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Environmental Enrichment in Captive Marmosets and
Tamarins
By Dr. Hannah Buchanan-Smith
"Hannah Buchanan-Smith does not believe that
marmosets should be kept as pets at all, but given that they are, the attached article
suggests ways as to how to enrich their captive lives."
The author discusses the three main
criteria which constitute a good captive environment.
They are: good physical health, breeding success, and an
animal's ability to acquire and retain behavioral skills
needed to cope successfully with his or her natural
environment. Through her field studies, the author has
learned that a variety in diet, innovative foraging
devices, indoor/outdoor enclosures, natural settings, and
a comfortable social environment are vital for the
well-being of captive primates. She illustrates how
altering conditions can promote natural behaviors in
captive marmosets and tamarins.
Introduction
Diet
and Foraging
Cages
and Furnishings
Social
Environment
Conclusion
References
About
the author
INTRODUCTION
Concern for the psychological well-being of captive
primates is not new, but a number of recent publications
have illustrated that it is perhaps becoming more
prominent. In this paper I shall briefly describe what
the criteria are for a good captive environment, and I
shall illustrate this with some recent studies which have
looked at how altering conditions can promote natural
behaviors in marmoset and tamarin monkeys. The same
principles can be applied to almost any wild animal kept
in captivity.
First, what constitutes a good captive environment? There
have been three main criteria put forward in a recent
article by Snowdon and Savage (1989). The first is a
veterinary medical criterion, defined as good physical
health and freedom from disease. The second is a
biological criterion, which basically relates to the
breeding success of the animals. However, this criterion
should be divided into two levels: breeding and rearing.
Many captive animals do breed successfully, but the
infants need to be hand-reared, because the parents will
not do so successfully. Generally the hand-reared
individuals are incapable of rearing their own young, as
they have lacked a normal social development. This is
particularly true of marmosets and tamarins, and I shall
be elaborating on this point later. The third criterion
is a behavioral ecological criterion, which relates to
the animal's ability to acquire and retain behavioral
skills they need to cope successfully with their natural
environment.
It should be noted that these three criteria overlap and
directly affect each other in that an animals' physical
well-being is directly affected by its psychological
well-being. For instance, it is now known that the social
environment can affect the immune system. Animals housed
in good social environments are better able to defend
against disease (Coe, Rosenberg, Fischer & Levine,
1987).
The starting points for developing a good captive
environment are to reproduce some of the salient features
of the wild environment, and to create opportunities for
captive animals to develop skills they might need in the
wild. Obviously, to be able to do this we require data
from the field. I have done research on the red-bellied
tamarin (Saguinus labiatus) and the saddle backed tamarin
(S. fuscicollis) in northern Bolivia, and I shall be
taking examples from my own data throughout the paper.
These two species of tamarins formed stable mixed species
troops (Buchanan-Smith, 1990). I collected detailed data
on the ranging behavior and activity patterns of the tamarins. I trapped individuals of both species and put
radio-collars on certain individuals, and then
radio-tracked them from dawn to dusk. This made them easy
to locate and observe what they were feeding on, and it
allowed me to follow them from a distance to find out
what sizes their ranges were and how often the two
species were together (Buchanan-Smith, 1990, 1991).
However, not all species of marmosets and tamarins have
been studied in the wild, and from those that have been
studied, we know that different species may behave very
differently. Before creating or improving a captive
environment for marmosets and tamarins, we must first
find out all we can about that specific species. If the
species has not been studied in the wild, we should look
to the data for the most closely related species which
has. The captive environment should then be modeled on
what is known about the natural habitat and behavior in
the wild.
Many would argue that there is no way to evaluate the
effect of environmental manipulations on psychological
well-being. Basically, my view is that a change in
behavior is shown to be beneficial if it becomes closer
to the natural behavior of the monkeys. This includes not
only the presence of the behavior, but the frequency of
it as well. For instance, not only is it important to
give the monkeys opportunities to forage for food in ways
that they do in their natural habitat, but they should
spend about the same amount of time foraging in captivity
as they do naturally.
I shall now go through examples of how researchers have
changed aspects of the environment of marmosets and tamarins, especially in three areas of the environment:
diet and foraging, cages and furnishings, and the social
environment.
DIET
AND FORAGING
We know that marmosets and tamarins have a very varied
diet in the wild. My research on the red-bellied tamarins
and saddle backed tamarins in Bolivia shows that the
tamarins consume fruits from at least 16 different
species of trees. They also consume nectar from flowers
(family Guttiferae; Symphonia globuliferae), and resin
from a bean-like pod (family Mimosaceae; Parkia pendula [Willd.] Benth ex
Walp.). In addition to this they spend
much of their time foraging for insects (Buchanan-Smith,
1990, 1991). Although I never saw the tamarins eat any
other animal material, field data from other species
indicates that they eat birds' eggs, frogs, and lizards (Neyman, 1977; Sussman & Kinsey, 1984).
