowing activity, suggesting that the expression of this behavior like nestbuilding also fulfills a strong biological need.
Waiblinger and König (2004) furnished the cages of gerbil families with an artificial burrow system consisting of a nest box and an angled access tube. In a choice test, the animals clearly preferred a dark burrow system over a transparent one. They spent about 80 percent of the 24-hour day in the dark burrow. The importance of a dark burrow is in agreement with the fact that gerbils prefer partially darkened cages over transparent standard cages (Van den Broek et al., 1995).
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Jansen (1969) showed in golden hamsters that both females and males quickly learn to press a bar to obtain small strips of paper (Figure 12). They would typically push the strips into their cheek pouches, return to their home cages, retrieve the paper and do some nestbuilding, then return to the test chamber, press again and continue with the hoarding of this highly valued material. These observations demonstrate that paper serves as a potent positive reinforcement for hamsters, comparable to food and water.
Ottoni and Ades (1991) showed that hamsters prefer a dark shelter over a transparent one (Figure 13), and a relatively large shelter over a small one (730 cm2 x 10 cm vs. 320 cm2 x 10 cm).
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Figure 13 A dark nestbox with nesting material should not be regarded as environmental enrichment but as basic furniture, ensuring basic comfort needs of the caged hamster. |
There are no published data on species-appropriate shelters for guinea pigs, even though there is a general consensus that the animals are easily startled and, therefore, need adequate provision of cover during alarming situations, which are unavoidable in the research laboratory (Gray, 1988; Reinhardt, 2002; Banjanin et al., 2004; Ottesen et al., 2004; Figure 14).
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Hansen and Berthelsen (2000) furnished the 3540-cm2 single-cages of NZW and French Lop rabbits with 44 x 25 x 19 cm wooden boxes with perforated plastic floors and roofs (Figure 15). After a 3-month habituation period, the rabbits hardly made use of the box (about 1 percent of the time) as a place for rest or escape but spent about 56 percent of the video-recorded time on its roof. Obviously, the animals had no need for a shelter but benefited from an elevated look-out.
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| Figure 15 There are no data published assessing the effect of shelters on the compatibility of group-housed rabbits. (Photo by Natasha Down, York University, Toronto, Canada) |
Patterson-Kane et al. (2002) showed that individually caged female Hooded Norway rats will readily work, by pressing a lever, to get access to a cage containing three other female rats, but not to get access to a cage that is empty but larger than their home cage. Companionship, evidently, was of greater importance for them than unstructured space. When the rats could choose between cages containing one, three, five or 11 rats and the stocking density was kept constant (20 cm2 per subject), they showed a clear preference for five rats (Patterson-Kane et al., 2004).
Moncek et al. (2004) reported significantly higher plasma concentrations of corticosterone in male Wistar rats kept in groups of ten in large cages (500 cm2 /subject) furnished with toys, tunnels, swings and running wheels than in rats kept in groups of three or four in relatively small unfurnished cages (290 cm2 /subject). Unfortunately, it is not made clear whether the difference in corticosterone levels was related to the difference in group size, cage size or cage equipment. Living with more partners in a larger and enriched cage probably increased the overall level of the subjects' activity, which may have resulted in a biologically normal, intermittent endocrine activation reflecting eustress.
Brown and Gunberg (1995) compared the stress status of female and male Wistar rats housed either alone in a large (1010 cm2 ) barren cage or in small groups of four under crowded conditions in a much smaller (100 cm2 /female; 160 cm2 /male) barren cage. Female rats had significantly higher plasma corticosterone levels when they were caged singly than when they shared a small cage with three other females, but the opposite was true for males. Male rats had relatively low corticosterone levels when they were alone but higher levels when they had to share a small cage with three other males. While the key stressor for female rats was social deprivation, crowding was the key stressor for males.
Rank-related conflicts are not common in caged rats (Grant and Chance, 1958), and there are no published reports of serious problems associated with overt aggression in same-sex pairs or groups. However, low-ranking group members may experience social distress under the given constraint of artificial confinement and competition for resources (Blanchard et al., 1995; Hurst et al., 1996; Hurst et al., 1999).
Van Loo et al. (2001) gave male BALB/c mice the choice of staying in either an empty cage or in a divided cage of the same size with one half already occupied by an unfamiliar male mouse who could be seen and smelled through a transparent wall with holes. The separating wall served as a precaution against overt aggression for which male mice are notorious. The test mice showed an overall preference for the inhabited cage, which indicates that "even" male mice prefer the company of another male mouse over being alone.
