Autumn 2004 • Volume XIII, Number 4

Lab Stress 24/7
By Jonathan Balcombe, Ph.D.

Throughout history, human societies have dealt with criminals by confining them in small cells. Not only does imprisonment remove the offender from daily life, but by taking away the inmate’s freedom and autonomy, it constitutes punishment. Further reductions of social contact represent additional penalties to the wrongdoer.

Though guilty of no crime, the animals caged in laboratories find themselves in comparable circumstances. From birth, they are kept in small, barren “shoe-box” cages, usually stacked in an enclosed, windowless room, with no tunnels or boxes to hide in and no material with which to build nests. Lumps of dull commercial food are placed overhead, where it can be nibbled only between the cage bars. For most, the only dependable source of stimulation is each other, though many are consigned to solitary confinement at weaning. Because most animals spend their entire lives in small cages, suffering caused by inappropriate housing is typically of greater duration than that caused by the experiments themselves.

These conditions contrast starkly with those in the wild, where most home ranges are thousands of times larger. Animals have the opportunity to forage, burrow, climb, take cover, explore, and nest, and the freedom to behave according to their needs and choose compatible social partners.

Standard laboratory settings also introduce undesirable intrusions. These highly sensitive animals react stressfully to people entering the room, being picked up, and having their cages moved or cleaned (Balcombe et al. in press). They are often housed in close proximity to laboratory equipment such as video and computer monitors, cage washers, and ventilation systems, which emit ultrasonic sounds to which they are sensitive. In one study, rats moved less and spent significantly more time in the corners of their cages in proximity to an oscilloscope and a computer monitor (Sales et al. 1988).

Not surprisingly, the deleterious effects of laboratory housing on rodents are considerable. Since the 1960s, it has been known that rodent brains—like those of humans—become stunted by lack of mental stimulation, which in turn can profoundly influence the animals’ normal behavior. Some 50 percent of the tens of millions of mice now housed in laboratories develop functionless repetitive behavior patterns termed “behavioral stereotypies.” These include gnawing at the cage bars, rapidly jumping up and down on the hind paws, patterned running, backward somersaulting, and weaving (pacing and rearing to and fro over the same point). Stereotypies arise from frustration of natural behaviors, including nesting, hiding, foraging, exploration, and attempts to escape. They may be repeated tens of thousands of times daily and are widely believed to reflect suffering.

PCRM has been reviewing published studies documenting the effects of standard laboratory housing conditions on rodents, whose welfare is typically given low priority by policy-makers and ethical review committees. There is clear evidence that these animals perceive their conditions as undesirable with regard to spatial confinement, lack of stimulation, and social pressures. Here are some examples from our findings:

• Rats lever-pressed an average 73 times for access to a standard cage containing three familiar rats (Patterson-Kane et al. 2002).
• Rats housed alone were more stressed than rats housed four per cage (n=8), based on significantly higher heart rates and arterial blood pressures recorded in the solitary rats (Sharp et al. 2002).
• Rats, particularly when they are young, are highly motivated to engage in social play (Knutson et al. 1998), and the 50kHz vocalizations they make during these interactions are believed analogous to primate laughter (Panksepp and Burgdorf 2003).
• Mice presented with cages of various sizes made more visits to larger cages than to smaller cages, spent more time in them, and worked harder to gain access to them (Sherwin and Nicol 1997).
• Rats preferred larger cages to smaller ones both in isolation and with other cagemates (Patterson-Kane 2002).
• Mice work for access to extra space, shelters, an exercise wheel, nesting materials, and other mice (Sherwin 1996a, Sherwin and Nicol 1997), and show preferences for shelters (Sherwin 1996b), nesting materials (Sherwin 1997) and specific soiling sites (Sherwin 1996c).
• Mice in standard cages drank more water containing an anti-anxiety drug than did mice given more resources (nest box, running-wheel, nesting material), indicating that depriving them of these resources is stressful (Sherwin and Olsson, 2004).
• Rats living in larger than normal cages with stimulus objects still had smaller brains than did rats living in a large (81 cubic meter) outdoor enclosure (Rosenzweig et al. 1978).
• Rats spent four times longer in a more complex cage than in less complex cages (Denny 1975).
• Rats raised in isolation in small hanging cages self-administered amphetamine more than did group-housed rats raised in more enriched environments (Bardo et al. 2001).
• Mice preferred a standard cage inhabited by another mouse to an equivalent but uninhabited cage or a barren cage (Van Loo et al. 2004).
• Juvenile rats also became significantly more active when anticipating 30 minutes of interaction with another free moving rat compared with a confined juvenile rat (van den Berg et al. 1999).
• Cages including toys, running wheels, or other distractions still represent confinement, and an unnatural degree of temporal and spatial monotony. Several studies have reported behavioral stereotypies in animals kept in relatively “enriched” cages (Würbel et al. 1998, Powell et al. 2000, Callard et al. 2000).

