Livestock Science 167 (2014) 305–314

Contents lists available at ScienceDirect

Livestock Science
journal homepage: www.elsevier.com/locate/livsci

Behaviour and welfare of growing rabbits housed in cages

and pens
Angela Trocino a,n, Eirini Filiou b, Marco Tazzoli b, Daniela Bertotto a,
Elena Negrato a, Gerolamo Xiccato b
a
Department of Comparative Biomedicine and Food Science, University of Padova, Viale dell’Università 16, I-35020 Legnaro, Padova, Italy
b
Department of Agronomy Food Natural Resources Animal and Environment (DAFNAE), University of Padova,
Viale dell’Università 16, I-35020 Legnaro, Padova, Italy

a r t i c l e i n f o abstract

Article history: The present study compared behaviour, fear and stress levels of 456 crossbred rabbits
Received 3 February 2014 reared in bicellular wire-net cages (2 rabbits/cage) with top and wire floor or open-top
Received in revised form collective pens (20 to 54 rabbits/pen) with wooden slatted floor. The effect of pen size
30 May 2014
(small vs. large) and stocking density (12 vs. 16 rabbits/m2) in collective pens was also
Accepted 31 May 2014
evaluated. The rabbits kept in collective pens rested more than those in bicellular cages
(82.1% vs. 77.6% of observed time; Po 0.01), spent less time feeding (7.8% vs. 10.9%),
Keywords: allo-grooming (0.65% vs. 1.58%) and more time moving (0.81% vs. 0.35%) (P o 0.01). The
Housing percentage of rabbits sensitive in the tonic immobility test was lower in rabbits kept
Behaviour
collectively compared to those in bicellular cages (76.6% vs. 93.8%; P¼ 0.03). In the open
Reactivity
field test, the rabbits kept in collective pens moved less (40.4 s vs. 57.2 s; P o 0.001) and
Corticosterone
Growing rabbits explored the arena for a shorter time (345 s vs. 371 s; P o 0.001) than rabbits housed in
bicellular cages; instead, these rabbits stood still for a longer period of time (82.1 s vs.
38.7 s; P o 0.001). The rabbits kept in collective pens displayed a higher hair corticoster-
one level (15.7 ng/g vs. 6.7 ng/g for rabbits from the cages; P o0.001). Within collective
housing systems, stocking density had no effect whereas increasing pen size numerically
reduced the time rabbits spent eating (8.30% vs. 6.55%), self-grooming (6.39% vs. 5.47%)
and time spent resting (81.1% vs. 84.1%). In conclusion, rabbits housed in collective pens
displayed a more complete behavioural pattern, despite resting more; they were more
bold toward humans, but more fearful in a new environment than rabbits from cages. In
the tested conditions, pen size and stocking density within collective systems exerted only
a weak effect on behaviour, fear and stress levels of meat rabbits.
& 2014 Elsevier B.V. All rights reserved.

1. Introduction exploring and alerting (Trocino and Xiccato, 2006; Verga

et al., 2007). When rabbits are reared in groups of two or
When rabbits raised for meat production are housed in more animals, both the cage/pen dimensions and the
bicellular (2 animals) or small-size (4 to 6 animals) cages, group size may affect the expression of different beha-
as are used in European Countries, they are unable to viours and the quality of social interactions (Buijs et al.,
express typical behavioural patterns, such as hopping, 2011a, 2011b, 2011c; Morisse and Maurice, 1997; Postollec
et al., 2006, 2008).
Unsuitable environment and social relationships/isola-
n
Corresponding author. Tel./fax: þ39 49 8272583. tion may negatively affect stress levels and behaviours
E-mail address: angela.trocino@unipd.it (A. Trocino). and, consequently, the animal immune response and

http://dx.doi.org/10.1016/j.livsci.2014.05.035
1871-1413/& 2014 Elsevier B.V. All rights reserved.
306 A. Trocino et al. / Livestock Science 167 (2014) 305–314

growth performance (Forkman et al., 2007; Koolhaas et al., equipped with 4 (small pens) or 8 (large pens) feeders
1999; Sevi, 2009). (43.5 cm  11.5 cm  30.0 cm-height) for the manual dis-
Useful information regarding rabbit welfare may be tribution of feed at the side walls and 4 (small pens) or 8
derived from behavioural indicators based on ethograms (large pens) nipple drinkers on the back side.
and reactivity to humans or a new environment and from The line of bicellular cages was in front of the line of
physiological indicators such as the levels of glucocorti- pens and the two lines were separated by a 2.0-m-wide
coids or their metabolites. The tonic immobility test may alley used by operators for controls. From the back of the
be used to assess the level of fear that rabbits have towards pens, rabbits saw a 3-m-wide alley used for the passage of
humans (Ferrante et al., 1992; Verwer et al., 2009); the people entering the stable.
open field test is used to measure fear in an unknown The rabbits were allocated into five experimental
environment (Ferrante et al., 1992; Meijsser et al., 1989; groups that differed in the housing system, the pen size
Trocino et al., 2013). Glucocorticoids or their metabolites and the stocking density, as detailed below:
may be measured in the blood and in other matrices, such
as faeces and hair (Monclús et al., 2006; Palme, 2012),  group B18: 40 bicellular cages with top (2 rabbits/cage,
even though these measurements have only been used 18 animals/m2, n ¼80 rabbits);
recently in rabbits kept under commercial conditions  group S12: 4 collective small open-top pens (20 ani-
(Buijs et al., 2011a; Comin et al., 2012; Prola et al., 2013). mals/pen, 12 animals/m2, n ¼80 rabbits);
The present study aimed at evaluating whether and  group S16: 4 collective small open-top pens (27 ani-
how behaviour, fear and stress levels of rabbits may be mals/pen, 16 animals/m2, n ¼108 rabbits);
affected by the housing system (wire net bicellular cages  group L12: 2 collective large open-top pens (40 ani-
with top vs. collective open-top pens with wooden slatted mals/pen, 12 animals/m2, n ¼80 rabbits);
floor) and, within collective pens, by pen size (small vs.  group L16: 2 collective large open-top pens (54 ani-
large) and stocking density (12 vs. 16 rabbits/m2). mals/pen, 16 animals/m2, n ¼108 rabbits).