The social housing of male mice can jeopardize the safety of the animals. There is usually one dominant male who vigorously defends his territorial boundaries (Mackintosh, 1970). In order to avoid conflicts, subordinate males try to keep at a safe distance or simply leave the territory. The constraints of confinement usually make this impossible, and considerable, often sustained fighting between males becomes a common event. Subordinate males never retaliate when attacked by the dominant mouse but may demonstrate distress behavior such as flight attempts and submissive/defensive postures, often accompanied by squealing. Bolam (2005) reported a 25 percent incidence of injuries in 70 male CD-1 mice who were housed in pairs or trios. Due to aggressive incompatibility eight percent of the animals had to be separated during a ten-month study. Although fighting does not necessarily lead to serious injury, the dominant male may fiercely attack over and over again and even kill other males. Emond et al. (2003) report a case in which 0.3 percent of the annual population of 37,566 group-housed male CD-1 mice had to be removed due to serious injuries. Out of concern, animal care technicians started separating dominant males who threatened, attacked or chased other males. As a result, only 0.13 percent of the next annual population of 25,802 male mice had to be removed due to serious wounds resulting from aggression.
Haemisch and Gärtner (1994) and Bergman et al. (1994/95) demonstrated in trios of male DBA/2J and HLG/Zte mice that the provision of vertical dividers may increase rather than decrease aggressive conflicts, presumably because the dividers can serve as territorial boundaries for the most dominant male, while providing subordinate animals insufficient escape options. Marashi et al. (2003) kept male CS mice in groups of four either in barren 835-cm2 standard cages or in spacious 4000-cm2 terraria that were enriched with several climbing structures, hemp ropes, several platforms at different levels, and a ladder. Mice in the enriched environment were engaged in agonistic conflicts significantly more often than non-enriched mice, presumably because the various structures in the enriched terraria promoted the establishment of territories marked by visual landmark boundaries. The increased level of territorial disputes was reflected in increased stress, as measured by significantly higher plasma levels of glucocorticoids compared with mice living in barren cages. However, this was counterbalanced by significantly higher rates of positive social behaviors sitting together with body contact, playing, and allogrooming in the enriched mice.
Aggression-related problems with the social housing of female mice have not been reported in the literature.
Arnold and Estep (1990) observed male golden hamsters placed with another littermate in a specially designed enclosure that allowed them to stay away from, or in proximity to each other. During 46-hour test sessions individuals spent 67 percent of the time in proximity to each other. Arnold and Gillaspy (1994) confirmed these findings in a follow-up study of female hamsters, and concluded that hamsters do not prefer social isolation regardless of the fact that social housing is typically associated with overt aggression, and hence may be more stressful for the animals.
The social needs of guinea pigs, especially in relation to gender, have not yet been assessed. There is, however, a general consensus that guinea pigs should always be housed in a social environment (Lawlor, 1997; North, 1999; Raje and Stewart, 2000; Banjanin et al., 2004; Ottesen et al., 2004; Sachser, 2004).
Aggressive interactions among females are rare and of no serious consequences under normal conditions (Reinhardt, 1971). Overt aggression can be a problem in males. Agass and Ruffle (2005) inserted a clear plastic partition in the cages of groups of four. Each group was divided into two pairs who maintained uninterrupted visual contact with each other. The authors do not provide data but make the statement that implementing these cage dividers "considerably reduced the incidence of bullying ... and there have been no further significant incidents of biting or aggression within pairs." Beer and Sacher (1992) compared the plasma glucocorticoid levels of males kept in pairs and in groups of six or twelve. Average corticosterone concentrations were significantly lower in pairs, suggesting that group-housed males were more stressed.
Whary et al. (1993) kept female NZW rabbits individually in 3600-cm2 barren cages or as a group of eight in a floor pen (3750 cm2 /subject) furnished with a resting shelf, a litter box and a PVC tube serving as potential shelter. Both categories of rabbits were monitored on a regular schedule over a 12-week period. Single and group-housed animals did not show significant differences in immune responses, plasma corticosterone concentration and growth rate, indicating that research-sensitive physiological parameters measured in the conventional single-housing system were not affected by the unconventional group-housing arrangement. Group-housed rabbits did not show either an increased incidence of infectious disease or any injuries traceable to aggression. Group-housed rabbits benefited from the increased available space and were frequently observed lying in the rabbit-typical full stretched-out, lateral recumbent position, which singly caged rabbits usually cannot adopt due to insufficient space (Gunn-Dore, 1997).
Turner et al. (1997) kept does in groups of four or five in large pens (16,700 cm2 /subject) provisioned with straw bedding, cardboard boxes and raised shelves. High- and low-ranking members of each group were identified and their immune status compared. No evidence of immunosuppression related to social rank was found either in NZW or Dutch x California breeds.
