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CALLITRICHID

HUSBANDRY MANUAL

VINCE SODARO AND NANCY SAUNDERS, EDITORS


CHICAGO ZOOLOGICAL PARK
ACKNOWLEDGMENT
I would like to thank the following people and organizations for their work and support of this manual: Anne
Baker, Andrew Baker, Melinda Pruett-Jones, Chicago Zoological Park, and the AZA Neotropical Primate
Taxon Advisory Group. I offer special thanks to Carol Sodaro for her advice about the trials and tribulations of
organizing a husbandry manual. Thanks to Nancy Saunders and Diane Cavalieri of Chicago Zoological Park
for editorial and design services, respectively.

CONTRIBUTORS
Noha Abou-Madi, D.V.M., Cornell University; Andrew J. Baker, Ph.D., Philadelphia Zoo; Sue Crissey, Ph.D.,
Chicago Zoological Park; Jeffrey E. Fite, University of Nebraska at Omaha; Jeffrey A. French, Ph.D.,
University of Nebraska at Omaha; Donna M. Ialeggio, D.V.M., Philadelphia Zoological Gardens; Barbara
Lintzenich, Chicago Zoological Park; Suzan Murray, D.V.M., Ft. Worth Zoo; Anne Savage, Ph.D., Roger
Williams Park Zoo; Kerri Slifka, Chicago Zoological Park; Vince Sodaro, Chicago Zoological Park; Jacqueline
M. Zdziarski, D.V.M., Chicago Zoological Park.

© 1999 Neotropical Primate Taxon Advisory Group. Second printing. All rights reserved.

Front cover: Golden-headed lion taramarin. © 1986 Vince Sodaro

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TABLE OF CONTENTS

Housing Callitrichids and Callimico in Zoological Parks .......................................................................................1


Vince Sodaro, Chicago Zoological Park

Housing and Exhibiting Mixed Species of Neotropical Primates ...........................................................................7


Vince Sodaro, Chicago Zoological Park

Social Management of Callitrichids and Callimico.............................................................................................. 35


Andrew J. Baker, Ph.D., Philadelphia Zoo; and Anne Savage, Ph.D., Roger Williams Park Zoo

Reproduction in Callithrichid Primates ................................................................................................................ 41


Jeffrey A. French, Ph.D., and Jeffrey E. Fite, University of Nebraska at Omaha

Diets for Callitrichids—Management Guidelines ................................................................................................ 53


Sue Crissey, Ph.D., Barbara Lintzenich, and Kerri Slifka, Chicago Zoological Park

Enrichment and Operant Conditioning of Callitrichids........................................................................................ 64


Michelle Farmerie, Don Neiffer, VMD, and Karen Vacco, The Pittsburg Zoo

Handrearing Callitrichids and Callimico in Zoological Parks.............................................................................. 90


Vince Sodaro and Sue Crissey, Ph.D., Chicago Zoological Park

Handrearing Callimico Goeldii in Zoological Parks .......................................................................................... 100


Vince Sodaro, Chicago Zoological Park

Preventive Medicine ........................................................................................................................................... 105


Jacqueline M. Zdziarski, D.V. M., Chicago Zoological Park

Restraint and Anesthesia of New World Primates ............................................................................................. 108


Suzan Murray, D.V.M., Ft. Worth Zoo

Hematology and Clinical Chemistries ................................................................................................................ 110


Noha Abou-Madi, D.V.M., Cornell University

Wasting Marmoset Syndrome ............................................................................................................................ 123


Donna M. Ialeggio, D.V.M., Philadelphia Zoological Gardens

Bibliography ....................................................................................................................................................... 124

New World Primate Necropsy Procedure .......................................................................................................... 146

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HOUSING CALLITRICHIDS AND CALLIMICO IN ZOOLOGICAL PARKS
Vince Sodaro

INTRODUCTION

Callitrichids rose in popularity as laboratory animals in the early 1960s and, as a result, numerous descriptions
of cage size and design, temperature and humidity parameters, feeding regimens, and other factors deemed
necessary for maintenance and breeding were published (Hampton et al. 1965, 1966; Epple 1970). The housing
and husbandry parameters that were established for laboratories later became the foundation for the successful
maintenance and propagation of callitrichids in zoological institutions.

CAGING

Space constraints within the laboratory setting often led to cage housings that approached the minimum for
maintenance and breeding. Gengozian et al. (1978) housed Callithrix and Saguinus in galvanized metal units
measuring 18 x 20 x 42 in. per six animals. Pairs were housed in cages measuring 18 x 18 x 20 in. Hampton et
al. (1965) provided pairs of Callimico and Saguinus with plexiglass cages measuring 48 x 24 x 36 in. and
suggested that 36 in. was the minimum height that could provide qualities of an arboreal environment.

Nevertheless, the space requirements needed to maintain socially well adjusted breeding groups of callitrichids
are relatively modest. Both the Golden Lion Tamarin Management Committee (Rettberg-Beck 1990) and the
Cotton-top Tamarin SSP© (Savage 1995) recommend a minimum cage size of 3 x 2 x 2.5 m for family groups
of these species.

By contrast, many modern zoological institutions are able to provide callitrichid groups with optimum
enclosure sizes and environmental conditions that promote a full range of naturalistic behaviors, social
interactions, and locomotor patterns. The recent trend in "soft releases" that was pioneered by the National
Zoological Park for the golden lion tamarin reintroduction project (Bronikowski et al. 1989) demonstrates that
no "enclosure" is too large for callitrichids, provided that group members can be monitored and easily retrieved.
Saguinus oedipus have also been successfully maintained in free-ranging groups in zoological park settings
(Price et al. 1989).

While there is no strict definition of optimum or ideal exhibit size for callitrichids, such an enclosure should
allow the animals to exercise the full range of their natural physical activities. These enclosures should provide
enough horizontal space for animals to leap up to several feet between branches or other furnishings and should
offer as much height as possible. All genera of callitrichids are arboreal and normally range to heights of up to
at least 10 meters above the ground in their natural habitats (Kleiman et al. 1988; Pook and Pook 1981;
Snowdon and Soini 1988; Soini 1988; Stevenson and Rylands 1988). Therefore, it is fairly safe to say that
within the confines of an indoor exhibit no height is too great to be used.

Many callitrichid species are capable of rapid reproduction and increased family size within a relatively short
period of time. (Leontopithecus in captivity are capable of producing three litters of twins in one year.)
Managers should anticipate the possibility of increased stress and tension in rapidly growing family groups
housed in smaller enclosures.

MATERIALS

A variety of materials suitable for cage construction have been described (Mallinson 1975; Xanten 1990;
Gengozian et al. 1978). In colony situations where exhibit aesthetics are not a consideration, cages are
frequently constructed of wooden framing with steel or wire mesh (Beck et al. 1982; Snowden et al. 1985).
Wire-mesh cagefronts can facilitate sexing of young animals, diagnosing pregnancy, and easily observing

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animals (Rettberg-Beck 1990). Ensure that cages constructed of wood are sealed. USDA regulations require
that interior building surfaces of nonhuman primate facilities be impervious to moisture so that they may be
readily sanitized (USDA 1992). Hollow-steel tubing is also sometimes used for cage framing with partitions
between cages constructed of opaque PVC (Mallinson 1975).

Many modern zoological exhibits are constructed of textured rockwork (concrete or epoxy), which creates a
more naturalistic appearance. Tree, vines, and other features of these exhibits may also be constructed of
concrete or epoxy. These exhibits are often glass- or wire-fronted with fine semi-transparent mesh. Other
exhibits display animals at distances far enough from public access areas that barriers become unnecessary.

FURNISHINGS

Wherever possible, the primary furnishings of callitrichid enclosures should consist of natural tree branches
arranged to create a variety of arboreal pathways leading to all of the principle features within the enclosure,
including nestboxes or sleeping sites, shelving, and food and water bowls. Other furnishings, such as rope or
vines, may also be provided.

Furnishings should include both rigid and flexible, vertical and horizontal supports of varying diameters placed
at varying angles. When furnishing an enclosure, avoid placing branches directly above food or water sources.
This will minimize the chance of contamination from urine and feces. Provide as many horizontal branches or
other furnishings as possible in enclosures of minimum size. Callitrichids are adept at climbing or locomoting
on diagonal or vertical branches, but prefer level furnishings for resting and social activities. Horizontal
furnishings, such as natural branches, should be a minimum of 1.5-inch diameter but preferably 2-3 inches to
allow animals to sit or rest comfortably and to engage in normal social interactions, such as grooming. Many
adult callitrichids, with the possible exception of Cebuella, have difficulty maintaining balance on perches less
than one inch diameter and will avoid sitting or resting on them except where they meet a vertical crosspiece to
which they can cling for support.

Regardless of enclosure size, place ample furniture in the upper two-thirds of the exhibit or enclosure to provide
as much of an arboreal environment as possible. Keepers find enclosures furnished in this way are easily
cleaned and maintained.

In naturalistic exhibits, enclosures may also be planted with a variety of live plants or trees. However, exercise
caution and avoid the use of toxic plants.

Provide at least one nestbox per enclosure for callitrichid groups. Although many species in the wild have
infrequently been observed to sleep in tree cavities (Soini 1988; Rylands 1982; Snowden and Soini 1988),
nestboxes are readily used by several species in captivity as sleeping sites or as retreats when stressed or
startled. Stevenson (1975) reported that Callithrix jacchus slept in a wooden nestbox (28 x 22 x 26 cm) with an
entrance hole 10 cm diameter. The Cotton-top Tamarin SSP© (Savage 1995) recommends a nestbox measuring
30 x 30 cm with a 10 x 15 cm hole cut in the middle of the box. For Leontopithecus rosalia, the Golden Lion
Tamarin Management Committee recommends a minimum of two wooden nestboxes per enclosure of
sufficient size to house a family group (Rettberg-Beck 1990). Cebuella at Kilverstone Wildlife Park (Challis
1993) did not use a nestbox that was provided for them. Similarly, Beck et al. (1982) found that Callimico did
not sleep in nestboxes, but would use them for short-term seclusion or play. For all species, the entrance to any
nestbox should be large enough to permit adults carrying offspring to easily enter or exit.

Many institutions that maintain callitrichids clean and replace branches, perches, and other features of
enclosures infrequently to retain scent-mark secretions (DuMond 1972; Stevenson 1975; Beck et al. 1982;
Young and Carroll 1993). Rettberg-Beck (1990) recommends "spot" cleaning feces and food remains for
Leontopithecus rosalia as opposed to major cleaning. Still, it is important to integrate such practices with
effective cleaning and disinfecting protocols to minimize the risk of pathogenic infections. Epple (1970) found
that occasionally replacing branches, nestboxes, and shelves reduced the likelihood of self-infection by parasitic
helminthes.

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Although natural materials, such as tree branches, are preferred as enclosure furniture, callitrichids can be
successfully maintained on a wide variety of materials. Callimico goeldii at Brookfield Zoo were housed in
enclosures furnished with plastic pipe (2.5 to 5 cm in diameter) and perches of wood and wire mesh (Beck et al.
1982). Cage furniture used later at Brookfield for Callimico, Leontopithecus chrysomelas, and Saguinus
oedipus consists of 2- and 3-inch diameter PVC pipe. PVC "trees" were given a roughened texture to prevent
slipping and to retain scent-mark secretions. These furnishings were combined with corion shelving and natural
tree branches that could be frequently replaced.

A variety of substrate materials can be used in enclosures, including wood shavings or bark chips. Solid floors
of sealed concrete can be used. If births are anticipated, concrete floors should be bedded with wood shavings
to prevent possible injuries to infants.

TEMPERATURE AND HUMIDITY REQUIREMENTS

Callitrichids inhabit warm and frequently humid areas of the neotropics. Captive animals are typically provided
with a range of temperatures and humidity levels that approximate those of natural conditions. A sample of
published recommendations (Beck et al. 1982; DuMond 1972; Hampton et al. 1966; Mallinson 1975; Savage
1995; Stevenson 1975; Rettberg-Beck 1990) ranges from a minimum of 60°F to 85°F with humidity ranges of
40-80% (Table 1). Lorenz (1972) reported decreased activity in Callimico at temperatures above 28°C (82°F)
and found that they became lethargic at temperatures above 35°C (95°F). Beck et al. (1982) found that
humidity levels below 60% caused Callimico to wipe their faces on cage surfaces and to sneeze excessively,
while higher humidity levels resulted in saturated pelage and swollen eyes. Humidity levels over 80% can also
increase fluidity of scent secretions in Leontopithecus, resulting in matted pelage and irritated eyes.

Despite the recommendations by most authors to provide callitrichids with a warm environment, species
maintained outdoors in temperate climates have, on occasion, proven remarkably tolerant of low temperatures
if provided with suitable shelter. Mallinson (1977) found that a family of Callithrix penicillata x Callithrix
jacchus was able to remain outdoors throughout the entire winter of 1975-76 at Jersey, Channel Islands.
January temperatures as low as -3°C were recorded. These animals were provided with a draught and
waterproofed fiberglass box fitted with a Perspex front for shelter. Mallinson also described marmosets housed
outdoors in various locations in England, which enjoyed playing in snow.

TABLE 1. TEMPERATURE AND HUMIDITY RECOMMENDATIONS FOR CALLITRICHIDS

Author Species Temperature Humidity


Beck et al. (1982) C. goeldii 25° C 60%
DuMond (1972) L. rosalia minimum of 60° F above 50%
(optimum 60-80%)
Hampton et al. (1966) S. oedipus approximately 80° F above 50%
Lorenz (1969) C goeldii 21-25° C (70-77° F)
Mallinson (1976) C. Jacchus 18-27° C (65-80° F) 60-75%
C. argentata
C. goeldii
S. fuscicollis
S. oedipus
Savage (1995) S. oedipus 50-70%
25-29° C (76-85° F)
Stevenson (1975) C. jacchus 20-30° C average 50%
(range 40-60%)

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PHOTOPERIOD

In captivity, callitrichids should be provided with 12 to 14 hours of daylight. The distribution of


callitrichids in the neotropics where little variation in day length occurs has led several authors to
recommend a 12L:12D photoperiod (Snowdon et al. 1985; Stevenson 1975; Savage 1995; DuMond 1972).
Beck et al. (1982) preferred a photoperiod of 14L:10D for Callimico. At least five hours of light were
provided after the afternoon feed. Rettberg-Beck (1990) recommends 12 to 14 hours of daylight for
Leontopithecus rosalia, as well as 30 to 60 minutes of exposure to ultraviolet light to provide Vitamin D 3.

FEEDING

The nutritional aspects and management guidelines for callitrichid diets are addressed in a separate chapter
of this manual (see Diets for Callitrichids chapter, this volume) and will not be addressed here.

Many feeding schedules and practices have successfully maintained callitrichids in captivity. Although
Stevenson (1975) demonstrated that Callithrix jacchus could be maintained on one feeding per day, at least
two daily feedings are preferred for enrichment and stimulation. Snowdon et al. (1985) offered food to
Saguinus oedipus three times daily. The main meal was offered at midday. Supplemental feedings of fruit
and high protein items were offered early in the morning and late in the afternoon. These feedings created
opportunities for caretakers to observe animals more frequently.

Beck et al. (1982) found that less than 14 hours of light prevented adequate food consumption for
Callimico. Rettberg-Beck (1990) recommends feeding schedules for Leontopithecus rosalia allow 4 to 5
hours between feedings.

For larger family groups, provide multiple feeding stations at widely spaced locations within an enclosure
to insure that subordinate individuals can feed without interference from more dominant group members.

Live prey forms a significant part of the diet of all genera of callitrichids (Kleiman et al. 1988; Snowdon
and Soini 1988; Soini 1988; Stevenson and Rylands 1988) and crickets and mealworms are commonly
offered to captive animals. Commercially raised hairless mouse pups ("pinkies") have also been offered as
live prey items but have recently been implicated in fatal outbreaks of viral callitrichid hepatitis (Ballou
1993) at several zoological institutions in North America. As a result, the Golden Lion Tamarin
Management Committee (Rettberg-Beck 1990) recommends eliminating mouse pups from the diet of
Leontopithecus rosalia.

PEST CONTROL

Callitrichid husbandry programs should include rigorous pest control. Mice and cockroaches are common
pests in zoos and can become vectors for a variety of diseases affecting callitrichids. Feral mice have been
implicated as vectors of toxoplasmosis as well as callitrichid hepatitis, both of which have been contracted
by Leontopithecus rosalia that caught and ate mice in their enclosures (Ballou 1993). A fatal outbreak of
leptospirosis in Saguinus labiatus in a zoo was also linked to the presence of rodents (Reid et al. 1993).

Cockroaches have been identified as intermediate hosts for several debilitating and often fatal diseases in
callitrichids. The German cockroach Blatella germanica was found to be the intermediate host for larvae of
the nematode Pterygodermatites nycticebi, which caused morbidity and mortality in Leontopithecus rosalia
(Montali et al. 1983). B. germanica was also identified as the host of Prosthenorchis elegans in an outbreak
at the Utica Zoo that led to the deaths of two Saguinus oedipus, and several other primate species (Nielsen
1980).

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GENERAL HOUSING CONSIDERATIONS

For some taxa, it is important to prevent visual contact between neighboring groups of conspecifics housed
in the same area. Kleiman (1977) found lion tamarins (Leontopithecus sp.) to be aggressive to extra-
familial animals and cautioned that groups should not have access to each other. Kleiman et al. (1982)
recommends preventing visual interactions between neighboring reproductive groups to reduce stress and
social tension. Savage (1995) considers visual separation of neighboring groups of Saguinus oedipus
critical to preventing territorial behavior. Olfactory and auditory contact, on the other hand, does not
disrupt normal behavior or reproduction in neighboring groups of this species. Beck et al. (1982) found that
Callimico goeldii could thrive in close proximity to conspecifics. Auditory contact and some olfactory and
visual contact had no apparent negative affects on health or reproduction, although prolonged visual contact
resulted in extensive display and other signs of disturbance.

The potential risk of disease transmission or the spread of pathogens between groups of callitrichids should
be a concern only if groups are in close proximity. Housing several groups of callitrichids in a single
building may increase the vulnerability of the entire collection to epizootic diseases. Where practical,
managers should consider dispersing groups throughout an institution or facility to safeguard against such
an outbreak.

Managers should be equally concerned about the proximity of callitrichids to cebids, and should avoid
housing them in the same rooms or holding areas. This is particularly true of Saimiri. Squirrel monkeys are
believed to be the principal host for Herpesvirus-T, which has been linked to fatal epizootics in Saguinus
nigricollis and Saguinus oedipus (Hunt et al. 1978).