Because of the diversity in their natural diet, it is
important to provide a wide variety of different food
types in captivity. However, we should remember that in
the wild, animals rarely encounter food in great
abundance, and often they must search for it. In the
wild, foraging occurs throughout the day and can occupy
up to 50-60% of the time available (Garber, 1984; Yoneda,
1984). Therefore, in order to more closely approximate
natural conditions, we should distribute food over the
course of the day and make it more difficult to find.
A recent study has demonstrated how introducing
unfamiliar foraging devices which are explicitly designed
to make it harder to secure food treats can have a
significant influence on the activity budgets of golden
lion tamarins (Leontopithecus rosalia; Molzen and French,
1989).
This species are described as being extractive foragers,
and feeding devices were fashioned to stimulate these
extractive foraging skills. These were food containers
with small holes drilled in them which were filled with
broken corn-cob and a few raisins. These devices were
suspended approximately 27cm below the top of the cage,
so that the only way the tamarins could get access to the
raisins was either by hanging upside down by his or her
hind limbs, which they are very proficient at doing, or
by sitting on the bowl and grasping one of the device's
suspension wires for support.
Once the tamarins discovered that the suspended bowls did
contain some raisins, the devices then became objects of
focused attention. To introduce uncertainty in food
availability, the tamarins were given both a baited and
an unbaited device. These devices were used in addition
to the normal rations which the tamarins received in
ceramic dog bowls. Behavior in normal feeding protocols
was compared with normal feeding protocols and the
foraging devices. The results show that time spent
actively exploring the environment increased, foraging
increased, and adults travelled more, while time spent
eating and drinking decreased, and adults rested less and
engaged in fewer social interactions such as grooming
when the device was present than when it was not. The
authors made no comparison between the activity budgets
of wild golden lion tamarins and their captive tamarins,
and so it is not known whether the changes in behavior
profiles drew closer to the activity budgets of the
tamarins in their natural habitat. However, because the
tamarins were using natural foraging skills which they
had not had the opportunity to use before, the change in
behavior was positive.
Another simple technique to increase time spent in food
acquisition is to spear whole apples or oranges on to the
end of a stick, like a bamboo cane, and suspend this from
a branch in the cage. Marmosets and tamarins will hang
upside down and spend much time picking off bits of apple
or orange (pers. obs.) in a similar fashion to how they
would forage naturally.
I prefer these foraging situations to scattering food
items in the wood shavings or other floor coverings,
which is another method of increasing foraging time
(McKensie, Chamove & Feistner, 1986). Many species of
marmosets and tamarins do not go to the ground regularly
in the wild, or if they do they are especially cautious
as they may be more vulnerable to predation. I do not
think that this technique of increasing foraging time
should be encouraged in captivity unless it is known that
the species does go to the ground regularly, and for long
periods, in the wild. The tamarins I observed in Bolivia
were extremely reluctant to descend to less than 2-3m in
the forest canopy. In relation to this, it should also be
noted that consideration should be taken about the
positioning of food dishes in the cage. A recent
observation on cotton-top tamarins showed that group
members carrying infants were reluctant to approach food
dishes placed near floor level. This was remedied by
placing food dishes at least a meter from floor level --
whereupon tamarins carrying infants readily approached
food dishes and fed (Snowdon & Savage, 1989).
Furthermore, by providing a meal in two sets of dishes in
larger groups, competition between group members may be
reduced, and each individual is more likely to get a more
varied diet and an equal share of the preferred food
items (Price & McGrew, 1989).
My final point on diet and foraging relates to gum
feeding in marmosets. Marmosets have teeth which are
specialized for gnawing holes in trees to get the gum to
exude, which they then eat. One study on the pygmy
marmoset (Cebuella pygmaea) reports that these monkeys
spend 32% of their total activity time in the procurement
and ingestion of gum (Ramirez, Freese & Revilla,
1977). To mimic gum feeding in the wild, as we see in the
marmosets, a simple inexpensive sap feeder has been
devised, which consists of sections of dowel drilled
length-wise with holes which are filled with gum arabic.
Captive common marmosets (Callithrix jacchus) readily
learn to gnaw at this device to extract gum arabic using
the full range of gum foraging patterns as in the wild
(McGrew, Brennan & Russell, 1986).
