INTRODUCTION
Recent interest in the welfare of captive animals has led to the
use of techniques to stimulate normal patterns of behaviour and
maintain healthy, reproductively viable individuals.18,19 Techniques include
naturalistic methods such as foraging and clearly artificial ones,
as with a variety of problem solving devices.10 Such techniques are
relatively high profile in that they may create an 'immediate'
change in the time budgets of behavioural activities in a more
'favourable' direction, i.e. individuals spend less time engaged
in activities that are considered to be counter-productive to
their welfare.15 Many laboratory animals however, do not live in environments
that are specifically designed to enrich their behaviour. In fact,
experimental protocols frequently require forms of standardised
and uniform environments. In such cases the cages used are often
determined by commercial constraints and folklore among institutions.
Moreover, National and International guidelines of the dimensions
of cage sizes and furnishings for different species are based,
for example, upon body weight and postural propensities and not
upon empirical comparisons of behavioural and/or physiological
responsiveness among animals in commonly used conditions of laboratory
housing. This is an omission both on welfare and scientific grounds.
We advocate that one critical aspect of welfare studies should
be to compare directly the behaviour of the same species of animal
in different, commonly occurring laboratory conditions, including
variations in temperature, humidity, light, cage size and furnishings.
Cage size, for example, is an especially contentious issue and,
in the absence of comparative research, people tend to assume
that increases in space for the same social density and composition
will be automatically beneficial in stimulating activities such
as locomotion and exploration. In fact, studies with different
species of callitrichid for instance, have shown that this is
not necessarily so.3,13 Moreover, studies with various primate taxa show that
the issues are complex, and deserve close scrutiny for different
species.2
The present report concerns the cotton
top tamarin (Saguinus oedipus oedipus). This species is
of interest on welfare grounds due to its endangered and highly
precarious position in nature, its frequent use in biomedical
research, and the fact that it does not do well under a variety
of 'standard' laboratory maintenance. Indeed, attention has been
drawn to high incidences of infant mortality and abortion; in
short, to poor breeding success.11 Among those few establishments that have maintained
healthy viable breeding colonies of cotton tops, it has been observed
that association with large complex and changing environments
in which there is variety and frequent social and physical stimulation
is of benefit.20
The aim of the present study was to compare the behaviour of pairs
of tamarins in conditions that are more frequently found in laboratories,
and in which for economic and other reasons, specific programmes
of enrichment and variety are not provided. It was of particular
interest to compare the behaviour of tamarins in a commercial
custom built rack system with that which provided considerably
more space and furniture with reference to equivalent social density.
Further, single adult male female pairs of tamarins were selected
because this is the breeding unit that is set up for callitrichid
species in captivity.
METHODS AND MATERIALS
A total of seventeen adult male, female pairs of cotton tops were
observed. Their ages ranged from 3 to 9 years. With the exception
of one of the pairs, none had bred successfully.
Condition I
Eight pairs were selected at random
from a total of sixteen pairs, housed together in one room that
contained two horizontal rows of eight cages, with one row independently
racked above the other. Each cage measured 1.0 m wide x 0.7 m
high and 0.5 m deep. It was equally divided vertically with a
wooden dowel as a perch along the length of the cage. [FIGURE
I].
Two observers simultaneously scanned the
behaviour of separate pairs of animals from within a hide which
made them invisible to the monkeys. Observations were made between
11 a.m. and 3 p.m. on three days per week (Monday, Wednesday,
Friday) over a period of seven consecutive weeks. Each pair was
observed for 10 min per session with the prearranged order in
which the pairs were watched, randomised over days. A maximum
of four, 10 min observations was made on anyone group of tamarins
on anyone day. A total of 2,400 ten-second time samples of behaviour
was recorded for each animal in this condition.
Condition 2
Three pairs of cotton tops were included. Two of these pairs
lived in one room with no other tamarins present. The third pair
was one of two pairs living in a different, but identically arranged
room. All these monkeys lived in wooden frame and wire mesh cages
of dimensions 1.7 m high x 0.75 m deep and 0.9 m wide. The cage
furniture consisted of a nest box (as in Condition 1, but
made of wood), two triangular platforms, and three branches -
one horizontally across the cage, and two vertically across the
cage at 45º [Figure 2].
As before, observations were made on the behaviour of each pair simultaneously - from a hide, 2,400 ten-second time samples of behaviour were recorded per animal, this time over 5 days per week during a five consecutive week period, with the order of pairs again randomised.