REFERENCES

Ballou, J. D. 1993. 1992 International Studbook Golden Lion Tamarin Leontopithecus rosalia.
Washington, D.C.: Smithsonian Press..
Beck, B. B., D. Anderson, J. Ogden, B. Rettberg, C. Brejla, R. Scola and M. Warneke. 1982. Breeding the
Goeldi's monkey Callimico goeldii at Brookfield Zoo. Chicago International Zoo Yearbook 22:106-
114.
Bronikowski, E. J., Jr., B. B. Beck and M. Power. 1989. Innovation, exhibition and conservation: free-
ranging tamarins at the National Zoological Park. AAZPA Annual Conference Proceedings pp. 540-
546.
Challis, M. G. 1993. The maintenance and Management of Marmosets (Callithrix and Cebuella) at
Kilverstone Wildlife Park. In: Marmosets and Tamarins in Captivity (Proceedings of Symposium 17 of
Association of British Wild Animal Keepers), ed. R. Colley, pp.6-14. Bristol: Association of British
Wild Animal Keepers.
Cotton-top Tamarin SSP© 1995. In: Cotton-top Tamarin SSP© Husbandry Manual, ed. A. Savage, pp. (V)
1-15. Providence: Roger Williams Park Zoo.
DuMond, F. 1972. Recommendations for a basic husbandry program for lion marmosets. In: Saving the
Lion Marmoset, ed. D. Bridgewater. Wheeling, WV:WAPT.
Epple, G. 1970. Maintenance, breeding, and development of marmoset monkeys (Callitricidae) in captivity.
Folia Primatologica 12:56-76.
Gengozian, N., J. S. Bastson and T. A. Smith. 1978. Breeding of marmosets in a colony environment. In:
Primates in Medicine Volume 10, eds. E. I. Goldsmith and J. Moor-Jankowski, pp. 71-78. Karger:
Basel.
Hampton, J. K., Jr., S. H. Hampton and B. T. Landwehr. 1965. A special breeding cage for small primates
such as marmosets. Laboratory Animal Care 15:178-183.
———. 1966. Observations on a successful breeding colony of the marmoset, Oedipomidas oedipus. Folia
Primatologica 4:265-287.
Hunt, R. D., M. P. Anderson and L. V. Chalifoux. 1978. In: Primates in Medicine Volume 10, eds. E. I.
Goldsmith and J. Moor-Jankowski, pp. 239-253. Karger: Basel.
Kleiman, D. G. 1977. Progress and problems in lion tamarin, Leontopithecus rosalia rosalia, reproduction.
International Zoo Yearbook 17:92-97.

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Kleiman, D. G., J. D. Ballou and R. F. Evans. 1982. An analysis of recent reproductive trends in captive
golden lion tamarins, Leontopithecus r. rosalia, with comments on their future demographic
management. International Zoo Yearbook. 22:94-105.
Kleiman, D. G., R. J. Hoage and K. M. Green. 1988. The lion tamarins, genus Leontopithecus. In: Ecology
and Behavior of Neotropical Primates Volume 2, eds. R. A. Mittermeier, A. B. Rylands, A. F.
Coimbra-Filho and G. A. B. da Fonseca, pp. 299-347. Washington, D.C.:World Wildlife Fund.
Lorenz, R. 1969. Notes on the care, diet and feeding habits of Goeldi's monkey, Callimico goeldii.
International Zoo Yearbook 9:150-155.
———. 1972. Management and reproduction of the Goeldi's Monkey Callimico goeldii (Thomas, 1904).
Callimiconidae, Primates. In: Saving the Lion Marmoset, ed. D. D. Bridgewater, pp. 92-109. Wheeling,
WV:WAPT.
Mallinson, J. 1975. The design of two marmoset complexes at the Jersey Zoological Park. Jersey Wildlife
Preservation Trust Annual Report 12:21-26.
———. 1977. Acclimatisation of tropical mammals in the northern hemisphere with special reference to
the family Callitrichidae. Jersey Wildlife Preservation Trust Annual Report 14:34-40.
Montali, R. J., C. H. Gardiner, R. E. Evans and M. Baush. 1983. Pterygodermatites nycticebi (Nematoda:
Spirunda) in golden lion tamarins. Laboratory Animal Science 33(2):pp.
Nielsen, D. H. 1980. Prosthenorchis elegans infection in a primate colony. Annual Proceedings of the
American Association of Zoo Veterinarians, pp. 113-116.
Pook, A. G., and Pook, G. 1981. A field study of the socio-ecology of the Goeldi's Monkey (Callimico
goeldii) in North Bolivia. Folia Primatologica 35:288-312.
Price, E., A. T. C. Feistner, B. Carroll and J. A. Young. 1989. Establishment of a free-ranging group of
cotton-top tamarins Saguinus oedipus at the Jersey Wildlife Preservation Trust. Dodo, Journal Jersey
Wildlife Preservation Trust 26:60-69.
Reid, H. A. C., A. J. Herron, M. E. Hines, II, E. A. Orchard and N. H. Altman. 1993. Leptospirosis in a
white-lipped tamarin (Saguinus labiatus). Laboratory Animal Science 43(3):258-259.
Rettberg-Beck, ed. 1990. Husbandry protocol for golden lion tamarins (Leontopithecus rosalia rosalia).
Washington, D.C.: National Zoo.
Rylands, A. B. 1982. The behavior and ecology of three species of marmosets and tamarins (Callitrichidae,
Primates) in Brazil. Unpubl. doctoral dissertation, University of Cambridge: Cambridge.
Snowdon, C. T., A. Savage and P. B. McConnell. 1985. A breeding colony of cotton-top tamarins
(Saguinus oedipus). Laboratory Animal Science 35(5):477-480.
Snowdon, C. T., and P. Soini. 1988. The tamarins, genus Saguinus. In: Ecology and Behavior of
Neotropical Primates, Volume 2, eds. R. A. Mittermeier, A. B. Rylands, A .F. Coimbra-Filho and G.
A. B. da Fonseca, pp. 233-298. Washington D.C.: World Wildlife Fund.
Soini, P. 1988. The pygmy marmoset, genus Cebuella. In: Ecology and Behavior of Neotropical Primates,
Volume 2, eds. R. A. Mittermeier, A. B. Rylands, A. F. Coimbra-Filho and G. A. B. da Fonseca, pp.
79-129. Washington D.C.: World Wildlife Fund.
Stevenson, M. 1975. Maintenance and breeding of the Common Marmoset Callithrix jacchus with notes on
hand-rearing. International Zoo Yearbook 16:110-116.
Stevenson, M., and A. B. Rylands. 1988. The marmosets, genus Callithrix. In: Ecology and Behavior of
Neotropical Primates, Volume 2, eds. R. A. Mittermeier, A. B. Rylands, A. F. Coimbra-Filho and G.
A. B. da Fonseca, pp. 131-222, Washington D.C.: World Wildlife Fund.
United States Department of Agriculture (USDA). Animal and Plant Inspection Service Subchapter A--
Animal Welfare; Subpart D-Specifications for the Humane Handling, Care, Treatment and
Transportation of Nonhuman Primates, October 1992.
Xanten, W. A., 1990. Marmoset behaviour in mixed-species exhibits at the National Zoological Park,
Washington. International Zoo Yearbook 29:143-148.
Young, J. A. and B. Carroll. 1993. The genus Leontopithecus in captivity at the Jersey Wildlife
Preservation Trust. In: Marmosets and Tamarins in Captivity (Proceedings of Symposium 17 of
Association of British Wild Animal Keepers), ed. R. Colley, pp. 23-30. Bristol: Association of British
Wild Animal Keepers.

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HOUSING AND EXHIBITING MIXED SPECIES OF NEOTROPICAL PRIMATES
Vince Sodaro

INTRODUCTION

Housing or exhibiting Neotropical primates of different species together or housing and exhibiting Neotropical
primates with other species of animals can have several benefits. These combinations can create more
interesting exhibits and alleviate cage-space problems, as well as offer behavioral and social enrichment to the
animals. Many species of neotropical primates are sympatric over large areas of their ranges. Polyspecific
associations in the wild, either incidental or deliberate, have been documented for several species (Pook and
Pook 1982; Rylands 1982; Torborgh 1983). Some species combinations may be considered for mixed-species
housing or exhibition. Many other combinations, whether zoogeographically correct or not, have been tried at
various zoological institutions with mixed results. The success or failure of mixed-species introductions can be
influenced by several factors, including exhibit size; method of introduction; group composition; age and sex
ratio of the animals; and personality differences of individuals.

A short questionnaire was distributed in April 1995 to approximately 70 AZA-accredited institutions listed on
ISIS as holding Neotropical primates. To gather information about zoos’ experiences with mixed-species
combinations of Neotropical primates, the institutions were asked to describe mixed-species introductions.
Specifically: 1) which species of neotropical primate(s) were mixed successfully; 2) which species of
neotropical primate(s) were mixed unsuccessfully; 3) the age/sex composition of the groups involved in the
introductions; and 4) the methods of introduction. The respondents were asked the same questions to describe
introductions between Neotropical primates and other species of animals.

Responses demonstrate that there is no rule of thumb to predict which species combinations are likely to be
successful. Moreover, species combinations that have been successful in some situations were unsuccessful in
others. The responses further demonstrate that the social dynamics of mixed-species combinations can change
over time, and that combinations that appear successful in the short term may break down later.

CALLITRICHIDS IN MIXED-SPECIES EXHIBITS

Based on responses to the questionnaire, callitrichid species are most frequently involved in mixed-species
attempts. Attempts to combine two or more callitrichid species or one or more species of callitrichid with
another species of animal are fairly common and fairly successful. Their size, relatively modest space
requirements, and the ease with which they can be transferred into or out of enclosures make them well suited
to many types of zoo exhibits. Callitrichids are occasionally exhibited in mixed-species combinations with
various species of cebidae and are no less likely to be successful provided that the differences in dietary and
nutritional requirements can be managed.

Sixteen species of callitrichids were reported by institutions to have been tried in mixed-species combinations
including :
Callimico goeldii Saguinus fuscicollis
Callithrix melanura Saguinus geoffroyi
Callithrix jacchus Saguinus imperator subgriscecens
Callithrix geoffroyi Saguinus labiatus
Callithrix kuhli Saguinus leucopus
Cebuella pygmaea Saguinus midas
Leontopithecus chrysomelas Saguinus mystax
Leontopithecus rosalia Saguinus oedipus

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CEBIDAE IN MIXED-SPECIES EXHIBITS

Questionnaire respondents indicated that eight of the eleven genera of Cebidae have been attempted in mixed-
species combinations, including Alouatta, Aotus, Ateles, Callicebus, Cebus, Lagothrix, Pithecia, and Saimiri.
Combinations of Cebidae species with other species, primate or otherwise, are apparently less common in
zoological institutions than mixed-species combinations involving Callitrichidae. A total of fifteen institutions
reported thirty-five accounts involving Cebidae in mixed-species exhibits. Of these, only nine reported
combinations of two or more genera of Cebidae and in only two of these were three species of Cebidae mixed.
Thirteen accounts reported combining Cebidae species with callitrichid species. Twenty-one of these thirty-five
accounts involved species of animals other than primates, either alone or in mixed primate-species
combinations.

Alouatta caraya and Pithecia pithecia were the cebidae species most frequently involved in mixed-species
combinations.

Several accounts of mixed-species attempts involving Callicebus Sp. (C. moloch or C. donacophilus) suggest
that this genus may not be well suited for mixed-species exhibition. Although a group of Callicebus was
successfully combined with a group of Leontopithecus rosalia, and also with Myoprocta pratti, Choloepus
didactylus, and Euphractus sexcinctus at the National Zoo, they were severely intimidated by a group of
Callithrix melanura that was introduced to them. In a separate incident at the National Zoo, Kerodon rupestris
chased attacked, and bit titi monkeys (Xanten 1990). Similarly, a male titi monkey housed with 3.0 Saguinus
imperator at Lincoln Park Zoo was separated after the titi appeared intimidated by the tamarins. A trio of 2.1 C.
donacophilus at the Chicago Zoological Park were extremely intimidated by a handreared female callimico that
attacked them in their enclosure. Although separated from the callimico in less than a week, the stress of this
incident led to a chronic case of enteritis in one of the adult male titis.

NEOTROPICAL PRIMATES IN MIXED-SPECIES COMBINATIONS WITH NON-PRIMATE SPECIES

A variety of bird, mammal, and reptile species have been combined successfully with Neotropical primates in
mixed-species exhibits. The majority has been mixed with callitrichid species or with Pithecia or Aotus in
exhibits of small mammals. These species include approximately 25 bird species, four reptile species, and 18
mammal species. Many others might also be suitable. Questionnaire respondents indicated few problems with
bird/primate combinations provided that the birds have ample perches for resting, enough space to evade the
monkeys, and can be fed without problems.

Reptile species mixed with Neotropical primates were limited to Iguana Sp. and one species of tortoise
(Geocheloni carbonaira). Tamarins at the Woodland Park Zoo in Seattle reportedly chewed on the crests of
adult green iguanas, resulting in one young tamarin being bitten on the tail by the iguana. The possibility of
salmonella contamination from reptiles to primates was a concern and led the zoo to separate the tamarins from
the iguanas, although no evidence of salmonella was actually found.

Mammal species exhibited with Neotropical primates included:


Golden-rumped agouti (Dasyprocta cristata) Prehensile-tailed porcupine (Coendu prehensilis)
Green acouchi (Myoprocta pratti) Ground cuscus (Phallanger gymnotis)
Chinchilla (Abrocoma Sp.) La Plata three-banded armadillo (Tolypeutes
Coatimundi (Nasua nasua) matacus)
Degus (Octodon degus ) Six-banded armadillo (Euphractus sexcinctus)
Giant anteater (Myrmacophagia tridactyla) Brazilian tapir (Tapiris terrestris)
Rock cavies (Kerodon rupestris) Mexican red brocket deer (Mezama americana
Two-toed sloth (Choloepus didactylus and temama)
C.hoffmanni) Tamandua (Tamandua tetradactyla)
Three-toed sloth (Bradypus sp.) Meerkat (Suricata suricata)

8
The mammal species most frequently mixed with Neotropical primates are apparently acouchis, agoutis, rock
cavies, and two-toed sloths. Of these four genera, the two-toed sloth appeared to be the species most
successfully mixed with primates. In three of the four cases in which the sloths were mixed with Aotus, close
bonds developed between the sloths and the monkeys, with the monkeys sleeping on or with them. Sloths were
also successfully mixed with callitrichid species at several institutions.

While acouchis, agoutis, and rock cavies are commonly chosen for exhibition with small primates in small-
mammal exhibits, the questionnaire responses indicate that all are prone to aggression towards primates and
have been responsible for the injuries or deaths of various callitrichid species. They were similarly aggressive
with Callicebus and Pithecia in mixed-species exhibits.

At Folsom Children’s Zoo, acouchis were reported to prey upon newborn tamarins that fell to the ground. At
Virginia Zoo, a Callithrix jacchus mixed with Coendu prehensilis and Myoprocta pratti sustained a bite wound
on its arm that most likely was inflicted by an acouchi. At the Philadelphia Zoo, two unexplained deaths of
Saguinus labiatus, each several years apart, occurred while the animals were housed with agoutis. Also, an
adult pygmy marmoset was found dead in its enclosure four days after being introduced to a group of 1.3
Saguinus labiatus and 2.0 agoutis. Due to these deaths, the Philadelphia Zoo decided to discontinue mixing
agoutis with primates. Similarly, at Roger Williams Park Zoo, agoutis reportedly killed a juvenile cotton-top
tamarin and injured an adult white-faced saki in mixed-species housing. At the Riverbanks Zoo, a male golden
lion tamarin was severely bitten while housed with black howlers and agoutis.

At the Little Rock Zoo, rock cavies (Kerodon rupestris) were responsible for the death of an infant Pithecia
pithecia after having previously been observed chasing sakis. Kerodon in mixed species exhibits at the National
Zoo were reported to chase Callimico goeldii, Callithrix argentata, Leontopithecus rosalia, and to have chased
and bitten Callicebus moloch. Similarly, Kerodon at Philadelphia Zoo and Riverbanks Zoo were reported to
have attacked tamarins.

Although some institutions have housed acouchis, agoutis, and rock cavies with neotropical primates without
incident, managers considering housing these species with small neotropical primates should view such
combinations as risky, approach them with caution, and implement them under continued careful observation.

METHODS USED TO INTRODUCE MIXED SPECIES FOR HOUSING AND EXHIBITION

Different methods of interspecies introductions and extensive preparation for introductions are used to
maximize the chances that mixed-species combinations will succeed. Most if not all of these methods and
preparations are the same as those that institutions use to introduce new or unfamiliar conspecifics. Introduction
techniques reported in the questionnaire included a variety of approaches, from simply putting two groups of
unrelated species into a new enclosure with no prior contact with each other or the enclosure to relatively long
preintroduction exposure of species or individuals through opposite sides of cage mesh.

Most of the introduction methods allowed the two species to become familiar with the enclosure without the
other species present. If the introduction occurred in an enclosure in which one of the species was already
living, the new species was given some time alone to become familiar with the enclosure.

When two species in adjacent cages or enclosures were introduced with the intention of then letting them have
the combined space of both areas, each species was first allowed visual, olfactory, and auditory contact with the
other through the wire mesh or other types of dividers that separated them. They also were given time to
explore the others' enclosure prior to the introduction.

Giving each species time to become familiar with an enclosure prior to an introduction allows animals to learn
the physical terrain and layout of rockwork, trees, vines, or other features of the exhibit. This potentially
reduces the likelihood that individuals will be injured through falls or other accidents if chased or harassed by
others.

9
With species that exhibit territoriality, zoos can attempt introductions in an enclosure that neither species
inhabited previously.

Several institutions reported successful introductions of a new species to the enclosure of another simply by
introducing the new animal in an air kennel. After a short period of allowing the two species to adjust to each
other, the new animals were released.

The outcome of mixed-species introductions, as reflected in the results of the questionnaire, suggests that even
the best planning and preintroduction methods do not guarantee a successful combination of species. The social
and group dynamics of interspecies combinations involving neotropical primates, like intraspecies interactions
and relationships, should be regarded as everchanging, and should be accompanied by continued careful
monitoring by keepers and managers.

