Inanimate Enrichment: Refinement
Reduction of aggression
Rodents
Ambrose N, Morton DB 2000. The use of cage enrichment to reduce
male mouse aggression. Journal of Applied Animal Welfare Science
3, 117-125
"Aggression was significantly reduced by the addition
of novel enrichment [cardboard box, softwood block, cardboard
tube]. This reduction was expected as the provision of environmental
enrichment for naive animals would decrease the familiarity of
the cage and, therefore, lead to reductions of aggression. ...
Even a simple enrichment aid such as a glass water bottle can
significantly reduce postcage-cleaning aggression compared with
mice kept in a barren cage."
Armstrong KR, Clark TR, Peterson MR 1998. Use of cornhusk nesting
material to reduce aggression in caged mice. Contemporary Topics
in Laboratory Animal Science 37(4), 64-66
The provision of cornhusk reduced aggressive interactions by
offering subordinate animals cover and escape routes.
Arnold CE, Westbrook RD 1997/1998. Enrichment
in group-housed laboratory golden hamsters. Animal Welfare
Information Center (AWIC) Newsletter 8(3/4), 22-24
"Enriched hamsters [four same-sexed animals per group]
showed varied behavior and less aggression toward their cagemates.
The hamsters preferred jars to pipes" probably "because
the jars' greater height, as compared to pipes, made it easy to
look outside the cage."
*Cozens M 2006. Evaluation of the provision of
hay to guinea pigs at GlaxoSmithKline. Animal Technology and
Welfare 5, 31-32
"Two males in the group 3 had to be euthanized due to
bite wounds from fighting with cage mates - this aggression is
something we have also experienced in older male guinea-pigs where
it is not possible to feed hay." Male groups who received
hay were less difficult to handle and they were less aggressing
among each other than animals who had no access to hay.
Gwinn LA, Krauthauser CL, Kerr
JS 1999. Impact of home cage alterations on aggression in mice.
Abstracts of the AALAS [American Association for Laboratory
Animal Science] Meeting , 35 (Abstract)
PVC straight pipes, plumbing elbows and T pipes, and shreddible
nesting squares were evaluated. "Nesting squares appear to
be the most effective enrichment object for reducing the incidence
of aggression in group-housed male mice."
Jones RB, Nowell NW 1973. The effects of familiar visual and olfactory
cues on the aggression behaviour of mice. Physiology and Behavior
10, 221-223
Decreasing the familiarity of the environment and providing
flexible avenues of escape lead to reduced levels of inter-male
aggression. Greatest levels of aggression were found in cages
that had ungergone incomplete cleaning, such as renewal of substrate
only.
Marashi V, Barnekow A, Sachser
N 2004. Effects of environmental enrichment on males of a docile
inbred strain of mice. Physiology and Behavior 82, 765-776
"Environmental enrichment is intended to improve the welfare
of laboratory animals. However, regarding male mice, numerous
studies indicate an increase in aggressive behavior due to cage
structuring. On the one hand, this might be a problem concerning
animal welfare. On the other hand, enrichment is thought to hamper
environmental standardization and to increase variability of data.
... From weaning until day 77+/-3 of life, animals [male mice]
were kept in stable sibling groups of four under three different
housing conditions: (A) nonstructured Makrolon type III laboratory
cages ("standard housing"=S); (B) equivalent laboratory
cages that were enriched with a box and scaffolding ("enriched
housing"=E); and (C) spacious terrariums that were structured
richly ("super-enriched housing"=SE). No differences
in agonistic behavior, levels of plasma corticosterone (CORT),
and activities of adrenal tyrosine hydroxylase (TH) existed among
S-, E-, and SE-housed ABG males. Play behavior and general activity
increased significantly with increasing enrichment. ...Enrichment
did neither hamper standardization nor negatively influence the
variability of physiological parameters. In summary, using a docile
strain of mice revealed the positive effects of environmental
enrichment also on male mice. The lack of adverse effects on behavior,
physiology, standardization, and variability of data defuses these
arguments against providing docile male mice with enrichment."
McClure DE, Thomson JI 1992.
Cage enrichment for hamsters housed in suspended wire cages. Contemporary
Topics in Laboratory Animal Science 31(4), 33 (Abstract)
"Golden Syrian hamsters (n=99) were housed individually
in suspended wire cages so that spilled food and excreta could
be removed. After 8 days, the hamsters developed bizarre aggressive
behavior which consisted of growling, hissing, aggressive posturing
toward humans, destruction of water bottle rubber stoppers, and
attacking objects introduced into the cage. Many developed inappetence
which progressed to anorexia, depression, and unresponsiveness.
... When cotton nestlets were provided to all of the hamsters,
their appetite and responsiveness improved, but the aggressive
behavior remained unchanged. The nestlets were replaced by a 13-cm
length of 5.5-cm-diameter polyvinyl chloride pipe (PVC). The water
bottles were replaced by an automatic watering system. After adding
the PVC, the aggressive behavior diminished in 3 days and was
unnoticeable in 14 days. In conclusion, when these hamsters were
provided with nesting material their well-being was improved as
indicated by resolution of inappetence and depression. Providing
the PVC apparently resolved the aggressive behavior problem by
providing a means for seclusion in addition to functioning as
a burrow and as a toy."
Morrison P 2001. The rat floor pen: Fact or fantasy? Animal
Technology 52, 33-34
"Aggression between rats is also decreased when they are
housed in pens - no fights have been observed in a year. ... We
feel that the floor pen offers many advantages for the animals
besides increasing job satisfaction for the technicians."
Rabbits
Mis J, Warren F 2003. A novel and cost-effective approach to New
Zealand White Rabbit enrichment. Tech Talk 8(6), 4
"A round children's pool is being used to serve as part
of our enrichment program. .. We started our program by handling
the [group-housed] rabbbits more frequently. . .We also noticed
a dramatic decrease in rabbits showing aggressive behavior. ..
They are a lot easier to handle not only for blood collection,
but also when techniques such as nail clipping and routine exams
are given."
Reduction
of anxiety, fear and excitability
Rodents
Chapillon P, Manneché C, Belzung C, Caston J 1999. Rearing
environmental enrichment in two inbred strains of mice: 1. Effects
on emotional reactivity. Behavior Genetics 29, 41-46
Access to three times larger cages furnished with tunnels and
running wheels reduced anxiety-like behavior.
Engellenner WJ, Goodlett CR, Burright RG, Donovick PJ 1982. Environmental
enrichment and restriction: Effects on reactivity, exploration
and maze learning in mice with septal lesions. Physiology and
Behavior 29, 885-893
Mice from enriched living conditions showed less fear responses
[resistance to capture, handling; vocalization] than mice from
barren standard housing conditions .
Levine S 1985 A definition of stress? In Animal Stress.
Moberg GP (ed), 51-69. Waverly Press, Baltimore, MD
Rats living in a more complex housing environment explored
objects longer and more frequently than rats kept in barren standard
cages, suggesting that enrichment buffers anxiety responses to
potential stressors.
Manosevitz M, Pryor JB 1975. Cage size as a factor in environmental
enrichment. Journal of Comparative and Physiological Psychology
89, 648-654
"Cage size significantly affected 38-day gross body weight,
open-field activity and defecation, running-wheel activity, exploration,
and water consumption. .. Rearing in large cages, either wire
or Plexiglas, appears to reduce emotionality... The results of
this experiment indicate that cage size is one of the important
factors of the enriched-environment-rearing experience."
Meijer MK, Kramer K, Remie R, Spruijt BM, van Zutphen L. F. M.,
Baumans V 2002. Refinement of routine procedures: Can environmental
enrichment reduce the stress response of laboratory mice. Fourth
World Congress on Alternatives and Animal Use in the Life Sciences
- Program and Abstracts , 97 (Abstract)
Female mice housed in trios in enriched cages and handled daily
reacted with less anxiety to procedures than female mice housed
singly in barren cages and handled only when necessary.
Morrison P 2001. The rat floor pen: Fact or fantasy? Animal
Technology 52, 33-34
Rats "in [enriched] floor pens have better body condition
and appear cleaner [than animals housed in cages]. They are also
much more inquisitive and friendly than caged rats and come out
when the technicians do their morning checks, because they appear
less fearful of humans and want to interact with them."
Prior H, Sachser N 1994/95. Effects of enriched housing environment
on the behaviour of young male and female mice in four exploratory
tasks. Journal of Experimental Animal Science 37, 57-68
The provision of plastic boxes and wooden scaffoldings in cages
reduced anxiety in mice, increased their open-field activity and
improved sensorimotor skills.
Rabbits
Hansen LT, Berthelsen H 2000. The effect of environmental enrichment
on the behaviour of caged rabbits (Oryctolagus cuniculus) .
Applied Animal Behaviour Science 68, 163-178
Rabbits kept in conventional single-cages, showed more restlessness,
excessive grooming, bar-gnawing and timidity than rabbits kept
in cages that were provisioned with a platform and a shelter.
Reduction
of stress
Rodents
Chamove AS 1989. Cage design reduces emotionality in mice. Laboratory
Animals 23, 215-219
"The results of this study clearly showed that the presence
of vertical partitions in the cages of mice reduced the stressfulness
of caging and also led to mice which were less reactive when tested
outside their cages. ... When reared in the more complex cages,
the animals gained more weight and were more active."
