An experimental study of social attraction and spacing between the sexes in sheep
1 Centre de Recherches sur la Cognition Animale, Université Paul
Sabatier, F-31062, France
2 Laboratoire de Comportement et d'Ecologie de la Faune Sauvage, INRA, 31326
Castanet-Tolosan cedex, France
3 UMR Elevage des Ruminants en Région Chaude, Agro-M-INRA-CIRAD,
34060 Montpellier Cedex 1, France
4 Laboratoire de Comportement, INRA-CNRS, 37380 Nouzilly, France
5 Service d'Ecologie Sociale, Université Libre de Bruxelles,
Bruxelles
* Author for correspondence (e-mail: michelen{at}cict.fr)
Accepted 29 September 2005
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Summary |
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Key words: sheep, Ovis aries, attraction, spacing, sex discrimination, open field test
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Introduction |
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In vertebrates, individuals of different age and sex classes do not mix
randomly, but are assorted by phenotypes
(Krause et al., 2000;
Ward and Krause, 2001
;
Croft et al., 2003
). In
ungulates, individual animals tend to associate and/or interact primarily with
conspecifics belonging to the same (social) category, e.g. sex and age
(Bon and Campan, 1996
; see also
Conradt, 1998
). Social
segregation between the sexes is a characteristic of the socio-spatial
organization at a population level in social and dimorphic ungulates, and may
result from several mechanisms, before and/or after fusion
(Bon et al., 2005
). For
example, group fusion could be dependent upon the capacity of individuals to
discriminate the activity or the phenotype of conspecifics at a distance.
Weckerly et al. (2001
)
observed that Roosevelt elk Cervus elaphus roosevelti females avoid
male groups exceeding six individuals. Bon and Campan
(1996
) proposed that social
segregation between adults could result from social ontogeny juvenile
males being more motivated to interact than females using pseudo-sexual and
agonistic-like interactions. As a result females may avoid or be indifferent
to males. This would result in a social autosegregation, i.e. males and
females would prefer to associate with same-sex peers, which can have
long-lasting effects during adulthood (Bon
et al., 2001
). Avoidance between sexes or a preference for
same-sex individuals would lead to a deficit of mixed-sex groups. Mathematical
and theoretical models have been developed to demonstrate how internal group
structure may result from an interplay between the social forces or motives,
i.e. attraction and repulsion (Warburton
and Lazarus, 1991
;
Guéron et al., 1996
).
However these models are not founded on experimental data and precise measures
of the behaviour of animals are needed to validate them
(Dumont and Boissy, 2000
;
Camazine et al., 2001
;
Couzin and Krause, 2003
).
In freely moving groups, the interindividual distance can reflect different
attraction or avoidance (Warburton and
Lazarus, 1991; Whitehead,
1997
). Moreover individual distances may vary seasonally, or with
the sex, phenotype and other individual characteristics of the group members
(Marler, 1956
;
Brown and Orians, 1970
;
Syme et al., 1975
;
Walther, 1977
;
Hinch et al., 1990
;
Stolba et al., 1990
).
Most studies on individual distance have been performed on groups without
taking into account the dynamics of the interactions between individuals
(Keeling, 1995;
Shiyomi and Tsuiki, 1999
;
Shiyomi, 2004
). However, at
any moment, inter-individual distances result from different possible
interactions between the individual and there is no doubt that these
interactions include stochastic components. Hence continuous recording of
individual movements over a sufficient period of time is a prerequisite to
understanding how individuals maintain a social distance to group members.
Pérez-Barbería et al.
(2005) performed binary choice
indoor experiments to study the social preferences of Soay sheep. They
detected that adults preferred the individuals of their own sex. In the
present study we attempted to gain further insights into these mechanisms
involved in social segregation by testing social choice in relatively
freeranging outdoor conditions, i.e. sheep were observed in the pasture where
they graze. For this purpose, we registered the movement of freely moving
individual merino sheep Ovis aries in an open field arena. In order
to rule out the effect of movement and social interactions by conspecifics
(e.g. affinitive, agonistic), we restrained their movement in space. We also
measured the distances because (i) proximity can reflect attraction and social
discrimination and (ii) the sexes may differ in `social distance', and finally
to assess how unrestrained sheep regulated the distance to conspecifics over
time. Three series of binary choice experiments were performed with sheep of
both sexes. In all tests the attractiveness of conspecifics was assessed by
recording the pattern of movement of the test sheep. If sheep can discriminate
the sex of conspecifics at a distance, we expected that they would move more
readily towards confined individuals of the same sex rather than towards
opposite sex animals. If a choice occurs at closer distances, the time spent
near the same-sex should be longer than near the opposite-sex peer.