Condition 3
Six pairs of cotton tops were distributed among three rooms with
each of the two pairs per room living in a cage that measured
1.6 m x 2.4 m x 2.0 m. Branches were placed horizontally across
the room at two levels, and a wooden nest box was also provided
as in Condition 2 (Figure 3).
The pairs were simultaneously observed
by one of us (BR) for a total of 3000 thirty-second time samples
of behaviour over a period of twenty five weeks. Once again, the
order in which the pairs were observed was randomised. There was
no hide but the animals were well accustomed to the observer as
these observations were part of a larger project.
In all conditions, the tamarins were fed an ad lib diet of monkey
chow, fresh fruits, vegetables and animal protein. Humidity levels
ranged around 55-60%. The temperature in the three conditions
varied in that Condition 1 was maintained at around 76°F (±2)
with that in the other conditions at around 74°F (±2).
All the keeping rooms were lit by artificial lighting for 12 hours
per day. Rooms in the first two conditions also had a single opaque
window in one end wall.
Categories of behaviour
Behaviour was recorded directly on to data sheets, and cued electronically
into ear pieces for the observers. The categories were:
- Movement - involving all four limbs.
- No movement - in which a monkey was not moving but did not engage
in another recorded activity such as grooming.
- Huddling - stationary side to side body contact.
- Autogrooming - manipulation of an animal's own pelage.
- Social grooming - close visual inspection and manipulation of
the pelage of another animal.
- Feeding - ingestion of food items.
- Drinking - taking water from water bottle.
- Stereotyped behaviour - repetitive atypical behaviour of the
normal repertoire for the species.
In addition, recordings of proximity, i.e. when individuals were within 30 cm of one another (for whatever activity except moving) was observed in Conditions 1 and 2. A similar constraint applied to observations of the animals present in their next boxes. Finally, we decided to record the total instances (within a number of 10 sec. intervals) of both scent marking (with anogenital and suprapubic separately) and aggression, regardless of their occurrences at time sample intervals. Aggression was recorded when one individual threatened or attacked another.
RESULTS
The occurrence of the categories of behaviour was calculated as
an average percentage of the total observation sample for each
of the three conditions.
Statistical comparisons were made initially on these common categories.
Because no difference in behaviour was found among males and females,
that is no correlation (Spearmans, rho) was found within male/female
pairs for any condition, comparisons of all categories of behaviour
were made by Mann-Whitney U test (two tailed). The only significant
difference was that females scent marked anogenitally more than
males in Conditions 2 and 3 (U = 3.5, df=8, p<0.05). No such
difference was found in Condition 1.
A central interest was to test for significant differences among
common behavioural categories in the relatively small, 'medium'
and large cages; comparisons were made by using a Kruskal-Wallace
test. Two significant differences were found. The tamarins in
Condition 3 (the largest) were significantly more active in terms
of gross locomotor activity (movement category) than those in
and between Conditions 1 and 2 (k=1694.6, k=166.3, p<.01).
There was also significantly less close physical contact (huddling
category) within pairs in condition 3 than those in and between
Conditions 1 and 2. It was of particular interest however, to
find that stereotyped behaviour (head bobbing) was only observed
in Condition 1 and among females especially. We may note that
not all the females exhibited the behaviour, but that it was a
prevalent activity that we have never observed under any other
laboratory condition. Subsequently, it was of interest to examine
whether there were significant correlations between the behaviour
of tamarins which lived in the same rooms. In fact, there were
not. Moreover, the arrangement of condition 1 gave an opportunity
to compare the behaviour of animals caged in different positions
in the room (Mann-Whitney). The eight groups that we observed
were labeled from left to right in each case, A,B, 1 and 2 on
the top rack, and C, D, 3 and 4 on the lower rack. We found that
those tamarins that were housed on the left hand (window) side
of the room showed significantly more gross locomotor behaviour
than those on the right hand side. Groups A+C vs 2+4 (df=4, U=0.00,
p<0.05) - groups A+C+B+D vs 1+2+3+4 (df=8, U=5.0, p<0.01).
Again, those tamarin that were housed in the top bank of cages
1+2+A+B showed significantly more close physical contact (huddling)
than those housed on the bottom bank 3+4+C+D (df= 8, U=8, p<0.01).