Foulkes A 2004. Do
laboratory rats benefit from more cage space? AWI Quarterly
53(3), 18-19
"Laboratory rats do not benefit from more cage space, unless
the space is provisioned with proper enrichment such as a PVC
tube. Being confined in a small standard cage is a much more stressful
experience for rats than being confined in a larger cage furnished
with a PVC tube. Access to a PVC tube reduces a rats stress level
in a small cage, but the stress is still much higher than in a
large cage with PVC tube." The animals stress status was
reflected in their food consumption with rats living in barren
cages eating much more food and gaining significantly more weight
than rats living in the enriched cages. Rats kept in the typical,
barren standard cages very often become obese. The present findings
indicate that this problem is related to stressful living conditions,
similarly to obesity in modern people living in stressful environments.
Hennesy MB, Foy T 1987. Non-edible material elicits chewing and
reduces the plasma corticosterone response during novelty exposure
in mice. Behavioral Neuroscience 101, 237-245
If mice were placed in a novel environment with metal foil
or cardboard available, they chewed these materials. These animals
had lower plasma corticosterone levels than mice in the same environment
without access to these chewable items.
Van Loo PLP, Van der Meer E, Kruitwagen CLJJ, Koolhaas JM, Van
Zutphen LFM, Baumans V 2004. Long-term effects of husbandry procedures
on stress-related parameters in male mice of two strains. Laboratory
Animals 38, 169-177
"Long-term provision of nesting material and its transfer
during cage cleaning was found to influence several stress-related
physiological parameters. Mice housed in cages enriched with nesting
material had lower urine corticosterone levels and heavier thymuses,
and they consumed less food and water than standard-housed mice.
.. We conclude that the long-term provision of nesting material,
including the transfer of nesting material during cage cleaning,
reduces stress and thereby enhances the welfare of laboratory
mice."
Reduction
of abnormal behavior
Rodents
Callard MD, Bursten SN, Price EO 2000. Repetitive backflipping
behaviour in captive roof rats (Rattus rattus) and the
effect of cage enrichment. Animal Welfare 9, 139-152
"Repetitive stereotyped behaviours are often performed
by both wild and domestic rodents in small laboratory cages. In
this study, a behaviour resembling a backwards somersault or backflip
is described and quantified in captive roof rats (ship or black
rats, Rattus rattus). ... Cage enrichment in the form of a wooden
nest box resulted in dramatically lower rates of performance.
Increased cage height resulted in delayed development of backflipping,
as well as changes in the form of the behaviour. Results are consistent
with the hypothesis that the development and expression of backflipping
in young roof rats may be triggered by weaning and maintained
by a heightened state of arousal in a relatively impoverished
environment with limited opportunities for perceptual and locomotor
stimulation."
DeLuca AM 1997. Environmental
enrichment: does it reduce barbering in mice? AWIC Newsletter
8(2), 7-8
"In order to alleviate barbering, their environment was
enriched with toys and other objects at two different times. ..
The toys were replaced every other week; at no time was the same
toy used for more than 2 weeks. ... The extent of the barbering
behavior was decreased by the enrichment program. If the environment
was enriched as soon as the mice were gang-caged, barbering was
kept at a minimum that is, only the smallest mice (less than 2
percent of the total number of animals) were barbered. If the
enrichment was delayed for a month or more, barbering occurred
to about 23 percent of the mice. Barbering in control mice (no
enrichment) was about 60 percent."
*Gebhardt-Henrich SG, Vonlanthen. E.M., Steiger
A 2005. How does the running wheel affect the behaviour and reproduction
of golden hamsters kept as pets? Applied Animal Behaviour Science
95, 199-203
"Hamster females with a functional wheel showed significantly
less climbing and stereotypical bar-mouthing than females with
non-functional wheels."
*Hadley C, Hadley B, Ephraima S, Yang
M, Lewis MH 2006. Spontaneous stereotypy and environmental enrichment
in deer mice (Peromyscus maniculatus): Reversibility of
experience. Applied Animal Behaviour Science 97, 312-322
"Enriched housing (24-84 day of age) was associated with
substantially lower levels of stereotypy. Moreover, environmental
enrichment experienced later in development (84-124 days of age)
was as effective as early enrichment. This was not the case, however,
for older animals (11-14 months of age) that experienced the same
duration of enriched housing. The beneficial effects of early
enrichment were found to persist as mice placed in standard cages
following enrichment exhibited lower levels of stereotypy than
controls. These findings support a sensitive period for the amelioration
of abnormal repetitive behavior and suggest a neuroprotective
effect of this form of early experience."
Orok-Edem E, Key D 1994. Responses
of rats (Rattus norvegicus) to enrichment objects. Animal
Technology 45, 25-30
" Two objects, a tongue depressor made of birch wood and
a wooden block constructed of a stainless steel clip and cut broom
handle were each introduced into two groups while the third group
served as control. Aberrant behaviours like fighting and chewing
of metal cage bars were drastically reduced."
Powell SB, Newman HA, McDonald TA, Bugenhagen P, Lewis MH 2000.
Development of spontaneous stereotyped behavior in deer mice:
effects of early and late exposure to a more complex environment.
Developmental Psychobiology 37, 100-108
"We hypothesized that spontaneous stereotypies exhibited
by deer mice housed under standard laboratory conditions were
the result of environmental restriction and that a sensitive period
exists for the development/prevention of stereotypies. Exposure
to a more complex environment early in the post-weaning period
resulted in substantially less stereotypy in the complex environment."
Waiblinger E, König B 2004.
Refinement
of gerbil housing and husbandry in the laboratory. ATLA
(Alternatives to Laboratory Animals) 32(Supplement), 163-169
An artificial burrow system is described that prevents the
development of stereotypic digging.
Waiblinger E 2002. Refinement of gerbil housing and husbandry
in the laboratory. Fourth World Congress on Alternatives and
Animal Use in the Life Sciences - Program and Abstracts ,
101 (Abstract)
"Stereotypic digging was caused by the lack of a burrow
.... stereotypic bar chewing was caused by premature separation
of juveniles from their family before the birth of younger siblings."
Wiedenmayer C 1997. Stereotypies resulting from a deviation in
the ontogenetic development of gerbils. Behavioural Processes
39, 215-221
The provision of an artificial external burrow reduces stereotypic
digging.
Würbel H, Chapman R, Rutland C 1998. Effect of feed and environmental
enrichment on development of stereotypic wire-gnawing in laboratory
mice. Applied Animal Behaviour Science 60, 69-81
Enrichment significantly reduced stereotypic wire-gnawing in
pair-housed male mice by 40%, presumably as a consequence of the
cover provided by the cardboard tubes. This is substantiated by
observations that the tubes were used as a place to retreat upon
disturbance as well as for resting. As a consequence the animals
showed more resting and less grooming in cages containing a cardboard
tube-shelter.
Rabbits
Biczak M, Pellecchia D 2002. Environmental enrichment for rodents
and rabbits. TriBranch Symposium 2002 , unpublished poster
presentation
Provision of various toys and gnawing block resulted in a "significant
reduction, or even elimination of hair loss and bar biting"
in rabbits.
Hansen LT, Berthelsen H 2000. The effect of environmental enrichment
on the behaviour of caged rabbits (Oryctolagus cuniculus) .
Applied Animal Behaviour Science 68, 163-178
Rabbits kept in conventional single-cages, showed more restlessness,
excessive grooming, bar-gnawing and timidity than rabbits kept
in cages that were provisioned with a platform and a shelter.
Krohn TC, Ritskes-Hoitinga J, Svendsen P 1999. The effect of feeding
and housing on the behaviour of the laboratory rabbit. Laboratory
Animals 33, 101-107
"Feeding the animals at 14:00 h [wild rabbits forage primarily
late in the afternoon and during the night!] reduced abnormal
behaviour during the dark period compared to feeding at 08:00
h.
Moore S, Beeston D 1999. Rabbit caging developments at Zeneca.
Animal Technology 50, 157-161
A well structured single-cage - including protruding front,
hay rack and platform - and a floor-pen system are described.
"The incidence of this [persistent tail biting] has been
greatly reduced by introducing more enrichment items to the pens,
but avoiding those that encourage confinement of the animal, i.e.,
long tubes/drainpipes."
Potter MP, Borkowski GL 1998. Apparent psychogenic polydipsia
and secondary polyuria in laboratory-housed New Zealand White
rabbits. Contemporary Topics in Laboratory Animal Science
37, 87-89
Three single-caged rabbits with psychogenic polydipsia [excessive
drinking without apparent physiological reason] were given toys
for cage enrichment, "and the abnormal behavior decreased
in all three cases."
Brain function
Benefield AC, Greenough WT 1998. Effects
of experience and environment on the developing and mature brain:
Implications of laboratory animal housing. ILAR [Institute
for Laboratory Animal Research] Journal 39(1), 5-11
"Immune system function appears to be enhanced in EC (complex
environmental) rats relative to controls housed in standard cages."