TABLE 1A. SUCCESS/FAILURE RATES OF MIXED-SPECIES COMBINATIONS FOR CALLITRICHIDAE


Callitrichids Species Success Failure
Callimico Leontopithecus chrysomelas 5 2
Callicebus donacophilus 0 1
Callithrix melanura 1 0
Callithrix melanura Callicebus moloch 0 1
Callimico goeldii 1 0
Leontopithecus rosalia 1 0
Callithrix jacchus Ateles geoffroyi 1 0
Saguinus oedipus 0 2
Pithecia pithecia 0 1
Callithrix geoffroyi Cebuella pygmaea 0 1
Leontopithecus chrysomelas 2 1
Saguinus leucopus 1 0
Callithrix kuhli Leontopithecus rosalia 1 0
Cebuella pygmaea Callicebus moloch 0 2
Callithrix geoffroyi 0 1
Leontopithecus rosalia 2 0
Leontopithecus chrysomelas 2 1
Saguinus imperator 1 0
Saguinus leucopus 0 1
Leontopithecus chrysomelas Callimico goeldii 5 2
Callithrix geoffroyi 2 0
Cebuella pygmaea 2 1
Leontopithecus rosalia 1 0
Saguinus mystax 1 0
Saguinus oedipus 1 0
Alouatta caraya 1 1
Callicebus moloch 1 0
Callithrix melanura 1 0
Callithrix kuhli 1 0
Pithecia pithecia 0 1
Saguinus geoffroyi 1 0
Saguinus midas midas 2 0
Saguinus imperator Cebuella pygmaea 0 1
Saguinus labiatus Cebuella pygmaea 1* 0
Saguinus oedipus 0 1
Saguinus leucopus Callithrix geoffroyi 1 0
Saguinus midas midas Alouatta caraya 1 0
Leontopithecus rosalia 2 0
Saguinus geoffroyi 0 1
Saguinus mystax Leontopithecus chrysomelas 1 0

10
Leontopithecus rosalia 1 0
Saguinus oedipus Alouatta caraya 1 0
Callithrix jacchus 0 2
Lagothrix lagotricha 1 0
Leontopithecus chrysomelas 1 0
Pithecia pithecia 2 1
Saguinus labiatus 0 1
Saimiri sciureus 1 0
* An otherwise successful introduction at Philadelphia Zoo ended in a Cebuella death by K. rupestris after four
days.

TABLE 1B. SUCCESS/FAILURE RATES OF MIXED SPECIES COMBINATIONS OF CEBIDAE


Cebidae Species Success Failure
Alouatta caraya Callicebus Sp. 0 1
Cebus albifrons 0 1
Cebus apella 0 1
Leontopithecus rosalia 1 1
Pithecia pithecia 2 0
Saguinus midas midas 1 0
Saimiri sciureus 1 0
Aotus Saimiri Sp. 1 0
Ateles geoffroyi Callithrix jacchus 1 0
Cebus apella 1 0
Cercopithecus diana 1 0
Saimiri Sp. 1 0
Callicebus Sp. Alouatta caraya 0 1
Callimico 0 1
Callithrix melanura 0 1
Cebuella pygmaea 0 2
Leontopithecus rosalia 1 0
Saguinus imperator 0 1
Cebus apella Alouatta caraya 0 1
Ateles geoffroyi 1 0
Cebus Hybrid 1 0
Saimiri Sp. 1 0
Cebus albifrons Alouatta caraya 0 1
Saguinus midas 1 0
Lagothrix lagotricha Pithecia pithecia 1 1
Saguinus oedipus 1 0
Saimiri Sp. 1 0
Pithecia pithecia Alouatta caraya 2 0
Callithrix jacchus 0 1
Lagothrix lagotricha 1 1
Saguinus oedipus 2 1
Saimiri Sp. 1 0
Saimiri Sp. Alouatta caraya 1 0
Aotus Sp. 1 0
Ateles geoffroyi 1 0
Cebus apella 1 0
Lagothrix lagotricha 1 0
Pithecia pithecia 1 0
Saguinus oedipus 1 0

APPENDIX 1. RESULTS OF MIXED-SPECIES COMBINATIONS FOR CALLITRICHIDAE

11
Callimico goeldii

Chicago Zoological Park


Successful
1.0 w/1.0 Leontopithecus chrysomelas
1.0 w/1.0 Leontopithecus chrysomelas
Comments: The same callimico was housed with two different tamarins. Paired in "neutral" cage to offset
any dominance advantage that might result from pairing occurring in home territory of either animal. No
serious problems were observed, but chasing of the tamarin from the food bowl by the Callimico at feeding
time was initially a problem. Pair is now given two separate bowls.

1.0 w/0.1 Leontopithecus rosalia


Comments: Pair lived together for several years with no problems.

Unsuccessful
1.1 w/1.1 Leontopithecus chrysomelas
Comments: Callimico pair was introduced into the tamarins' cage and interactions were closely observed
for the first two hours. Female callimico exhibited prosexual behaviors and directed pilo-solicit display
towards male tamarin. The following day the female callimico and female tamarin fought resulting in a
severe bite wound to the tamarin. Pair was immediately separated.
0.1 Handreared w/2.1 Callicebus donacophilus
Comments: The callimico was very imprinted on people and had fought with conspecifics in several
housing situations. She began to attack the titis the day after being introduced into their enclosure. They
had shown no aggression towards her and seemed to be intimidated by her presence. She was removed
from their enclosure after less than one week.

Dickerson Park Zoo


Successful
1.0 w/0.2 Leontopithecus chrysomelas (mother/ juvenile daughter)
2.0 (father/son) w/1.1 Leontopithecus chrysomelas (adult pair)
Comments: Used howdy stalls for approximately one month or so, depending on aggression or activity.

Unsuccessful
1.0 W/3.0 Leontopithecus chysomelas
Comments: L. chrysomelas attacked callimico. Tried to howdy for approximately three months without
success.

Dreher Park Zoo


Successful
0.3 w/1.1 Leontopithecus rosalia
Comments: Callimico group was first introduced to the male tamarin. Female introduced later. Animals
were simply put together into the same exhibit without prior exposure to each other.

National Zoological Park


Successful
Group (no numbers given) w/0.0.2 Kerodon rupestris
Comments: Kerondon chased the callimico but no aggression by the younger rodents was ever observed.
Grooming of the young K. rupestris by the callimico occurred daily (Xanten 1990).
1.0 w/1.0 Callthrix melanura and 1.0 Leontopithecus rosalia
Comments: Housed in an outdoor exhibit during summer months. No aggression observed during early
stage of introduction and animals were grooming and huddling together within two weeks. Trio did well
together until separated after being brought indoors to avoid cold weather (Xanten 1990).

Saint Louis Zoological Park

12
Successful
1.3 (pair and two daughters) w/2.0 Leontopithecus chrysomelas (siblings)
Comments: First introduced through mesh that separated holding cages. Actual introduction occurred on
exhibit to give animals more room. Some initial chasing of the tamarins by oldest juvenile callimico, but
never any fights. Allogrooming has been seen between species.

Callithrix melanura

National Zoological Park


Successful
1.0 w/1.0 Callimico goeldii and 1.0 Leontopithecus rosalia
Comments: Housed in an outdoor exhibit during summer months. No aggression observed during early
stage of introduction and animals were grooming and huddling together with two weeks. Trio did well
together until being separated after being brought indoors to avoid cold weather (Xanten 1990).
Unspecified number of individuals w/Myoprocta pratti, Octodon degus (Xanten 1990)

Unsuccessful
Unspecified number of individuals w/Kerodon rupestris
Comments: Kerodon chased the marmosets. Aggressive kerodon were removed and replaced with
younger animals. Combination worked for nearly 12 months until these animals also began to chase the
marmosets.
1.1 w/1.1 breeding pair Callicebus moloch and 1.1 offspring
Comments: Initially, both groups appeared to be frightened of each other, but the marmosets settled down
within two days. No actual aggression observed but the titis showed signs of being severely intimidated by
the titis, spending all of their time at floor level in the exhibit. The marmosets were removed from the
exhibit thereafter (Xanten 1990).

Callithrix jacchus

Audubon Zoological Garden


Successful
2.1 w/0.2 Ateles Sp.
Comments: Both species housed on an island during the day and brought into indoor holding cages at
night. Original introduction was done by putting the marmosets inside of a 2 1/2' x 2 1/2' cage with a
nestbox and putting the cage on the spider monkey island. This was done for two weeks, bringing the
spider monkeys into a holding area at night while leaving the marmosets on the island. They were then
given access to the island alone for two days. The spider monkeys were then given access to the island
with the marmosets. Introduction was uneventful.

Columbus Zoological Gardens


Successful
Adult breeding pair w/many offspring combinations w/1.1 two-toed sloth (Choloepus didactylus)
Comments: Sloths placed in the exhibit after the marmosets had acclimated.

Happy Hollow Zoo


Unsuccessful
1.0 w/0.1 Saguinus oedipus

Omaha's Henry Doorly Zoo


Unsuccessful
1.2 w/1.1 Saguinus oedipus
Comments: Both species were free ranging in large rainforest exhibit. The marmosets were removed after
aggressive attacks by the tamarins.
Virginia Zoo

13
Successful
1.0 w/1.1 prehensile-tailed porcupine (Coendu prehensilis) and 0.1 green acouchi (Myoprocta pratti)
Comments: This combination is described as being successful although the marmoset sustained a bite
wound on its arm which was believed to have been inflicted by the acouchi. Exhibit is approximately 22'
long x 12' deep x 8' high.

Little Rock Zoological Garden


Unsuccessful
1.1.1 w/1.3 Pithecia pithecia, 1.0 two-toed sloth (species?)
Comments: All three species lived in complete harmony. The male saki became very protective of the
marmosets. The sloth was in a nocturnal situation and only came out at night while primates were sleeping.
This combination failed only because the marmosets preferred to eat the canned primate food that was
intended for the sakis resulting in an imbalance of Vitamin D3. Originally, the marrmosets were placed in
air kennel in exhibit for several hours before releasing them. No problems were observed.

Callithrix geoffroyi

Philadelphia Zoo
Successful
3.0 (siblings—three year old and two-and-a-half-year-old twins) w/2.0 Leontopithecus chrysomelas
1.2 ( 8-year-old female and three-year-old male twins) w/2.0 Leontopithecus chrysomelas
Comments: In both introductions, marmosets were brought into the tamarin exhibit in a kennel case and
remained there for a short period of time before being released. Behavior was closely monitored
throughout the day following release.
1.0 (one year old ) w/1.0 (six year old) Saguinus leucopus

Unsuccessful
1.0 and 1.0 Saguinus leocopus w/1.0 Cebuella pygmaea
Comments: This introduction was unsuccessful because the other two animals intimidated the Cebuella.
He spent most of the time hiding in the exhibit. The other two animals ate the special diet made for the
Cebuella no matter where it was placed. Introduction was done with the Cebuella being put into the exhibit
in a howdy cage for a short time and then eventually released.
4.5 (breeding pair and seven offspring) w/1.3 six-banded armadillos (Euphractus sexcinctus)
Comments: Only problem occurred when an injured marmoset fell to the ground and was bitten by the
female armadillo.
1.1.2 family group. w/0.1 acouchi (Myoprocta pratti)
Comments: Combination worked well until two of the younger marmosets were bitten during the
confusion of two catch ups within days of each other. Acouchi was then moved to a larger exhibit.
12-15 group of large, mixed-sex, various-aged group w/1 saffron toucanet (Baillonicus bailloni)
Comments: Marmosets attacked the toucanet.
12-15 group of large, mixed-sex, various-aged group w/2 kerodons
Comments: Combination worked well until the breeding female marmoset gave birth. The marmosets
then attacked the kerodons.
4.5 w/1.1 six-banded armadillos and 1.0 kerodon
Comments: Marmosets displayed minor aggression towards the kerodon. Kerodon removed from exhibit
after one-and-a-half weeks.
1.0 w/1.0 Saguinus leucopus and 1.0 kerodon
Comments: Kerondon attacked the tamarin on two separate occasions, inflicting a bite wound in one of
them. Kerodon was removed from the exhibit after one month. Callithrix geoffroyi has also been reported
to have been successfully exhibited with Callicebus moloch, Cebuella pygmaea, Leontopithecus rosalia,
and Myoprocta pratti (Xanten 1990).

Callithrix kuhli

14
Indianapolis Zoo
Successful
1.1 adults w/1.1 adult Leontopithecus rosalia, unspecified numbers of Brazilian cardinals, saffron finches,
turquoise tanagers, Dsyprocta, yellow-footed tortoise
Comments: The marmosets and tamarins were housed next to each other in small cages before put
introduction in large exhibit. The male marmoset was put in after the others were in the exhibit and was
released with no previous exposure to the others. No problems noted. The marmosets have caught and
eaten one of the saffron finches.

Cebuella pygmaea

Lincoln Park Zoo


Successful
2.1 w/1.1 Saguinus imperator subgrisescens (handreared twins) w/1.1 Saguinus imperator subgrisescens
(breeding pair)
Comments: Put into side-by-side holding cages and then into the same holding cage. Allowed into exhibit
for first time together. The tamarins are fed separately in holding to prevent them from eating the
marmosets' food.

Folsom Children’s Zoo


Successful
Unspecified number w/Iguana iguana and red-footed tortoise (Geocheloni carbonaira)

National Zoological Park


Successful
1.0 w/1.1 adult and 1.2 juvenile Leontopithecus rosalia
Comments: The marmoset was shy and spent a great deal of time during the first two months of the
introduction hiding from the tamarins in thick foliage. He eventually began to run and interact with the
tamarins as well as groom, huddle, and sleep with them.

Unsuccessful
1.1 w/1.1 adult Callicebus moloch and 1.1 offspring
Comments: Both marmosets developed intestinal inflammation that was considered to be stress-related.
2.1 w/1.1 adult Callicebus moloch and 1.1 offspring
Comments: Combination lasted only one day because one of the male marmosets was stressed by attacks
by the other male marmoset (Xanten 1990).

Philadelphia Zoo
Successful
6.1 (breeding female and six male offspring) w/1.1 Leontopithecus chrysomelas
Comments: These groups were first combined unsuccessfully while the female marmoset's mate and sire
of the six offspring was part of the group. See below under "Unsuccessful."
7.1 w/1.3 Saguinus labiatus (adult male and 3 female offspring) and 2.0 golden-rumped agoutis (Dasyprocta
cristata)
Comments: Marmoset group is same as above but with addition of six-year-old breeding male. Mixture of
primate species seemed to work well, but four days after the initial introduction the breeding male
marmoset was found dead with injuries most likely inflicted by one of the agoutis.

Unsuccessful
7.1 w/1.1 Leontopithecus chrysomelas
Comments: Same group of marmosets and tamarins as listed above but with the addition of breeding male
marmoset. This individual periodically intensely chased the female tamarin, which caused her to hide and
prevented her from obtaining food.
1.0 w/1.0 Callithrix geoffroyi and 0.1 Saguinus leucopus

15
Comments: The marmoset was intimidated by the other two animals and spent most of the time hiding
from them in the exhibit. The other two animals ate the special diet made for the marmoset regardless of
where it was placed. Eventually, he was removed due to failing health.

Sedgwick County Zoo


Successful
2.0 w/1.1 Leontopithecus rosalia and Hoffman's two-toed sloth (Choelopus hoffmanni)
2.0 w/1.1 Leontopithecus chrysomelas and Hoffman's two-toed sloth (Choelopus hoffmanni)
Comments: One Leontopithecus species was exhibited with the marmoset pair for short periods of time (1
week). Alternated weekly between the Leontopithecus pairs.

Leontopithecus chrysomelas

Chicago Zoological Park


Successful
1.0 w/1.0 Callimico goeldii
1.0 w/1.0 Callimico goeldii
Comments: Both tamarins were housed with the same callimico on separate occasions. Paired in "neutral"
cage to offset any dominance advantage that might result from pairing occurring in home territory of either
animal. No serious problems were observed, but chasing of the Leontopithecus from the food bowl by the
Callimico at feeding time was initially a problem. Pair is now fed in separate bowls.
1.0 w/0.1 Saguinus oedipus
Comments: Pair copulates frequently. Female is contracepted with melangesterol acetate implant.

Unsuccessful
1.1 w/1.1 Callimico goeldii
Comments: Callimico pair was introduced into the tamarins' cage and interactions were closely observed
for the first two hours. Female callimico exhibited prosexual behaviors and directed pilo-solicit display
toward male tamarin. The following day the female callimico and female tamarin fought resulting in a
severe bite wound to the tamarin. Pair was immediately separated.

Dickerson Park Zoo


Successful
0.2 (mother and daughter) w/1.0 Callimico
1.1 w/2.0 (father and son) Callimico
Comments: howdy stalls for approximately one month, depending on aggression or activity.

Unsuccessful
3.0 (adults) w/1.0 adult Callimico
Comments: Callimico was attacked by the tamarins. Attempted to reintroduce by housing the callimico in
howdy cage for approximately three months, but reintroduction failed.

Folsom Children’s Zoo


Successful
Leontopithecus chrysomelas (no numbers/age/sex composition cited) w/green acouchi (Myoprocta pratti).
Leontopithecus chrysomelas (no numbers/age/sex composition cited) w/two-toed sloth (Choloepus didactylus)
Comments: Achouchis will eat newborn tamarins that fall to the ground.
1.0 w/1.0 Leontopithecus rosalia and 0.1 Saguinus mystax.
Comments: New animal was put into air kennel for 1 day and then released in exhibit. No aggression
observed.

Philadelphia Zoo

16
Successful
1.1 w/6.1 Cebuella pygmaea
Comments: These groups were first combined unsuccessfully while the female marmoset's mate and sire
of the six offspring was part of the group. See below under "Unsuccessful."
2.0 w/3.0 Callithrix geoffroyi (siblings—three years old and one-and-a-half-year-old twins)
2.0 w/1.2 Callithrix geoffroyi
Comments: In both introductions, marmosets were brought into the exhibit of the tamarins in a kennel
case and remained there for a short period of time before being released. Behavior was closely monitored
throughout the day following release.

Unsuccessful
1.1 w/7/1 Cebuella pygmaea
Comments: Same group of marmosets and tamarins as listed above but with the addition of breeding male
marmoset. This individual periodically intensely chased the female tamarin female that caused her to hide
and prevented her from obtaining food. For introduction, the tamarins were brought into the exhibit in a
kennel and introduced as in the previous cases.

Saint Louis Zoo


Successful
2.0 (siblings) w/1.3 Callimico goeldii (breeding pair and juvenile daughters)
Comments: Some initial chasing of the tamarins by oldest juvenile callimico, but never any fights.
Allogrooming has been seen between species. The tamarins were separated from the adult female
callimico for several weeks after she gave birth and then reunited without problems.

Sedgwick County Zoo


Successful
1.1 w/2.0 Cebuella pygmaea and Hoffman's two-toed sloth (Choloepus hoffmanni)
Comments: This tamarin pair is housed with the above species for short periods of time and then
alternated with L. rosalia.

Leontopithecus rosalia

Audubon Zoological Garden


Successful
1.0 w/1.1 Alouatta caraya and 2.2 Pithecia pithecia
Comments: The tamarin was first introduced to the female howler without incident in November 1992.
The male howler was added to this combination in June 1993, again without incident. 2.1 sakis were
introduced to the group in October 1993. In November 1993, the tamarin was observed grooming and
thrusting against the male howler. In December 1993, the tamarin attacked the male howler, inflicting
wounds on his hands and feet. The tamarin began to chase the howler frequently. After a few weeks the
howler reestablished dominance and problems ceased.