CAGES
AND FURNISHINGS
Marmosets and tamarins range over large areas in the
wild, and there is now a trend to release groups of
tamarins into woods, or on to islands which are obviously
more naturalistic settings (Price et al., 1989). Most
zoos provide both indoor and outdoor enclosures for their
marmosets and tamarins, and these outdoor enclosures are
particularly important as they give the monkeys the
opportunities to face the elements, take shelter from the
rain, and find sunny spots to bask themselves in. Outdoor
enclosures also often attract insects, and the marmosets
and tamarins will readily forage for insects, as they do
in the wild, if given the opportunity (pers. obs).
If their home cage cannot be reasonably sized in
captivity, it is important to provide the monkeys with
large exercise areas. These areas can be shared by
several different groups, and the monkeys can be given
voluntary access to these cages using plastic tunnelling
of 15cm diameter (Price & McGrew, 1990). This ducting
can also be used to move monkeys to new housing, and
obviates the need for catching and handling of monkeys,
which is likely to be stressful.
Let us now turn to cage furnishings. When the golden lion
tamarin (L. rosalia) reintroduction program began, the
tamarins appeared to be physically unable to cope with
natural substrates and were deficient in appropriate
locomotory behavior (Kleiman et al., 1986). So, if
possible, captive enclosures should be furnished with a
high density of natural branches as well as ropes to
simulate vines. These provide surfaces on which the claws
can get a good grip, and they should be arranged so that
they have a variety of textures, diameters and degrees of
firmness. Some of the branches should be quite firm so
that they do not give when the animal lands on them,
while others should be quite loose, so that the animals
must learn to accommodate their jumping to these
different surfaces.
As most marmosets and tamarins are highly arboreal, the
branches should be positioned well above ground level,
although many captive monkeys do not go to the ground in
captivity to forage for dropped food; therefore a few
branches should be positioned near the ground so that if
the monkeys are startled when on the ground, they can
easily leap to a higher position. The diameter and
orientation of the branches within the cage should also
be chosen with care. I found that in the wild, saddle
backed tamarins (S. fuscicollis) often locomoted by
jumping between vertical trunks, while red bellied
tamarins (S. labiatus) more often jumped from branch to
branch and used thick near-horizontal branches for
quadrupedal travel. Certainly from my own field
observations, it seemed that most social interactions
were performed on large horizontal or gently sloping
branches which were relatively out in the open --
possibly to give good predator detection viewing (pers.
obs.). A recent comparative study on captive
callitrichids has revealed that species do have
preferences for certain diameters and orientations of
branches (Seymour & Kinghorn, pers. comm.), so again
the important point here is to provide variability in
branch orientation and diameter.
Branches should obviously be cleaned to provide adequate
sanitation. To my knowledge, no research has been done on
the effect of cleaning marmoset and tamarin cages.
However, as scent marking is an important means of
communication for these monkeys, care should be taken not
to clean the branches too regularly as this might result
in abnormally high frequencies of scent marking. It may
be that it is best to clean only half the branches at any
one time, which would give the monkeys more stability in
their habitat. It may also be important to replace
branches in a new configuration, as this would reduce the
likelihood of any motor stereotypies and facilitate the
maintenance of the essential skill of acquiring spatial
knowledge of new environments (Kleiman, 1989; Redshaw
& Mallinson, 1991).
Cover should also be provided for animals, so that they
can hide if they wish to. At the Jersey Wildlife
Preservation Trust, marmosets and tamarins can freely
move between their indoor and outdoor enclosure, and the
indoor enclosure is out of bounds to the public, which
allows the marmosets and tamarins some degree of privacy
(Mallinson, 1975). They also have a reasonable amount of
dense natural foliage in their outdoor enclosures to
provide cover. If natural foliage cannot be provided to
give cover, hanging screens, such as strips of curtains,
can visually divide a large cage area, and this does have
positive behavioral results (Mackensie, Chamove &
Feistner, 1986).
My final point to note on cage furnishings is the benefit
of providing more than one nest box. If there is any
aggression in the group an individual may be excluded
from the nest box, and if there is only one, s/he would
not have a safe sleeping area. However, I know of no
research in this area.
SOCIAL
ENVIRONMENT
Marmosets and tamarins have a cooperative rearing system
where the mother generally gives birth to twins, and the
father and other group members care for the young by
carrying, possibly food sharing, and perhaps by looking
out for predators (e.g. Buchanan-Smith, 1984; Price,
1992; Rylands, 1985; Cleveland & Snowdon, 1984).