Bennett EL, Diamond MC, Krech D, Rosenzweig MR 1964. Chemical
and anatomical plasticity of brain. Science 146, 610-619
"The control animals are kept under colony conditions,
housed three in a cage and exposed to ongoing activity in the
room. ... For enhanced experience, animals were given Environmental
Complexity and Training [groups of 10 to 12 animals in large cages
provided with toys]. ... For the third condition - reduced experience
- animals are caged singly in a dimly lit and quiet room where
they cannot see or touch another animal. ... Our observations
demonstrate that rats given enriched experience develop, in comparison
to restricted littermates, greater weight and thickness of cortical
tissue and an increase in total acetylcholinesterase activity
of the cortex. ... These changes have been produced consistently
in many replications ... they are found in adult as well as young
animals. Control experiments have demonstrated that these changes
cannot be attributed primarily to differential handling or locomotor
activity. ... The demonstration of such changes merely helps to
establish the fact that the brain is responsive to environmental
pressure."
Guilarte TR, Toscano CD, McGlothan JL, Weaver SA 2002. Environmental
enrichment: Beneficial effects in a rodent model of lead neurotoxicity.
Fourth World Congress on Alternatives and Animal Use in the
Life Sciences - Program and Abstracts , 236 (Abstract)
"Using a rodent model of lead-induced neurotoxicity, we
show that environmental enrichment reverses cognitive and molecular
deficits induced by this developmental neurotoxicant. .. At weaning,
pups were removed from the lead exposure and housed in isolation
or environmental enrichment cages (8 per cage). Enrichment cages
were larger and contained toys, mazes, a running wheel, and a
hammock. Rats exposed to lead and reared in an isolated environment
were significantly impaired in acquiring spatial learning task.
On the other hand, lead-exposed rats reared in an enriched environment
perform as well as control enriched rats and better than control
isolated rats. ... Findings suggest that the living environment
is an important modifier on the effect of toxins on the central
nervous system."
Kempermann G, Kuh HG, Gage FH 1997. More hippocampal neurons in
adult mice living in an enriched environment. Nature 386,
493-495
Mice reared in an environment enriched with running wheels,
tunnels and toys possess more hippocampal neurons than litter
mates reared in barren standard cages. It is likely that these
extra neurons contribute to the enhanced performance in learning
tasks showed by enriched versus non-enriched mice.
Morley-Fletcher S, Rea M, Laviola G 2004. Environmental enrichment
during adolescence reverses the effects of prenatal stress on
anxiety-related behaviour and stress in rats. Animal Welfare
13(S), 251 (Abstract)
Environmental enrichment during adolescence reverses the effects
of prenatal stress on anxiety-related behavior.
Tagney J 1973. Sleep patterns related to rearing rats in enriched
and impoverished environments. Brain Research 53, 35-361
Rats housed in enriched versus barren cages show brain changes
indicative of enhanced cerebral activity.
Learning performance
Cooper RM, Zubek JP 1958. Effects of enriched and restricted early
environments on the learning ability of bright and dull rats.
Canadian Journal of Psychology 12, 159-164
"The bright animals reared in enriched environments [group-housing
with numerous enrichment gadgets] showed no improvement in learning
ability over bright controls reared under normal laboratory condition
[group-housing in barren cage]. The dull animals, on the other
hand, benefited greatly from the enriched experience and attained
a level of performance equal to that of the bright animals. Rearing
in restricted environments had converse effects. The dull animals
suffered no impairment as compared with dull controls, while the
bright animals were retarded to the levels of the dulls in learning
performance."
Molina-Hernández M, Téllez-Alcántara NP 2004.
Rats socially-reared and full fed learned an autoshaping task,
showing less levels of fear-like behaviour than fasted or singly-reared
rats. Laboratory Animals 38, 236-245
"During the learning of instrumental tasks, rats are usually
fasted to increase reinforced learning. However, fasting produces
several undesirable side effects. The aim of this study was to
test the hypothesis that control rats, i.e. full-fed and group-reared
rats, will learn an autoshaping task to the same level as fasted
or singly-reared rats. The interaction between fasting and single-rearing
of rats was also tested. Results showed that control rats and
fasted rats acquired the autoshaping task similarly, independently
of rearing or gender. However, fasted or singly-reared rats produced
fear-like behaviour. .. In conclusion, control rats learned the
autoshaping task to the same level as fasted or singly-reared
rats. However, fasting or single-rearing produced fear-like behaviour.
Thus, the training of control rats in autoshaping tasks may be
an option that improves animal welfare."
Patterson-Kane EG, Hunt M, Harper DN 1999. Behavioral indexes
of poor welfare in laboratory rats. Journal of Applied Animal
Welfare Science 2, 97-110
Problem solving ability was improved when rats were kept in
groups in enriched cages rather than in barren single cages.
Immune function
Kingston SG, Hoffman-Goetz L 1996. Effect of environmental enrichment
and housing density on immune system reactivity to acute exercise
stress. Physiology and Behavior 60, 145-150
Keeping mice in enriched cages rather than barren standard
cages seems to enhance immune function. "Environmentally
enriched mice behave immunologically much like nonstressed animals."
Animals in enriched environment showed a less variable, better
regulated immune response.
Wound healing
Coviello-Mclaughlin GM, Starr SJ 1997. Rodent enrichment devices
- evaluation of preference and efficacy. Contemporary Topics
in Laboratory Animal Science 36(6), 66-68
"When animals wearing wound clips were exposed to the
preferred enrichment, premature wound clip removal decreased,
suggesting a positive effect of enrichment on the psychological
well-being of surgically manipulated mice."
Prevention of
obesity
Eskola S, Kaliste-Korhonen E 1998. Effects of cage type and gnawing
blocks on weight gain, organ weights and open-field behaviour
in Wistar rats. Scandinavian Journal of Laboratory Animal Science
25, 180-193
"Rats gnawed blocks about four time more in GFCs [grid
floor cages without bedding] than in SBCs [solid bottom cages
with bedding]. .. The presence of blocks in cages decreased the
weight gain in both cage types."
Van Berkum LE 2000. Use of a feeder insert to reduce obesity in
rats. AALAS [American Association for Laboratory Animal Science]
51st National Meeting Official Program , 125 (Abstract)
"By inserting a modified stainless steel plate into the
feeder, area of exposed food is reduced, and may result in increased
exploratory activity, which may lead to decrease in body weights
and food consumption values (all while continuing to provide ad
libitum access to food). .. Although body weights and food consumption
were not significantly different for weeks 1-9, weeks 10-14 showed
a trend towards lower body weights and food consumption in the
treated groups. .. The study will be continued ."
Wrightson D, Dickson C 1999. Diet restriction through hopper design.
Animal Technology 50, 45-46
Group-housed rats were induced to 'work' for their food by
soldering metal plates over their food hoppers, so that only 3%
of the original area remains available. It was felt that this
method of food restriction was preferable to giving less food
[to avoid obesity]. ... Rather than rapidly eating a reduced ration
and feeling hungry for long periods, the rats worked harder for
their food, which enabled them to burn more calories and eat throughout
the day. This reduces the incidence of obesity and its associated
disorders and also encourages more 'natural' behaviour patterns,
both of which improve welfare."
Social
Enrichment: Refinement
Social buffer: Reduction of anxiety,
fear and stress
Rodents
Conger JJ, Sawrey WL, Turrell ES 1957. An experimental investigation
of the role of social experience in the production of gastric
ulcers in hooded rats. American Psychologist 12, 410 (Abstract)
Rats in a chronic approach-avoidance conflict situation alone
had significantly greater resultant ulceration than animals tested
together.
Davitz JR, Mason DJ 1955. Socially facilitated reduction of a
fear response in rats. Journal of Comparative and Physiological
Psychology 48, 149-151
The presence of a conspecific mediates fear responses to a
stressful situation.
Kaiser S, Kirtzeck M, Hornschuh G, Sachser N 2003. Sex specific
difference in social support - a study in female guinea pigs.
Physiology and Behavior 79, 297-303
"In female guinea pigs social support can be provided
by social partners. In contrast to males, however, not only the
bonding partner is able to reduce the female's stress responses,
but also a familiar conspecific, though in a less effective way."
Latané B 1969. Gregariousness
and fear in laboratory rats. Journal of Experimental Social
Psychology 5, 61-69
In a novel open-field environment rats showed less signs of
fear [number of fecal boluses excreted] when tested in pairs versus
alone.
Latané B, Glass D 1968. Social and nonsocial attraction
in rats. Journal of Personality and Social Psychology 9,
142-146
Single rats show a reduction of fear in a strange environment
when another - though anesthetized - rat is present.
Patterson-Kane EG, Hunt M, Harper DN 1999. Behavioral indexes
of poor welfare in laboratory rats. Journal of Applied Animal
Welfare Science 2, 97-110
Fearfulness associated with single-housing was alleviated by
pair-housing, and even further alleviated by group-housing in
enriched cages. Problem solving ability was improved when rats
were kept in groups in enriched cages rather than in barren single
cages.
Sharp JL, Azar T, Lawson D 2003. Does cage size affect heart rate
and blood pressure of male rats at rest or after procedures that
induce stress-like responses? Contemporary Topics in Laboratory
Animal Science 42(3), 8-12
"Close interaction between group-housed rats appears to
be more important to stress reduction than is providing increased
floor space per animal."