They also showed significantly less behaviour recorded as 'non-movement'
than those housed on the bottom bank (df=8, U=1, p<0.01). No
other significant differences in any other category of behaviour
was found in either of these regards.
Finally, we may comment briefly on differences in those categories
of behaviour that were recorded in Conditions 1 and 2 only. For
example, despite considerable differences in the space available
between these conditions, the tamarins spent similar amounts of
the observation time in their nest boxes. The males were very
similar in this regard with the females in each case spending
more time than their pair mates.
We also recorded more drinking in Condition 1. Given that this
applied to both males and females, the differences are likely
to be attributable to differences in the amount of water available
in the diet, and for the higher temperature in Condition 1, than
as suggesting reproductive condition (as early pregnancy) in the
females, for instance.
Further, our measures of proximity within pairs of tamarins in
Condition 1 were nearly twice those of Condition 2. This may be
hardly surprising given the overall size differences of the cages.
However, these differences do not necessarily indicate any measure
of social integration. Differences between the two conditions
in close contact scores, for example, were not significant.
DISCUSSION
Our results show significant differences in the behaviour of pairs
of cotton top tamarins maintained in different conditions of housing.
One such difference, and one that might not have been intuitively
suggested, relates to the relative position of cages in a single
keeping room (Condition 1). Hence, those pairs of tamarins that
lived in cages in the half of the room nearer to the one opaque
window, including both top and bottom racks in this half, were
more active (gross ambulation) than those housed on the other
side. Further, the animals that lived in the top rack of cages
in the whole room engaged in more close contact amicable behaviour
of huddling, and less behaviour recorded as inactive, than those
on the bottom rack.
There are few reports from which hypotheses are suggested to account
for such findings, but one variable that is at least partially
relevant concerns the relative amounts of light available in the
room. Hence, although we did not actually measure levels of illumination
in the different areas, there are similar findings to our own,
albeit in another callitrichid of a different genus. The results
are worthy of discussion for their implications for laboratory
management. Hence, Heger and Neubert (1988) describe the maintenance
of a colony of common marmosets (Callithrix jacchus) in
which male, female pairs lived in cages 70 x 70 x 50 cm. Some
pairs lived in rooms that were darker than the original colony
room in which marmosets continued to live.
Breeding records showed a lower breeding rate for these marmosets,
than for those in the lighter, original room. Moreover, because
records were taken over several years, it is reasonable to discount
the influence of disturbance by moving the animals. Further, subsequent
manipulation of relative illumination levels confirmed the novel
finding.8 Again,
differences in fertility were also found between animals living
in upper racked (lighter) cages than in lower ones. Most important,
breeding success (pregnancy rate and litter size) could be reliably
increased by manipulating light levels. We have no records of
the long term breeding success on the cotton tops in our Condition
1, but they were not breeding successfully at the time of our
observations. In our study, different levels of illumination were
linked to significantly different levels of locomotion. This is
similar to Scott's (1991) finding for a system in her laboratory
in which single common marmosets, housed in two tier racks in
cages 75 cm high x 50 cm wide x 60 cm deep showed significantly
less locomotor activity in the lower tier than in the higher,
lighter one. It is difficult to know whether the animals in lighter
conditions gained any advantage in terms of 'well being'. Certainly
activity is important to prevent joint stiffness for example,
but it is not necessarily the case that a lower level of activity
has deleterious effects. It is critical, however, that light per
se, can clearly be influential in stimulating behavioural and
reproductive activity. There is also information to suggest interesting
and therapeutic influences of light and visual stimulation in
ways that are, as yet, inextricably mixed.
Some studies have shown an advantageous influence of access to
windows upon health and mood in humans21,17 which in this context one notes that rotating monkeys
into lighter, more visually stimulating areas in a keeping room
may present a valuable source of environmental enrichment.
Another interesting aspect of the results from the present study
concerns the fact that observers frequently encounter the concern
that the behaviour of particular animals or social groups are
indeterminately influenced by the behaviour of the animals in
the same immediate environment; that such influences may turn
out to be uncontrolled variables in many studies. It was of interest
to test for this effect in our study, and to find that there was
no such pervasive influence. It was also of interest to examine
the occurrence of gender differences in behaviour. In fact, the
only significant difference here, and one that is in line with
many reports in the literature;2 is that females scent marked more anogenitally than
males in both Conditions 2 and 3, but not in Condition 1. It is
unusual to find a captive situation in which females living with
males do not scent mark more. The reasons why this should not
have been the case in Condition 1 remain obscure.