Huls et al. (1991) observed NZW does who were pair-housed in two interconnected 2580 cm2 cages. Partners spent on average 88 percent of the observations in the same half of the cage and were in direct body contact with each other about 20 percent of the time. Brooks et al. (1993) conducted a similar study in which adult pair-housed NZW does also chose to stay together in the same half of a double cage 90 percent of the time. Held et al. (1995) gave individual members of groups of four adult female NZW or Dutch x California rabbits the choice of (a) joining the other three group members in a large pen or (b) moving into a solitary, yet equally large and equally furnished pen. Both low-ranking and high-ranking does showed a consistent, albeit moderate, preference not for the pen with the other companions, but for the solitary pen. Together, these findings indicate that female rabbits do have a strong affinity to each other, but that they want to be alone at times.
Aggression is a normal social behavior that has its intrinsic value in establishing and confirming dominance-subordinance relationships. However, within the constraints of artificial confinement social aggression can become a problem, because the animals are forced to stay in close proximity all the time.
Domesticated rabbits are remarkably docile with humans and demonstrate hardly any fear responses, but both sexes tend to be more aggressive among themselves than their wild counterparts are (Kraft, 1979a; Kraft, 1979b). Rabbits should be housed in a social setting, but it can be a challenge to minimize the risk of aggressive incompatibility (Morton et al., 1993).
Tamburrino et al. (1999) assessed the clinical records of 135 sexually mature female rabbits of unspecified breed. The animals were housed in groups of five in pens (5200 cm2 /rabbit) that were covered by a 10-cm layer of woodchips topped by 14-cm of straw. Each pen contained half of a 58-cm-diameter plastic barrel shelter. Over the course of a nine-month period 23 (17 percent) rabbits sustained minor, and two (1.5 percent) sustained major fight wounds.
Based on the clinical records of several thousand group-housed female NZW rabbits, Love and Hammond (1991) and Love (1994) offer the following recommendations to minimize injurious aggression:
An anecdotal report by Howard et al. (1999) suggests that the provision of a visual barrier behind which subjects can "escape" and tubes in which subjects can hide minimizes aggression among group-housed, probably female, Dwarf Lop rabbits. Held et al. (1994) concluded from observations of a group of 20 NZW and a group of 20 Dutch x California does kept in 3-m2 floor pens that raised platforms reduced agonistic interactions by allowing the pursued animals to move out of sight. Statistical data analysis, however, did not support this presumed effect.
Chu et al. (2004) recorded the behavior of non-littermate female NZW rabbit pairs over a five-month period as the animals matured from juveniles to mature does. The animals were kept in 9270-cm2 cages without structures that would have allowed them to get away from each other. Companions spent on average about 27 percent of the time in physical contact with each other. One of the four study pairs, however, had to be separated due to persistent aggression resulting in serious bite wounds at the end of the study, after the two partners had become sexually mature. Bigler and Oester (1994) witnessed injurious aggression in one of eight pairs during a seven-month study period. Nevalainen et al. (2003) kept littermate female NZW rabbit pairs in 7200-cm2 cages that were furnished with a raised shelf but no structures for privacy. During a 4.5-month study occasional fighting between cage companions was seen, but after the animals had reached sexual maturity more frequent and more serious fighting necessitated early termination of the study.
Once they reach sexual maturity male rabbits become even more intolerant of each other than females. This makes their housing in a social setting not advisable (Morton et al., 1993; Love, 1994).
Kalagassy et al. (1999) castrated Flemish Giant x Giant Chinchilla prepubertal males to see whether this would make them more suitable for social housing. A total of ten intact and twelve castrated male littermates were housed in pairs in 12,700-cm2 cages each furnished with a wooden nest box and provisioned regularly with vegetables and hay. Behavioral observations revealed that castrated males engaged in aggression significantly less often (0.02 vs. 0.3 percent), but spent significantly more time (41 vs.19 percent) resting in body contact with each other than intact males. While three of the five intact male pairs had to be separated due to injurious aggression, none of the six castrated male pairs required separation during an unspecified follow-up period.
Castration does not necessarily resolve aggressive incompatibility among male rabbits in all cases. Raje et al. (1997) kept a group of five castrated male NZW rabbits in an enclosure furnished with corncobs and cornhusk bedding and PVC pipes. Six days after the establishment of the group, a major conflict resulted in all but one rabbit suffering some kind of minor injury. The group was split into a pair and a trio. It is not made clear if this intervention was a long-term solution of the aggression problem.
Confined rodents and rabbits have no choice but to spend all of their time on the floor of their primary enclosure. Appropriate flooring is, therefore, an essential condition for their general well-being. A 1999 survey of 12 United States-based pharmaceutical and contract toxicology laboratories showed that more than 80 percent of the rodents used were housed in wire-bottom cages (Stark, 2001).