Burnett Park Zoo


Successful
1.1 w/0.2 blue-crowned motmot (Momotus momota), 1.1 tinamou (Tinamus Sp.), 1.1 Troupial (Icterus icterus),
1.1 yellow-billed cardinal (Paroaria capitata), and 1.1 crested cardinal (Paroaria coronata)
Comments: Birds were added to the exhibit (with the addition of numerous perching sites) singly or in
pairs. The tamarins show little interest in the birds, but eat their food.

Cape May County Zoo


Successful
1.0 w/0.1 Saguinus midas midas
Comments: The L. rosalia was put into a 2' x 2' x 3' bird cage which was then put into the 7'x 7' x 7' cage
in which the S. midas was living. The L. rosalia was left in the small cage for a few days and then released.

17
Introduction went well. Grooming has been observed between the pair. Pair is now housed in an outdoor
run approximately 20'x 40'x 10' high with a 10'x 12' off-exhibit area.

Chicago Zoological Park


Successful
0.1 w/1.0 Callimico goeldii
Comments: Pair lived together for several years with no problems.
Various age/sex combinations of breeding pair and 2 - 5 offspring (various age/sex composition) w/2.1
breeding pair of Hoffman's two-toed sloth (Choloepus hoffmanni) w/one offspring and 2.0 green acouchi
(Myoprocta pratti)
Comments: Species has been exhibited with two-toed sloths more or less uneventfully since 1984. Group
composition of tamarins is now 0.2 offspring of original breeding pair sharing the exhibit with a single
female sloth. Exhibit is an "island" with naturalistic trees. Tamarins are trained to come into a holding area
at night where they are fed. Sloth remains in the exhibit at night and is fed there after the tamarins are
brought in. Sloth inflicted a serious bite wound on the hand of one of the tamarins resulting in fracture.
This has only occurred once. Tamarins are no longer exhibited with acouchis, but few interactions
occurred between the species when they were together. The island on which the tamarins and sloth are
exhibited is part of a much larger exhibit from which the island is isolated. Several species of free-ranging
birds have at times lived in the exhibit and occasionally land momentarily on the island and are usually
chased away by the tamarins. These species have included Toco toucans (Rhamphastos toco), keel-billed
toucans (Rhamphastos sulfuratus), cattle egrets (Ardeola ibis), red-crested cardinals (Paroaria coronata),
Mexican cacicques (Cassiculus melanicterus), king vultures (Sarcoramphus papa), bare-throated bellbirds
(Procnias nudicollis), turquoise tanagers (Tangara mexicana), sun conures (Aratinga solstitialis), piping
guans (Arburria pipile), saffron toucanet (Baillonicus bailloni), plush-crested jays (Cyanocorax chrysops),
blue-crowned Motmot (Momotus momota), and common trumpeters (Psophia creptitans).
0.2 w/1.0 agouti (Dasyprocta cristata)
Comments: One of the tamarins routinely "rode" the agouti, clinging to its back. Agouti was very docile
and no negative interactions occurred.

Dreher Park Zoo


Successful
1.1 w/0.3 Callimico goeldii
Comments: The male tamarin was introduced to the callimico group first. The female was introduced
later. The animals were simply put into the exhibit together without prior exposure.

El Paso Zoo
Successful
2.2 w/red-crested cardinals, green aracari (Pteroglossus viridis), common trumpeters (Psophia crepitans), red-
rumped caciques (Cacicus haemorrhous), white-crown pigeon (Zenaida asiatica) and silver-beaked
tanagers (Ramphocelus carbo)
Comments: Also have been exhibited with green acouchis (Myoprocta pratti). All animals put in the with
the tamarins are first introduced to the exhibit in "howdy" cage from 2-3 days. Aggression has never been a
problem. Trumpeters steal mealworms/food from the tamarins and will occasionally chase them or peck at
them. No injuries occurred to date.

Folsom Children’s Zoo


Successful
Leontopithecus rosalia (no numbers/age/sex composition cited) w/green acouchi (Myoprocta pratti)
Leontopithecus rosalia (no numbers/age/sex composition cited) w/two-toed sloth (Choloepus didactylus)
Comments: No special introductions. Acouchis will eat newborn tamarins that fall to the ground.

Gulf Breeze Zoo


Successful
1.0 w/1.0 Leontopithecus chrysomelas and 0.1 Saguinus mystax
1.0 w/1.0 Saguinus midas midas
Comments: New animal was put in air kennel for 1 day then released in exhibit. No aggression observed.

18
Indianapolis Zoo
Successful
1.1 w/1.1 Callithrix kuhli and unspecified numbers of Brazilian cardinals, saffron finches, turquoise tanagers,
dasyprocta (species?), yellow-footed tortoises
Comments: The marmosets and tamarins were housed next to each other in small cages before being put
together in the large exhibit. The male marmoset was put in after the others were the exhibit and was
released with no prior exposure them.

National Zoological Park


Successful
1.0 w/1.0 Callimico goeldii and 1.0 Callithrix melanura
Comments: Housed in an outdoor exhibit during summer months. No aggression observed during early
stage of introduction and animals were grooming and huddling together within two weeks. Trio did well
together until being separated after being brought indoors to avoid cold weather (Xanten 1990).
2.3 (breeding pair and 1.2 juveniles) w/1.0 Cebuella, Myoprocta pratti, Euphractus sexcinctus, and Choloepus
didactylus (Xanten 1990).
Comments: Xanten (1990) reports that 1.0 Cebuella was introduced to 1.1 adult and 1.2 juvenile
Leontopithecus rosalia. The Cebuella was shy and spent a great deal of time during the first two months of
the introduction hiding from the tamarins in thick foliage. Eventually, he began to run and interact with the
tamarins as well as groom, huddle, and sleep with them.
Family group (no numbers/age/sex composition cited) w/2.1 Callicebus moloch
Comments: The tamarins were housed in an outdoor enclosure separated from a heavily planted indoor
enclosure by a wiremesh introduction door. The titis were put into the indoor enclosure. Introduction door
was removed after one week. The titis were initially intimidated by the tamarins, particularly the males,
who would rush towards them as a group. The titis would spend time on the floor of the enclosure to avoid
the tamarins but, after three weeks, shifted their perching area to another part of the enclosure where they
felt more secure. This combination is reported to have been successful (Xanten 1990).

Unsuccessful
Unspecified number w/1.1 Pithecia pitheca
Comments: Combination broke down after approximately one year. Males of both species fought
resulting in injuries to both.

Omaha's Henry Doorly Zoo


Successful
1.1 w/1.1 Saguinus geoffroyi
Comments: See previous entry. The pair of Saguinus geoffroyi seemed to coexist well with the golden
lion tamarins with virtually no signs of aggression following the removal of the Saguinus midas pair until
the golden lion tamarins died.
Unsuccessful
1.1 w/1.1 Saguinus geoffroyi and 1.1 Saguinus midas midas
Comments: This combination was successful for seven months until the S. geoffroyi began attacking the
male S. midas. The Saguinus midas were removed from the exhibit. A reintroduction was attempted but
with the same results.

Pueblo Zoo
Successful
Unspecified number w/unspecified number of Myoprocta pratti
Comments: Introduced in a “howdy” cage to see interactions. Interactions between the species were
apparently not problematic but the acouchis were separated from the tamarins because of health problems
of the acouchis associated with the amount of marmoset diet that they were eating.

19
Roger Williams Park Zoo
Successful
Unspecified number w/red-capped cardinal (Paroaria coronata), blue-grey tanager (Thraupis episcopus),
southern lapwing (Vanellus chilensis), and green basilisk
Comments: Smaller animals were briefly placed in a “howdy” cage within the tamarin's exhibit.

Riverbanks Zoo
Unsuccessful
Unspecified number of animals w/Alouatta caraya and Dasyprocta cristata
Comments: Mix reported to have worked for a while, but the male tamarin was found severely bitten.
Unknown which other species caused the wound but the tamarin was removed.

Sedgwick County Zoo


Successful
1.1 w/2.0 Cebuella pygmaea and two-toed sloth (Choloepus hoffmanni)

Saguinus fuscicollis

Riverbanks Zoo
Successful
Saguinus fuscicollis (no numbers/age/sex composition cited) w/Phallanger gymnotis
Comments: Reported to have mixed these species without difficulty.

Saguinus geoffroyi

Omaha's Henry Doorly Zoo


Successful
1.1 w1.1 Leontopithecus rosalia
Comments: See previous entry under "Unsuccessful." The pair of Saguinus geoffroyi seemed to co-exist
well with the golden lion tamarins with virtually no signs of aggression following the removal of the
Saguinus midas pair. This combination was successful until the golden lion tamarins died.

Unsuccessful
1.1 w/1.1 Saguinus geoffroyi and 1.1 Saguinus midas midas
Comments: This combination was successful for seven months until the S. geoffroyi began attacking the
male S. midas. The Saguinus midas were removed from the exhibit. A reintroduction was attempted but
with the same results.
1.1 w/1.1 Saguinus oedipus and 1.1 Leontopithecus rosalia
Comments: All three species were free ranging in rainforest exhibit. Cotton-tops removed because of
aggression towards the Geoffrey’s tamarins.
1.1 w/1.1 Leontopithecus rosalia and 1.1 Saguinus midas midas
Comments: This combination was successful for seven months. Geoffrey’s tamarins began attacking the
male Saguinus midas. The Saguinus midas were removed from the exhibit. A reintroduction was attempted
but with the same results.

Pueblo Zoo
Successful
Unspecified number w/unspecified number of Myoprocta pratti
Comments: Introduced in a “howdy” cage to see interactions. Interactions between the species were
apparently no problem, but the acouchis were separated from the tamarins because of health problems of
the acouchis associated with the amount of marmoset diet that they were eating.

20
Saguinus imperator

Lincoln Park Zoo


Successful
1.1 w/2.1 Cebuella pygmaea
Comments: Put in side-by-side holding cages then into same holding cage. Allowed into exhibit for first
time together. The tamarins were fed separately in holding to prevent them from eating the marmosets'
diet.

Sunset Zoological Park


Successful
1.0 w/unspecified number of green acouchi (Myoprocta pratti), unspecified number of green iguana, and
unspecified number of red-footed tortoise (Geocheloni carbonaira) and unspecified number of emerald green
toucanets
Comments: The exhibit in which all introductions took place was built to house tamarins. For each
introduction of additional animals after the tamarins, the tamarins were placed in a "howdy" cage for a
time such that the keepers and curatorial staff felt the other species in the exhibit had become use to them.
Potentially aggressive species were then put into the "howdy" cage. The tamarins were released to allow
them to become more familiar with the exhibit so that if aggression occurred the monkeys would know
where to go for security and so that they would not panic and injure themselves navigating the exhibit. The
emerald green toucanets can be aggressive. There were some minor nips from them with only a torn nail as
any injury recorded. Eventually the tamarin became bold enough and could face down the toucanets in a
confrontation. They continue to be mildly hostile towards each other.

Saguinus labiatus

Burnett Park Zoo


Unsuccessful
1.1 w/1.1 Saguinus oedipus
Comments: Cotton-tops were too aggressive for the red-bellied tamarins.

National Zoological Park


Successful
Group (no numbers/age/sex composition cited) w/green acouchi (Myoprocta pratti), La Plata three-banded
armadillo (Tolypeutes matacus), degus (Octodon degus), and Kerodon rupestris (Xanten 1990)

Philadelphia Zoo
Successful
1.3 (14-year-old male and three female offspring) w/2.0 golden-rumped agoutis (Dasyprocta cristata)
Comments: This group was a successful mix to a certain extent. There were no signs of aggression seen
between the two species but there were two unexplained deaths of tamarins several years apart. They were
obviously due to cage-mate aggression, but the source was unconfirmed.

Unsuccessful
1.3 w/(same group as above) w/2.0 golden-rumped agoutis (Dasyprocta cristata) and 7.1 Cebuella pygmaea
Comments: The marmoset group was introduced into the enclosure of the tamarins and agoutis. The
agoutis took an interest in the fast movements and small body size of the marmosets as soon as they were
introduced. The marmosets were just as curious and tended to venture close to the agoutis. After hours of
observation the marmosets began to stay away from the agoutis and monitoring of the exhibit slowly
decreased. The two primate species seemed to work well together, but four days after the initial
introduction, the breeding male marmoset was found dead with injuries most likely caused by the agoutis.

21
Saguinus leucopus

Philadelphia Zoo
Successful
0.1 w/1.0 Callithrix geoffroyi

Unsuccessful
0.1 w/1.0 Callithrix geoffroyi and 1.0 Kerodon rupestris
Comments: Kerodon attacked the tamarin on two separate occasions, inflicting a bite wound in one of
them. Kerodon was removed from the exhibit after less than a month.

Saguinus midas midas

Cape May County Zoo


Successful
1.0 w/0.1 Leontopithecus rosalia
Comments: The golden lion tamarin was put into a 2' x 2' x 3' bird cage which was then put into the 7'x 7’
x 7' cage in which the Saguinus midas was living. The golden lion tamarin was left in the small cage for a
few days and then released. Introduction went well. Grooming has been observed between the pair. Pair is
now housed in an outdoor run approximately 20'x 40'x 10' high with a 10'x 12' off-exhibit area.

Gulf Breeze Zoo


Successful
1.0 w/1.0 Leontopithecus rosalia
Comments: New animal was put into air kennel for one day then released into exhibit. No aggression
observed.

Omaha's Henry Doorly Zoo


Successful
1.1 w/2.2 Alouatta caraya, 0.1 agouti (Dasyprocta agouti), 2.2 ringed teal, 2.2 white-faced whistling duck, 2.2
green iguana
Comments: Island-type exhibit. Primary introduction was done in holding areas prior to release on the
island. Inter- and intraspecies introductions always occur in the holding areas. Initially, the species are
given access to a common fence for limited periods of time, with keeper supervision. As the integration
progresses, both species are allowed to investigate each other's cages and transfer alleys. In most situations,
the cages are set up in a pattern that allows for many escape routes. In the final phase of the introduction,
each species is given access to the island without the other species present. This enables each group to
familiarize itself with the habitat without the pressure of defending a territory. The species in holding can
see the other species on the island, and the groups are switched daily. After the keepers are comfortable, an
introduction is performed with supervision throughout the day. The animals are separated at night in the
sleeping quarters if any antagonism is exhibited.

Unsuccessful
1.1 w/1.1 Leontopithecus rosalia and 1.1 Saguinus geoffroyi
Comments: This combination was successful for seven months until the S. geoffroyi began to attacking
the male S. midas. The S. midas were removed from the exhibit. A reintroduction was attempted but with
the same results.

Santa Ana Zoo


Successful
3.0 w/1.2 two-toed sloths (Choloepus hoffmanni), 0.2 agouti (Dasyprocta cristata), 1.1 toucan, 2.0 tinamou
(Tinamu Sp.), and 2.5 green iguana
Comments: All of these species were housed in a 50' x 25' x 16' heavily planted, outdoor, welded-wire
exhibit with a 10' x 20' attached indoor building to which all animals had constant access. Each species
introduced as it finished quarantine.

22
Saguinus mystax

Gulf Breeze Zoo


Successful
0.1 w/1.0 Leontopithecus rosalia and 1.0 Leontopithecus chrysomelas

Saguinus oedipus

Akron Zoological Park


Successful
1.3 w/1.0 green iguana and 1.1 chinchilla (Abrocoma Sp.)
Comments: All three species were put into the exhibit at the same time with no problems.

Burnett Park Zoo


Unsuccessful
1.1 w/1.1 Saguinus labiatus
Comments: Cotton-tops were too aggressive for the red-bellied tamarins.

Chicago Zoological Park


Successful
0.1 w/1.0 Leontopithecus chrysomelas
Comments: Pair copulates frequently. Female contracepted with melangesterol acetate implant.

Happy Hollow Zoo


Unsuccessful
0.1 w/1.0 Callithrix jacchus
Comments: No other information given.

Houston Zoological Gardens


Successful
1.1 (handreared) w/1.1 Alouatta caraya
Comments: Both species are housed in a naturalistic exhibit during the day and are trained to respond to
separate auditory signals to come into separate holding cages at night. Both species are freely offered
primate chow and canned diets but do not receive produce unless they come off exhibit at night. The
tamarins are well trained and regularly come off exhibit at night.

Omaha's Henry Doorly Zoo


Successful
1.1 w/1.0 Lagothrix lagotricha, 2.0 Pithecia pithecia, 2.4 Saimiri Sp., 1.1 Tapiris terrestris, 1.1 American avocet
(Recurvirosta americana), 1.1 spurwinged plover, 1.1 crested screamer (Chauna torquata), 1.1 green iguana, 1.0
tamandua (Tamandua tetradactyla)
Comments: Island-type exhibit. Primary introduction was done in holding areas prior to release on the
island. Inter- and intraspecies introductions always occur in the holding areas. Initially, the species are
given access to a common fence for limited periods, with keeper supervision. As the integration
progresses, both species are allowed to investigate each other's cages and transfer alleys. In most situations,
the cages are set up in a pattern that allows for many escape routes. In the final phase of the introduction,
each species is given access to the island without the other species present. This enables each group to
familiarize itself with the habitat without the pressure of defending a territory. The species in holding can
see the other species on the island, and the groups are switched daily. After the keepers are comfortable, an
introduction is performed with supervision throughout the day. The animals are separated at night in the
sleeping quarters if any antagonism is exhibited.

23
Unsuccessful
1.1 w/1.2 Callithrix jacchus
Comments: Both species free-ranging in large rainforest exhibit. Common marmosets were removed after
aggressive attacks by the cotton-tops.

Pueblo Zoo
Successful
Unspecified number w/unspecified number of Myoprocta pratti
Comments: Introduced in a “howdy” cage to see interactions. Interactions between the species were
apparently not problematic but the acouchis were separated from the tamarins because of health problems
of the acouchis associated with the amount of marmoset diet that they were eating.

Riverbanks Zoological Park and Botanical Garden


Unsuccessful
1.1 w/sloths and acouchis (Myoprocta pratti)
Comments: Tamarins reported to have attacked both species.

Roger Williams Park Zoo


Successful
0.0.1 w/two-toed sloth
Comments: Animals were all placed together in a new exhibit.

Unsuccessful
1.0 w/1.0 Pithecia pithecia
Comments: Males were housed in adjoining enclosures for several weeks. Animals were allowed access
to each other’s enclosures under close observation by the keeper staff. On the first day, male saki became
aggressive towards the tamarin. The tamarin became aggressive towards the saki on the second day. On the
third day, the two were separated after the saki suffered superficial injuries.

Unspecified number w/golden-rumped agouti (Dasyprocta cristata)


Comments: Agouti killed a juvenile tamarin and injured an adult. Animals were all placed together in a
new exhibit.

Saint Louis Zoological Park


Successful
0.2 w/1.1 Pithecia pithecia
Comments: First introduction done through screen between holding cages. Actual introduction was done
on exhibit to give animals more room. Some chasing of the tamarins by the male saki but no contact or
fighting. Species were left together thereafter with no problems. Little interaction was obsreved between
the species. Fed separately due to separate diets.