Sharp JL, Zammit TG, Azar TA, Lawson DM 2002. Stress-like responses
to common procedures in male rats housed alone or with other rats.
Contemporary Topics in Laboratory Animal Science 41(4),
8-14
"We concluded that under resting conditions, rats housed
four per cage were less stressed than were rats housed alone,
that common procedures induce noteworthy stress-like responses
in male rats, and that the magnitude and duration of these responses
are reduced by group housing."
Sharp JL, Zammit T, Azar TA, Lawson DM 2003. Stress-like responses
to common procedures in individually and group-housed female rats.
Contemporary Topics in Laboratory Animal Science 42(1),
9-18
"Procedure-induced arousal behaviors occurred in all housing
groups after the acute husbandry and experimental procedures,
but the occurrence of these behaviors was less frequent and of
shorter duration in group-housed rats than rats housed alone.
In light of these results, we conclude that under resting conditions
group housed rats were somewhat less stressed than were rats housed
alone. Further, we conclude that common procedures induce significant
stress-like responses in female rats, and the magnitude and duration
of these responses are reduced by group housing."
Taylor GT 1981. Fear and affiliation in domesticated male rats.
Journal of Comparative and Physiological Psychology 95,
685-693
"Unfamiliar conspecifics were just as effective in allaying
fear as familiar animals. Even the individually reared rats, unused
to other rats, were less fearful with conspecifics than when they
were stressed alone. These findings simply attest to the strength
of the capability of conspecifics to reduce fear."
Group and pair
housing: Alleviation of abnormal behavior
Rabbits
Chu L, Garner JP, Mench JA 2004. A behavioral comparison of New
Zealand White rabbits (Oryctolagus cuniculus) housed individually
or in pairs in conventional laboratory cages. Applied Animal
Behaviour Science 85, 121-139
The beneficial effects of pair housing in decreasing abnormal
behaviors and increasing locomotion suggest that pair housing
should be considered as an alternative to individual housing for
caged laboratory rabbits."
Held SDE, Turner RJ, Wootton RJ 2001. The behavioural repertoire
of non-breeding group-housed female laboratory rabbits (Oryctolagus
cuniculus). Animal Welfare 10, 437-443
"Trichophagy and stereotypic behaviors observed in singly
caged rabbits were not observed in group-housed does."
Krohn TC, Ritskes-Hoitinga J, Svendsen P 1999. The effect of feeding
and housing on the behaviour of the laboratory rabbit. Laboratory
Animals 33, 101-107
"While the [individually housed] rabbits in cages spent
2-5% of the time performing abnormal behaviour like biting the
bars or scratching the bottom of the cage, these activities were
virtually absent in group-housed rabbits in floor pens."
Lehmann M 1987 Interference of a restricted environment - as found
in battery cages - with normal behaviour of young fattening rabbits.
In Rabbit Production Systems Including Welfare. Auxilia
T (ed), 257-268. Official Publications of the European Communities,
Luxembourg, Belgium
Single-caged rabbits were not able to hop in rabbit-typical
fashion; they were less active but more restless [frequent activity
changes] and showed more stereotypical gnawing of the wire cages
than group-housed animals.
Metz JHM 1987 Behavioural problems of rabbits in cages. In Rabbit
Production Systems Including Welfare. Auxilia T (ed), 221-230.
Official Publications of the European Communities, Luxembourg,
Belgium
Group-housed rabbits interacted with hay 11% of the 24-h day.
Single-caged rabbits appeared to be more restless and showed more
self-directed behavior than group-housed rabbits.
Training
to Cooperate: Refinement: Reduction of Stress
Rodents
Huang-Brown KM, Guhad FA 2002. Chocolate, an effective means of
oral drug delivery in rats. Lab Animal 31(10), 34-36
"We trained the animals to smell the chocolate and develop
a taste for it by holding the animal and placing the chocolate
into its mouth using a blunt metal applicator (in our project
we used a 14-gauge oral gavage needle). No esophageal contact,
nor any placement more proximal than the oral cavity was necessary.
We handled the rats gently to avoid association of chocolate with
averse stimuli. To train the rats to expect the treatment, we
opened and closed the cage before chocolate administration. ..
After individual administration and return of the animal to the
cage, the caregiver then offered drug-free chocolate as a "reward"
at the front of the cage with the blunt end of the gavage needle
to condition the animals to this manner of treatment. ...Results
from this technique demonstrated appropriate levels of drug absorption.
.. The animals do not require individual housing, enhancing their
social environment and reducing space usage. .. Housing the animals
used for this study in groups of three per cage allowed for easy
identification of animals as they received their chocolate pellets.
...The chocolate vehicle is ideal for timed delivery or when a
drug needs to be administered at a certain time of day. .. In
this study, 3 of 57 rats (5%) failed to become accustomed to the
chocolate even after the training period and had to be restrained
for drug administration."
Shyu WC, Nightingale CH, Tsuji A, Quintiliani R 1987. Effect of
stress on pharmacokinetics of amikacin and ticarcillin. Journal
of Pharmaceutical Sciences 76, 265-266
Aberrant serum ticarcillin concentrations were measured when
the "animals were simply picked out, put on a laboratory
bench, and wrapped in a towel to restrain them" for blood
collection. No aberration occurred in quasi trained rats who were
"handled daily for 3-4 d prior to study and then held and
petted by the investigator throughout the experimental period.
No towel was needed to restrain these rats." In the amikacin
group, 'trained' rats showed a much slower absorption process
compared with conventionally handled rats. Alterations in renal
flow due to the stress resulting from the traditional handling
procedure may have affected pharmacokinetics.
Rabbits
Marr JM, Gnam EC, Calhoun J, Mader JT 1993. A non-stressful alternative
to gastric gavage for oral administration of antibiotics in rabbits.
Lab Animal 22(2), 47-49
"Generally, rabbits receive oral medication by gastric
intubation, a method that frequently requires more than one technician,
is time consuming, and places unnecessary stress on the animal."
A very simple but effective training technique is described which
ensures that rabbits voluntarily cooperate during oral drug administration.
"We coated the tip of the syringe with sucrose sample. Inserting
the syringe through the bars of the cage, we placed it in the
animal's mouth and injected the sucrose solution slowly to allow
the rabbit to taste and drink the fluid. We repeated the procedure
three times a day for a total of 15 minutes per session, and within
two days, 80% of the [10] animals voluntarily swallowed the fluid
from the syringe. The [2] rabbits that did not seek out the syringe
usually took it with only minimal encouragement. At the onset
of the therapy, we substituted the antibiotic for the sucrose
solution. .... We continued coating the tip of the syringe with
sucrose granules throughout the therapy, apparently masking any
unpleasant sensations produced by the antibiotic." Eight
of the ten rabbits cooperated within two days. They "would
stand with their paws on the front of the cages, protrude their
faces from between the bars, and appear to beg for the syringe
containing the antibiotic. " This non-stress method of "giving
tosufloxacin was successful in producing the desired serum and
bone concentrations."
Variables
Single Housing, Solitary
Confinement, Barren Cage & Understimulation
Rodents
Baenninger LP 1967. Comparison of behavioural development in socially
isolated and grouped rats. Animal Behaviour 15, 312-323
Single-housed males showed reduced activity and a greater incidence
of stereotypical tail manipulation [substitute social response?]
and pawing with hind legs than males housed in groups.
Baer H 1971. Long-term isolation stress and its effects on drug
response in rodents. Laboratory Animal Science 21, 341-349
"This review of the literature has illustrated that isolation
stress, especially long-term isolation stress in rats and mice,
can affect the growth, behavior, physiological condition, and
response to a wide variety of drugs. ... Isolation stress in mice
produces abnormal behavior (such as aggressiveness, excitability,
and nervousness); changes in body weight; and organ weights; blood
changes (leukopenia, eosinopenia); and frequently increased adrenal
function over that of community housed mice."
Cambardella P, Greco AM, Sticchi R, Bellotti R, Di Renzo G 1994.
Individual housing modulates daily rhythms of hypothalamic catecholaminergic
system and circulating hormones in adult male rats. Chronobiology
International 11, 213-221
Male rats housed individually had higher levels of corticosterone
and prolactin than did those housed six per cage.
Chance MRA 1956. Environmental factors influencing gonadotrophin
assay in the rat. Nature 177, 228-229
The variation in ovary weight (test response) was greater if
the cages were small, if there was frequent disturbance by changing
cages and cage-mates, and if the rats were caged either singly
or in groups larger than two, with the floor area per rat roughly
constant.
Fiala B, Snow FM, Greenough WT 1977. Impoverished rats weigh more
than enriched rats because they eat more. Developmental Psychobiology
10, 537-541
Rats housed in barren environments consume more food due to
boredom and are heavier than enriched rats.
Heath M 1999. Preliminary behaviour data for single and pair housed
rats. Animal Technology 50, 47-48
"Singly housed rats spent most of the time in the back
of the cage, while pairs spent most time by the food hoppers.
This may have been exacerbated by the presence of humans, as pair
housed rats were more confident overall. Activity patterns were
very different between singly and pair housed rats, in term of
both the total time spent doing different things and the time
when specific activities occurred. In particular, single rats
spent far less time playing than pair housed rats."
