THE MANAGEMENT AND
HUSBANDRY OF GEOFFROY'S
MARMOSET
BY VAL WAKENSHAW
9 Park Court, Chillaton, Lifton, Devon PL16 OHN, U.K.
Introduction
Geoffroy's marmoset (Callithrix geoffroyi) originally occurred throughout
the Atlantic forest area of southern Bahia, Espirito Santo and adjacent
parts of Minas Gerais in south-eastern Brazil. Through habitat destruction
and capture for the pet trade, it is now restricted to small forest fragments
and has been pushed into the 'endangered' status.
A general husbandry survey was devised and distributed to 15 collections
exhibiting the species, of which seven (46%) responded. These were Banham
Zoo, Belfast Zoo, Colchester Zoo, Jersey Wildlife Preservation Trust and
Shaldon Wildlife Trust, U.K.; Emmen Zoo, the Netherlands; and Zoo de La
Palmyre, France.) The survey was designed to be relatively quick and easy
to complete, with questions covering the following subjects: group structure,
social interaction, breeding, development and care of young, nutrition,
feeding, environmental enrichment, housing and behavioural enrichment.
Geoffroy's marmosets are relatively uncommon in captivity, and it is hoped
that the data collected will continue to encourage and improve the management
and welfare of the species.
Social structure
C. geoffroyi are diurnal primates and depend primarily on vision,
smell, sound and display for social recognition. Social groups in the wild
vary in size from three or four up to 20 individuals. While marmosets typically
form groups which contain a number of adults of each sex, breeding is usually
restricted to the dominant pair. Infant care and carrying is predominantly
by the male, but all group members will participate. This releases the
female from the energetic demands of pregnancy, lactation and infant carrying,
which she would otherwise be constantly forced to endure. The infants are
weaned and independent at about 5-6 months, reaching sexual maturity at
about 15-18 months.
In captivity, offspring should remain with their parents for at least this
length of time to ensure that they have gained experience in infant care
and other normal behaviour. Inexperienced youngsters who have not had the
opportunity to care for younger siblings sometimes destroy their first
- and possibly successive - litters. However, a family group should not
extend to more than about 12 individuals, as above this number stress-related
illness may break out or some group members may be evicted. The dominant
pair are recognised and respected by all the group. Dominance is enforced
by scent-marking, scolding, cuffing or eye command, never biting. This
mild form of discipline seems to work well and the offspring never seem
cowed. The dominant behaviour of the breeding female, accentuated apparently
by pheromones produced in her scent glands, inhibits ovulation in subordinate
females, who are thus normally unable to breed as long as they remain in
the group. But there is less of a hierarchy among the males. In fact, while
only one of the males normally mates with the breeding female, more promiscuous
behaviour has sometimes been observed, and marmosets appear to be among
the few mammals which may under certain circumstances mate polyandrously
(Ferrari, 1989).
There is always a certain amount of upheaval when a dominant animal dies,
and incest can occur when the normal group structure breaks down (pers.
comm., D. Wormell). At Jersey, after the death of the breeding male, a
new male was introduced but was attacked by the original male's sons (see
Table 1 [not reproduced]). In the light of this episode, it may be advisable
to set up a new alpha pair in a different enclosure from the previous male's
sons. No reason was given for the aggression between the breeding female
and her daughter at La Palmyre Zoo.
Grooming
Mutual grooming is an important behaviour in the social lives of C.
geoffroyi. Not only does it serve a hygienic function in keeping the
skin and pelage in good condition, but it may also help to strengthen affiliative
bonds within the group. At Shaldon, grooming most often occurred with either
the male being groomed by an offspring, or the female being groomed by
the male. Mutual grooming sessions appeared to increase when the animals
were re-housed to an outside enclosure, although it may have taken place
unobserved in the privacy of the nest box when they were housed indoors.
When a 'groomee' solicits grooming, he will lie down flat facing the groomer
in an inviting position. As he is being groomed he relaxes completely,
with an air of total contentment, only moving to present a different part
of his body for inspection. The groomer slowly searches through the fur,
separating the hairs with the fingers and claws, watching intently for
any foreign bodies, which are picked up with the lips and/or teeth. Groomer-initiated
bouts appear to be concentrated on accessible sites, while groomee-initiated
bouts generally involve less accessible sites, e.g. head, neck, and back.
Vocalisation
The following vocalisations were noted in juveniles:
'Phee' - a high-pitched distress call. Response to being forcibly dismounted
by an adult carrier. A fundamental vocalisation that develops into the
adult contact call.