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Materials and methods |
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Males bear horns and were heavier than ewes (mass 61.4±9.3 vs 49.4±5.4 kg, respectively, means ± S.D., Student's t-test t64,62=8.85, P<0.01). At the time of testing, the mean age of the males and females was 3.7 (range=28) and 8.9 years (range=511), respectively.
Each ewe was treated with a vaginal sponge containing 3040 mg of progesterone (replaced every 14 days) to block estrus and prevent any sexual interactions related to estrus. Animal care and experimental manipulations were in accordance with the rules of the French committee of animal experimentation ethics.
Experimental set-up and procedure
Individual sheep were tested with one confined stimulus peer of either the
same or opposite sex vs an empty cage. In further experiments, test
individuals were given a conflicting choice, i.e. confronted with two stimuli,
one male/one female. Social attraction and sex discrimination were controlled
by exposing sheep, respectively, to two empty cages and two confined peers of
their own sex (Table 1).
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Tests were conducted in 25 m arenas containing three wire cages (1.5 mx1 mx1 m). Two cages symmetrically located at the periphery of the arena were used as stimulus cages, containing a sheep or not, depending upon the treatment. The test sheep was placed into the third cage (releasing cage), located at the periphery of the arena, equidistant from stimulus cages. This cage was positioned on the side of the observation tower located at 22.5 m from the arena centre (Fig. 1). All test animals were familiar with the pastures as they regularly grazed on them throughout the year.
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Data collection
The experiments were carried out in winter and summer 2003 and in winter
2004 (see Table 1 for the
chronology of experimental conditions). In winter, data were collected from
8:00 h to 18:00 h and in summer, from 6:00 h to 10:00 h and 18:00 h to 21:00 h
because of animal inactivity (idling) during the highest temperatures of the
day.
On each digital snapshot, the location of the test individual was visually
tracked on a monitor using mouse click tracker software. Two points were
specified corresponding to the on-ground projections of the hemi-distance
between the forelegs and the hind legs. Then, classical 3D-reconstruction of
object attitudes out of 2D-images was performed based on true perspective
projection (Horn, 1999). The
accuracy of sheep location was assessed by comparing the coordinates of sheep
extracted from digital snapshots (c) to those obtained in the field
by using a laser rangefinder (l) (Impulse model 200LR, Laser
Technology Society Inc., Englewood, CO, USA). The coordinates obtained by each
method were highly correlated, the estimated error on locations extracted from
snapshot being <0.5 m (respectively x and y coordinated:
xc=1.005xxl0.123, r=0.99,
N=226, P<0.001 and
yc=0.987xyl0.196, r=0.99,
N=226, P<0.001).
Spatial analyses
We extracted several variables from the spatial distribution of each sheep,
i.e. the area used, based on the 90% Convex Polygon method using Ranges V
software (Sargeant et al.,
1993), the corresponding centroid, and the distance walked. This
latter was approximated by the cumulated linear distances between consecutive
locations.
Circularity of distribution was analysed using the Moore test
(Zar, 1999). Lateral symmetry
of the distribution in the arena without stimulus sheep was tested using a
paired-data Student t-test. Attraction by conspecifics, supposed to
result in a spatial skew, was tested by using a second order test of the
significance of the mean (Zar,
1999
).
We also considered the distribution of location density, computed by segmenting the arena into virtual 2 m rings(02 m, 24 m, etc) centred on the centre of the side of both cages adjacent to the arena. In order to compare the social conditions, the distributions of location density were normalised by the total number of locations.
We predicted that if the stimulus sheep exerted a strong social attraction, the distribution of location density of test sheep should be biased towards the corresponding cage, and the part of arena explored (i.e. area used and distances walked) would be small compared to random movement in the arena without social attraction.
The minimum distances to the cages within the first 4 min after release were also compared. This interval of time was chosen because the distance of approach to stimulus cages was smaller than the distance of the centroid of locations over the 30 min period for 94% of test animals.
Activity budget of test sheep
In freely moving groups, sheep mainly engage in feeding when active,
therefore the distance between individuals reflects movements during grazing.