Hockly E, Cordery PM, Woodman B, Mahal. A, van Dellen. A, Blakemore
C, Lewis CM, Hannan AJ, Bates GP 2002. Enrichment slows disease
progression in R6/2 Huntington's disease mice. Annals of Neurology
51, 235-242
Housing mice in standard laboratory cages increased the rate
of disease progression while housing them in enriched cages slowed
the progress to a more 'normal' rate. "Mice housed in such
deprived conditions are unlikely to prove a good model of disease,
and the effects of enrichment represent a partial reversal of
the deleterious effects of relative environmental impoverishment."
Hurst JL, Barnard CJ, Nevison CM, West CD 1997. Housing and welfare
in laboratory rats: Welfare implications of isolation and social
contact among caged males. Animal Welfare 6, 327-347
Singly housed males showed reduced activity and a greater incidence
of self-directed behaviors, especially tail manipulation and self-grooming
than males housed in small groups of three. They also performed
"behaviors apparently related to escape or seeking social
information.
Kaliste-Korhonen E, Eskola S, Rekilä T, Nevalainen T 1995.
Effects of gnawing material, group size and cage level in rack
on Wistar rats. Scandinavian Journal of Laboratory Animal Science
22, 291-299
"In open field, the animals living alone were less active
and they moved slower from the peripheral to central area than
the animals living in groups The singly housed rats showed in
general more variation in behavioural measures than the animals
with cage mates."
Mackintosh JH 1962. Effect of strain and group size on the response
of mice to "sconal" anaesthesia. Nature 194,
1304
The variance of the response to a barbiturate anaesthetic was
greater if male mice were caged either singly or in groups of
eight than if they were caged in pairs.
*Meijer MK, Kramer K, Remie R, Spruijt BM, van
Zutphen LFM, Baumans V 2006. The effect of routine experimental
procedures on physiological paramters in mice kept under different
husbandry conditions. Animal Welfare 15, 31-38
Single-housing in a non-enriched environment significantly
elevated heart rate and blood pressure and recovery time following
routine experimental procedures relative to social-housing in
an enriched environment.
Pérez C, Canal JR, Dominguez
E, Campillo JE, Guillén M 1997. Individual housing influences
certain biochemical parameters in the rat. Laboratory Animals
31, 357-361
Individual as opposed to group-housing of female rats provoked
variations in certain biochemical parameters [glucose, triglycerides,
food intake]. It was concluded that this circumstance could make
scientific data unreliable or even dubious.
Shaw DC, Gallagher RH 1984 Group or singly housed rats? In Standards
in Laboratory Animal Management. The Universities Federation
for Animal Welfare 65-70. The Universities Federation for Animal
Welfare, Potters Bar, UK
"In both sexes singly housed animals showed a markedly
lower survival rate than group-housed animals. This effect became
apparent when the animals reached the age of about 80 weeks. No
specific cause could be identified."
Sherwin CM, Olsson IAS 2004. Housing conditions affect self-administration
of anxiolytic by laboratory mice. Animal Welfare 13, 33-38
"Standard cages for laboratory rodents may induce greater
anxiety than enriched cages."
Späni D, Arras M, König B, Rülicke T 2003. Higher
heart rate of laboratory mice housed individually vs in pairs.
Laboratory Animals 37, 54-62
"Many studies have shown that housing mice individually
over a long period significantly alters their physiology, but
in most cases measurement has required human interference and
restraint for sampling. Using a radio-telemetry system with implantable
transmitters, we recorded heart rate (HR), motor activity (ACT)
and body temperature (BT) of freely moving male mice (NMRI) housed
either individually or in pairs with an ovarectomized female.
.. Even after several weeks of habituation to the social conditions,
HR was increased in mice housed individually compared with mice
housed in pairs, although their measured ACT did not differ. ..
Furthermore, individually-housed mice had more, but shorter, resting
bouts, indicating disruption of the normal circadian sleep pattern.
Enhanced HR in individually-housed mice does not necessarily indicate
stress, but might be an important physiological indicator of discomfort.
The fact that individual housing alters basic physiological parameters
in laboratory mice highlights the need to control for housing-dependent
variation, especially in experiments that are sensitive to changes
in these parameters."
Valzelli L 1973. The "isolation syndrome" in mice. Psychopharmacologia
31, 3055-320
Socially isolated mice differ from group-housed mice not only
behaviorally, but also in their immunological responses, hormone
levels, brain neurochemistry, learning ability, pain thresholds,
and sensitivity to drugs.
Rabbits
Bigler L,Lehmann M 1991 Schlußbericht über die Prüfung
der Tiergerechtheit eines Festwandkäfigs für Hauskaninchen-Zibben.
Bern, Switzerland: Bundesamt für Veterinärwesen
Single-housed young rabbits revealed inactivity atrophies as
a result of modified behaviors and lack of exercise in small,
conventional cages. The provision of functional areas (e.g., elevated
shelf and dark area for withdrawal) can reduce the incidence of
behavioral disorders.
Gunn D, Morton DB 1995. Inventory of the behaviour of New Zealand
white rabbits in laboratory cages. Applied Animal Behaviour
Science 45, 277-292
Detailed ethogram of singly caged rabbits. "The level
of mobility (1.2%) reflected their inability to hop normally and,
in addition, they were unable to sit up, rear fully or stretch
out because of spatial restriction. All rabbits showed stereotyped
activities (11%). .... Any gregarious animal chronically housed
in isolation should be considered abnormal."
Lehmann M 1984 Beurteilung der Tiergerechtheit handelsüblicher
Batteriekäfige für Mastkaninchen. Bern, Switzerland:
Bundesamt für Veterinärwesen (Bericht)
Single-housed young rabbits revealed inactivity atrophies and
poor bone growth as a result of modified behaviors and lack of
exercise in small, conventional cages.
Loeffler K, Drescher B, Schulze G 1991. Einfluß unterschiedlicher
Haltungsverfahren auf das Verhalten von Versuchs- und Fleischkaninchen
[German text with English abstract]. Tierärztliche Umschau
46, 471-478
Rabbits kept individually in conventional wire-floored cages
showed species-atypical patterns of locomotion and resting, and
behavioral disorders which were absent in group-housed animals
kept in floor pens. "The findings confirm that housing rabbits
in cages is not to be recommended."
Wagner JL, Hackel DB, Samsell AG 1974. Spontaneous death in rabbits
resulting from gastric trichobezoars. Laboratory Animal Science
24, 826-830
"Hairball formation in humans occurs most frequently in
emotionally disturbed females below the age of 30. It is possible
that individual caging of rabbits over long periods of time could
affect their psychological health and bring about abnormal grooming
habits, thus contributing to hairball formation."
Stress
From Laboratory Procedures:
(Restraint & handling,
blood collection, injection, etc.)
Balcombe JP, Barnard ND, Sandusky C 2004. Laboratory routines
cause animal stress. Contemporary Topics in Laboratory Animal
Science 43(6), 42-51
Based on a literature review the conclusion was drawn that
"routine handling, venipuncture, and orogastic gavage lead
to elevations of heart rate, blood pressure, and glucocorticoid
concentrations that persist for 30 to 60 min or more following
the event, suggesting that despite their routine use in laboratory
studies, these procedures are acutely stressful for animals."
Barrett AM, Stockham MA 1996. The effect of housing conditions
and simple experimental procedures upon corticosterone level in
the plasma of rats. Journal of Endocrinology 26, 97-105
Routine procedures such as handling and weighing and i.p. injections
of saline induce significant increases in plasma corticosterone
concentrations wihich remain supernormal for at least 2 hr.
Berkey DL, Meeuwsen KW, Barney CC 1990. Measurements of core temperature
in spontaneously hypertensive rats by radiotelemetry. American
Journal of Physiology 258, R743-749
Handling and restraint can cause significant increases in core
temperature.
Besch EL, Chou BJ 1971. Physiological responses to blood collection
methods in rats. Proceedings of the Society for Experimental
Biology and Medicine 138, 1019-1021
Plasma glucose levels are related to the length of handling
time during blood collection.
*Bolam S 2005. Multiple housing of male CD-1 mice
for toxicological studies. Animal Technology and Welfare
4, 86-87
"Aggression peaked around 10 weeks into the [10 months]
study and was usually observed following dosing or cage cleaning,
ceasing once human activities in the room were completed."
*Bonnichsen M, Dragsted N, Hansen AK
2005. The welfare impact of gavaging laboratory rats. Animal
Welfare 14, 223-227
A significant correlation between heart rate and dosage was
observed until 10 min after gavaging.
Briese E, Cabanac M 1991. Stress
hyperthermia: Physiological arguments that it is fever. Physiology
and Behavior 49, 1153-1157
Manual restraint increases body temperature in rats.
Guhad FA, Nevalainen T, Lang CM 2003. Fecal corticosterone: A
noninvasive method of stress assessment in rats. AALAS [American
Association for Laboratory Animal Science] 54th National Meeting
Official Program , 93-94 (Abstract)
"Repeated mild restraint with bare hands or confinement
in a plexiglas tube also increased fecal coritcosterone levels
(p<0.05). Control animals, which only witnessed others being
restrained, also showed a significant increase in fecal corticosterone
levels (p<0.05)."