Sunset Zoological Park


Successful
2.1 w/unspecified number of green acouchi (Myoprocta pratti), unspecified number of green iguana, and
unspecified number of red-footed tortoise (Geocheloni carbonaira)
Comments: The exhibit in which all introductions took place was built to house tamarins. For each
introduction of additional animals after the tamarins, the tamarins were placed in a "howdy" cage for a
time such that the keepers and curatorial staff felt the other species in the exhibit had become use to them.
Potentially aggressive species were then put into the "howdy" cage. The tamarins were released to allow
them to become more familiar with the exhibit so that if aggression occurred the monkeys would know
where to go for security and so that they would not panic and injure themselves navigating the exhibit.

24
APPENDIX 2. RESULTS OF MIXED-SPECIES COMBINATIONS FOR CEBIDAE

Alouatta

Audubon Zoological Garden


Successful
1.1 Alouatta caraya w/1.0 Leontopithecus rosalia And 2.2 Pithecia pithecia
Comments: The tamarin was introduced first to the female howler without incident in November 1992.
The male howler was added to this combination in June 1993, again without incident. 2.1 sakis were
introduced to the group in October 1993. In November 1993, the tamarin was observed grooming and
thrusting against the male howler. In December 1993, the tamarin was observed attacking the male howler,
inflicting wounds on his hands and feet. The tamarin began to chase the howler frequently. After a few
weeks the howler reestablished dominance and problems ceased. The howler/saki introduction went well.
The male saki is an easily intimidated animal and seemed stressed by the male howler's activity. Sakis and
howlers are separated at night. A female saki was born into this group following the original introduction
of 2.1 sakis to the howlers. This individual has no fear of the howlers and sits against them and tries to steal
food from their mouths.

Folsom Children’s Zoo


Successful
Alouatta caraya (no numbers/sex given) w/meerkat (Suricata suricata) adults of both species
Comments: Combination was an experiment to determine how the howlers would react to another animal
because institution plans on mixing howlers with a callitrichid species in the future.

Houston Zoological Gardens


Successful
1.1 Alouatta caraya w/1.1 handreared Saguinus oedipus
Comments: Both species are housed in a naturalistic exhibit during the day and are trained to respond to
separate auditory signals to come into separate holding cages at night. Both species are freely offered
primate chow and canned diets but do not receive produce unless they come off exhibit at night. The
tamarins are well trained and regularly come off exhibit at night.

1.1 Alouatta caraya w/1.2 chickens (Gallus gallus)


Comments: Chickens were introduced as an experiment to see how the howlers would do with birds.
Occasionally, the male howler would hang by his tail and try to play with the rooster by grabbing feathers.
The chickens have since been removed.

Unsuccessful
1.1.1 Alouatta caraya w/0.0.1 yellow-knobbed currasow (Crax daubentoni)
Comments: Howlers were instantly aggressive to the currasow, possibly being protective of infant.

Lincoln Park Zoo


Successful
1.2.1 Alouatta caraya w/3.3 Saimiri sciureus
Comments: Saimiri were given access to exhibit for a couple of days prior to the howlers being given
access. No problems were observed with the introduction. Each group enters and exits exhibit through
separate shift doors. Fed main meal off exhibit in separate holding areas.

Unsuccessful
1.0 Alouatta caraya w/1.0 Callicebus Sp.
Comments: This pairing was successful for about one year. Titi monkey sustained wound on tail, but the
cause was unknown. Pair was then separated.

25
Omaha's Henry Doorly Zoo
Successful
2.2 Aloutta caraya w/1.1 Saguinus midas midas, 0.1 agouti (Dasyprocta agouti), 2.2 ringed teal, 2.2 white-faced
whistling duck, 2.2 green iguana
Comments: Island-type exhibit. Primary introduction was done in holding areas prior to release on the
island. Inter- and intraspecies introductions always occur in the holding areas. Initially, the species are
given access to a common fence for limited periods, with keeper supervision. As the integration
progresses, both species are allowed to investigate each other's cages and transfer alleys. In most situations,
the cages are set up in a pattern that allows for many escape routes. In the final phase of the introduction,
each species is given access to the island without the other species present. This enables each group to
familiarize itself with the habitat without the pressure of defending a territory. The species in holding can
see the other species on the island, and the groups are switched daily. After the keepers are comfortable an
introduction is performed, with supervision throughout the day. The animals are separated at night in the
sleeping quarters if any antagonism is exhibited.

Unsuccessful
2.2 Alouatta w/1.3 Cebus albifrons and 2.2 Saguinus midas midas
Comments: Cebus were removed from the exhibit after three months because the howlers attacked them.
Cebus usually instigated confrontations with short, aggressive attacks on the howlers.

Pittsburgh Zoo
Successful
2.1 Alouatta caraya w/1.1 Pithecia pithecia
Comments: Animals have been together for four years, both species having reproduced. Species were put
together off-exhibit first, then allowed up on exhibit. Introduction was not unusual or significant.

Alouatta caraya w/Pithecia pithecia and Dasyprocta cristata and Bradypus Sp.
Comments: Non-primate species were introduced to the exhibit first. This allowed them to get
comfortable with the exhibit and to find their nest boxes, etc.

Riverbanks Zoological Park


Unsuccessful
Unspecified number of animals w/unspecified number of Leontopithecus rosalia and agoutis
Comments: Species were exhibited together for an unspecified amount of time until a male tamarin was
found severely bitten. Source of the bite wounds was unknown, but the tamarins were removed from the
exhibit.

Santa Ana Zoo


Unsuccessful
1.1 Alouatta caraya w/1.2 Cebus apella
Comments: Introduced to a large, open, island-type exhibit with 25' trees, and a water-filled moat and a
vertical back wall with entry tunnels for off-exhibit holding. The two species were first indoors with wire
between them. Each species was then given an opportunity to explore the outdoor exhibit. The two species
were then released together and were a successful combination for about one year until the group
composition changed. The female howler attacked one of the female cebus, causing a severe injury. This
cebus then had to be removed to heal and it became impossible to introduce any cebus thereafter.

Aotus

Caldwell Zoo
Successful
1.1 w/1.1 Saimiri Sp.
Comments: Both Aotus were approximately 18 years old. The female Saimiri was 11 years old and the
male was under one year. They were kept side by side for a short time prior to introducing the Saimiri to
the Aotus exhibit.

26
Unspecified number now housed with sloth.

Chicago Zoological Park


Successful
0.0.1 w/0.0.1 Choloepus hoffmanni
Comments: Aotus used the sloth as a "hammock" and slept on its stomach as it hung upside down.

Little Rock Zoological Gardens


Successful
1.1 aotus sp. w/1.1 two-toed sloth
Comments: The Aotus were released into the sloth exhibit after being held in a flight kennel in the exhibit
for several hours. No problems observed. The Aotus have actually been observed sleeping with and on the
stomach of the sloths.

Virginia Zoo
Successful
1.1.2 w/1.2 two-toed sloths (Choloepus hoffmanni) and 1.0 green acouchi (Myoprocta pratti)
Comments: Aotus have been observed clinging to the stomachs of the sloths.

Ateles

Audubon Zoological Garden


Successful
0.2 Ateles geoffroyi w/2.1 Callithrix jacchus
Comments: Both species housed on an island during the day and are brought into indoor holding cages at
night. Original introduction was done by putting the marmosets inside of a 2 1/2' x 2 1/2' cage with a
nestbox and putting the cage on the spider-monkey island. This was done for two weeks, bringing the
spider monkeys into a holding area at night while leaving the marmosets on the island. The marmosets
were then given access to the island alone for two days. The spider monkeys were then given access to the
island with the marmosets. Introduction was uneventful.

Chicago Zoological Park


Successful
3.5 Ateles geoffroyi w/group of up to 22 Saimiri Sp. of various age/sex composition, group of up to 14 Cebus
aaella of various age/sex composition, 1.0 Myrmacophagia trydactylus and 1.1 Tapirus terrestris
Comments: All species are exhibited together in a large (approximately 75'x 75’ x 70' high) naturalistic
exhibit with 30- 35' tall gunite trees connected by networks of vines, with cliffs, waterfalls, and a river. All
species are brought into separate holding areas at night. Ateles were introduced to the exhibit after the
Saimiri had first become familiar with the exhibit and were reliably coming into their holding cages at
night. Cebus apella were introduced to the exhibit after the Saimiri, followed by the Ateles. The tapirs and
giant anteater were introduced to the exhibit last. This combination of primates and mammals has been
extremely successful over the years. A post-reproductive female Ateles geoffroyi vellerosus formerly
exhibited developed a mutually affiliative relationship with the Saimiri group and seemed to be extremely
attracted to infant Saimiri. The Saimiri are seasonal breeders and each year after the infants had been born
it was difficult to get this female to come off of exhibit until after the Saimiri had gone into their holding
area. The Saimiri (adults as well as juveniles) engaged in social interactions with her and frequently sat on
her "lap" or clung to her back. The female Tapiris terrestris is a very docile animal and several of the
Ateles have been observed sitting on her back. The Giant anteater is also a docile animal but neither the
Ateles nor the other primates bother him. Negative interactions involving the spider monkeys have been
rare in this exhibit but one female chased separate male Saimiri out of the tops of trees in the exhibit on
two consecutive days, resulting in the death of one of them. After observing this behavior, this particular
female was kept off of exhibit for several weeks to break her of this pattern of behavior. An adult male
Ateles geoffroyi is very aggressive to two adult male Cebus apella and cannot be exhibited with them.
These two Cebus are alternated daily on exhibit with the male spider monkey so that the combination of
these three animals is never together.

27
A variety of bird species have also lived in the exhibit since its completion in 1984. These have
included Toco toucan (Ramphastos toco), keel-billed toucan (Ramphastos sulfuratus), cattle egret (Ardeola
ibis), red-crested cardinals (Paroaria coronata), Mexican Cacique (Cassiculus melanicterus), king vulture
(Sarcoramphus papa), bare-throated bellbirds (Procnias nudicollis), green and gold tanager (Tangara
schrankii), turquoise tanager (Tangara mexicana), sun conures (Aratinga solstitialis), piping guans (Aburria
pipile), saffron toucanet (Baillonicus bailloni), plush-crested jay (Cyanocorax chrysops), blue-crowned
motmot (Momotus momota), common trumpeters (Psophia crepitans), and black-faced dacnis (Dacnis
lineata). The large size of this exhibit makes interactions between the birds and the other animals rare.

Great Plains Zoo


Successful
1.0 Ateles geoffroyi W/1.0 Cercopithecus diana
Comments: Housed together in an off-exhibit area. No special introduction, animals were simply put
together.

Little Rock Zoological Gardens


Unsuccessful
1.4.2 Ateles Sp. w/1.2 Coatimundis (Nasua nasua)
Comments: Lived together for approximately one year, after which the spider monkeys were observed
catching coatimundis by the tails and lifting them off the ground. Coatimundis subsequently sustained
broken and infected tails, which in one instance had to be amputated.

Cacajao

Although there were no reports of Cacajao in mixed-species combinations from institutions to which the
questionnaire was sent, there are a few published accounts of various interspecific interactions between Cacajao
calvus rubicundus and other species of neotropical primates at Monkey Jungle in Goulds, Florida. This species
was formerly exhibited with Saimiri sciureus, Alouatta seniculus, Callimico goeldii, and Saguinus fuscicollis.
Social grooming between Saimiri and Cacajao has been observed in this exhibit (Abordo et al. 1975).
Infants and juveniles there reportedly exhibited play behaviors towards tamarins, while interactions
between adult Cacajao and Aloutta seniculus were described as hostile. Male uakaris frequently chased howlers
and caused the death of one by aggressively chasing it and causing it to fall from a tree (Fontaine 1981).

Callicebus

Chicago Zoological Park


Unsuccessful
1.2 w/0.1 handreared callimico
Comments: The handreared female callimico was very imprinted on people and had fought with
conspecifics in several housing situations. She began to attack the titis on the day after being introduced
into their enclosure. They had shown no aggression towards her and seemed to be intimidated by her
presence. She was removed from their enclosure after less than one week.

Lincoln Park Zoo


Unsuccessful
1.0 w/1.0 Alouatta caraya
Comments: Both animals allowed to become familiar with the exhibit while also being within visual
contact of the each other. This pairing was successful for about one year. The titi monkey sustained wound
on tail, but the cause was unknown. Pair was then separated.
1.0 w/3.0 Saguinus imperator subgriscecens
Comments: The titi monkey appeared to be intimidated by the group of tamarins.

28
National Zoological Park
Successful
2.1 Callicebus moloch w/unspecified number of Leontopithecus rosalia
Comments: The tamarins were housed in an outdoor enclosure separated from a heavily planted indoor
enclosure by a wiremesh introduction door. The titis were put into the indoor enclosure. Introduction door
was removed after one week. The titis were initially intimidated by the tamarins, particularly the males,
who would rush towards them as a group. The titis would spend time on the floor of the enclosure to avoid
the tamarins but after three weeks shifted their perching area to another part of the enclosure where they
felt more secure. This combination is reported to have been successful (Xanten 1990).
Callicebus moloch w/unspecified numbers of Myoprocta pratti, Euphractus sexcinctus, and Choloepus
didactylus (Xanten 1990)

Unsuccessful
1.1 Callicebus moloch and 1.1 offspring w/1.1 Cebuella pygmaea
Comments: Both marmosets developed intestinal inflammation that was considered to be stress-related
(Xanten 1990).
1.1 Callicebus moloch and 1.1 offspring w/2.1 Cebuella pygmaea
Comments: Combination lasted only one day because one of the male marmosets was stressed by attacks
by the other male marmoset (Xanten 1990).
1.1 Callicebus moloch and 1.1 offspring w/1.1 Callithrix melanura
Comments: Initially, both groups appeared to be frightened of each other but the marmosets settled down
in two days. No actual aggression observed but the titis showed signs of being severely intimidated by the
marmosets, spending all of their time at floor level in the exhibit. The marmosets were removed from the
exhibit thereafter (Xanten 1990).
Unspecified number of Callicebus moloch w/Kerodon rupestris
Comments: Kerondon chased and attacked the titis causing bite wounds (Xanten 1990).

Cebus

Chicago Zoological Park


Successful
Group of up to 14 Cebus apella of various age/sex composition, 3.5 Ateles geoffroyi, group of up to 22 Saimiri
Sp. of various age/ sex composition, 1.0 Myrmacophagia trydactylus and 1.1 Tapirus terrestris
Comments: All species are exhibited together in a large (approximately 75'x 75’ x 70' high) naturalistic
exhibit with 30- 35' tall gunite trees connected by networks of vines, with cliffs, waterfalls, and a river. All
species are brought into separate holding areas at night. Saimiri were introduced to the exhibit first,
followed by the Cebus, and finally the Ateles. The tapirs and giant anteater were introduced to the exhibit
after the primates. This combination of primates and mammals has been extremely successful over the
years. The cebus rarely, if ever interact with the tapirs or giant anteater. Negative interactions among the
primates have been relatively rare in this exhibit. An adult male Ateles geoffroyi is very aggressive to two
adult male Cebus apella and cannot be exhibited with them. These two Cebus are alternated daily on
exhibit with the male Ateles so that the combination of these three animals is never together.
Several of the juvenile Saimiri have also had close relationships with some of the juvenile Cebus apella
females and would often sit on their "laps" and engage in play behavior with them.
For approximately seven months from September 1994 through April 1995 this exhibit was closed for
renovations. Throughout this period, the two holding cages of the Saimiri, which are adjacent to the two
holding cages of the Cebus, were opened by a shift door to allow the two species to intermingle in all four
cages. No negative interactions were ever seen between the two species. Two female Cebus which are
subordinate in the group of seven other Cebus permanently share holding cages with the Saimiri because
they are too afraid to enter the holding cages of the Cebus group.
A variety of bird species have also lived in the exhibit since its completion in 1984. These have
included Toco toucan (Ramphastos toco), keel-billed toucan (Ramphastos sulfuratus), cattle egret (Ardeola
ibis), red-crested cardinals (Paroaria coronata), Mexican cacique (Cassiculus melanicterus), king vulture
(Sarcoramphus papa), bare-throated bellbirds (Procnias nucicollis), green and gold tanager (Tangara
schrankii), turquoise tanager (Tangara mexicana), sun conures (Aratinga solstitialis), piping guans (Aburria

29
pipile), saffron toucanet (Baillonicus bailloni), plush-crested jays (Cyanocorax chrysops), blue-crowned
motmot (Momotus momota), common trumpeters (Psophia crepitans), and black-faced dacnis (Dacnis
lineata). The large size of this exhibit makes interactions between the birds and the other animals rare.
However, Cebus apella in this exhibit seem to be opportunistic predators and have attacked ill or injured
birds that had landed on the ground.

Happy Hollow Zoo


Successful
1.0 Cebus apella w/0.1 Cebus hybrid

Omaha's Henry Doorly Zoo


Unsuccessful
1.3 Cebus albifrons w/2.2 Alouatta caraya and 1.1 Saguinus midas midas
Comments: Cebus were removed after three months because the howlers attacked them, although the
cebus usually instigated confrontations with short, aggressive attacks on the howlers.

Santa Ana Zoo


Unsuccessful
1.2 Cebus apella w/1.1 Alouatta caraya
Comments: Introduced to a large, open island-type exhibit with 25' trees, and a water-filled moat and a
vertical back wall with entry tunnels for off-exhibit holding. The two species were first introduced indoors
with wire between them. Each species was then given an opportunity to explore the outdoor exhibit. The
two species were then released together and were a successful combination for about one year until the
group composition changed. The female howler attacked one of the female cebus, causing a severe injury.
This cebus then had to be removed to heal and it became impossible to introduce any cebus thereafter.

Lagothrix lagotricha

Omaha's Henry Doorly Zoo


Successful
1.0 w/1.1 Saguinus oedipus, 2.0 Pithecia pithecia, 2.4 Saimiri Sp., 1.1 Tapirus terrestris, 1.1 American avocet
(Recurvirosta americana), 1.1 spurwinged plover, 1.0 tamandua (Tamandua tetradactyla)
Comments: Island-type exhibit. Primary introduction was done in holding areas prior to release on the
island. Inter- and intraspecies introductions always occur in the holding areas. Initially, the species are
given access to a common fence for limited periods of time, with keeper supervision. As the integration
progresses, both species are allowed to investigate each other's cages and transfer alleys. In most situations,
the cages are set up in a pattern that allows for many escape routes. In the final phase of the introduction,
each species is given access to the island without the other species present. This enables each group to
familiarize itself with the habitat without the pressure of defending a territory. The species in holding can
see the other species on the island, and the groups are switched daily. After the keepers are comfortable an
introduction is performed, with supervision throughout the day. The animals are separated at night in the
sleeping quarters if any antagonism is exhibited.

Unsuccessful
Group listed above under "successful" but with addition of 1.0 2-year-old handreared Pithecia pithecia
Comments: The wooly monkey attacked the handreared saki six months after it was introduced to the
grouping listed above. This saki did not socialize with any of the other primates and spent most of his time
on the ground by the tapirs.