'Tsik, tsik, tsik' -a sharp, loud distress call. Response to extremely
rough treatment by mount. It develops into the adult alarm call.
'Nga' - distress squeal. A contact call which stimulates adults to nursing
response.
'Twitter' - a rapid sequence of short, high-pitched notes. A contact call.
The number of notes in the twitter varies according to age, infants giving
2-12 notes, adults 2-20 notes. (Epple, 1968).
Adult calls are very similar to the juvenile ones, but more stereotyped
and specific in function.
Courtship behaviour
C. geoffroyi establish contact by sniffing each other's muzzles
and genitalia. This activity, combined with marking objects, licking, grooming
and huddling, is a regular part of pre- and post-copulatory courtship.
As the female nears oestrus, both partners will increase associated behaviour.
There may be some tension and aggression before both reach their sexual
peak. Female oestrus cycles vary from 14 to 21 days. The post-partum oestrus
takes place at from two to 14 days after giving birth, at which time conception
can take place. Post-partum copulation reinforces the pair bond at a time
when the dominant male is essential for the care of the young. The gestation
period is usually 140-149 days, with an interval between births of approximately
150-160 days.
Of the zoos surveyed, four (57%) observed courtship behaviour.
Birth and the newborn
Most births take place at night or in the early hours of the morning. Normally
twins are born, but singletons and triplets also occur. Triplets can present
problems, as the female only has two nipples. In captivity, hand-rearing
would be a possibility, but the constant care and carrying required by
the infants would make it unlikely that more than one or two young of a
litter of three would survive in the wild. Labour may take up to an hour
and infants are born at 2-3 minute intervals. The male is present at the
birth and may assist by licking the film of mucus from each baby, before
handing them back to the mother for suckling. Other members of the group
may watch or assist by helping to eat the placenta. Newborn infants instinctively
grasp the mother's fur and find a nipple unaided. She will suckle the infants
at the same time. After their feed, the male takes each infant and places
them on his back. He alone will carry the infants for the first week. After.
this, all members of the family group try to take turns in carrying.
In captivity, to allow the female time to recover for the first week after
the birth, the group should be disturbed as little as possible, with the
exception of a quiet, familiar keeper to ensure that she is receiving adequate
nutrition and that all is well.
Nutrition
In the wild, C. geoffroyi eat a wide range of foodstuffs, including
small birds and mammals (e.g. nestlings), eggs, lizards, frogs and crustaceans,
plus fruit, flowers and tree-buds, insects, and essential amounts of resin.
In captivity a varied and balanced diet should be provided. Food may be
presented more than once a day, ensuring that all the essential food groups,
minerals and vitamins are given in the first feed of the day when the animals
are hungry. Later feeds can supply favourite foods and extras. These can
be foraged for to prevent boredom or used in feeding enrichment activities.
The first feed of the day could contain a nutritionally balanced pellet.
Although these are not popular with all animals, palatability can be improved
by soaking in a fruit drink. This may be preferred by infants. Marmoset
jelly is another product designed to provide the majority of the daily
nutrient requirements, and can be mixed with pieces of fruit to enhance
flavour. This would be beneficial for pregnant and nursing mothers and
infants, or animals in poor health, although care is needed not to give
too much. Rovimix D3 powder may be given with combinations of Milupa baby
cereal or baby milk to provide a sweet nectar breakfast.
Marmosets especially need vitamin D3 in their diet. It is essential for
metabolism of calcium and phosphorus for bone formation. In nature, animals
obtain Vitamin D3 by conversion of pro-vitamins in the skin, through exposure
to ultraviolet light from the sun. In captivity, requirements vary with
season, sunlight and temperature. Therefore a supplement has to be added
to the diet. A concentrated vitamin D3 powder can be obtained from Roche
Products Ltd. Other products that can be given to increase the animals'
vitamin intake are Cytacon B12, Abidec and SA37 (see products list, below).
Wild marmosets may spend up to 70% of their time foraging and processing
food. In captivity the animals are provided with a nutritionally balanced
diet, but a meal may be consumed in a matter of minutes, leaving long stretches
of time before the next feed. More naturalistic feeding can be encouraged
by feeding-enrichment activities. This is particularly important for animals
which are to be released into a wild environment where a knowledge of how
to forage is essential. Foraging behaviour can be encouraged by feeding
many items whole or by hiding or scattering food around the enclosure,
e.g. on platforms, wire roof or branches. However , care must be taken
not to let the food become contaminated by bird droppings. Live food such
as locusts, crickets, stick insects and mealworms can be scattered in the
substrate. Retrieving this food requires hand-eye coordination and concentration
and is very intensive. Hand-made insect dispensers can be inexpensive to
make and effective in use, and also create an element of unpredictability.