There are many published reports that if offspring are
removed from their group before they have had experience
with rearing infants, they have a much lower likelihood
of raising offspring themselves (S. fuscicollis, Epple,
1978; L. rosalia, Hoage, 1977; S. oedipus, Cleveland
& Snowdon, 1984, Snowdon, Savage & McConnell,
1985, Tardif, Richter & Carson, 1984a, 1984b). It is
recommended that marmosets and tamarins should have
experience with at least two sets of rearing episodes;
otherwise they will not make good parents themselves
(Snowdon & Savage, 1989). This applies to sons as
well as daughters, because fathers as well as mothers
care for the young. Most marmoset and tamarin keepers do
allow this, but I understand that there are still some
laboratories which remove individuals from the group
before they have had this experience, either for testing,
or because the cage is too small to house a greater
number of monkeys. The problem is that once this habit
has started it is difficult to reverse.
If it is really not possible to keep marmosets and
tamarins in large family groups, giving them opportunity
for a good social development and social activities such
as allogrooming, infant care, and in some species food
sharing, then there are ways around this. Giving monkeys
the opportunity to watch others may increase their
quality of life, although being in continual close visual
contact and proximity may be stressful for them. A neat
way around this is to allow monkeys an opportunity to
peep through a small hole at a neighboring group. A
recent study on cotton-top tamarins (S. oedipus) found
that when a small peephole was made (initially by
accident) group members were keen to use it to observe
their neighbors (Moore, Cleland & McGrew, 1991).
Their neighbors did not know they were being watched and
so it is unlikely that it had any detrimental effects on
them.
Another way to provide a varied social environment is to
keep marmosets and tamarins in mixed exhibits (Xanten,
1990). My personal feelings are that if mixed exhibits
are to be set up, they should be between species which
are sympatric in the wild, which not only is likely to be
more successful, but which also provides a more realistic
zoographic enclosure with greater educational value.
Tamarins often form stable mixed associations with other
tamarins -- such as the saddle backed and red-bellied
tamarins I studied in Bolivia. These two species spent
85% of their time within 50m of each other and often much
closer, and the associations were long lasting and stable
in that each mixed species group shared a common
territory which they jointly defended against neighboring
mixed species troops (Buchanan-Smith, 1990). Saddle
backed tamarins also form stable associations with
emperor tamarins (S. imperator, Terborgh, 1983) and with
moustached tamarins (e.g., S. mystax, Garber, 1988), and
black mantle tamarins (S. nigricollis, Hernandez-Camacho
& Cooper, 1976). We have recently set up mixed groups
of red-bellied tamarins and saddle backed tamarins
successfully at Belfast Zoological Gardens, Northern
Ireland. Further details are provided in: Hardie, S.M.,
Day, R.T. & Buchanan-Smith, H.M. (1993) Mixed species
Saguinus groups at Belfast Zoological Gardens.
CONCLUSION
There is a clear relationship between the environment and
behavior. An impoverished environment leads to a decrease
in social behaviors such as grooming, playing and other
behaviors such as scent marking and locomotion (C.
jacchus, Schoenfeld, 1989). Furthermore, there is clear
evidence that environmental stress can also affect the
reproductive success of marmosets. A recent study has
demonstrated that parity was suppressed and the number of
spontaneous abortions increased when a common marmoset
(C. jacchus) colony was disrupted by nearby construction
work (Johnson et al., 1991).
This has been a rather a brief outline of the many
different aspects of how to improve conditions in
captivity and promote naturalistic behaviors. Already
many zoos and laboratories are implementing environmental
enrichment techniques, not only to improve the quality of
life of the monkeys but to enhance the education value of
zoo exhibits.
I should like to end by emphasizing the importance of
collecting behavioral data to determine if the change you
have made in the environment has actually had the desired
effect. This data collection will give you some objective
measure relating to how the behavior has changed. The
different data recording techniques and information on
how to set up a scientific study to measure behavior are
provided in Martin and Bateson (1986) and Shepherdson
(1989).
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About
the author
Hannah Buchanan-Smith
Ph.D.
University of Stirling
Stirling, Scotland
Dr. Hannah Buchanan-Smith graduated from St.
Andrews University in Scotland with a B.Sc. in Psychology
in 1985. As part of her degree, she studied marmosets at
the Jersey Wildlife Preservation Trust. She went on to
Reading University, England to conduct her doctoral
research, which combined both behavioral observations of
captive tamarins and field research on tamarins and other
primates in Bolivia.
Since completing her Ph.D., Hannah has
conducted research and taught at St. Andrews and Stirling
Universities in Scotland.
For more information, the author can be reached at Department of Psychology, University of
Stirling, Stirling, FK9 4LA, Scotland.
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