2. Materials and methods

2.2. Behavioural recordings

2.1. Animals and housing

The behaviour of the rabbits was video-recorded in 20

The study was approved by the Ethical Committee for
bicellular cages (40 rabbits), one L12 pen (40 rabbits), one
Animal Experimentation of the University of Padova. All
L16 pen (54 rabbits), two S12 pens (40 rabbits) and two S16
animals were handled according to the principles stated in
pens (54 rabbits) allowing observation of 228 rabbits. The
the EC Directive 86/609/EEC regarding the protection of
video-recording was performed for 24 h at 52 and 73 d.
animals used for experimental and other scientific purposes.
Two minutes were analysed for each half-hour from each
The trial was performed in a non-air-conditioned stable
cage and pen. During the night, minimal light (about 20 l  )
during the months of September and October. The tem-
was used to avoid disturbing the activities of the rabbits. The
perature ranged from 12 to 25 1C, and a natural photo-
following behaviours were analysed as percentages of the
period (11–13 h daylight) was maintained.
observed time: resting (crouched body, with abdomen in
A total of 456 rabbits of both genders from the Hyplus
contact with the floor, or stretched body, with both fore and
crossbred line (Hypharm, Groupe Grimaud, Roussay,
hind legs stretched beside the abdomen in contact with the
France) were given ad libitum access to a commercial diet
floor), self-grooming, allo-grooming, feeding, drinking, mov-
for growing rabbits. Rabbits were individually identified by
ing, running, standing still, biting and sniffing (Dal Bosco et
ear mark and their performance was controlled from
al., 2002; Morisse et al., 1999; Trocino et al., 2013). The
weaning at 35 d of age to 76 d. Further details were
occurrence (n) of rearing, hops, aggressive interactions and
reported by Xiccato et al. (2013), including the growth
stereotypic behaviours (intense and repeated biting of cage
performance, carcass and meat quality results obtained in
wire net) was recorded.
this study.
Eighty rabbits were put into 40 bicellular cages
(28 cm  40 cm  28 cm-height; available surface per rab- 2.3. Test of tonic immobility
bit: 560 cm2). The floors, roofs and walls of cages were
made of wire net. The cage was equipped with a nipple The test of tonic immobility was performed at 55 and
drinker and a feeder for the manual distribution of feed. 72 d on a total of 160 rabbits (80 rabbits  2 ages). The test
The remaining 376 rabbits were put into 12 collective pens was performed on different animals for the two test ages
located in the same room as the bicellular cages. Eight to avoid the rabbits becoming accustomed to the test. One
small pens (1.40 m  1.20 m ¼1.68 m2) and 4 large pens rabbit per housing system was tested in sequence for 16
(1.40 m  2.40 m ¼3.36 m2) were used. Within each type replications at each age. In total, 32 rabbits from each
of pen, 12 and 16 animals/m2 stocking densities were group (B18 group: 1 animal  16 bicellular cages  2 ages;
tested. L12 group: 8 animals  2 pens  2 ages; L16 group: 8
The collective pens had wooden slat floors (sections of animals  2 pens  2 ages; S12 group: 4 animals  4
the slat: 8 cm  8 cm; distance between the slats: 3 cm), pens  2 ages) were tested.
wooden side walls (105 cm-height), and front and back The test was performed in a contiguous room in the
walls covered by a galvanised wire net. The pens were same barn where the cages and pens were placed. The
 A. Trocino et al. / Livestock Science 167 (2014) 305–314 307