Pittsburgh Zoo
Successful
Unspecified number w/unspecified number of Coendu prehensilis and Dasyprocta agouti
Comments: Non-primate species were introduced to the exhibit first. This allowed them to get
comfortable with the exhibit and to find their nest boxes, etc.

30
Pithecia pithecia

Audubon Zoological Garden


Successful
2.2 w/1.1 Alouatta caraya and 1.0 Leontopithecus rosalia
Comments: The tamarin was first introduced to female howler without incident in November 1992. The
male howler was added to this combination in June 1993, again without incident. 2.1 sakis were introduced
to group in October 1993. Howler/saki introduction went well. The male saki is an easily intimidated
animal and seemed stressed by the male howler's activity. Sakis and howlers are separated at night. A
female saki was born into this group following the original introduction of 2.1 sakis to the howlers. This
individual has no fear of the howlers and sits against them and tries to steal food from their mouths.

Dallas Zoo
Successful
1.1 w/1.2 two-toed sloths (Choloepus hoffmanni)
Comments: No special introduction. Animals were simply put together in the same cage.

Little Rock Zoological Gardens


Unsuccessful
1.3 w/1.1.1 Callithrix jcchus ad 1.0 two-toed sloth (species?)
Comments: All three species lived in complete harmony. 1.0 Pithecia became very protective of the
marmosets. Sloth was in a nocturnal situation and only came out at night while primates were sleeping.
This combination failed only because the marmosets preferred to eat the canned primate food that was
intended for the Pithecia resulting in an imbalance of Vitamin D3. The marmosets were placed in an air
kennel in the exhibit for several hours before releasing them. No problems observed.
1.1.1 w/0.3 Kerodon repestris
Comments: Combination was successful for approximately six months. Kerodon began to chase the sakis
causing stressful situations. Kerodon killed infant saki.

National Zoological Park


Unsuccessful
1.1 w/unspecified number of Leontopithecus rosalia
Comments: Combination broke down after approximately one year, resulting in a fight between the male
saki and a male tamarin. Both animals injured.

Omaha's Henry Doorly Zoo


Successful
2.0 w/1.0 Lagothrix lagotricha, 1.1 Saguinus oedipus, 2.4 Saimiri Sp., 1.1 Tapirus terrestris, 1.1 American
avocet (Recurvirosta americana), 1.1 spurwinged plover, 1.0 tamandua (Tamandua tetradactyla)
Comments: Island-type exhibit. Primary introduction was done in holding areas prior to release on the
island. Inter- and intraspecies introductions always occur in the holding areas. Initially, the species are
given access to a common fence for limited periods of time, with keeper supervision. As the integration
progresses, both species are allowed to investigate each other's cages and transfer alleys. In most situations,
the cages are set up in a pattern that allows for many escape routes. In the final phase of the introduction,
each species is given access to the island without the other species present. This enables each group to
familiarize itself with the habitat without the pressure of defending a territory. The species in holding can
see the other species on the island, and the groups are switched daily. After the keepers are comfortable an
introduction is performed, with supervision throughout the day. The animals are separated at night in the
sleeping quarters if any antagonism is exhibited.

Unsuccessful
1.0 two-year old handreared w/2.0 other Pithecia pithecia, 1.0 Lagothrix lagotricha, 1.1 Saguinus oedipus, 2.4
Saimiri Sp., 1.1 Tapirus terrestris, 1.1 American avocet (Recurvirosta americana), 1.1 spurwinged plover, 1.0
tamandua (Tamandua tetradactyla)
Comments: This animal was introduced to the same group listed above under "successful" and was
removed after six months after an attack by the wooly monkey. The saki was handreared and did not

31
socialize with any of the other primates (including the other two sakis). Spent most of his time on the
ground with the tapirs.

Pittsburgh Zoo
Successful
1.1 w/2.1 Alouatta caraya
Comments: Animals have been together for four years, both species having reproduced. Species were put
together off-exhibit first, then allowed up on exhibit. Introduction was not unusual or significant.
Pithecia pithecia w/Alouatta caraya, Dasyprocta cristata, and Bradypus Sp.
Comments: Non-primate species were introduced to the exhibit first. This allowed them to get
comfortable with the exhibit and to find their nest boxes, etc.

Roger Williams Park Zoo


Unsuccessful
1.0 w/1.0 Saguinus oedipus
Comments: Males were housed in adjoining enclosures for several weeks. Animals were allowed access
to each others enclosures under close observation of keeper staff. First day male saki became aggressive
towards the cotton-top. On the second day the tamarin became aggressive towards the saki. The animals
were separated on day three following superficial injuries to the saki.
Unspecified number of individuals w/golden-rumped agouti (Dasyprocta cristata)
Comments: Agouti injured a saki. The agouti had been placed in a howdy cage within the saki exhibit.

Saint Louis Zoological Park


Successful
1.1 w/0.2 Saguinus oedipus (adult siblings)
Comments: First introduced through screen in holding cages. Actual introduction was done on exhibit for
more room. Some chasing of the tamarins by the male saki, but no contact or fighting. Both species were
left together thereafter without problems. Little interaction was observed between the species. Fed
separately in holding cages due to different diets.

Saimiri

Caldwell Zoo
Successful
1.1 w/1.1 Aotus Sp.
Comments: Both aotus were approximately 18 years old. The female Saimiri was 11 years old and the
male was under one year. They were kept side by side for short time and then the Saimiri were moved into
Aotus exhibit.
Unspecified number w/sloth and agouti
Unspecified number w/unspecified numbers of tapirs, capybara, anteaters, king vultures, crested screamers,
conures, white ibis, and herons.
Comments: No special method of introduction. Species were selected that staff thought would work and
put them together in the exhibit.

Chicago Zoological Park


Successful
Group ranging in size from 10-22 individuals of various age and sex composition w/3.5 Ateles geoffroyi, group
of Cebus apella ranging in size from 9 - 14 individuals of various age and sex composition, 1.0 Myrmacophagia
trydactyla, and 1.1 Tapirus terrestris
Comments: All species are exhibited together in a large (approximately 75'x 75’ x 70' high) naturalistic
exhibit with 30- 35' tall gunite trees connected by networks of vines, with cliffs, waterfalls, and a river. All
species are brought into separate holding areas at night and fed there. Capuchins were introduced to the
exhibit after the Saimiri, followed by the spider monkeys. The spider monkeys were introduced to the
exhibit after the Saimiri and Capuchins had first become familiar with the exhibit and were reliably coming
into their holding cages at night. The tapirs and giant anteater were introduced to the exhibit last.

32
This combination of primates and mammals has been extremely successful since 1984. A post-
reproductive female Ateles geoffroyi vellerosus formerly exhibited developed a mutually affiliative
relationship with the Saimiri group and seemed to be extremely attracted to infant Saimiri. The Saimiri are
seasonal breeders and each year after the infants had been born it was difficult to get this female to come
off of exhibit until after the Saimiri had gone into their holding area. The Saimiri (adults as well as
juveniles) engaged in social interactions with her and frequently sat on her "lap" or clung to her back.
Several of the juvenile Saimiri have also had close relationships with some of the juvenile Capuchin
females and would often sit on their "laps" and engage in play behavior with them. A male king vulture
that formerly lived in this exhibit frequently perched in the tops of trees with his wings outstretched and
was often groomed by several of the Saimiri.
Negative interactions have been rare in this exhibit but one female Ateles chased separate male
Saimiri out of the tops of trees in the exhibit on two consecutive days, resulting in the death of one of the
males. After observing this behavior, this particular female was kept off of exhibit for several weeks to
break her of this pattern of behavior. Thereafter this behavior was not repeated.
Between September 1994 and May 1995, this exhibit was closed for renovations. Throughout this
period, the two holding cages of the Saimiri, which are adjacent to the two holding cages of the Cebus,
were opened by a shift door to allow the two species to freely mingle in all four cages. No negative
interactions were ever seen between the two species. Two female Cebus which are subordinate in the
group of seven other Cebus permanently share holding cages with the Saimiri because they are too afraid
to enter the holding cages of the Cebus group.
A variety of bird species have successfully shared this exhibit with primates since its completion in
1984. These have included Toco toucan (Ramphastos toco), keel-billed toucan (Ramphastos sulfuratus),
cattle egret (Ardeola ibis), red-crested cardinals (Paroaria coronata), Mexican cacique (Cassiculus
melanicterus), king vulture (Sarcoramphus papa), bare-throated bellbirds (Procnias nudicollis), green and
gold tanager (Tangara schrankii), turquoise tanager (Tangara mexicana), sun conures (Aratinga solstitialis),
piping guans (Aburria pipile), saffron toucanet (Baillonicus bailloni), plush-crested jay (Cyanocorax
chrysops), blue-crowned motmot (Momotus momota), common trumpeters (Psophia crepitans), and black-
faced dacnis (Dacnis lineata). Due to the large size of this exhibit interactions between the birds and the
other animals are rare.

Lincoln Park Zoo


Successful
3.3 w/1.2.1 Alouatta caraya
Comments: Saimiri were given access to the exhibit for a couple of days prior to the howlers being given
access. No problems were observed during the introduction. Each group enters and exits exhibit through
separate shift doors. Fed main meal off exhibit in separate holding areas.

Omaha's Henry Doorly Zoo


Successful
2.4 w/1.0 Lagothrix lagotricha, 1.1 Saguinus oedipus, 1.1 Tapirus terrestris, 1.1 American avocet (Recurvirosta
americana), 1.1 spurwinged plover, 1.0 tamandua (Tamandua tetradactyla)
Comments: Island-type exhibit. Primary introduction was done in holding areas prior to release on the
island. Inter- and intraspecies introductions always occur in the holding areas. Initially, the species are
given access to a common fence for limited periods of time, with keeper supervision. As the integration
progresses, both species are allowed to investigate each other's cages and transfer alleys. In most situations,
the cages are set up in a pattern that allows for many escape routes. In the final phase of the introduction,
each species is given access to the island without the other species present. This enables each group to
familiarize itself with the habitat without the pressure of defending a territory. The species in holding can
see the other species on the island, and the groups are switched daily. After the keepers are comfortable an
introduction is performed, with supervision throughout the day. The animals are separated at night in the
sleeping quarters if any antagonism is exhibited.

33
San Diego Wild Animal Park
Successful
Unspecified number w/Mexican red brocket deer (Mezama americana temama) and several bird species
Comments: Saimiri were introduced to the birds occupying the exhibit. Brocket deer were introduced last.
Additional primates were introduced from time to time after the initial introduction.

REFERENCES

Abordo, E. J., R. A. Mittermeier, J. Lee and P. Mason. 1975. Social grooming between squirrel monkeys and
uakaris in a seminatural environment. Primates 16:217-221.
Fontaine, R. 1981. The Uakaris, Genus Cacajao. In: Ecology and behavior of neotropical primates. Academia
Brasilera de Ciencias.
Pook, A. G., and G. Pook. 1982. Polyspecific association between Saguinus fuscicollis, Saguinus labiatus,
Callimico goeldii and other primates in north-western Bolivia. Folia Primatologica 38:196-216.
Rylands, A. B. 1982. The behaviour and ecology of three species of marmosets and tamarins (Callitrichidae,
Primates) in Brazil. Unpubl. Ph. D. dissertation. Cambridge, England: University of Cambridge.
Torborgh, J. 1983. Five new world primates. Princeton: University Press.
Xanten, W. A. 1990. Marmoset behaviour in mixed-species exhibits at the National Zoological Park,
Washington. International Zoo Yearbook 29:143-148.

34
SOCIAL MANAGEMENT OF CALLITRICHIDS AND CALLIMICO
Andrew J. Baker, Ph.D., and Anne Savage, Ph.D.

SOCIAL STRUCTURE

Zoological parks have typically housed callitrichids and Callimico in monogamous family groups composed of
a single breeding pair and their offspring. This choice of social structure is the result of the well-documented,
long-term instability of groups containing unrelated same-sex individuals (Epple 1978).

However, data are accumulating on "spontaneous" deviations from monogamy in captive callitrichids,
particularly regarding the occurrence of multiple breeding females within groups (Price and McGrew 1991;
Rothe and Koenig 1991). Additionally, field research is revealing substantial within-species variation in
structure of wild groups (Dietz and Baker 1993; Digby and Ferrari 1994; Savage et al. 1995; Terborgh and
Goldizen 1985). Aspects of these data relevant to captive management will be discussed later in this chapter.

HOUSING IN OTHER THAN FAMILY GROUPS

Callitrichids can be housed in a variety of situations other than the standard one-male/one-female family group:

FATHER AND OFFSPRING (e.g., after the death or removal of the breeding female)
This configuration is often stable for long periods of time. Reproduction usually does not occur (see under
"Reproductive Suppression" below).

MOTHER AND OFFSPRING (e.g., after the death or removal of the breeding male)
This configuration is often stable for long periods of time. Reproduction usually does not occur (see under
"Reproductive Suppression" below).

SAME-SEX SIBLINGS (e.g., after the death or removal of both parents)


This configuration may also be stable for long periods of time.

OPPOSITE-SEX SIBLINGS (e.g., after the death or removal of both parents)


This configuration may also be stable for long periods of time. Reproduction usually does not occur (see under
"Reproductive Suppression" below). This configuration is not recommended for Saguinus oedipus (per
Savage).

For all four configurations above, disruption of the group is likely in the months following the change in social
structure. For example, there was disruption in 11 of 15 groups of Callithrix jacchus that had lost one or both
breeding individuals, within a period of 2.5 to 24 months after the loss (Rothe and Darms 1993). Such groups
may become stable once again after one or more individuals are removed. Disruption occurred within a group
of 2.6 sibling Callithrix jacchus removed from their family group, with evictions occurring on days 5, 89, and
107. However, after these evictions, the group was stable until it was dissolved for other reasons after 299 days
(Rothe and Darms 1993).

SAME-SEX DUOS OR SMALL GROUPS


Same-sex groups formed of unrelated (or unfamiliar) individuals. Little systematic information exists on the
success rate or long-term stability of such groups, but anecdotal evidence indicates that they are stable in many
cases. It is unlikely that large, stable groups such as those that are kin-based can be formed this way. In one
study, efforts to form male trios of Callithrix jacchus resulted in the eviction of one member of the trio (Seiss
1988, cited in Rothe and Darms 1993). Wisconsin Regional Primate Center (WRPC) records indicate that
same-sex duos of Saguinus oedipus were usually successful, but that larger groups were more likely to become
problematic. WRPC records also indicate that handreared or otherwise improperly socialized animals were less
likely to integrate successfully in such groups.

35
MIXED SPECIES
Single same-sex or opposite-sex individuals of different species may also be housed together, which may be
desirable for social reasons. Again, little published information exists, but Xanten (1990) reports on male
Leontopithecus rosalia, Callimico, and Callithrix argentata housed together without aggression. When housing
opposite-sex individuals, keep in mind that various within-genus hybrids have been documented (Coimbra-
Filho et al. 1993; Hershkovitz 1977 for review).

PEER GROUPS
A number of reports in the literature cite the formation of mixed-sex groups containing multiple females and/or
multiple males (Abbott 1984; Rothe and Darms 1993; Kleiman 1978; Epple 1972, 1975; Carroll 1988). These
groups have usually been formed for experimental reasons and will not be discussed further here.

REPRODUCTIVE SUPPRESSION

Within callitrichid family groups, breeding is usually limited to a single pair. Daughters do not usually become
pregnant and sons do not engage in sexual behavior (Abbott 1984; Epple and Katz 1984; French et al. 1984;
Savage et al. 1988; French et al. 1989).

In females, reproductive suppression appears to be maintained through both olfactory cues and behavioral
mediation (Savage et al. 1988; Abbott 1984), and often includes suppression of hormonal cyclicity. Daughters
are typically acyclic in family groups of Saguinus fuscicollis (Epple and Katz 1984) and Saguinus oedipus
(French et al. 1984). In Callithrix jacchus (Abbott 1984) and Leontopithecus rosalia (French et al. 1989), on the
other hand, some daughters do cycle. The fact that the reproductively competent of these latter species typically
do not become pregnant suggests some form of inbreeding avoidance (Abbott 1984; Carroll 1986).

This inbreeding avoidance typically remains effective even after the death or removal of a breeding individual.
That is, rather than a son replacing his father as the breeding male or a daughter replacing her mother,
reproduction usually ceases in groups that have lost a breeder, even if the group remains together over a period
of years (Carroll 1986; Philadelphia Zoo records). If parent/offspring reproduction were for some reason
desired (e.g. for a highly endangered species with a very small captive population), temporary separation may
increase the chances of reproduction. Carroll (1986) reports that a six-month separation between a father and
daughter Callithrix penicillata resulted in pregnancy after reintroduction.

Reproductive suppression/inbreeding suppression can break down under certain circumstances:

1. Introduction of a stepfather. Introduction of a new male (e.g., following the original male's death) can
incite reproduction in an adult daughter in the group, sometimes resulting in multiple reproductive females
within one group (polygyny). Most cases of polygyny reported for Callithrix jacchus occurred when a new
male replaced the breeding male and both mother and daughter became pregnant (Rothe and Koenig
1991). In some cases, both mother and daughter reared young. Price and McGrew (1991) reported a
similar case for Saguinus oedipus, although neither female reared young. Mother-daughter polygyny
following male replacement is also typical of wild Leontopithecus rosalia (Dietz and Baker 1993).

Such multi-female groups appear to be typically unstable. Most of the polygynous and potentially
polygynous groups of Callithrix jacchus reported on by Rothe and Koenig (1991) were stable for a
maximum of two pregnancies for each female. However, Mager (cited in Rothe and Darms 1993)
documented a mother/daughter polygynous group of Cebuella pygmaea that was stable for many years.
Also, at the Philadelphia Zoo, a daughter reproduced twice in a group of Cebuella pygmaea with no
evidence of mother-daughter aggression, and was separated from the group only for management reasons.

2. Death or illness of a parent. As described above, callitrichid groups usually become non-reproductive after
the death of a breeding individual. However, there have been cases of pregnancy in daughters in groups in
which the breeding female has died or become ill (Price and McGrew 1991). Incestuous reproduction
occurred in four of fifteen groups of Callithrix jacchus that had lost one or both breeding individuals

36
(Koenig et al. 1988; Rothe and Darms 1993). Crook (1988) reported on mother-son reproduction following
the death of the breeding male in a group of Callthrix jacchus.

Finally, there have been reports of daughters becoming pregnant in intact family groups of several species
of callitrichids, including Cebuella pygmaea (Philadelphia Zoo records: daughter reared one infant from
two pregnancies), Callithrix jacchus (Anzenberger and Simmen 1987), Saguinus imperator (Knox and
Sade 1991; pregnancy was not carried full-term), and Saguinus oedipus (Price and McGrew 1991: no
infants reared from one pregnancy). It should be emphasized that such occurrences are exceptional.