Marmosets' small size, quick movements, sharp claws and long lower incisors
are well suited for effective capture of insects. Wild callitrichids spend
16-39% of their time foraging for, and feeding on, insects. (Terborgh,
1983; Garber, 1984).
Jersey Wildlife Preservation Trust suggests, however, that the phosphorus
content of insects needs to be balanced with a calcium intake in order
to maintain the ideal Ca:P ratio of between 1:1 and 2:1, as an imbalance
in this ratio can retard skeletal development, impair locomotion and decrease
reproductive output, and is therefore especially problematic during lactation
(Price, 1992; Garber, 1984). One way of increasing the marmosets' calcium
intake is to provide plant gums, which are high in calcium and form an
important part of the diet of wild marmosets. Gum feeding takes up as much
as 34% of their time in the wild (Coimbra-Filho and Mittermeier, 1976).
In addition, gums are rich in carbohydrates and may therefore be an important
source of energy for marmosets, especially during lactation.
C. geoffroyi are very proficient gum feeders. They gouge small wells
with their lower incisors, by using the upper incisors as an anchor in
the bark, and lap the exudates which ooze from the holes. Naturalistic
gum-feeding behaviour can be simulated by providing an artificial gum tree,
by smearing branches with gum, or simply by providing a small bowl of gum.
Six (86%) of the zoos surveyed used some form of feeding enrichment. Four
used insects in those activities, three mentioned insects as a preferred
food, but only two provided gum. (See Tables 3 and 4 [not reproduced].)
Medical problems
Belfast - Original breeding female lost weight and condition and
eventually died. Nutritional? (Pers. comm., M.G. Challis, Assistant Manager.)
Colchester - Male had a brief period of appearing 'under the weather'.
Symptoms included loss of appetite and condition. He was wormed as a precaution
with 0.05 ml Ivomec, and also given 0.05 ml Laurabolin steroid. He responded
well to this treatment. In addition, the female had a Caesarean birth for
her first litter of twins. Neither survived, but she made a full recovery
and has bred since. (Pers. comm., Dr.J. Lewis, International Zoo Veterinary
Group.)
Emmen - Problems were experienced in the adoption of a new diet,
mainly with animals who came from M. Schwarz, Brazil. The condition mostly
proved fatal in the end, in combination with pneumonia and neuritis worm
infection. (Pers. comm., H. Hiddingh, Director.)
Jersey - In the past they had bone problems, diarrhoea and pseudo-
tuberculosis. These seem to have been related to calcium deficiency. Health
improved once gum Arabic was provided. (Pers. comm., D. Wormell, Section
Head, Marmosets and Bats.)
La Palmyre - Haemolytic anaemia, possibly related to Vitamin E deficiency
and resulting in a wasting disease. (Pers. comm., Dr. T. Petit, Veterinarian.)
Of the medical problems recorded, those related to nutrition were the most
common, with incidences of bone problems, wasting disease and anaemia.
Vitamin D deficiency and also an incorrect calcium/phosphate ratio can
result in rickets and osteomalacia. As already stated, Jersey found that
health and also breeding success improved once gum Arabic was provided,
in conjunction with the correct ratio of phosphates. At Shaldon, also,
gum is provided for the animals, and no health problems have occurred.
Other medical problems were pseudo-tuberculosis and pneumonia, which may
be caused by bacteria or viruses, and can be passed on to the animals by
humans; early veterinary treatment is essential.
Worm infestation may be more easily remedied as long as there are no complications.
Medication can usually be given via food to reduce the stress of handling.
Environmental enrichment
A wild marmoset has to avoid predation, interact appropriately with
conspecifics, forage and find refuge in an ever-changing environment. Environmental
enrichment is an attempt to bring some of this diversity into the enclosure
of the captive animals, thus preserving not only genes but also behaviour-
an important consideration if the animals are ever to be returned to a
wild environment. Enrichment can be applied to all aspects of the zoo environment,
and can be achieved through manipulation of group size and structure, feeding
behaviour, enclosure design and furnishings, and also through interaction
of the captive animal with the keeper and the visiting public.