Kramer K, van de Weerd H, Mulder A, Van Heijningen C, Bauman V,
Remie R, Voss H-P, Van Zutphen BFM 2004. Effect
of conditioning on the increase of heart rate and body temperature
provoked by handling in the mouse. ATLA (Alternatives to
Laboratory Animals) 32(Supplement), 177-181
"Entering the animal room by the technician, without performing
the handling and/or the acoustic stimulus increased HR significantly.
. .. Handling further increased the HR. .. After repeatedly entering
the animal room at a fixed time point (2:30pm), HR was significantly
reduced after 12 days... After 2 weeks, the animals seem to habituate
to this type of disturbance, with the exception of the first entrance
in the morning (9:30am). Disturbance at this time point may cause
more stress than later on."
Krulich L, Hefco E, Illner P, Read CB 1974. The effects of acute
stress on the secretion of LH, FSH, prolactin and growth hormone
in the normal male rat, with comments on their statistical evaluation.
Neuroendocrinology 16, 291-311
Restraint stress is associated with a significant rise in plasma
prolactin and LH levels.
*Mikkelsen LF, Dragsted N, Hansen AK, Ottesen JL
2005. The effect of training for long term restraining of rats
evaluated by telemtry. ALTEX [Alternatives to Animal Experimentation]
22, 53 (Abstract)
Cardiovsacular stress responses were significant on all ten
days of 3-hour tube restraint periods.
Moynihan J, Brenner G, Koota
D, Breneman S, Cohen N, Ader R 1990. The effects of handling on
antibody production, mitogen responses, spleen number, and lymphocyte
subpopulations. Life Sciences 46, 1937-1944
The immune response was depressed when mice were picked up
by the tail and held gently in the palm without restraint. "From
the methodological point of view, handling of experimental animals
may be a significant uncontrolled factor in many in vivo experiments."
Pitman DL, Ottenweller JE, Natelson BH 1988. Plasma corticosterone
levels during repeated presentation of two intensities of restraint
stress: Chronic stress and habituation. Physiology and Behavior
43, 47-55
Corticosterone levels of control rats increased when the animals
witnessed stress reactions of conspecifics during forced restraint.
*Sharp J, Azar T, Lawson D 2005. Selective adaptation
of male rats to repeated social encounters and experimental manipulations.
Contemporary Topics in Laboratory Animal Science 44(2),
:28-31
"We concluded that male Sprague-Dawley rats adapted quickly,
albeit partially, to social encounters but did not adapt to repeated
injections, suggesting selective adaptation depending on the type
of stimulus used."
Tabata H, Kitamura T, Nagamatsu
N 1998. Comparison of effects of restraint, cage transportation,
anaesthesia and repeated bleeding on plasma glucose levels between
mice and rats. Laboratory Animals 32, 143-148
"Mice showed a fairly consistent rise in levels of blood
glucose if unaccustomed to [blood collection procedure] handling
or if the cages were transported to an adjacent room." The
same procedures when performed in rats "seemed to have small
or no observable effect on levels of plasma glucose."
Tuli J, Smith JA, Morton DB 1995. Corticosterone, adrenal and
spleen weight in mice after tail bleeding, and its effect on nearby
animals. Laboratory Animals 29, 90-95
Subjects did not habituate to the stress associated with blood
collection [tail bleeding].
Stress
from Husbandry Routine
Cage cleaning
Conn CA, Borer KT, Kluger MJ 1990. Body temperature rhythm and
response to pyrogen in exercising and sedentary hamsters. Medicine
and Science in Sports and Exercise 22, 636-642
Findings show that the cleaning of cages is one of the strongest
stressors in husbandry routine for hamsters.
Duke JL, Zammit TG, Lawson DM 2001. The effects of routine cage-changing
on cardiovascular and behavioral parameters in male Sprague-Dawley
rats. Contemporary Topics in Laboratory Animal Science
40(1), 17-20
"Half of the rats were moved to clean cages with fresh
wood-chip bedding; the other animals were left undisturbed. Systolic,
diastolic, and mean arterial blood pressures; heart rate; and
cage behavior (movement, rearing, grooming) increased promptly
and significantly when animals were placed in clean cages. These
cardiovascular and behavioral responses lasted for 45 to 60 min.
Those animals not moved to clean cages but present in the animal
room when this procedure was done did not show significant increases
in blood pressure, heart rate, or activity. When rats were moved
to clean cages that contained new bedding plus a small quantity
of the soiled bedding from their previous cage, the cardiovascular
and behavioral responses were similar to those of animals exposed
to completely fresh bedding. ... We conclude that ordinary animal
husbandry procedures such as moving rats to a clean cage can induce
transient, but significant, cardiovascular and behavioral changes.
Investigators and animal care staff should recognize that such
routine procedures could confound experiments conducted shortly
thereafter."
Gray S, Hurst JL 1995. The effects of cage cleaning on aggression
within groups of male laboratory mice. Animal Behaviour
49, 821-816
Dominant animals tend to be more aggressive in an environment
with familiar odor than in a strange environment. It was shown
that complete cage cleaning - new cage and new substrate - can
minimize aggression among male mice as compared with partial cage
cleaning.
Kuhnen G 1999. The effect of cage size and enrichment on core
temperature and febrile response of the golden hamster. Laboratory
Animals 33, 221-227
"Cleaning of cage "caused results similar to chronic
housing in small cages." For the comparison and assessment
of results, the description of the housing conditions seems to
be as essential as the description of the experimental procedure."
Saibaba P, Sales GD, Stodulski G, Hau J 1996. Behaviour of rats
in their home cages: daytime variations and effects of routine
husbandry procedures analysed by time sampling techniques. Laboratory
Animals 30, 13-31
"The cleaning regime [cages cleaned out and fresh sawdust
with shredded paper provided] appeared to have a greater effect
on behaviour [increased defecation and activity] than did time
of day and the effects of cleaning lasted for several hours after
the procedure had been completed.".
Sharp JL, Zammit T, Azar TA 2003. Are "by-stander" female
Sprague-Dawley rats affected by experimental procedures? Contemporary
Topics in Laboratory Animal Science 42(1), 19-28
Witnessing a routine cage change induced significant increases
in HR in rats which were equal to or greater than those induced
by witnessing decapitations.
Van Loo PLP, Kruitwagen CLJJ, Van Zutphen LFM 2000. Modulation
of aggression in male mice: Influence of cage cleaning regime
and scent marks. Animal Welfare 9, 281-295
"Group housing of male laboratory mice often leads to
welfare problems due to aggressive behaviour. ... Aggression peaks
after disturbances such as cage cleaning .. Our results indicated
that neither kinship nor distribution of urine marks affected
aggression. Olfactory cues from nesting and bedding material,
however, affected aggression to a marked degree: transfer of nesting
material reduced aggression significantly, while transfer of sawdust
containing urine and faeces seemed to intensify aggression. ...
We conclude that the transfer of nesting material will reduce
aggression, or at least slow down its development, and thus aid
the reduction of social tension due to cage cleaning."
Transfer
to unfamiliar environment, transportation
Damon EG, Eidson AF, Hobbs CH, Hahn FF 1986. Effect of acclimation
to caging on nephrotoxic response of rats to uranium. Laboratory
Animal Science 36, 24-27
It took rats a minimum of 3 to 5 days to behaviorally adjust
[feeding/drinking] to being transferred to a different cage type.
Drozdowicz CK, Bowman TA, Webb ML, Lang CM 1990. Effect of in-house
transport on murine plasma corticosterone concentration and blood
lymphocyte population. American Journal of Veterinary Research
51, 1841-1846
"A significant increase in plasma corticosterone concentration
was seen in mice immediately after [in-house] transport. The normal
circadian rhythm of plasma corticosterone concentration was altered
for the subsequent 24-hour period. .. The .. acute increase in
plasma corticosterone concentration was associated with alterations
in the cellular components of the immune system. Result of the
study indicated that routine in-house transport of laboratory
mice should be considered a stressful stimulus. .. Therefore,
in-house transport of laboratory animals should be viewed as an
experimental variable to be controlled by the investigator."
Duke JL, Zammit TG, Lawson DM 2001. The effects of routine cage-changing
on cardiovascular and behavioral parameters in male Sprague-Dawley
rats. Contemporary Topics in Laboratory Animal Science
40(1), 17-20
"Systolic, diastolic, and mean arterial blood pressures;
heart rate; and cage behavior (movement, rearing, grooming) increased
promptly and significantly when animals were placed in clean cages.
These cardiovascular and behavioral responses lasted for 45 to
60 min."
Euker JS, Meites J, Riegle GD 1975. Effects of acute stress on
serum LH and prolactin in intact, castrate and dexamethasone-treated
male rats. Endocrinology 96, 85-92
Placing rats into transfer boxes and moving them to another
room triggers a significant rise in plasma prolactin and LH.
Fenske M 1992. Body weight and water intake of guinea pigs: influence
of single caging and an unfamiliar new room. Journal of Experimental
Animal Science 35, 71-79
"No changes in body weight are observed if adult male
guinea pigs are removed from their groups and kept singly in their
home enclosure. In contrast, subjects markedly lose weight and
show a marked reduction of water intake if isolated from their
groups and caged singly in an unfamiliar test room."