A central point of concern of our study related to the potential
influence of space per se. The cages of the three different conditions
of housing varied considerably in overall space; they also varied
in the quantity of cage furniture available. However, none of
them was purposefully 'enriched' and represented types of cages
which are routinely found in different laboratories. We might
expect, as indeed we found, that tamarins living in Condition
3, in which the space was considerably larger than in either of
the other two conditions, moved around more. On the other hand,
it is worth noting that the present arrangement of our common
marmoset colony at Reading involves family groups living in large
cages 2 m wide by 4 m long by 3 m high. Here we find that adult
pairs (and especially males) move around relatively little; they
move around less than before in smaller cages and they tend to
maintain locational 'stations' spatially independent of all other
individuals for much of the time (Box and Smith, unpublished data).
In any case, it is important to point out that the interface between
space and social opportunities to express patterns of social interactions
among individuals of different age and gender is complex and a
largely unexplored area in animal welfare. However, in the present
study, no significant differences in locomotor activity was found
between Conditions 1 and 2. This may be regarded as an unexpected
finding given that the two conditions varied considerably in available
space. All this assumes that a major advantage of additional space
is to promote locomotor activity. It is also important,of course,
to examine the quality of interactions within social units of
individuals. Two points are salient here. One is that there was
no significant difference in close amicable behaviour as evidenced
by huddling at least, between the smaller commercial unit and
Condition 2. In fact, the significant difference in this regard
was that close contact was less frequent in the much larger Condition
3, where the animals moved around more. If we take into account
that there was no significant difference among the tamarins in
their social (and autogrooming) activities, and that neither was
there any difference in their overt aggressive behaviour (which
was very low anyway) then there were no 'immediate' social behavioural
indicators of response to environmental 'stressors.' On the other
hand, it is significant that we observed a stereotypic head bobbing
behaviour in Condition 1 only, and that this was far more prevalent
among females than males. Quite why there should be such a marked
gender difference in this respect is unknown, but it is certainly
worthy of further consideration from theoretical (stress responsiveness)
and practical (animal welfare and management) points of view.
Moreover, ' small cage' size has long been associated with stereotyped
movements in a wide variety of species6 and there are numerous
examples with primates.4,16,5,2 There does remain, however, the question of the extent
to which stereotypic movements indicate poor animal welfare. There
are those who argue in favour of such a view1 and others12
who claim that the argument remains open. Certainly, in our study,
we had no clearly unambiguous indicators of poor welfare such
as self mutilation. Moreover, if we allow the ambiguity of the
reference of stereotyped behaviour, then there are no obvious
and immediate behavioural grounds for choosing among the three
different conditions of housing that we used in this study. On
the other hand, the absence of clearly deleterious behaviour does
not necessarily lead us to advocate the environments we have described.
It is our belief that on both scientific and welfare grounds,
these animals are much better kept in enriched conditions that
take more account of their species propensities and characteristics,
and especially if we wish to promote successful breeding. However,
at this stage, we must also allow that although there is much
assumption about the deleterious and advantageous influences of
different types of laboratory caging for the health and welfare
of simian primates, empirical comparisons are rare.5 Moreover, studies of the influence
of environmental variables, such as cage size, require careful
methodological consideration. For example, one technique for comparing
the influence of specific cage conditions is to record behaviour
in one area, and then move the animals to the other area. In these
cases, the possibility that individuals are initially responding
to novel features of the 'new' environmenr4 should be allowed for by sufficiently long term observations
to reach acclimatisation. Another method of course, is to adopt
a cross sectional approach in which the equivalent social density
and structure of particular species are compared in different
degrees of the spatial density in which they are normally kept.
Both approaches are potentially useful and complementary in different
contexts. We adopted a cross sectional approach in this study
in order to answer some practical questions. Perhaps the most
important point to emphasise at this preliminary stage is that
sets of identically designed cages in a system that looks very
simple, with minimum expense and maintenance, that are arranged
economically with regard to the number of animals per unit space
may not, in fact, provide 'standard' laboratory conditions. The
implications of such findings should be recognised by those working
in laboratory animal science.
Acknowledgements
B.R. wishes to thank the British Council
for their financial support of her work at Reading University.
Special thanks are due to Adam Terlecki for all his help and friendliness
during the observations in Condition 1.
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