Wire-bottom caging is preferred by humans over solid-bottom caging because of the lower labor and monetary investment, but not by the animals who are at a high risk of developing pressure neuropathies and foot lesions on wire mesh floors (Fullerton and Gilliatt, 1965; Grover-Johnson and Spencer, 1981; Kraus, 1994; Kesel, 1995; Peace and Singer, 2001; Dimeo and Mitchell, 2005). When they have a choice, rodents will avoid wire mesh and make considerable efforts to get access to a solid floor.
From an economical standpoint solid-bottom caging is at a disadvantage as it requires absorbent litter for sanitary reasons. The caged animals themselves, however, prefer a bedded floor over a bare solid floor, probably for comfort and thermoregulation. They also show a markedly higher stress level as reflected in elevated blood pressure and elevated heart rate when they have to spend all the time on a wire mesh floor or a bare solid floor rather than on a bedded solid floor. This has been demonstrated in rats, and there is good reason to assume that it also applies to mice, guinea pigs, hamsters, gerbils and rabbits. It indicates that the provision of bedding material not only enhances animal welfare but also scientific methodology by minimizing stress.
Rabbits and most rodents prefer large fibrous bedding material such as straw, and shredded paper over sawdust. Gerbils prefer sand, which is their natural digging substrate (Ågren et al., 1989) and allows them to groom their fur in a species-typical manner (Pettijohn and Barkes, 1978).
It is characteristic of rodents but not of domesticated rabbits to be afraid of crossing an area that offers no cover or hiding place from a potential predator. The "open-field test" makes use of this disposition to assess a subject's level of anxiety and fear. Living quarters that are essentially permanent open fields are, therefore, not conducive to the confined subjects' well-being. A shelter not only provides protection, but can also be used as a relatively insulated nest box for resting, sleeping and the raising of pups, especially in conjunction with nesting material. If they are able to choose, rats, mice, gerbils and presumably also hamsters and guinea pigs prefer living quarters furnished with a shelter, or with a substrate that can be used to build a shelter, over unprotected, barren living quarters of the same size.
For rats the shelter should be dark and rectangular, made of solid material with all corners enclosed, and have one or two access holes. Such a structure simulates a burrow, and rats will spend most of their time in it (Boice, 1977). Soft paper strips are the preferred nesting material for them. For mice the shelter should be a rectangular, roofless, narrow frame with perforated walls, or even better a paper-based enclosed structure with one entrance. Mice have a very strong urge to construct their own nests. Soft paper nesting material is, therefore, more important to them than a pre-formed shelter.
Rats, mice and hamsters readily work for appropriate nesting material (Jansen, 1969; Oley and Slotnick, 1970; Roper, 1975; Collier et al. 1990; Manser et al., 1998b), indicating that it is an essential resource with which they should always be supplied.
Gerbils and hamsters, and presumably guinea pigs as well also need dark covered shelters. It is not clear whether non-breeding rabbits take advantage of enclosed shelters. A shelf may be preferable, because it offers a covered refuge and elevated resting site without reducing the floor area of the cage.
Housing rodents with same-sex companions in pairs or small groups rather than alone has several important benefits for the individual animal:
The assumption that certain regulatory authorities "prefer" single-housing should be challenged. Social-housing should become the norm whenever animals are compatible, and anything less has to be justified on the basis of sound science (Dean, 1999). Companionship is particularly important to female rats, who should never be caged alone.
Even male mice and hamsters, notorious for their aggressive propensities, prefer the company of a cagemate to being alone. This does not mean that they should always be kept in a social setting regardless of circumstances. In groups of male mice, there is usually only one animal who instigates fights. The removal of such an individual can often safeguard the integrity of the remaining group. The management of aggression in hamster groups has not yet been addressed in the scientific literature.
If they are not used for breeding, male guinea pigs are best housed in pairs. This eliminates social stress and the risk of injuries resulting from group-housing.
Injurious aggression can make the social housing of mature rabbits a challenge. It has been shown in pair- and group-housed nonhuman primates that the option of visual seclusion reduces aggressive tension while simultaneously promoting affiliative behaviors (Reinhardt and Reinhardt, 1991; McCormack and Megna, 2001). Does have a strong affinity to each other, but they also want to have the option of being alone at times. It is very likely that they would also benefit from sight barriers that allow companions to break visual contact with each other as needed, thereby avoiding aggressive tensions and fostering their long-term compatibility. Bucks are unlikely to tolerate each other. Single-housing is the safest, albeit not best, option for them.
Whenever it is deemed advisable to isolate rodents and rabbits for incompatibility reasons, it is an imperative to house the individual animal, including male rabbits (Batchelor, 1991), in an arrangement that allows him or her to at least see, hear and smell other conspecifics.
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