We were interested to study social attraction between individuals in pasture
conditions. However the stress associated with isolation could modify the
behaviour of sheep. We therefore recorded the activity of test animals
continuously using a Thomson dk 52 micro cassette recorder (Stanford, CT, USA)
to measure their time spent grazing, standing, walking, lying/idling and
bleating. From all animal tested (N=176), 24 were discarded: 2 ewes
escaped from the arena, 3 males entangled their horns in the fence net, 2
animals were lying down throughout the test, 1 stayed in the releasing cage
and 16 were idle (this occurred only in summer). Since the remaining sheep did
not leave the releasing cage instantaneously, we analysed the proportion of
time engaged in each activity. Because test sheep were mainly engaged in
feeding activity, to detect possible outliers we only considered the time
spent feeding. The proportion of time spent grazing (P) did not
follow a normal distribution, and was thus transformed using the
ln[arcsineP]. The Dixon Extreme Value test
(Dixon, 1953
) was used to
detect outliers of an assumed normal distribution of the grazing time. The
Dixon test identified 5 outliers, which were discarded from the analyses.
Statistical tests were performed with SPSS software. All reported values are
means ± S.D.
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Results |
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In experiments with one stimulus sheep, when considering the 1 min interval centred on each location, test subjects remained more distant from the confined sheep when it was bleating than when it was silent (distance 11±4.7 m vs 8.1±4.1 m, means ± S.D.; paired sample t-test: t27=4.7, P<0.01). Further analysis revealed that the probability of bleating by the stimulus animal increased linearly with the distance from the test subject: y=0.0194x+0.0922 (r=0.95, N=13, P<0.01). To detect whether bleating by stimulus sheep attracted the test animals, we calculated the difference of distance between both sheep at time t and t+1 min (N=29). A negative difference indicates that test sheep approached the cage, while a positive one indicates that it moved away. We then calculated the ratio of the number of approaches to the total number of movements (approach + withdrawal), when the stimulus sheep bleated, and when it did not, during the corresponding 1 min interval for each test sheep. Comparison of the distribution of these two ratios revealed that the confined sheep's bleating did not modify the probability of approach by the test sheep (ratio with bleats: 0.51±0.23, without bleats: 0.48±0.22, paired sample t-test: t23=0.45, P=0.66).
General activity of test sheep
When the door of the releasing cage was opened, 70% of test sheep
immediately left the cage and 91% exited the cage within the 30 first seconds
(8±3 s, range 098 s). The sex of the stimulus sheep had no
significant effect on the proportion of instantaneous exits for either females
or males (females: one stimulus sheep of the same and opposite sex,
respectively: 0.13 vs 0.31, Fisher exact test: N=23,
P=0.39; two stimulus sheep: 0.26 vs 0.36, N=31,
P=1; males: one stimulus sheep: 0.25 vs 0.29, N=29;
two stimulus sheep: 0.32 vs 0.46, N=33, both P=1).
When pooling data, no significant differences between males and females were
found in the proportion of instantaneous exits with no stimulus sheep
(2 test, 0.43 vs 0.23,
21=1.63, P=0.2), with one
stimulus (0.27 vs 0.23,
21=0.14,
P=0.71) or with two stimulus sheep (0.37 vs 0.3,
21=0.38, P=0.54).
In the arena, all test sheep spent more than 75% of the 30 min grazing (median=88%; Table 2). When not grazing, the most common activity was standing with head up (9%); 25% of test animals were never observed walking and those that did walk spent little time on this activity (median=2%).
When alone, males spent more time grazing than females (t29=3.19, P<0.01; Table 2). Two-way ANOVAs revealed that the sex of stimulus sheep did not significantly affect the time spent grazing by test sheep (one stimulus sheep: F1,52=0.87, P=0.36; two stimulus sheep: F1,64=1.72, P=0.2). However, the sex of test sheep was significant: males spent more time grazing than females (one stimulus sheep: F1,52=36.7, P<0.01; two stimulus sheep: F1,64=21.6, P<0.01). No significant interactions were found (one fixed: F1,52=1.72, P=0.2; two fixed: F1,64=1.3, both P=0.26).