C. geoffroyi are very active animals and may spend many hours chasing,
leaping and foraging. Thus, despite their small size, they need and use
a relatively large area. Of course a zoo cannot replicate the amount of
space a family of marmosets would occupy in the wild, but physically it
should provide enough space per animal to allow them to perform any natural
behaviour. Psychologically more important is how that space is filled,
and the well-being of the animals within.
Sifting through floor litter for insects and other tasty treats is a natural
behaviour of wild marmosets, as is play-wrestling on the ground. In captivity
space is limited and floor space has great potential for use. Therefore
efforts should be made to provide a stimulating, naturalistic ground covering,
at least in the outside enclosure. Chamove et at. (1982) experimented
with. the use of deep woodchip litter in the enclosures of different primate
species, including marmosets. Results showed that the addition of this
type of substrate significantly altered floor use. Time spent foraging
for food increased, play behaviour increased and agonistic behaviour decreased.
Studies have also shown that deep litter such as bark strippings, chippings
and bark mulch absorb more moisture, give off less odour, and have an inhibitory
effect on bacteria, and so may be left down for a greater length of time
with fewer risks of health problems. However, of course, droppings. and
excess food should be removed daily.
Of the seven zoos surveyed, one provided deep bark chippings, two provided
bark chippings with peat or grass, two provided sand, one provided grass
and one provided sand and grass, in the outside enclo- sures. (See Table
5[not reproduced].)
C. geoffroyi are tropical zone arboreal animals. Their habitat ranges
from lowland rainforest bordering the coast and river banks, semi-deciduous
forest, dry scrub or caatinga, to areas of forest savanna. They
prefer to stay in the dense, impenetrable cover of secondary growths, where
there is an abundance of food and protection from larger predators. Although
captive animals are safe from predation, it is important to provide a natural
refuge in which they can feel safe, forage and play. All the zoos surveyed
provided natural plantings, ranging from young to mature trees, small to
large shrubs, evergreens and conifers, to bamboo, pampas grass and climbing
plants. The animals' preferred interaction was with bushy shrubs and tall
trees. Although tree bark is chewed, there have been no reported problems
with plantings, and all have been successful.
It is important to equip the enclosure with an adequate framework of perching,
as marmosets prefer to move on horizontal branches. However, they are also
vertical clingers and leapers, and a redundant wall may be utilised by
attaching netting of very small mesh size; this could be detachable for
ease of wall cleaning. The same principle can be applied to smooth ceilings
-wire mesh roofs may provide a large area of space on which to climb and
hang, and it is far easier to put things in the space by attaching them
to the roof. At Belfast Zoo the roof of the outdoor enclosure is "made
of three-quarter inch (19 mm) nylon netting supported on nylon ropes. This
is the first time this type of construction has been tried for marmosets,
and provides a much lighter and less visually disruptive roofing system
(pers. comm., M.G. Challis). Branchwork should be changed when possible,
or scent-marked perches moved between different species, providing added
stimulus. However, when moving marmosets to a new enclosure it may be beneficial
to take one or two of their familiar scent-marked perches with them to
help settle I the animals (Moore, 1989).
At Shaldon I found that fresh foliage was much appreciated by the i marmosets,
especially the youngsters, who enjoyed chasing and leaping long distances
amongst the greenery which moved and swayed on landing, and the thin twigs
were ideal for infants to explore and chew. Foliage provides diversity
for the animals, and it is especially important if there are no natural
plantings in the enclosure. It may also encourage the visitor to look for
these small primates.
All the zoos surveyed had aviary-type outdoor enclosures, with access to
heated indoor areas kept at temperatures ranging from 18°C to 21°C,
with warmer spots of up to 25°C (Table 4 [not reproduced]). No problems
were mentioned regarding climatic conditions. As a precautionary measure
animals at both Colchester and Emmen are restricted to indoor areas when
the weather is extremely cold. A relative humidity of 50-60% is optimal.
Low humidity is bad for infants. Moist peat as a substrate helps to maintain
a high humidity. (Captive Care Working Party, 1987.)