Friedman SB, Ader R 1967. Adrenocortical response to novelty and
noxious stimulation. Neuroendocrinology 2, 209-212
It was found in rats that the magnitude of the stress response
to being transferred into an experimental cage is virtually the
same as that produced by electrical shock. ... Exposure to a new
environment, or novelty, may contribute significantly to the adrenocortical
response often attributed to the effects of noxious or painful
stimulation."
Gärtner K, Büttner D, Döhler R, Friedel J, Lindema
J, Trautschold I 1980. Stress response of rats to handling and
experimental procedures. Laboratory Animals 14, 267-274
Serum corticosterone levels increased significantly within
four minutes, reached a peak at 15 minutes and were back to control
values 60 minutes after cage displacement. Prolactin, TSH, LH
and FSH serum concentrations were also affected by cage movement.
"The results support the conclusion that rats are not disturbed
by the presence of people with whom they are familiar, such as
the usual animal attendant for that room, if they do not touch
the cage."
Landi MS, Kreider JW, Lang CM 1982. Effects of shipping on the
immune function in mice. American Journal of Veterinary Research
43, 1654-1657
Mice need at least 48 h after transportation by truck or aeroplane
to recover in terms of corticosteroid levels.
Sharp JL, Azar TA, Lawson DM 2003. Selective adaptation of male
rats to repeated social and experimental stimuli. AALAS [American
Association for Laboratory Animal Science] 54th National Meeting
Official Program, 126-127 (Abstract)
Persistently elevated blood pressure suggested that rats do
not adapt to being transferred to another room. This observation
"is similar to the blood pressure changes observed in conditioned
fear responses."
Tabata H, Kitamura T, Nagamatsu N 1998. Comparison of effects
of restraint, cage transportation, anaesthesia and repeated bleeding
on plasma glucose levels between mice and rats. Laboratory
Animals 32, 143-148
"Mice showed a fairly consistent rise in levels of blood
glucose if unaccustomed to [blood collection procedure] handling
or if the cages were transported to an adjacent room." The
same procedures when performed in rats "seemed to have small
or no observable effect on levels of plasma glucose."
Tuli J, Smith JA, Morton DB 1995b. Stress measurements in mice
after transportation. Laboratory Animals 29, 132-138
Subjects showed stress responses [cortisol, behavior] to being
moved in the familiar home cage from one room to another.
Ursin H, Murison R 1986. Facts, fiction and rational decisions.
Acta Physiologica Scandinavica 554(Supplement 1), 234-242
Rats showed a significant increase in plasma glucocorticosteroids
after being moved by lift from one room to another, even though
they remained in their home cages.
York JL, Regan SG 1982. Conditioned and unconditioned influences
on body temperature and ethanol hypothermia in laboratory rats.
Pharmacology, Biochemistry and Behavior 17, 119-124
An increase in body temperature occurred in animals whose individual
cages were removed from their usual position. After one hour at
the new location body temperature had increased 1.3ºC. Movement
of an entire cage rack, with the cages remaining in their usual
shelf position, caused only a relatively small elevation in body
temperature (about 0.3ºC) after one hour.
Young LA, Pavlovska-Teglia G, Stodulski G, Hau J 1996. Effect
of group housing and oral corticosterone administration on weight
gain and locomotor development in neonatal rats. Animal Welfare
5, 167-176
"The stress response of rats induced by transfer from
communal housing to single housing prior to parturition has a
negative influence of the offspring. This is manifested by slower
growth rate and a retardation in locomotor development."
Light
Bellhorn RW 1980. Lighting in the animal environment. Laboratory
Animal Science 30, 440-450
"What we basically have done to date is to provide lighting
suitable to our needs and assumed it was all right for the animal."
Light intensities in stacked cages vary substantially.
Clough G 1982. Environmental effects on animals used in biomedical
research. Biological Reviews 57, 487-523
"The intensity of light in animal cages is likely to be
the most variable environmental factor in the average animal room."
Clough G, Donnelly HT 1983 Light intensity influences the oestrous
cycle of LACA mice. In Standards in Laboratory Animal Management.
The Universities Federation for Animal Welfare (ed), 60. The Universities
Federation for Animal Welfare, Potters Bar, UK
The variation in light intensities in the center of multi-tier,
translucent rodent cages can exceed an 8-fold difference at bottom
rows from top rows.
Ross S, Nagy ZM, Kessler C, Scott JP 1966. Effects of illumination
on wall-leaving behavior and activity in three inbred mouse strains.
Journal of Comparative and Physiological Psychology 62,
338-340
"The results clearly indicated that illumination levels
is an important variable affecting the general activity of mice."
The animals showed less "fearfulness" and "emotionality"
under low illumination conditions.
Weihe WH, Schidlow J, Strittmatter J 1969. The effect of light
intensity on the breeding and development of rats and golden hamsters.
International Journal of Biometeorology 13, 69-79
"It was noticed that animals subjected to an illumination
of 2000 lux were tame and playful with handling, while those at
lower light intensities resisted handling and tried to bite when
vaginal smear was taken. ... The weight of some important organs,
such as adrenals and testes, and also the breeding performance,
showed a significant relationship to light intensity which was
not seen in the hamster. ... For practical purposes it can be
inferred, that, to obtain uniform results, rooms for rat breeding
need to be more equally illuminated. ... The different light intensities
from 1 to 5,000 lx, that we have found in animal rooms, may have
some effect on the responses of animals to experimental procedures."
Various
Exposure to stressed conspecific
Beynen AC 1992. Communication between rats of experiment-induced
stress and its impact on experimental results. Animal Welfare
1, 153-159
Stressful experimental procedures can give rise to signals
or odours that affect non-treated animals present in the same
or adjacent room.
De Laat JMT, Van Tintelen G, Beynen AC 1989. Transportation of
rats affects behavior on non-transported rats in the absence of
physical contact. Zeitschrift für Versuchstierkunde
32, 235-237
Exposure [visual, auditory and olfactory] to stressed conspecifics
was accompanied by an increase in cortisol levels.
Fuchs E, Fluegge G, Hutzelmeyer HD 1987. Response of rats to the
presence of stressed conspecifics as a function of day time. Hormones
and Behavior 21, 245-252
Corticosterone levels of non-handled rats increase when the
animals witness stress reactions of conspecifics during forced
restraint.
Guhad FA, Nevalainen T, Lang CM 2003. Fecal corticosterone: A
noninvasive method of stress assessment in rats. AALAS [American
Association for Laboratory Animal Science] 54th National Meeting
Official Program , 93-94 (Abstract)
"Repeated mild restraint with bare hands or confinement
in a plexiglas tube also increased fecal coritcosterone levels
(p<0.05). Control animals, which only witnessed others being
restrained, also showed a significant increase in fecal corticosterone
levels (p<0.05)."
Iimori K, Tanka M, Kohno Y 1982. Psychological stress enhances
noradrenaline turnover in specific brain regions in rats. Pharmacology
Biochemistry and Behavior 16, 637-640
Exposure [visual, auditory and olfactory] to stressed conspecifics
was accompanied by an increase in cortisol levels.
Mackay-Sim A, Laing DG 1980. Discrimination of odours from stressed
rats by non-stressed rats. Physiology and Behavior 24,
699-704
Placing a rat into a new cage triggers release of corticosterones.
This endocrine response is augmented if the new environment is
one in which other rats had previously been subjected to stress.
Pitman DL, Ottenweller JE, Natelson BH 1988. Plasma corticosterone
levels during repeated presentation of two intensities of restraint
stress: Chronic stress and habituation. Physiology and Behavior
43, 47-55
Corticosterone levels of control rats increased when the animals
witnessed stress reactions of conspecifics during forced restraint.
Sharp JL, Zammit TG, Lawson DM 2002. Stress-like responses to
common procedures in rats: Effect of the estrous cycle. Contemporary
Topics in Laboratory Animal Science 41(4), 15-22
"We conclude that cycling female rats show stress-like
effects when they are subjected to or witness common husbandry
and experimental procedures, but there is little to no effect
of the estrous cycle."
Separation from
companion
Ehlers CL, Kaneko WM, Owens MJ, Nemeroff CB 1993. Effects of gender
and social isolation on electroencephalogram and neuroendocrine
parameters in rats. Biological Psychiatry 33, 358-366
Separation resulted in significant sleep disturbances - as
measured in EEG responses - and increase in HPA activity.
Lawson DM, Churchill PC 2000. The effects of enrichment on parameters
in hypertensive rats . Contemporary Topics in Laboratory Animal
Science 39(1), 9-13
"Separation from a cage mate clearly induced the greatest
activation, causing sustained increases in systolic and diastolic
pressure and heart rate."
Cage level &
multi-tier system
Ader DN, Johnson SB, Huang SW, Riley WJ 1991. Group-size, cage
shelf level, and emotionality in nonobese diabetic mice - Impact
on onset and incidence of IDDM. Psychosomatic Medicine
53(3), 313-321
'Emotionality' or 'fearfulness' is higher in mice housed in
steel cages at the top of the rack.
Kaliste-Korhonen E, Eskola S, Rekilä T, Nevalainen T 1995.