INFANT-REARING EXPERIENCE

Studies on various callitrichids have indicated that experience with infant siblings is critical to the development
of parental competence, especially maternal competence. Neonatal mortality for mothers lacking such
experience is reported as higher than that for experienced females in studies of Saguinus oedipus (Tardif et al.
1984; Snowdon et al. 1985; Baker and Woods 1992), Saguinus fuscicollis (Epple 1975), Leontopithecus rosalia
(Hoage 1977; Baker and Woods 1992), and Callithrix jacchus (Stevenson and Sutcliffe 1978; Tardif et al.
1984). Thus, it has long been practice to leave callitrichids in their natal groups through the rearing of the next
one or more litters.

It should be noted that most reports on the effects of pre-reproductive infant experience have not separated
important confounding variables such as duration of natal group socialization and age at first reproduction (see
Baker and Woods 1992). It is possible that many of the inexperienced subjects were inexperienced precisely
because they were removed from their natal groups at an early age or because both parents died before
reproducing again, in either case depriving the young animal of a normal social environment. Earlier separation
from the natal group may also result in earlier pairing and reproduction.

Obviously, the conservative approach is to leave animals within natal groups through the birth of one or more
subsequent litters, and this should always be done when possible. However, it should be remembered that other
forms of socialization within the natal group may partially or fully compensate for lack of actual infant
experience. Thus, for example, in the case of the death of a breeding individual, leaving the youngest natal
animals with the remaining parent and older siblings into subadult or adulthood may be sufficient to produce a
competent parent. More extreme measures such as fostering into a breeding group or introducing a new
breeding individual specifically to provide experience may not be necessary.

WITHIN-GROUP AGGRESSION

Within groups, aggression sufficiently severe to require removal of group members is not atypical. Within
family groups, this aggression is typically, though not always, directed at natal rather than breeding individuals;
aggressors are typically the same-sex parent or a same-sex sibling (McGrew and McLuckie 1986; Kleiman
1979; Inglett et al. 1989; Stevenson and Rylands 1988). Fights between same-sex twins are particularly
characteristic (Stevenson and Rylands 1988; Kleiman et al.1988; Wisconsin Regional Primate Center records).
"Twin fights" may or may not escalate to involve attacks by other group members on one of the twins.

The age at which such aggression and resulting eviction of natal individuals will occur is variable and
unpredictable. For example, McGrew and McLuckie (1986) report on evictions of six Saguinus oedipus from
natal groups. Ages of eviction ranged from 16 to 29 months. Eleven Callithrix jacchus were evicted at between
11 and 19 months of age (Stevenson and Rylands 1988). However, individuals are often able to remain in the
natal groups well beyond these ages. For example, Rothe (1978) reported groups of Callithrix jacchus with up
to 19 members including natal individuals as old as five years. Introduction of a steparent may result in earlier
than normal eviction for natal individuals (Wisconsin Regional Primate Center records).

In Leontopithecus rosalia, a large proportion of aggressive incidents have been associated with changes in the
reproductive status of the breeding female (e.g., after the birth of infants, during estrus, or during the "false
estrus" [Kleiman and Mack 1977] of pregnancy [Kleiman 1979, Kleiman et al. 1988]). Kleiman et al. (1988)

37
suggests that individuals evicted during such periods may be able to be reintroduced after several days (see also
below). Extended or even short-term separations of a young animal may result in immediate aggression or
eviction at a much earlier age than usual. Kleiman et al. (1988) reported on a year-old male that was attacked
and killed after a two- to three-hour separation and on an 81-day old female killed approximately one month
after a 27-day medical separation.

Threat behavior, displacement, and intermittent chasing (McGrew and McLuckie 1986) or minor injuries,
especially cuts and scratches on the face (Kleiman 1979; Inglett et al. 1989) may precede eviction-type
aggression. The victim may separate itself from the rest of the group, show fearful behavior upon being
approached by other group members (sometimes involving only specific individuals), and often stays lower
than normal in the exhibit. Recognition of tensions preceding aggression is important, as fight can result in
death. For example, in a survey on Leontopithecus rosalia, Inglett et al. (1989) found that 20% of reported
attacks resulted in death of a tamarin.

There may be sex-related differences in age of eviction and severity of attack, which may vary from species to
species. McGrew and McLuckie (1986) reported that daughters were more likely to be evicted than sons in
Saguinus oedipus. However, Wisconsin Regional Primate Center records indicate that aggression between male
sibling was more likely than aggression between female siblings. Both Kleiman (1979) and Inglett et al. (1989)
noted that, in Leontopithecus rosalia, attacks on daughters appeared to be more severe in their effects than
attacks on sons.

Inglett et al. (1989) reported on a method for reintegration of Leontopithecus rosalia that had had to be
removed temporarily from natal groups due to severe aggression. Typically, the individual was placed beside or
(preferably) within the family cage inside a "howdy" cage and released with the group 1 to 20 days after the
attack. This method had a high success rate, but it should be noted that almost all of the tamarins with which
this was tried were male. Efforts to reintegrate evicted Saguinus oedipus daughters failed (McGrew and
McLuckie 1986) as have efforts to reintegrate natal individuals of either sex in Callithrix jacchus (Rothe and
Darms 1993).

Temporary separation may also allow reintegration of same-sex unrelated individuals (Callithrix geoffroyi:
Philadelphia Zoo records). In one case, a male trio was maintained over several episodes of aggression by
separating the aggressive individual and keeping the victim and the more "neutral" animal together for a period
of days. Then the victim and aggressor were housed together for a period of days before reuniting the entire
group.

BETWEEN-GROUP AGGRESSION

Callitrichids are typically territorial in the wild (see Goldizen 1987 for summary) and behave aggressively
toward neighboring groups or other intruders. In captivity, members of family groups are usually aggressive
toward strange individuals introduced into their cages (French and Snowdon 1981; Harrison and Tardif 1989;
Sutcliffe and Poole 1984; French and Inglett 1989).

To avoid injurious aggression, different groups of the same species should never be housed in a situation where
physical contact is possible. Close visual contact between conspecific groups should also be avoided. If
conspecific groups are housed in the same room, visual barriers should be used.

INTRODUCTIONS

Introductions between a single male and single female are almost always uneventful. A brief period of contact
through mesh or in a “howdy” cage and a brief period of observation after full contact are usually sufficient.

Although few data exist, introduction of unrelated same-sex individuals or of adults into family groups (e.g., to
replace a breeding individual that has died) is more likely to be problematic and should involve a longer
introduction and observation period. In the case of introduction into a family group, the likelihood of problems

38
probably increases with the age of any (especially same-sex) natal individuals present. For Saguinus oedipus,
introduction of a step-parent to youngsters less than seven months old is generally successful (although see note
above concerning early eviction), while introductions involving natal individuals greater than one year of age
are generally unsuccessful (Wisconsin Regional Primate Center records).

REFERENCES

Abbott, D. H. 1984. Behavioral and physiological suppression of fertility in subordinate marmoset monkeys.
American Journal of Primatology 6:169-186.
Anzenberger, A. A., and C. Simmen. 1987. Father-daughter incest in a family of common marmosets
(Callithrix jacchus). International Journal of Primatology 8:524 (Abstract).
Baker, A. J., J. M. Dietz and D. G. Kleiman. 1993. Behavioral evidence for monopolization of paternity in
multi-male groups of golden lion tamarins. Animal Behavior 46:1091-1103.
Baker, A. J., and F. Woods. 1992. Reproduction of the emperor tamarin (Saguinus imperator) in captivity, with
comparison to cotton-top and golden lion tamarins. American Journal of Primatology 26:1-10.
Carroll, J. B. 1986. Social correlates of reproductive suppression in captive callitrichid family groups. Dodo
23:80-85.
———. 1988. The stability of multi-female groups of Goeldi's monkey Callimico goeldii in captivity. Dodo
25:37-43.
Coimbra-Filho, A. F., A. Pissinatti and A. B. Rylands. 1993. Experimental multiple hybridism and natural
hybrids among Callithrix species from eastern Brazil. In: Marmosets and Tamarins: Systematics,
Behaviour, and Ecology, ed., A. B. Rylands, pp. 95-120. Oxford: Oxford University Press.
Crook, G. A. 1988. An incidence of breakdown of incest taboo in the common marmoset. Australian
Primatology 3:23.
Dietz, J. M., and A. J. Baker. 1993. Polygyny and female reproductive success in golden lion tamarins,
Leontopithecus rosalia. Animal Behavior 46:1067-1078.
Digby, L. J., and S. F. Ferrari. 1994. Multiple breeding females in free-ranging groups of Callithrix jacchus.
International Journal of Primatology 15:389-398.
Epple, G. 1972. Social behavior of laboratory groups of Saguinus fuscicollis. In: Saving the Lion Marmoset, ed.
D. D. Bridgewater, pp. 50-58. Wheeling, WV: The Wild Animal Propagation Trust.
———. 1975. The behavior of marmoset monkeys (Callitrichidae). In: Primate Behavior, Vol. 4, ed. L. A.
Rosenblum, pp. 195-239. New York: Academic Press.
———. 1978. Reproductive and social behavior of marmosets with special reference to captive breeding.
Primate Medicine 10:50-62.
Epple, G, and Y. Katz. 1984. Social influences of estrogen excretion and ovarian cyclicity in saddle-back
tamarins (Saguinus fuscicollis, Callitrichidae). American Journal of Primatology 6:215-227.
French, J. A., D. H. Abbott and C. T. Snowdon. 1984. The effect of social environment on estrogen excretion,
scent marking, and socio-sexual behavior of tamarins (Saguinus oedipus). American Journal of
Primatology 6:155-167.
French J. A., and B. J. Inglett. 1989. Female-female aggression and male indifference in response to unfamiliar
intruders in lion tamarins. Animal Behavior 37:487-497.
French, J. A., B. J. Inglett and T. M. Dethlefs. 1989. The reproductive status of nonbreeding group members in
captive golden lion tamarin social groups. American Journal of Primatology 18:73-86.
French, J. A., and C. T. Snowdon. 1981. Sexual dimorphism in responses to unfamiliar intruders in the tamarin,
Saguinus oedipus. Animal Behavior 29:822-829.
Goldizen, A. W. 1987. Tamarins and marmosets: communal care of offspring. In: Primate Societies, eds. B.B.
Smuts, D.L. Cheney, R. M. Seyfarth, R. W. Wrangham, and T. T. Struhsaker, pp. 34-43. Chicago:
University of Chicago Press.
Harrison, M. L., and S. D. Tardif. 1989. Species differences in response to intruders in Callithrix jacchus and
Saguinus oedipus. International Journal of Primatology 10:343-362.
Hoage, R. J. 1977. Parental care in Leontopithecus rosalia rosalia: sex and age differences and the role of prior
experience. In: The Biology and Conservation of the Callitrichidae, ed. D. G. Kleiman, pp. 293-305.
Washington, D.C.: Smithsonian Institution Press.
Inglett, B. J., J. A. French, L. G. Simmons and K.W. Vires. 1989. Dynamics of intrafamily aggression and
social reintregration in lion tamarins. Zoo Biology 8:67-78.

39
Kleiman, D.G. 1978. The development of pair preferences in the lion tamarin (Leontopithecus rosalia): male
competition or female choice? In: Biology and Behavior of Marmosets, eds. H. Rothe and J. P. Hearn, pp.
203-207. Goettingen: Eigenverlag Rothe.
———. 1979. Parent-offspring conflict and sibling competition in a monogamous primate. American
Naturalist 114: 753-760.
Kleiman, D. G., R. J. Hoage and K. M. Green. 1988. The lion tamarins, genus Leontopithecus. In: Ecology and
Behavior of Neotropical Primates, Volume 2, eds. R. A. Mittermeier, A. B. Rylands, A. Coimbra-Filho
and G. A. B. Fonseca, pp. 299-347. Washington, D.C.: World Wildlife Fund.
Kleiman, D. G., and D. S. Mack. 1977. A peak in sexual activity during mid-pregnancy in the golden lion
tamarin, Leontopithecus rosalia. Journal of Mammalogy 58:657-660.
Knox, K. L., and D. S. Sade. 1991. Social behavior of the emperor tamarin in captivity: components of
agonistic display and agonistic network. International Journal of Primatology 12:439-480.
McGrew, W. C., and E. C. McLuckie. 1986. Philopatry and dispersion in the cotton-top tamarin, Saguinus (o.)
oedipus: an attempted laboratory simulation. International Journal of Primatology 7:401-420.
Price, E. C., and W. C. McGrew. 1991. Departures from monogamy in colonies of captive cotton-top tamarins.
Folia Primatologica 57:16-27.
Rothe, H. 1978. Sub-grouping behavior in captive Callithrix jacchus families: a preliminary investigation. In:
Biology and Behavior of Marmosets, eds. H. Rothe and J. P. Hearn, pp. 233-257. Goettingen: Eigenverlag
Rothe.
Rothe, H., and K. Darms. 1993. The social organization of marmosets: a critical evaluation of recent concepts.
In: Marmosets and Tamarins: Systematics, Behavior, and Ecology, ed. A. B. Rylands, pp. 176-199.
Oxford: Oxford University Press.
Rothe, H., and A. Koenig. 1991. Variability of social organization in captive common marmosets (Callithrix
jacchus). Folia Primatologica 57:28-33.
Savage, A., L. H. Giraldo, L. H. Soto and C. T. Snowdon. 1995 (in press). Demography, group composition,
and dispersal in wild cotton-top tamarins (Saguinus oedipus oedipus). American Journal of Primatology
37.
Savage, A., T. E. Ziegler and C. T. Snowdon. 1988. Sociosexual development, pair bond formation, and
mechanisms of fertility suppression in female cotton-top tamarins (Saguinus oedipus oedipus). American
Journal of Primatology 14:345-359.
Siess, M. 1988. Experimente zur kooperativen Polyandrie beim Weissbuschelaffen Callithrix jacchus Erxleben,
1777). Unpublished diploma thesis, University of Gottingen, Gottingen.
Snowdon, C. T., A. Savage and P. B. McConnell. 1985. A breeding colony of cotton-top tamarins (Saguinus
oedipus). Laboratory Animal Science 35:477-480.
Stevenson, M. F., and A. B. Rylands. 1988. The marmosets, genus Callithrix. In: Ecology and Behavior of
Neotropical Primates, Volume 2, eds. R.A. Mittermeir, A. B. Rylands, A. Coimbra-Filho and G. A. B.
Fonseca, pp. 131-222. Washington, D.C.: World Wildlife Fund.
Stevenson, M. F., and A. G. Sutcliffe. 1978. Breeding a second generation of common marmosets Callithrix
jacchus in captivity. International Zoo Yearbook 18:109-114.
Sutcliffe, A. G., and T. B. Poole. 1984. An experimental analysis of social interaction in the common marmoset
(Callithrix jacchus jacchus). International Journal of Primatology 5:591-607.
Tardiff, S.D., C.B. Richter, and R. L. Carson. 1984. Effects of sibling-rearing experience on future reproductive
success in two species of Callitrichidae. American Journal of Primatology 6:377-380.
Terborgh, J., and A. W. Goldizen. 1985. On the mating system of the cooperatively breeding saddle-backed
tamarin (Saguinus fuscicollis). Behavioral Ecology Sociobiology 16:293-299.
Xanten, W. A. 1990. Marmoset behaviour in mixed-species exhibits at the National Zoological Park,
Washington. International Zoo Yearbook 29:143-148.

40
Reproduction in Callitrichid Primates
Jeffrey A. French, Ph.D., and Jeffrey E. Fite, M.A.

Introduction

Callitrichid primates long have been an important model species in basic studies of reproductive biology.
Attention to this taxon has derived from several aspects of the reproductive life history of species within the
family, which, taken together, make the reproductive biology of callitrichids unique among the primates.
These features include: (1) strong social influences on reproductive endocrinology (Abbott et al. 1993;
Ziegler et al. 1987b); (2) exceedingly high energetic costs of reproduction for breeding females (French
1997); (3) exquisite sensitivity of reproductive output to nutritional variables (Tardif and Jaquish 1994);
and (4) regular occurrence of multiple simultaneous ovulations and implantations with the consequent high
incidence of multiple births (Hearn 1983). Consequently, our knowledge base of reproductive parameters
for this group is fairly well established relative to other taxa of animals maintained and displayed in
zoological parks.

This chapter provides a systematic review of reproduction in callitrichids. We will present a comparative
analysis of reproductive parameters in callitrichids, and describe factors that are associated with good
reproductive outcomes and infant survivorship. In the final section, we outline two methodologies that
curators and keepers may find useful in monitoring reproductive function in callitrichids. First, we illustrate
techniques for training both animals and technicians to collect urine samples from unrestrained marmosets
and tamarins. Finally, we briefly describe general methods for measuring reproductive function through the
measurement of gonadal and pituitary hormones.

BASIC REPRODUCTIVE PARAMETERS

Table 1 presents a summary of the current information available on reproduction in callitrichids, including
gestation length, interbirth interval, nonconceptive ovarian cycle length, modal number of litters per year,
and the presence or absence of conceptive post-partum estrus. We recognize in evaluating the data in Table
1 that these parameters are estimates of typical reproduction in captivity for these species. Certainly,
exceptions to the general patterns might be expected, and the data in Table 1 represent typical values, or
central tendencies, rather than absolute landmarks for each parameter.

Relative to other primates, most aspects of callitrichid reproductive biology suggest that this group has
been subject to strong selection for high reproductive rates. Median litter size (twins) is unusual for
primates. Further, the ability to breed throughout the year, and the general absence of strong seasonal
effects on reproduction (except in Leontopithecus: see Kleiman et al. 1982; French et al. 1996) contributes
to a high reproductive rate. For species other than Leontopithecus, females typically deliver two sets of
litters per year, which therefore doubles the potential for annual production of offspring.

As is typical for primates, gestation length is prolonged relative to other mammals of similar body size
(e.g., squirrels). Within the callitrichids, however, species vary considerably in length of gestation.
Leontopithecus has the shortest gestation length at approximately 125 days. In contrast, S. oedipus has the
longest, with a reported gestation length of greater than 180 days (Ziegler et al. 1987a). The congeneric S.
fuscicollis has a considerably shorter gestation period of approximately 150 days (Heistermann and Hodges
1995). Marmosets of the genus Callithrix have very similar periods of gestation (144 days), and average
gestation length in Cebuella is likewise similar to the 20 week gestation in Callithrix (142 days: Ziegler et
al. 1990a).