operator took the rabbit out of the cage and induced tested from each group (B18 group: 1 animal  12 bicel-
immobility by turning the animal on its back and onto lular cages  2 ages; L12 group: 6 animals  2 pens  2
his arm. The immobile rabbit was laid down on its back on ages; L16 group: 6 animals  2 pens  2 ages; S12 group: 3
a V-shaped wooden structure (Ferrante et al., 1992). animals  4 pens  2 ages; S16 group: 3 animals  4
A maximum of three attempts to induce immobility were pens  2 ages).
performed, and rabbits were left in the immobility condi- A number of pellets of hard faeces were collected
tion for no more than 180 s. The number of attempts between 16.00 and 18.00 h directly from each animal by
necessary to induce immobility and the total duration of applying a gentle pressure at the perianal area. The hair
immobility were recorded per each rabbit. sample was collected by gently pulling hair from the back
and hind legs.
2.4. Test of open field The corticosterone levels in hard faeces and hair were
measured by microtitre radioimmunoassay (RIA) using
The test of open field was performed at 56 and 75 d on species-specific antibodies (Biogenesis, Poole, England,
a total of 160 rabbits (80 rabbits  2 ages). The rabbits UK) as described in detail by Simontacchi et al. (2009).
tested had not been previously submitted either to the Before RIA, steroids were extracted with 8 mL of diethyl
tonic immobility test or to the open field test. One rabbit ether from hard faeces (50 mg) and hair (30 mg) that were
from each housing system was tested in sequence for 16 thawed and pulverised in liquid nitrogen. Dry extracts
replications as described for the tonic immobility test. were then dissolved in 1 mL of phosphate buffer (PBS,
The test was performed contemporary in two arenas pH 7.2), and various aliquots were used for the assay
(1.5 m  1.5 m) with 0.80-m-high wooden walls and plas- depending on the steroid content in the sample. The
tic floors divided into nine numbered squares. The arenas anti-corticosterone serum showed the following cross-
were located in a contiguous room in the same barn where reactions: corticosterone 100%, 11-deoxycorticosterone
the cages and arena were placed. The rabbits were sub- 1%, cortisol 0.1%, progesterone 0.02%, testosterone
mitted to the open field test from 8.00 to 19.00 h. The total o0.01%. To validate RIA corticosterone measurements in
duration of each test was 10 min per animal. Each rabbit faeces and hair, parallelism and intra- and interassay tests
was put in a closed wooden box (22 cm  30 cm  30 cm- were performed. The tests of parallelism were carried out
high) connected to the arena by a sliding door. After by analysing serially diluted extracts from the matrices
1 min, the sliding door was opened. The number of with high corticosterone concentrations. The sensitivity of
attempts the rabbit made and the time (latency) spent to the assay was 1.5 pg/well and was defined as the dose of
enter the arena were recorded for 1 min. If, after this the hormone at 90% binding.
minute, the rabbit was still in the box, it was gently The displacement curves of the diluted extracts were
pushed into the arena, the sliding door was closed and parallel to the standard curve both in hair and hard faeces
the behaviour of the rabbit was video-recorded for 8 min. (Fig. 1). The corticosterone assay exhibited excellent pre-
The following behaviours were considered by Ferrante cision and reproducibility (hair: intra-assay coefficient of
et al. (1992), Meijsser et al. (1989), and Trocino et al. variation 1.61%, inter-assay coefficient of variation 12.5%;
(2013): total displacements, the number of squares that hard faeces: intra-assay coefficient of variation 2.99%,
each rabbit crossed in the arena; central displacements, inter-assay coefficient of variation 13.5%). The mean recov-
the number of times the rabbit crossed the square in the ery rates of corticosterone added to hair and faeces were
centre of the arena; movement, time spent in moving with 82% and 66%, respectively.
fore and hind legs among squares; running, time spent in
running among squares; exploration, the time spent mov-
2.6. Statistical analysis
ing with forelegs or standing while sniffing and looking
around inside the same square; escape attempts, the
The whole data set of behavioural data collected at two
number of rapid runs towards the corners of the arena;
ages on bicellular cages and collective pens was firstly
hops, the number of times the rabbit completely displaced
analysed by a mixed model in SAS (SAS (Statistical Analysis
its body by a hop; standing still, the time the rabbit spent
still with its fore and hind legs unstretched and on the
100
ground; rearing, the number of times the rabbit reared up 90
on its hind legs; grooming, the time spent self-grooming; 80
digging, the time spent digging inside the arena; biting, 70
the time spent biting elements of the pen; resting, the
% bound

60
time spent inactive with the body touching the floor and 50
fore and/or hind legs stretched on the floor; defecation, 40 Standard
the number of times the rabbit defecated; and urination, 30
Hair
the number of times the rabbit urinated. 20
Hard faeces
10
2.5. Corticosterone determination in hard faeces and hair 0
0.01 0.10 1.00 10.00 100.00
At 63 and 70 d of age, samples of hard faeces and hair Corticosterone (Log ng/g)
were collected from a total of 120 rabbits (12 rabbits  5 Fig. 1. Parallelism of the corticosterone standard curve to serial diluted
experimental groups  two ages), i.e. 24 rabbits were extracts from the hair and hard faeces of rabbits.
308 A. Trocino et al. / Livestock Science 167 (2014) 305–314