Recent research shows that both mice and rats bred for generations in the laboratory quickly revert to their ancestral behaviors when given the opportunity, and naturalistic housing would certainly be a great improvement to their welfare.
As long as animals remain in laboratory cages, it is essential to push for prompt and substantive reforms in their housing conditions. Ultimately, however, animals—and science—will be best served when the cages are not larger, but empty.

References
Balcombe JP, Barnard N, Sandusky C. In press. Laboratory routines cause animal stress. Contemp Top Lab Anim Sci.
Bardo MT, Klebaur JE, Valone JM, Deaton C. Environmental enrichment decreases intravenous self-administration of amphetamine in female and male rats. Psychopharmacol (Berl) 2001;155:278-284.
Callard MD, Bursten SN, Price EO. Repetitive backflipping behavior in captive roof rats (Rattus rattus) and the effects of cage enrichment. Anim Welf 2000;9:139-152.
Denny MS. The rat’s long-term preference for complexity in its environment. Anim Learning and Behav 1975;3:245-249.
Knutson B, Burgdorf J, Panksepp J. Anticipation of play elicits high frequency ultrasonic vocalizations in juvenile rats. J Comp Psychol 1998;112:1-9.
Panksepp J, Burgdorf J. “Laughing” rats and the evolutionary antecedents of human joy? Physiol & Behav 2003;79:533-547.
Patterson-Kane E. Cage size preference in rats in the laboratory. J Appl Anim Welf Sci 2002;5:63-72.
Patterson-Kane EG, Hunt M, Harper D. Rats demand social contact. Anim Welf 2002;11:327-332.
Powell SB, Newman HA, McDonald TA, Bugenhagen P, Lewis MH. Development of spontaneous stereotyped behavior in deer mice: Effects of early and late exposure to a more complex environment. Devel Psychobiol 2000;37L:100-108.
Rosenzweig MR, Bennett EL, Herbert M, Morimoto H. Social grouping cannot account for cerebral effects of enriched environments. Brain Res 1978;153f:563-576.
Sales G, Evans J, Milligan S, Langridge A. Effects of environmental ultrasound on behaviour of laboratory rats. In Laboratory Animal Welfare Research. pp 17-25. Proceedings of UFAW Symposium. 1998. Potters Bar: UFAW.
Sharp JL, Zammit TG, Azar TA, et al. Stress-like responses to common procedures in male rats housed alone or with other rats. Contemp Top Lab Anim Sci 2002;41:8-14.
Sherwin CM. Preferences of individually housed TO strain laboratory mice for loose substrate or tubes for sleeping. Lab Anim 1996a;30:245-251.
Sherwin CM. Preferences of laboratory mice for characteristics of soiling sites. Anim Welf 1996b;5:283-288.
Sherwin CM. Laboratory mice persist in gaining access to resources: a method of assessing the importance of environmental features. Appl Anim Behav Sci 1996c;48:203-214.
Sherwin CM. Observations on the prevalence of nest-building in non-breeding TO strain mice and their use of two nesting materials. Lab Anim 1997;31:125-132.
Sherwin CM, Nicol CJ. Behavioural demand functions of caged laboratory mice for additional space. Anim Behav 1997;53:67-74.
Sherwin CM, Olsson IAS. Housing conditions affect self-administration of anxiolytic by laboratory mice. Anim Welf 2004;13:33-39.
van den Berg CL, Pijlman FT, Koning HA, Diergaarde L, Van Ree JM, Spruijt BM. Isolation changes the incentive value of sucrose and social behaviour in juvenile and adult rats. Behav Brain Res 1999;106:133-142.
Van Loo PLP, Van de Weerd HA, Van Zutphen LFM, Baumans V. Preference for social contact versus environmental enrichment in male laboratory mice. Lab Anim 2004:38:178-188.
Würbel H, Chapman R, Rutland C. Effect of feed and environmental enrichment on development of stereotypic wire-gnawing in laboratory mice. Appl Anim Behav Sci 1998;60:69-81.

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