Spatial analyses
Experiments with no stimulus sheep
In the tests with two empty cages, both males and females walked relatively
large distances and explored on average 33% of the arena
(Table 3). Females dispersed
more rapidly in the arena, walked longer distances (Student t-test,
t29=3.24, P<0.01) and tended
to use larger areas (t29=1.86,
P=0.07) than males. The distribution of female locations relative to
the cages was similar to a random distribution
(Fig. 2A). Males tended to be
located more often at the periphery of the arena but they were uniformly
distributed in each angular sector (Moore test of circular uniformity:
R'=0.89, N=10, P=0.20). They were
found as often in the left and right halves of the arena and at similar
distances from the left and right cages
(Table 3). Female distribution
was slightly biased (R'=1.23, N=21,
P<0.05) as they more often used the angular sector of the
releasing cage (mean angular deviation to the releasing cage:
m=35°, second order test of the significance of
the mean: F2,19=3.47, P=0.05). They also
occurred more often in the right than in the left half arena (62±16% of
locations). However, no asymmetry in female location was detected when
considering the centroid of locations
(Table 3). Mean distance from
the cages remained stable over the 30 min test trial, except during the first
5 min within which sheep of both sexes slowly dispersed in the arena from the
releasing cage (distance to the nearest cage, respectively, during 05
min, 515 min and 1529 min: 10.3±3.1 m, 9±2.2 m and
9.2±2.3 m).
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Experiments with one stimulus sheep
The distributions of location density with one stimulus sheep differed
markedly from that obtained with no stimulus conspecific
(Fig. 2B,C). Test sheep of both
sexes stayed close to the stimulus sheep regardless of its sex, being most
often located in the corresponding half-arena
(Table 3). The attraction to
the stimulus sheep was clearcut during the experiment. During the first 4 min
following the release, sheep while grazing approached the cage containing the
stimulus more rapidly than in the experiments with empty cages (see nearest
location in Table 3).
Afterward, they diffused in the arena. Beyond these first minutes, sheep
tended to remain at a constant distance to the stimulus cage (distance to the
nearest cage during 05 min: 6.6±4 m; 515 min,
6.8±3.3 m and 1530 min, 7.5±3.2 m). This was also
observed in experiments without conspecifics, but the steady state was
achieved later and sheep were farther from the cages than in experiments with
one stimulus.
In the presence of one stimulus sheep, males' locations were concentrated
in the corresponding angular sector, regardless of whether the stimulus was a
male (Moore test for circular uniformity respectively,
R'=1.97, N=15, P<0.05; mean
angular deviation from the stimulus cage:
m=11°, second order test of the significance of
the mean: F2,13=44.95, P<0.05) or a
female (R'=1.54, N=14, P<0.05;
m=23°,
F2,12=10.36, P<0.05). Similar results
were found for females (female stimulus: R'=1.33,
N=9, P<0.05;
m=20°;
F2,7=6.64, P<0.05; male stimulus:
R'=1.76, N=14, P<0.05;
m=20°,
F2,12=14.75, P<0.05).
Within the first min, test females approached the stimulus sheep, whatever its sex, at closer distances than males. The latter approached the stimulus males more closely than the females. No significant differences between sexes were found regarding the distance of the centroid of location to the stimulus cage. However the sex of stimulus sheep and the interaction sex of test sheepxsex of stimulus were near significance. Males' locations (centroids) were closer to the stimulus cage when it contained a male than a female. In addition, males walked shorter distances and spread less than females. Test males also used smaller areas and walked less in the presence of a stimulus of the same sex than of the opposite sex (Tables 3, 4).
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Experiments with two stimulus sheep
The distributions of density location with two stimulus and no stimulus
sheep were similar (Fig. 2D,E).
After the first minutes following release, when the sheep spread out, the mean
distances to cages remained stable (distance to the nearest cage during
05 min, 10.3±3.5 m; 515 min, 8.2±2 m and
1530 min, 8.2±2 m), closer than in the tests with empty cages
but larger than when only one stimulus sheep was present. Females and males
used a smaller area and walked less with two stimulus sheep than without any.
One additional major difference with the one-stimulus experiments was that
test sheep did not approach any of the stimuli as closely either during the
first 4 min or during the entire 30 min session
(Table 3).
In contrast to what we expected, the presence of a same-sex sheep among the
two stimuli did not markedly affect the distribution and behaviour of test
animals, except that test females and males tended to graze nearer to the
same-sex than to the opposite-sex stimulus over the 30 min
(Table 3). Males also walked
more and used a larger area when a female stimulus was present than when not.