System Institute), 2013), i.e. PROC GLIMMIX with housing Differences among means with Po0.05 were accepted
system (bicellular cages vs. collective pens), age and their as representing statistically significant differences.
interaction as fixed effects and time of day as a random
effect. An underlying Poisson distribution was assumed for 3. Results
data expressed in percentage of the time of observation;
a binomial distribution was used for behaviours that 3.1. Behavioural patterns during the 24-h period
seldom happened and occurred (i.e. biting, running, rear-
ing, hops, aggressions, stereotypic behaviours). Data from The rabbits kept in collective pens spent less time
the same cage/pen were treated as repeated measures. feeding (7.8% vs. 10.9% of observed time; P o0.01), allo-
The behavioural data set collected at two ages on grooming (0.65% vs. 1.58%; P o0.001) and more time
collective pens was analysed with PROC GLIMMIX to test displacing (moving: 0.81% vs. 0.35%; P o0.001) and resting
the effect of pen size (large vs. small), stocking density (12 (82.1% vs. 77.7% of observed time; Po0.01) compared to
vs. 16 rabbits/m2) and age and their interactions with age those housed in bicellular cages. The rabbits from the pens
as a fixed effect and time as a random effect. The interac- were observed running, rearing and hopping and did not
tion between pen size and stocking density was not tested exhibit stereotypic behaviours (i.e., intense and repeated
because repeated units were not sufficient (only one cage biting of cage wire net) compared to the latter rabbits
L12 and one cage L16 were video-recorded). Data from the (Table 1). Some significant interactions were measured
same pens were treated as repeated measures. between the housing system and the age: feeding time
The data from the reactivity tests (tonic immobility test, decreased from 52 to 73 d of age only in rabbits kept in
open field test) from bicellular cages and collective pens collective pens; conversely, allo-grooming increased and
were firstly analysed by PROC GLIMMIX with housing moving and sniffing decreased from 52 to 73 d of age only
system (bicellular cages vs. collective pens), age and their in rabbits housed in bicellular cages. Time spent in resting
interaction as fixed effects, and cage/pen as random effect. with stretched body decreased from 52 to 73 d of age
An underlying Poisson distribution was assumed for data (Po0.001), but the reduction was more pronounced in
expressed in percentage of the time of observation. Then, rabbits in bicellular cages (from 12.7% to 0.87% of observed
the data from the reactivity tests performed on rabbits of time) than in those in collective pens (from 9.32% to
collective pens were analysed by PROC GLIMMIX to test 3.61%).
the effect of pen size (large vs. small), stocking density (12 Within the collective housing systems, rabbits in the
vs. 16 rabbits/m2) and age and their interactions as fixed larger pens shared a numerical decrease in the time
effects and cage/pen as a random effect. rabbits spent eating (8.30% vs. 6.55%), self-grooming
The data of corticosterone levels in faeces and hair was (6.39% vs. 5.47%), sniffing (1.53% vs. 1.19%), and more time
analysed by ANOVA using the PROC MIXED (SAS (Statistical resting (81.1% vs. 84.1%) (Table 2). During the resting time,
Analysis System Institute), 2013) with experimental group, the rabbits housed in the small pens stayed less with a
age and their interactions as factors of variability and the crouched body compared to the rabbits in large pens
pen/cage as random effect. The CONTRAST statements were (73.6% vs. 79.8% of observed time; P o0.01).
used to test the effect of the type of housing (bicellular cages In collective systems, changes of stocking density per se
vs. collective pens) and, within collective systems, pen size had only a weak effect but showed some significant
(small vs. large) and stocking density (12 vs. 16 rabbits/m2). interactions with age (Po0.01) (Table 2): feeding time

Table 1
Effect of housing system and age in rabbits reared in bicellular cages and collective pens: behaviours during video-recording (% of budget timea).

Housing system (H) Bicellular cages Collective pens Bicellular cages Collective pens P-value

Rabbit age (A) 52 d 52 d 73 d 73 d H A HA

Observations (n) 480 144 480 144
Drinking (%) 0.72 0.99 0.83 1.03 0.17 0.37 0.43
Feeding (%) 11.0 8.62 10.8 6.89 o 0.01 o 0.001 o0.001
Self-grooming (%) 5.55 4.91 8.30 7.30 0.24 o 0.001 0.86
Allo-grooming (%) 1.13 0.58 2.02 0.71 o 0.001 o 0.001 0.02
Moving (%) 0.45 0.80 0.24 0.81 o 0.001 o 0.001 o0.001
Sniffing (%) 2.40 1.18 1.21 1.68 0.332 o 0.01 o0.001
Total resting (%) 78.7 82.9 76.6 81.3 o 0.01 o 0.01 0.55
With stretched body (%) 12.7 9.32 0.87 3.61 o 0.001 o 0.001 o0.001
With crouched body (%) 66.0 73.5 75.7 77.7 o 0.01 o 0.001 o0.001
Biting (n) 0.00 0.05 0.00 0.03 n.e. n.e. n.e.
Running (n) 0.00 0.18 0.00 0.37 n.e. n.e. n.e.
Rearing (n) 0.00 0.04 0.00 0.06 n.e. n.e. n.e.
Hops (n) 0.00 0.03 0.00 0.12 n.e. n.e. n.e.
Aggressions (n) 0.00 0.00 0.00 0.02 n.e. n.e. n.e.
Stereotypies (n) 0.02 0.00 0.03 0.00 n.e. n.e. n.e.

n.e. non-estimable.
a
The sum of behaviours may be less than 100% because of some minor behaviours (biting, running, standing still) that took a minor percentage of
budget time but were not suitable for the statistical analysis and are not included in table.
 A. Trocino et al. / Livestock Science 167 (2014) 305–314 309

Table 2
Effect of pen size, stocking density and age in rabbits reared in collective pens: behaviours during video-recording (% of budget timea).