In the wild environment different species of animal may share the same
territory, and although each is adapted to its own particular niche within
that area, mutual benefits may be gained. In captivity, providing conditions
are suitable and the appropriate species are selected, it should be possible
to establish a mixed exhibit. This has been very successful for some species
of marmosets and tamarins, although C. geoffroyi appear to be less
tolerant of other animals than some callitrichid species. 'We [Jersey Zoo]
have found Geoffroy's to be unnaturally intolerant of other species. We
often house single animals of different species together for company, but
Geoffroy's have not agreed to this.' (Pers. comm., D. Wormell.) 'It should
be noted that our group [Colchester Zoo] of Geoffroy's attacked and fatally
wounded one lesser Malayan chevrotain (Tragulus jauanicus ). They
had been living with the animal for approximately three weeks with no problems,
and appear to have turned on her for no apparent reason. But they have
shared their exhibit with the spur-thighed tortoise, Testudo graeca,
for about eighteen months with no sign of aggression.' (Pers. comm.,
J. Lewis.) Colchester is the only zoo in the survey where C. geoffroyi
share an exhibit with another species of animal.
All the animals in the survey were exposed to moderate to high visitor
numbers. Two of the enclosures were only viewed from one side, and three
provided off-show indoor areas. All animals appeared to view the visiting
public with indifference or curiosity. However, C. geoffroyi are
sensitive animals and are prone to stress. Older individuals, particularly,
appear to habituate themselves less to the presence of visitors, and get
very agitated when approached. Therefore enclosures must be designed big
enough to allow the animals to achieve a reasonable distance between themselves
and the visitors if they so wish. Cover must be available and the opportunity
to go off-show must be provided. If possible, high perches should be provided
to give animals vantage points from which to look down onto the visitors,
restoring some level of control. Barriers between visitors and the edge
of the enclosures should be reasonably wide to provide extra reassurance
for the animals. (L. Dickie, 1994.)
Appendix
In 1991 a reintroduction programme began for the restoration of C. geoffroyi
populations in some forest fragments in the state of Espirito Santo,
south-eastern Brazil. Although none of the released groups successfully
established themselves in the area, concurrent studies of behaviour and
ecology of the wild marmoset groups, which began in 1993, are providing
much important data that will benefit introduced groups from future releases,
giving a better basis for the management of the species. (Passamani, M.,
and Passamani, J.A., 1995).
Acknowledgements
I would like to thank the Geoffroy's marmosets at Shaldon Wildlife Trust
for enriching my life. With special thanks to Stewart Muir of Shaldon,
and to my best friend Guy for the use of his computer and copying facilities.
My thanks, too, to all those who participated in the survey.
Products mentioned in the text
Abidec multivitamins, Warner Lambert Health Care, Lambert Court, Chestnut
Avenue, Eastleigh, Hampshire, U.K
Cytacon B12, Duncan Flockhart & Co. Ltd., 700 Oldfield Lane North,
Greenford, Middlesex, U .K. Gum Arabic and Acacia Gum (available from pharmacists
and specialist suppliers).
Marmoset Jelly and Mazuri Marmoset Diet, Special Diets Services Ltd, P.O.
Box 705, Witham, Essex CM8 3AD, U.K.
Milupa Infant Food, Milupa Ltd., Milupa House, Uxbridge Road, Hil- lingdon,
Uxbridge, Middlesex, U.K.
Rovimix D3 Powder, Roche Products Ltd., P.O. Box 8, Welwyn Garden City,
Herts. AL7 3AY, U.K. SA37 Multi-vitamin Powder, Intervet UK Ltd., Milton
Road, Science Park, Cambridge CB4 4FP, U.K.
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Deep wood chip litter: hygiene, feeding and behavioural enhancement in
eight primate species. International Journal for the Study of Animal
Problems 3 (4): 308-318.
Coimbra-Filho, A.F., and Mittermeier, R.A. (1976): Exudate-eating and tree-gouging
in marmosets. Nature 262: 630.
Dickie, L.A. (1994): Environmental Enrichment in Captive Primates: a
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and the University of Cambridge.
Epple, G. (1968): Comparative studies on vocalisations in marmosets (Hepalidae).
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Ferrari, S.F. (1989): Lilliput in the trees. BBC Wildlife Magazine 7
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Garber, P.A. (1984): Proposed nutritional importance of plant exudates
in the diet of the Panamanian tamarin, Saguinus oedipus geoffroyi. International
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Moore, M. (1989): Marmosets in Captivity. Basset Publications, Plymouth,
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Price, E.C. (1992): Nutrition of Geoffroy's marmoset. Dodo 28: 58-69.
Terborgh, J. (1983): Five New World Primates. Princeton University
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Reproduced with permission of International Zoo News.