Males and females were found as often in both halves of the arenas when tested
with two same-sex and opposite-sex stimuli. The angular distribution of
females was uniform (Moore test for circular uniformity:
R'=0.83, N=17, P=0.17) when
confronted with two females, whereas they were more often located in the
sector of the releasing cage when confronted with opposite-sex stimuli
(m=16°;
F2,12=7.45, all P<0.05). Males also
occurred more often in the sector corresponding to the releasing cage in both
social contexts (same-sex: R'=1.18, N=19,
P=0.03; mean angular deviation to the releasing cage:
m=26°; second order test of the
significance of the mean: F2,17=6.15;
opposite-sex: R'=1.36, N=14, P<0.01;
m=27°; F2,12=10,
P<0.01).
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Discussion |
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Sex differences were observed in the behaviour of the subject sheep. Males
remained closer to peers of their own sex. They also spent less time grazing
and more time standing head-up when a female was present in the arena,
regardless of whether a confined male was also present. Sex-specific
attraction by females was unclear since they tended to remain at equivalent
distances from male and female peers. This does not necessarily imply that
ewes cannot discriminate the sex of conspecifics
(Kendrick et al., 1995;
Gelez et al., 2004
;
Pérez-Barbería et al.,
2005
). Females seemed more stressed than males, reflected in
longer distances walked and more frequent vocalisations. However, conspecifics
exerted a clear attraction. Whether stress provoked by the experiments could
explain the indiscriminate female behaviour is unclear: why did females not
reduce the interindividual distance to reduce distress? These results
therefore only partly support the social affinity hypothesis
(Bon et al., 2005
).
When confronted with two stimulus peers, sheep displayed clear differences
in behaviour when compared to the tests with a single confined peer. They
approached the stimulus sheep less closely and spent more time at an
intermediate distance between the two cages in the former than in the latter
situation. Their oscillating movements probably reflect conflicting motives to
approach one peer while remaining not too far from the second one, so limiting
their walking. This was perhaps possible because by doing so they were still
within, or near, the limit of the social distance. The behaviour of the males
when confronted with one or two stimulus males was striking. Contrary to what
was expected and found by Pérez-Barbería et al.
(2005), the presence of a
same-sex peer among the two fixed animals did not substantially modify the
subjects' behaviour. The ability to move in a large pasture area perhaps
explains why no clearcut choice was found, as in experiments with only one
stimulus peer. Whether social choice depends on the distance between stimulus
cages or on the possibility of moving around the cages remains to be
tested.
The results we found in the presence of two peers suggest that within this
distance scale, merino sheep stayed at mid-distance from both peers and thus
limited group splitting. We previously observed a group containing 15 adults
of both sexes for 7 weeks. While grazing, merinos congregated in a very small
surface area, which may reflect strong inter-individual attraction of sheep,
limiting spreading of the group (Michelena
et al., 2004). With respect to that study, we also note that
individual distances were close to the individual distance measured in the
present experiment (see also Michelena,
2001
). The stability of the mixed-sex groups might be explained by
a similar level of attraction of both sexes for females. However, we also
found that pairs of sheep of the same sex were more frequent than expected
(Michelena et al., 2004
).
Social discrimination of males, as reflected by inter-individual distance, is
one factor that may have played a role in this social segregation on a small
scale. However, other behavioural or social mechanisms, such as differences in
activity budget, movement speed, or avoidance of males by females, may
contribute to social segregation. Further experiments are needed to explore
how the number of freely moving individuals and possibly other mechanisms
interact to influence spacing.
Various authors have hypothesized the existence of an individual personal
zone within which repulsion is higher than attraction to peers
(Moody et al., 1997;
Shiyomi and Tsuiki, 1999
;
Couzin et al., 2002
;
Shiyomi, 2004
). Our findings
suggest, however, that the repulsion is very low or nil, taking into account
that the sheep were not able to engage in agonistic interactions and that the
stimulus sheep could not avoid the test subjects. In these experimental
conditions, it is not possible to determine whether movement away from the
confined peer corresponds to repulsion or to search for food combined with the
inertia of walking. The inter-individual distance does not appear to be the
result of a balance between attraction and repulsion forces, but rather an
effect of attraction exerted by peers on the exploratory behaviour and
mobility rate of grazing sheep.
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Acknowledgments |
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