Pen size (P) Stocking density (rabbits/m2) (S) P-valueb

Small Large Small Large 12 16 12 16

Rabbit age (A) 52 d 52 d 73 d 73 d 52 d 52 d 73 d 73 d P S A PA SA

Observations (n) 96 48 96 48 72 72 72 72
Drinking (%) 0.99 0.93 0.92 1.26 1.13 0.82 1.07 1.08 0.65 0.57 0.37 0.12 0.16
Feeding (%) 9.06 7.53 7.54 5.56 7.19 9.49 6.60 6.35 0.08 0.39 o 0.001 0.21 o 0.01
Self-grooming (%) 5.27 4.12 7.50 6.81 4.49 4.84 7.81 6.55 0.06 0.57 o 0.001 0.17 o 0.01
Allo-grooming (%) 0.79 0.12 0.34 1.13 0.45 0.21 0.35 1.11 0.30 0.53 o 0.001 o0.001 o 0.001
Moving (%) 0.85 0.68 0.87 0.67 0.73 0.79 0.85 0.69 0.11 0.68 0.96 0.90 0.27
Sniffing (%) 1.39 0.67 1.66 1.72 1.20 0.78 1.76 1.62 0.07 0.16 o 0.001 o0.01 0.10
Total resting (%) 81.4 85.7 80.7 82.5 84.4 82.7 80.9 82.4 0.06 0.94 0.09 0.28 0.13
With stretched body (%) 10.4 6.34 4.36 2.11 10.3 6.44 3.03 3.04 o 0.001 0.10 o 0.001 0.08 o 0.001
With crouched body (%) 70.7 79.2 76.4 80.3 73.6 76.1 77.7 79.0 o 0.01 0.34 o 0.01 0.03 0.56
Biting (n) 0.03 0.07 0.01 0.08 0.05 0.04 0.01 0.04 0.03 0.51 0.36 0.29 0.35
Running (n) 0.14 0.25 0.31 0.45 0.17 0.21 0.46 0.31 0.06 0.61 o 0.01 0.74 0.24
Rearing (n) 0.05 0.02 0.04 0.10 0.04 0.02 0.07 0.06 0.93 0.51 0.28 0.17 0.84
Hops (n) 0.03 0.02 0.08 0.19 0.01 0.04 0.13 0.12 0.92 0.31 0.02 0.24 0.24

a
The sum of behaviours may be less than 100% because of some minor behaviours (biting, running, standing still) that took a minor percentage of
budget time but were not suitable for the statistical analysis and are not included in table.
b
Probability of P  S  A non-estimable.

Table 3
Effect of housing system and age in rabbits reared in bicellular cages and collective pens: response to the tonic immobility test.

Housing system (H) Bicellular cages Collective pens Bicellular cages Collective pens P-value

Rabbit age (A) 55 d 55 d 72 d 72 d H A HA

Rabbits (n) 16 64 16 64
Sensitive rabbits (%)a 87.5 81.3 100 71.9 0.03 0.43 0.06
Attempts (n) 1.94 2.19 1.94 2.30 0.30 0.86 0.86
Immobility (s) 46.5 36.4 31.5 26.3 0.47 o 0.001 0.31

a
Rabbits that exhibited immobility within three attempts.

was less in rabbits stocked at 12 rabbits/m2 compared to the collective systems (pen size, stocking density)
those at 16 rabbits/m2 at 52 d of age (7.19% vs. 9.49%) (Table 4). The total duration of immobility significantly
whereas differences disappeared at 73 d of age (6.60% vs. decreased (41.5 s vs. 28.9 s; Po0.001) when the age of
6.35%); time spent in grooming was similar at 52 d of age rabbits increased from 55 d to 72 d (Table 3). Within
(self-grooming: 4.49% vs. 4.84%; allo-grooming: 0.45% vs. collective systems, at 55 d of age rabbits exhibited a higher
0.21%) but differed at 73 d of age (self-grooming: 7.81% vs. immobility when kept in large pens compared to those in
6.55%; allo-grooming: 0.35% vs. 1.11%). The increase in age small pens and when housed at 12 rabbits/m2 compared to
from 52 to 73 d significantly affected the behaviour of the those at 16 rabbits/m2. Differences among groups by pen
rabbits (Table 2). The older rabbits spent more time self- size or by stocking density disappeared at 72 d of age
grooming, allo-grooming, sniffing, and running. Older (probability of the interaction pen size x age (P o0.001)
rabbits also exhibited more hops and reduced feeding and stocking density x age (P o0.05), Table 4).
time. The resting time was slightly less at 73 d (81.7%) In the open field test, the rabbits kept collectively in
than at 52 d of age (83.6%) and the stretched position was pens crossed fewer squares (30.8 vs. 47.5; Po0.001),
less preferred (8.37% to 3.24%) by older rabbits. moved less (40.4 s vs. 57.2 s; P o0.001) and explored less
(345 s vs. 371 s; P o0.001) the arena than the rabbits from
3.2. Reactivity tests the bicellular cages and stood still for a longer period of
time (82.1 s vs. 38.7 s; Po0.001) (Table 5). Significant
In the tonic immobility test, the percentage of sensitive interactions between housing system and age were also
rabbits (which turned immobile within three attempts) measured: the number of total displacements was much
was significantly lower in the rabbits kept collectively lower in rabbits of collective pens than in those of
compared to those reared in bicellular cages (76.6% vs. bicellular cages at 75 d of age rather than at 56 d of age.
93.8%; P ¼0.03) (Table 3) regardless of pen size and stock- A similar trend was recorded for the number of central
ing density (Table 4). Among the rabbits sensitive to the displacements and the time spent running. Time spent
test, neither the number of attempts nor the time of biting measured at 56 d of age was less than at 75 d of age
immobility differed according to the housing system (Table 5). Within the collective systems, pen size had no
(bicellular vs. collective) (Table 3) or the conditions of effect whereas stocking density only affected the time that
310 A. Trocino et al. / Livestock Science 167 (2014) 305–314

Table 4
Effect of pen size, stocking density and age in rabbits reared in collective pens: response to the tonic immobility test.