Effects of gnawing material, group size and cage level in rack
on Wistar rats. Scandinavian Journal of Laboratory Animal Science
22, 291-299
The animals living on the highest shelf of the rack differed
from the others in their latency times of rearing and grooming."
Noise
Anthony A, Ackerman E, Lloyd JA 1959. Noise stress in laboratory
rodents. I. Behavioral and endocrine response of mice, rats and
guinea pigs. Journal of the Acoustical Society of America
31, 1430-1436
Noise affects the endocrine system.
Anthony A, Harclerode JE 1959. Noise stress in laboratory rodents.
II: Effects of chronic noise exposure on sexual performance and
reproductive function of guinea pigs. Journal of the Acoustical
Society of America 31, 1437-1440 Chronic noise impacts
reproductive performance in guinea pigs.
Barrett AM, Stockham MA 1996. The effect of housing conditions
and simple experimental procedures upon corticosterone level in
the plasma of rats. Journal of Endocrinology 26, 97-105
Deliberate exposure to noise resulted in a highly significant
increase in the plasma corticosterone level of rats housed in
groups of 20.
Color of cage
Sherwin CM, Glen EF 2003. Cage colour preferences and effects
of home cage colour on anxiety in laboratory mice. Animal Behaviour
66, 1085-1092
'Home cage colour had a significant effect on body weight and
food consumption as well as on behaviour in a raised plus maze."
Observer effect
Döhler KD, Gärtner K, Mühlen AV, Döhler U
1977. Activation of anterior pituitary, thyroid and adrenal glands
in rats after disturbance stress. Acta Endocrinologica
86, 489-497
Cortisol levels increased within 5 minutes after the entry
of an investigator and reached peak levels after 15 minutes.
Gärtner K, Büttner D, Döhler R, Friedel J, Lindema
J, Trautschold I 1980. Stress response of rats to handling and
experimental procedures. Laboratory Animals 14, 267-274
"The results support the conclusion that rats are not
disturbed by the presence of people with whom they are familiar,
such as the usual animal attendant for that room, if they do not
touch the cage."
Kramer K, van de Weerd H, Mulder A, Van Heijningen C, Bauman V,
Remie R, Voss H-P, Van Zutphen BFM 2004. Effect
of conditioning on the increase of heart rate and body temperature
provoked by handling in the mouse. ATLA (Alternatives to
Laboratory Animals) 32(Supplement), 177-181
"It can be concluded that entering the animal room, even
without handling of the animals, increases HR and BT. After 2
weeks, the animals seem to habituate to this type of disturbance,
with the exception of the first entrance in the morning (9:30am).
In order to mimic standard procedures as much as possible, the
daynight cycle was not reversed. Thus, the first entrance is in
the beginning of the animals rest period. Disturbance at this
time point may cause more stress than later on. Repeated handling
with or without conditioning by an acoustic stimulus reduces the
increase in HR after 12 days especially in the afternoon. .. Thus,
it can be concluded that conditioning of mice can be effective
in attenuating the stress effects of routine procedures."
Environmental
enrichment
Augustsson H, Van de Weerd HA, Kruitwagen CLJJ, Baumans V 2003.
Effect of enrichment on variation and results in the light/dark
test. Laboratory Animals 37, 328-251
"The aim of this study was to investigate if cage enrichment
induces an effect on experimental mean values and on inter-individual
variation in the light/dark paradigm using diazepam as the anxiolytic
drug. The behaviour of 216 naive adult male mice of two different
strains (BALB/c and C57BL/6) was studied. The animals were housed
in groups of four in 'non-enriched', 'enriched' (nesting material)
or 'super-enriched' (nest-box, nesting material, wooden gnawing
stick and PVC tube) cages. .. Mice housed in enriched and super-enriched
cages gained more weight than mice in non-enriched cages, although
food intake was not affected. Generally, the strain of mouse had
the greatest impact on both mean values and variation. .. None
of the [statistical] methods showed any significant differences
between standard and enriched conditions on variability in any
of the parameters measured."
Species-Typical
Behavior
Rodents
Rats
Anne 2005. Norway
Rat Behavior Repertoire - An informal description of rat behavior.
Web site
Excellent description of species typical rat behavior.
Berdoy M 2003. The
Laboratory Rat: A Natural History [a 27 min. video]. Berdoy,
M., Oxford, UK
"Shot as a wildlife documentary over several months, this
27 min film follows the lives of domestic rats after being released
in a large outdoor enclosure where they have to compete, like
their wild cousins, for food, shelter and mates. When keeping
animals in captivity, it is important to know what they have evolved
to do. Progress in animal welfare is, to a large extent, driven
by a combination of awareness, willingness and facts. This film
aims to be relevant to all three by reviewing the range of behaviours
and needs which, despite generations of domestification, remain
innate and ready to be expressed when given the opportunity. The
topics covered in the film include the following: 1. Food selection;
2. The benefits of living in groups; 3. Learning abilities; 4.
Dominance hierarchies;5. Anti-predation; 6. Communication (olfactory
and ultrasonic); 7. Habitat selection and orientation; 8. Mating
strategies and sexual selection; 9. Neophobia; 10. Birth &
Infanticide."
Jegstrup IM, Vestergaard R, Vach W, Ritskes-Hoitinga M 2005. Nest-building
behaviour in male rats from three inbred strains: BN/HsdCpb, BDIX/OrIIco
and LEW/Mol. Animal Welfare 14, 149-156
It was demonstrated in three inbred strains [BN, BDIX, LEW]
of pair-housed male rats that naïve animals who 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 large cages with aspen wood chips bedding, each furnished with
a roofed wooden nest box measuring 28.5 x 20.5 x 12.5 cm. The
box had two entrance holes with a 6 cm diameter on two different
sides. Aspen wood wool and autoclaved straw were placed outside
the box. The nest was removed and the box along with the two rats
transferred to a new cage every two weeks. Additional fresh bedding
material and straw was added twice a week, and wood wool once
a week. The wooden nest box was machine-washed every two months.
All animals built a new nest in the box in the two week period
between the cage changing procedure. The animals began with the
removal of all aspen bedding material form the nest box. They
continued with the collection of straw and wood wool, forming
a mat inside the empty nest box. This mat could be several centimeters
thick and formed into a cup-shape nest. The actual construction
of the nest consisted of fibers of both straw and wood wool, with
straw forming a larger part of the nest structure itself.
Mice
Latham N, Mason G 2004. From house mouse to mouse house: the behavioural
biology of free-living Mus musculus and its implications
in the laboratory. Applied Animal Behaviour Science 86,
261-289
The species-typical behavior of free-living mice is described
and analyzed in reference to its implication to the research laboratory
setting.
Guinea Pigs
Kunkel P, Kunkel I 1964. Beiträge zur Ethologie des Hausmeerschweinchens
Cavia aperea f. porcellus (L.) [Contribution to the ethology
of the domesticated guinea pig (German text with English summary)].
Zeitschrift für Tierpsychologie 21, 602-641
Comprehensive report on the behavior of group-housed guinea
pigs; with numerous photographs.
Reinhardt V 1971 Soziale Verhaltensweisen und soziale Rollen
des Hausmeerschweinchens [Social behavior and social roles of
guinea pigs]. Söcking/Starnberg, Germany: Dissertationsdruck
Novotny
The social and individual behavior of heterosexually group-housed
and isosexually pair-housed guinea pigs is described and analyzed.
The role of olfactory and behavioral factors as social communicators
and social buffers is underscored. The protective effect of submission
is described and analyzed: If a male stops counter-aggression
in a dispute with another male and yields without panic reaction,
the victor will treat him like a female. Rather than showing submissive
gestures, the subordinate partner will behave like an estrus female
and stop emitting the male-typical pheromones. This trick effectively
saves him from further attacks, and the dominant male will now
treat him like a female and display courtship rather than aggressive
behaviors. In fact, males are strictly inhibited from overt aggression
against females, and the subordinate male who plays the female
role runs no risk boxing the dominant opponent in typical female
fashion. Running away stimulates rather than inhibits aggression
if there is no place to hide.
Gerbils
Roper TJ, Polioudakis E 1977. The behaviour of Mongolian gerbils
in a semi-natural environment with special reference to ventral
marking, dominance and sociability. Behaviour 61, 207-237
The species-typical behavior of gerbils is described.
Rabbits
Kraft R 1978/79. Vergleichende Verhaltensstudien an Wild- und
Hauskaninchen. I. Das Verhaltensinventar von Wild- und Hauskaninchen
(pp. 140-162); II. Quantitative Beobachtungen zum Sozialverhalten
(pp. 165-179) [German text with English summary]. Zeitschrift
für Züchtungsbiologie 95, 140-162 & 165-179
Detailed, comparative description of rabbit-specific behavior
of wild and domesticated animals.
Lehmann M 1991. Social behaviour of young domestic rabbits under
semi-natural conditions. Applied Animal Behaviour Science
32, 269-292
Detailed description of species-typical behavior patterns.
Mykytowycz R 1958. Social behaviour of an experimental colony
of wild rabbits (Oryctolagus cuniculus L.) 1. Establishment
of the colony. CSIRO Wildlife Research 3, 7-25
Description of natural social behaviors and social relationships
in rabbits.