Pen size (P) Stocking density (rabbits/m2) (S) P-valueb

Small Large Small Large 12 16 12 16

Rabbit age (A) 55 d 55 d 72 d 72 d 55 d 55 d 72 d 72 d P S A PA SA PS

Rabbits (n) 32 32 32 32 32 32 32 32
Sensitive rabbits (%)a 81.3 81.3 71.9 71.9 84.4 78.1 68.7 75.0 0.99 0.99 0.21 0.52 0.67 0.84
Attempts (n) 2.03 2.34 2.28 2.31 2.05 2.34 2.78 2.31 0.51 0.51 0.66 0.58 0.58 0.72
Immobility (s) 31.8 42.2 27.0 27.1 41.9 32.0 29.1 25.2 0.43 0.26 o 0.001 o 0.001 0.05 0.86

a
Rabbits that exhibited immobility within three attempts.
b
Probability of P  S  A, P4 0.05.

Table 5
Effect of housing system and age in rabbits reared in bicellular cages and collective pens: behaviours during the open field test.

Housing system (H) Bicellular cages Collective pens Bicellular cages Collective pens P-value

Rabbit age (A) 56 d 56 d 75 d 75 d H A HA

Rabbits (n) 16 64 16 64
Entered animalsa,b (%) 75.0 51.6 62.5 54.7 0.11 0.99 0.37
Attempts (n) 0.31 0.34 0.31 0.36 0.74 0.94 0.95
Latency (s) 34.2 43.3 40.8 41.6 0.24 0.04 0.001
Total displacements (n) 46.2 34.1 48.8 27.5 o 0.001 o 0.01 o0.001
Central displacements (n) 0.38 0.51 1.00 0.23 0.28 0.76 o0.01
Exploration (s) 371 345 371 344 o 0.001 0.98 0.88
Movement (s) 58.9 42.7 55.4 38.1 o 0.001 o 0.01 0.34
Running (s) 2.56 2.41 3.56 1.09 0.19 0.06 o0.001
Standing still (s) 38.2 77.5 39.1 86.7 o 0.001 0.02 0.15
Grooming (s) 1.50 1.58 1.75 1.96 0.86 0.23 0.84
Biting (s) 3.56 2.41 6.31 6.56 0.68 o 0.001 0.03
Digging (s) 1.88 0.49 1.00 0.45 0.12 0.07 0.19

a
Rabbits that entered the arena spontaneously within 60 s.
b
Probability of χ2 test.

the rabbits groomed (P¼ 0.02) (Table 6). Significant inter- 11.6 ng/g in rabbits of the groups B18, L12, L16, S12 and
actions between pen size and age were measured for S16, respectively, at 63 d of age and 6.8, 19.7, 21.2, 17.7 and
minor behaviours like running, grooming, biting and 19.6 ng/g at 70 d of age in the same groups) (Fig. 2b).
digging (Table 6). The major interaction between stocking
density and age (Po0.001) was recorded for the latency to 4. Discussion
enter the arena which was higher in rabbits housed at 12
animals/m2 compared to those at 16 animals/m2 at 56 d of 4.1. Effect of the housing system: cages vs. pens
age and lower in the rabbits of the former group at 75 d of
age (Table 6). Housing in bicellular cage is recognized as a cause of
When the age of rabbits increased, the rabbits in poor welfare in rabbits reared for meat production due to
collective pens showed a lower number of total and movement constraints and the lack of environmental and
central displacements, spent less time moving, running social interactions (EFSA (European Food and Safety
and grooming, whereas they increased the time spent in Authority), 2005; Szendrő and Dalle Zotte, 2011). Whether
standing still and biting (Table 6). these conditions affect fear and stress levels in animals is
not yet clear (Trocino et al., 2013; Verga et al., 2007).
3.3. Corticosterone in hard faeces and hair In our trial, rabbits housed in bicellular cages exhibited
poorer behavioural patterns because rabbits were not
The corticosterone level in hard faeces did not vary allowed to run, rear or hop, due to the small available
with treatments (Fig. 2a), whereas the hair corticosterone surface and the low height of the cages. Previous authors
level was higher in the rabbits reared in collective pens observed that rabbits kept collectively performed more
compared to those in bicellular cages (15.7 ng/g vs. activities and rested less than rabbits in bicellular cages
6.7 ng/g; P o0.001) and in rabbits at 70 d of age compared (Princz et al., 2008). However, in our study, rabbits in
to those at 63 d of age (17.0 vs. 10.7 ng/g; P o0.001) collective pens rested for a longer time. We hypothesise
(Fig. 2b). A significant interaction between the housing that, especially during the first weeks of the trial, the
system and the age of animals was also measured; the hair rabbits were afraid to move across the slatted wooden
corticosterone levels increased with age only in rabbits floor of the collective pens because of the large space
reared in collective systems (6.5, 10.5, 14.1, 11.0 and between slats (3 cm). These limitations likely led to
 A. Trocino et al. / Livestock Science 167 (2014) 305–314 311

Table 6
Effect of pen size, stocking density and age in rabbits reared in collective pens: behaviours during the open field test.

Pen size (P) Stocking density (rabbits/m2) (S) P-valuec

Small Large Small Large 12 16 12 16

Rabbit age (A) 56 d 56 d 75 d 75 d 56 d 56 d 75 d 75 d P S A PA SA PS

Rabbits (n) 32 32 32 32 32 32 32 32
Entered animalsa,b (%) 46.9 50.0 40.6 50.0 46.9 50.0 46.9 43.0 0.48 0.99 0.72 0.86 0.97 0.80
Attempts (n) 0.41 0.28 0.27 0.43 0.37 0.31 0.31 0.38 0.85 0.98 0.98 0.17 0.53 0.40
Latency (s) 43.7 43.3 39.9 43.7 45.7 41.4 39.9 43.6 0.68 0.96 0.13 0.07 o 0.001 0.37
Total displacements (n) 32.7 36.1 27.6 27.9 35.7 33.2 28.8 26.8 0.66 0.55 o0.001 0.17 0.99 0.77
Central displacements (n) 0.09 0.52 0.00 0.00 0.39 0.13 0.00 0.00 0.98 0.98 o0.001 0.98 0.98 o 0.001
Exploration (s) 352 334 348 338 343 342 340 345 0.10 0.83 0.93 0.27 0.38 0.25
Movement (s) 43.3 41.4 39.5 36.1 41.5 43.2 36.9 38.6 0.47 0.64 o0.001 0.44 0.92 0.71
Running (s) 2.12 3.27 0.33 1.79 2.63 2.63 0.58 1.02 0.14 0.69 o0.001 o 0.01 0.20 0.28
Standing still (s) 69.6 82.8 78.3 96.1 74.8 77.1 89.9 83.7 0.17 0.88 o0.001 0.42 0.01 0.26
Grooming (s) 32.7 36.1 27.6 27.9 35.7 33.2 28.8 26.8 0.17 0.02 0.01 o 0.001 0.07 0.81
Biting (s) 1.35 2.76 8.08 4.52 1.74 2.14 5.37 6.81 0.88 0.62 o0.001 o 0.001 0.88 0.28
Digging (s) 0.18 0.22 0.00 0.00 0.29 0.13 0.35 0.00 0.28 0.99 0.99 o 0.001 0.99 0.25

a
Rabbits that entered the arena spontaneously within 60 s.
b
Probability of χ2 test.
c
Probability of P  S  A, P40.05.

55 cages) in the first period of observation (52 d) further

63 d
supports this hypothesis: the crouched position could have
70 d
50 47.6 been perceived as safer on the wooden slatted floor, with a
46.7 45.9 45.9
45 43.5
lower risk of falling into the spaces among slats. On the
41.5 42.5 other hand, at later observations (73 d of age), the very low
40.0 40.0 40.3
40 time spent resting in a stretched position by rabbits in
ng/g

bicellular cages (0.87%) has likely to be ascribed to the

35
space limits of the bicellular cage itself.
30 As a consequence of experience or environment, animals
may show different attitudes both towards humans (tonic
25
immobility test) and towards an unknown environment
20 (open field test). In our trial, rabbits kept in collective pens
B18 S12 S16 L12 L16 displayed less fear (meaning a lower percentage of rabbits
Group were sensitive to immobility) towards humans in the tonic
immobility test, whereas they were less prone to move-
ment and less curious towards a new environment during
25
63 d the open field test compared to rabbits in bicellular cages.
70 d 21.2e
19.6e 19.7e The congruence of rabbit behaviours during the tonic
20 17.7d immobility test and the open field test has not been
proven definitively. In fact, in contrast with our results,
15 14.1cd previous studies reported that rabbits in bicellular and
ng/g

11.0c 11.6c small collective cages (9 animals per group) had similar
10.5bc
10 behaviours towards humans and were less fearful in the
6.5a 6.8
ab tonic immobility test compared to rabbits kept in indivi-
5 dual cages (Trocino et al., 2013). Rabbits kept collectively
were reported as more bold during the open field test
compared with rabbits kept in individual or bicellular
0
B18 S12 S16 L12 L16 cages (Schepers et al., 2009; Trocino et al., 2013). This
Group finding was partly related to social isolation, the need for
group reinstatement and curiosity, similar to what has
Fig. 2. Corticosterone levels (ng/g) in hard faeces (a) and hair (b) at 63
and 70 d of age in rabbits reared in bicellular cages (B18), small collective
been described for birds and sheep (Forkman et al., 2007).
pens at 12 rabbits/m2 (S12) and 16 rabbits/m2 (S16), and large collective In the conditions of our trial, the possibility of expres-
pens at 12 rabbits/m2 (L12) and 16 rabbits/m2 (L16). [Means without a sing wider social behaviours with more conspecifics in the
common superscript letter differ, Po 0.05]. collective pens seems to have improved the animal reac-
tion toward humans. On the other hand, the fearful
decreased time spent eating and allo-grooming compared reaction of these rabbits towards a new environment
to rabbits raised in bicellular cages. may be explained by the negative experience they had
The body position assumed during resting (more time when moving on the wooden slatted floor of their pens,
in a crouched position in collective pens than in bicellular especially at an early age (post-weaning period), or by the
312 A. Trocino et al. / Livestock Science 167 (2014) 305–314

stress induced by the social isolation during the open In our conditions, rabbits rested more time in the
field test. crouched position in the large pens compared to the small
The higher levels of hair corticosterone measured in the pens and especially at early ages compared to later
rabbits reared in collective pens compared to those kept in observations (92.4% and 86.8% of resting time in large
bicellular cages may also signal the more stressful condi- and small pens, at 52 d of age; 97.3% and 95.7% of resting
tions for the rabbits housed in collective pens. Whether time in large and small pens at 73 d of age); this result is
this stress came from the housing conditions per se difficult to explain and deserves further investigation to
(bicellular cages vs. collective pens) or could be attributed assess the real space requirements by rabbits. Buijs et al.
to other factors, such as the difficulty of establishing a (2011b) reported that growing rabbits showed increased
stable social hierarchy due to the high number of con- sternal lying (i.e. abdomen in contact with the floor,
specifics, needs to be elucidated. The significant interac- without specifying the position of the fore and hind legs)
tion between the housing system and the age of the with decreasing space allowance (same group size in pens
animals, with hair corticosterone concentrations increas- of decreasing size). This lying was considered a filling
ing from 63 to 70 d of age only in rabbits kept in collective behaviour, rather than a comfort behaviour.
pens, suggests that behaviours associated with establish- The small differences in behaviour among the rabbits
ing social hierarchy or oncoming sexual maturation kept collectively were not associated with changes in fear
(Szendrő et al., 2009) could have an effect on glucocorti- or stress levels due to the pen size or the stocking density.
coid levels. This trend could be even accentuated in the This change has been previously reported by other authors
actual genetic lines selected for fast growth rate (Pascual using the tonic immobility and open field tests (Trocino
et al., 2013). et al., 2004, 2008; Zucca et al., 2012) or measuring
Hair cortisol concentrations have been used as an index glucorticoid metabolite concentrations in rabbit faeces
of chronic stress in various animal species. To our knowl- (Buijs et al., 2011a). For rabbits kept in groups under
edge, little information is available about these measure- alternative housing conditions (free range on ground),
ments in rabbits (Comin et al., 2012). In contrast with our the reduction of stocking density from 16 to 12 rabbits/
results, glucocorticoid metabolites and corticosterone con- m2 moved the reactivity of rabbits during the open field
centrations in hard faeces have been found to differ among test towards a more active behaviour (Verga et al., 1994).
growing rabbits reared in different housing conditions
(with or without enrichment), subjected to transport 4.3. Effects of rabbit age
stress (Buijs et al., 2011a), among rabbits of different
breeds, between rabbits at different physiological states Rabbits spend most of their time resting in both a wild
that were kept in different housing conditions (cage size environment (with variations depending on the vegetation
and presence of plastic foot mat) (Prola et al., 2013), and structure and food availability) (Kolb, 1986; Lombardi et
among wild rabbits after exposure to a stress stimulus al., 2007) and in farm conditions (Morisse and Maurice,
(predator odour) (Monclús et al., 2006). 1997; Princz et al., 2008; Trocino et al., 2013; present trial).
Based on the different accumulation pathways, we Under farm conditions, the main activities are resting,
could hypothesise that corticosterone in faeces may be self-grooming, and feeding regardless of the housing
useful to measure an acute stress whereas corticosterone system used or rabbit age (Dal Bosco et al., 2002; Buijs
in hair may measure a chronic stress in rabbits as it et al., 2011b; Trocino et al., 2008, 2013).
happens in other species (Cook, 2012). Few measurements change with increasing age. Feed-
ing time decreases and grooming increases (Martrenchar
et al., 2001; Morisse et al., 1999; Trocino et al., 2013). There
4.2. Effect of pen size and stocking density in collective pens is also a higher frequency of running and hopping (Trocino
et al., 2013; present trial), which may be associated with
In our study, the differences in behaviour, reactivity and the appearance of aggressive interactions among animals.
stress levels according to pen size and stocking density In the present trial, as the rabbits aged, the prevalence of
within collective pens were rather scarce. In small pens, the crouched position during resting further increased.
rabbits rested less and spent more time performing other Whether the crouched or the stretched position is the
activities (eating, self-grooming, sniffing) in comparison most comfortable for the rabbit is difficult to assess; we
with rabbits kept in large pens. Other authors did not find can state that the crouched position is preferred based on
substantial changes in the budget time of rabbits housed at its prevalence during resting at all ages.
different pen/cage sizes at the same stocking density (15 In the tonic immobility test, the duration of immobility
animals/m2) (Martrenchar et al., 2001; Postollec et al., decreased from 55 to 75 d of age in rabbits both in bicellular
2006, 2008) or at different stocking densities (Buijs et al., cages and collective systems, proving a reduction of the fear
2011b). Only the frequencies of runs and consecutive hops level towards humans. Differences in pens size or stocking
were significantly higher in rabbits kept in large pens (50 density were detected only in younger rabbits and were no
rabbits) compared with rabbits in small pens or standard longer present a few days before slaughter. In the open field
cages (6–10 rabbits) (Martrenchar et al., 2001; Postollec et test, the lower attitude of animals to move in a new
al., 2006). This latter result may indicate that rabbits have environment at older ages mainly depended on the differ-
specific requirements for the total available surface on ences in behaviour of rabbits reared collectively.
which to perform some typical activities, rather than a We avoided unbiased responses due to habituation of the
minimum individual space requirement. animals to the test. In previous trials where the reactivity
 A. Trocino et al. / Livestock Science 167 (2014) 305–314 313

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tests (Trocino et al., 2013; Xiccato et al., 1999). Therefore, horses. Physiol. Behav. 92, 340–374.
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This study was funded by the University of Padova (Year Princz, Z., Dalle Zotte, A., Radnai, I., Bíró-Németh, E., Matics, Z.s.,
2011; Research Project CPDA119830- CUP: C21J11000500005). Gerencsér, Z.s., Nagy, I., Szendrő, Z.s., 2008. Behaviour of growing
rabbits under various housing conditions. Appl. Anim. Behav. Sci. 111,
The Authors wish to thank Dr. Andrea Zuffellato (Veronesi 342–356.
Verona S.p.A.) for his technical assistance during the trial. Prola, L., Cornale, P., Renna, M., Macchi, E., Perona, G., Mimosi, A., 2013.
Effect of breed, cage type, and reproductive phase on fecal corticos-
terone levels in doe rabbits. J. Appl. Anim. Welfare Sci 16, 140–149.
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