PUBERTY
One reproductive parameter that is difficult to estimate in callitrichid primates is age at puberty. As
discussed in the chapter by Baker and Savage (see Social Management of Callitrichids and Callimico, this

41
TABLE 1. REPRODUCTIVE PARAMETERS IN CALLITRICHID PRIMATES
Species Gestation Interbirth Cycle Length Litters per Post-partum Reference
(days) Interval (d) (days) Year1 Ovulation?
Harding et al. 1982; Hearn 1983; Box &
Callithrix jacchus 144 154 – 158 30 2 Yes – 10.5 d Hubrecht 1987; König et al. 1990; Tardif
et al. 1984

Callithrix kuhli 143.1 + 1.6 156.3 + 2.9 24.9 + 0.6 2 Yes - 13.6 d French et al. 1996

Cebuella pygmaea 142 166* 27 2 Yes – 15.6 d Ziegler et al. 1990

Leontopithecus 21.1 + 1.0 1 Yes French et al. In press


chrysomelas Nonconceptive

Leontopithecus 23.0 + 2.0 1 Yes French et al. In press


chrysopygus Nonconceptive

Leontopithecus 125 194 19.6 + 1.9 1 Yes Baker & Woods 1992; French & Stribley
rosalia. nonconceptive 1985; French et al. In press

Saguinus fuscicollis 149.7 167, 185 25.7 1-2 Yes – 17.4 d Heistermann & Hodges 1995; Tardif et al.
1984

Saguinus imperator 262 1 Baker & Woods 1992

Saguinus oedipus 183.7 208, 235 23.6 1–2 Yes – 19 d Brand 1981;French 1983; French et al.
1983; Tardif et al. 1984; Ziegler et al.
1987

42
volume), there are strong social influences on reproduction in this taxon. In marmosets and tamarins (genus
Saguinus), breeding is typically limited to a single adult female. Some or all daughters and/or subordinate
females experience ovarian anomalies, ranging from complete ovarian suppression (French et al. 1984;
Ziegler et al. 1987b; Abbott et al. 1993) to abnormal ovulatory cycles (e.g., short or “oligocyclic” ovarian
cycles and luteal insufficiency characterized by low progesterone production: Saltzman et al. 1994; Smith
et al. 1997). Thus, it is difficult to estimate physiological and endocrinological puberty, since the normal
timing of this period of development is intertwined with the profound effects of social housing and group
demography.

Notwithstanding these difficulties, both endocrine assessment and management records can help produce
estimates of the age at which females undergo ovarian maturation and are capable of reproduction. In S.
oedipus, daughters in family groups display increased estrogen and gonadotropin excretion around 16 to 18
months of age (Ziegler et al. 1987b). Females in the species removed from family groups and exposed to
stimuli from unfamiliar males show increases in hormone production at earlier ages. In Callithrix kuhli and
C. jacchus, some daughters in undisturbed family groups express ovarian cycles as early as 12 to 14 months
of age (Smith et al. 1997; Saltzman et al. 1997). In Cebuella pygmaea, small proportions of daughters in
intact family groups ovulate, whereas in “motherless” social groups, all daughters over 15 months of age
showed signs of ovulation (Carlson et al. 1997). Finally, female Leontopithecus (rosalia and chrysomelas)
less than 12 months of age have low levels and acyclic patterns of estrogen excretion. In contrast, all
daughters older than 16 months of age exhibit ovarian cycles that are qualitatively and quantitatively
identical to those of adult breeding females (French and Stribley 1985; French et al. 1989; French et al. In
press; van Elsacker et al. 1994).

The dynamics and timing of male puberty has been assessed in three species: C. jacchus, L. rosalia, and C.
kuhli. In males of the genus Callithrix, testosterone concentrations rise throughout development, reaching
levels close to those of adults at 12 months of age (Abbott and Hearn 1978; Dixson 1986; French and
Schaffner 1995). There is some suggestion that testosterone is suppressed in sons and subordinate males
relative to breeding males (Abbott 1993; French and Schaffner 1995). In Leontopithecus, older sons in
family groups have testosterone titers that are not different from those of adult males (and, in fact, tend to
be higher: French et al. 1989). The age at which viable sperm are capable of being ejaculated from males is
not known, although 60-week-old male C. jacchus housed in same-sex pairs possess mature spermatozoa
(Jackson and Edmunds 1984). Again, however, management records suggest that males are capable of
inseminating females and producing fertilized ovum as early as 12 months of age.

LACTATION AND FERTILITY


Among many primate species, lactation by females is associated with a prolonged period of postpartum
infertility and/or anovulation (McNeilly et al. 1988). Lactation appears to have little effect on female
reproductive function in callitrichid primates. French (1983) examined interbirth intervals (IBI) in female
cotton-top tamarins that were nursing two, one, or zero infants in the postpartum period. No significant
differences in time to the subsequent birth were noted. The lack of a lactional effect in this species is
surprising, since the time to first ovulation is delayed by several days in nursing females relative to non-
nursing females (Ziegler et al. 1990a). Baker and Woods (1992) reported longer IBIs in nursing females
than in non-nursing females in three species: S. imperator, S. oedipus, and L. rosalia. There was
considerable overlap, however, in the distributions of IBIs for the two classes of females.

In most species (see Table 1), a postpartum ovulation follows within two or three weeks of parturition,
corresponding to the time of maximal infant suckling. That a high proportion of these postpartum
ovulations are fertile, especially in marmosets (e.g., 92% of first postpartum ovulations are fertile in C.
kuhli: French et al. 1996) further supports the notion of a lack of lactational influences on fertility.

Factors Affecting Reproductive Performance And Infant Survivorship


Research has identified a considerable number of factors that may influence the likelihood of successful
reproduction and infant survivorship in callitrichid primates. These factors can be placed in one of two

43
broad categories of influences: (1) those factors dealing with the breeding female, and (2) other contextual
or social factors.

FEMALE-ASSOCIATED CHARACTERISTICS
The overall condition of a breeding female may influence her fertility status, since the number of ova
produced during each ovulatory event is strongly correlated with a female’s overall body weight (C.
jacchus: Tardif and Jaquish 1997). Female parity is one of the most significant predictors of offspring
survival. This effect has been documented in S. oedipus (Price and McGrew 1990; Snowdon et al. 1985;
Johnson et al. 1991), C. jacchus (Poole and Evans 1982; but see Rothe et al. 1992), and L. rosalia (French
et al. 1996). It is not known to what extent the reproductive benefits of parity are produced by simple aging
effects, but it may be that age at first breeding alone might contribute to increased reproductive
performance in females. Previous experience with infants as a “helper” (See Social Management of
Callitrichids and Callimico chapter, this volume) has also been associated with increased offspring
survivorship in a variety of species (see citations above). As Baker and Woods (1992) pointed out,
however, no studies of breeding performance have dissociated the effects of ”helping” per se, independent
of age at first reproduction. In a recent analysis of breeding performance in Leontopithecus, French et al.
(1996) showed that females had similar levels of infant survivorship, regardless of whether they had
experience with infants as helpers (helping effect) or experience with their own infants (parity effect). First-
time mothers that did not have helping experience had poor reproductive outcomes, but multiparous
females that had previous helping experience did not experience higher infant survivorship than
primaparous females with helping experience or multiparous females that lacked helping experience. Litter
size is a significant variable associated with infant survivorship, especially during the first 60 days of life.
Infants from larger litters have poorer survival than infants from smaller litters (Jaquish et al. 1997).

CONTEXTUAL/SOCIAL FACTORS
An early report suggested that wild-caught tamarins have better reproductive performance than captive-
born tamarins (Epple 1978), but more recent reports show no influence of this variable (Johnson et al.
1991). Infant survivorship in C. pygmaea appears to be influenced by seasonal factors (possibly relative
humidity), since mortality among infants was higher in those born in fall and winter months in Wisconsin
than in those born in spring and summer months (Ziegler et al. 1990a).

One of the most conspicuous pieces of “common lore” regarding reproductive success in marmosets and
tamarins is the importance of helpersthe notion that nonbreeding helpers serve as crucial components of
the infant care system in social groups. Data from wild tamarins suggests that this might be the case, since
infant survivorship is correlated with the number of male helpers in the group (Garber et al. 1984).
However, others have failed to find such an effect (Dietz and Baker 1993). In captive C. jacchus, for
instance, Koenig et al. (1993) and Jaquish et al. (1997) found no association between the presence of
helpers and higher infant survivorship. Even if an effect were noted, it would be critical to separate out the
effects of helpers from other correlated variables (such as female parity and female age), since older,
multiparous females obviously will be living in groups with subadult and juvenile helpers.

Training Animals For Noninvasive Sample Collection


The noninvasive collection of biological samples for reproductive monitoring (urine and feces) has distinct
advantages over blood sampling, which has been the traditional means of sample collection for endocrine
monitoring. Perhaps the most important advantage is that it is relatively stress-free. This is not only
beneficial to the animals’ emotional and physical well being, but it also eliminates confounding effects of
stress on endocrine profiles and behavioral or social disruptions to the animal’s group. Since the equipment
needed for collection is reusable, such as metal pans, aluminum baking pans, and plastic sheeting, the
procedure is cost-effective. During sample collection, animals interact with keepers and technicians in non-
threatening, positive contexts.

Our method of urine collection is designed to shape the behavior of the marmosets and tamarins through
operant conditioning. Highly preferred food items, such as marshmallows and mealworms, are used as
positive reinforcers. Technicians and students enter marmoset colony rooms immediately prior to the

44
scheduled “lights-on” phase of the photoperiod, so that the animals are under observation upon emergence
from the sleeping site. The animals are followed around the cage by a technician holding an aluminum pan,
to which the animals have been habituated. Whenever an animal urinates, they are immediately given a
reinforcer to create an associative relationship between urination and the reward. After several weeks of
pairing urination and reinforcement, most animals become accustomed to moving to a certain, predictable
location (e.g., a particular location on a branch, or the front of the enclosure) and urinating.

The process of reinforcing animals for urinating in the sample collection devices can often begin at two
months of age, when infant marmosets are becoming independent. In fact, individuals conditioned at an
early age are often the most responsive and easiest to work with as adults. We have, however, had success
training adult marmosets to urinate as well. In addition to consistency and immediacy of reinforcement, it is
also important to consider each monkey’s individual behavior during the conditioning process. These
differences in behavior become quite apparent during regular training and urine-collection sessions. For
example, some marmosets prefer to urinate through the wire of their home cage, while others urinate while
scent marking branches or other objects in their cage. Conditioning appears to be most efficient when we
reinforce urination that is consistent with an individual’s everyday behavior. Thus, with time and patience,
callitrichid primates can easily be trained to urinate. With a dedicated staff of 3-4 persons, we routinely
collect urine on each of 40-50 marmosets three times each week, with the entire collection process rarely
taking more than two hours.

The marmosets are provided with apple juice during the evening prior to a collection day. The juice serves
as a natural diuretic that the monkeys readily drink. Early morning sample collection thus allows us to
capitalize on the diuretic effect of late-afternoon fluid consumption of the previous day. More importantly,
collecting the first-void sample of the day is also an effective way to eliminate intra- and inter-individual
variability in hormone concentrations. The stored urine in the bladder effectively integrates the hormonal
concentrations cleared from the body in the time since the last urination prior to retirement on the previous
day (typically 10-12 hours). Thus, moment-to-moment variation in hormone production is minimized. The
collection process can become very quick and efficient, when (1) it occurs on a regular basis, (2) urination
is immediately reinforced, and (3) the methods used by collectors are consistent from day to day.

Endocrine Assays in the Service of Reproductive Monitoring


As mentioned above, traditional endocrinology has relied on the measurement of hormonal levels in blood.
In contrast, the practice of noninvasive hormone monitoring requires the measurement of steroid (or
peptide) hormones in samples that can be collected without the need of a blood sample, such as urine,
feces, or saliva. Fortunately, the mechanisms of peptide and especially steroid metabolism renders these
forms of biological samples useful for estimating circulating levels of hormones. The liver and kidneys are
the primary sites for removing steroid hormones from the blood stream and ultimately from the body.
Enzymatic action in liver and kidney reduces the steroid molecules and creates sites on the molecule for the
introduction (“conjugation”) of hydrophilic groups, such as sulfates or glucuronides. This process converts
the steroid molecule into a compound that is readily soluble in water. In the kidney, steroid conjugated with
sulfate or glucuronide can be easily eliminated from the body via urine. In the liver, conjugated steroid
molecules are soluble in bile, and can be passed into the gut and eliminated via the feces. With regard to the
ovarian and fetoplacental steroid hormones, progesterone and estrogen, the liver is the major site of
metabolism. Progesterone is converted primarily to pregnanediol, conjugated to glucuronide, and excreted
in urine and feces. Estradiol and estrone (interconvertable forms of estrogen) are also metabolized and
conjugated in the liver, and excreted as both glucuronide and sulfate forms (Norman and Litwack 1987).

With regard to pituitary gonadatropins, such as LH (luteinizing hormone) and chorionic gonadotropin
(CG), less information is available regarding its metabolic fate. Proteolytic enzymes of hepatic origin serve
to inactivate these glycoprotein hormones, and the water-soluble by-products are excreted in the urine.
Fortunately for the purposes of monitoring the peak in gonadotropin that accompanies the periovulatory
period (LH) and the onset of pregnancy (signaled by increases in CG), the inactivation of LH/CG in the
liver does not alter the ability of antisera directed toward gonadotropin to recognize the excretory form of
gonadotropin.

45
The use of competitive binding techniques, also referred to as immunoassay, is the most common method
to assess quantitatively hormone concentration. These procedures take advantage of the ability of certain
proteins (antibodies) to preferentially bind hormones. In addition to the antibody directed against the
hormone and the “native” hormone contained in the biological sample, immunoassays utilize two
additional reagents: a known quantity of the hormone that has been labeled with a compound that allows
detection (a radioactive isotope in the case of radioimmunoassay [RIA], and a peroxidase enzyme in the
case of enzyme immunoassay [EIA]), and known quantities of an unlabeled version of the hormone of
interest.

The outline of the process of immunoassay is fairly straightforward. Antibody is made available in a known
but limited quantity. Radioactively or enzymatically labeled hormone is added to the reaction in a known
amount, as is the biological sample that contains an unknown quantity (e.g., high or low pregnanediol) of
the hormone in question. Concentration of hormone in the biological samples is determined with reference
to a standard curve, which is calculated by performing the competitive binding assay with known amounts
of both native and labeled hormone. The sensitivity of immunoassays is exquisite, and these techniques can
measure hormones in nanogram (10-9 g) and picogram (10-12 g) quantities.

Figures 1 and 2 provide typical examples of reproductive profiles that can be generated using noninvasive
sample collection techniques and immunoassays for hormones. Figure 1 presents three consecutive
nonconceptive ovarian cycles in a female L. rosalia. The top panel shows concentrations of urinary steroid
excretion (PdG = pregnanediol glucuronide, and E1C = estrone conjugates) and the bottom panel presents
concentrations of LH. The data reveal a clear pattern of ovulations (signaled by the LH spike) followed by
elevated steroid excretion, which reflects steroid production by the corpus luteum. Abnormal or atypical
ovarian function can easily be detected with reference to the normative patterns for each species. Figure 2
presents concentrations of urinary and fecal estrone conjugates in samples collected simultaneously from a
nonpregnant, cycling female L. rosalia. Although fecal steroid concentrations are more variable than
urinary concentrations, similar endocrine dynamics can be derived from profiles generated from fecal
hormone analyses.

Many zoological parks with research programs routinely screen animals for endocrine status using one of
the methods described briefly above. Curators that are interested in initiating a reproductive monitoring
program, but do not have the technical capability to do so, should be aware that a variety of laboratories are
currently assisting institutions in the conduct of these assays. Interested persons can contact the senior
author of this chapter (Jeff French, 402-554-2558; jfrench@unomaha.edu) for advice and consultation on
establishing a monitoring program.

46
60 25000

PdG (ng/mg Cr)


E1C (g/mg Cr)
50 Er 20000
40 15000
30 10000
20 5000
10 0
0
180
LH/CG (ng/mg Cr)

100
80
60
40
20
0
0 20 40 60 80

Days

Figure 1. Concentrations of urinary estrogen and progesterone metabolites (top panel)


and urinary gonadotropin concentrations (bottom panel) in samples collected from a
female L. rosalia housed with a vasectomized male. Four periovulatory LH peaks are
identifiable (Days 12, 28, 50, and 73), each of which is followed by a luteal elevation in
both estrogen and progesterone metabolite excretion. (E1C = Estrone conjugates, PdG =
Pregnanediol Glucuronide.)

47
Urinary E1C
70
Fecal E1C 5000
60
Urinary E1C (g/mg Cr)

Fecal E1C (ng/g feces)


4000
50

40 3000

30
2000
20

1000
10

0 0
0 10 20 30 40

Day

Figure 2. Concentrations of urinary and fecal estrone conjugates in urine and fecal
samples collected simultaneously from an unpaired female L. rosalia. As shown in
above in Figure 1, the periovulatory phase of the cycle is marked by the lowest
concentrations of urinary steroid excretion (Days 18-19 and Days 27-28_. Although
fecal steroid concentrations tend to be more variable than urinary profiles, similar
endocrine events are reflected in the fecal profiles.

48
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French, J.A., B.J. Inglett, and T.M. Dethlefs. 1989. The reproductive status of nonbreeding group members
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French, J.A., and J.A. Stribley. 1985. Patterns of urinary oestrogen excretion in female golden lion tamarins
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French, J.A., K. Vleeschouwer, T.E. Smith, L. van Elsacker, M. Heistermann, S.L. Monfort, E. Ribeiro, A.
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Harding, R.D., M.J. Hulme, S.F. Lunn, C. Henderson, and R.J. Aitken. 1982. Plasma progesterone levels
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Heistermann, M., and J.K. Hodges. 1995. Endocrine monitoring of the ovarian cycle and pregnancy in the
saddleback tamarin (Saguinus fuscicollis) by measurement of steroid conjugates in urine. American
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Jackson, M.R., and J.G. Edmunds. 1984. Morphological assessment of testicular maturity in marmosets
(Callithrix jacchus). 1984. Laboratory Animals 18: 173-178.

Jaquish, C.E., T.B. Gage, and S.D.Tardif. 1991. Reproductive factors affecting survivorship in captive
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Jaquish, C.E., S.D. Tardif, and J.M. Cheverud. 1997. Interactions between infant growth and survival:
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Kleiman, D.G., J.D. Ballou, and R.F. Evans. 1982. An analysis of recent reproductive trends in captive
golden lion tamarins (Leontopithecus r. rosalia) with comments on their future demographic
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König, A., U. Radespiel, M. Siess, H. Rothe, K. Darms. 1990. Analysis of pairing-parturition- and
interbirth-intervals in a colony of common marmosets (Callithrix jacchus). Zeitschrift fur
Säugetierkunde 55: 308-314.

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Human Fertility: Social and Biological Determinants, eds. P. Diggory, M. Potts, and S. Teper pp. 102-
117. London: MacMillan Press.

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Poole, T.B., R.G. Evans. 1982. Reproduction, infant survival and productivity of a colony of common
marmosets (Callithrix jacchus). Laboratory Animals 16: 88-97.

Price, E.C., and W.C. McGrew. 1990. Cotton-top tamarins (Saguinus (o.) oedipus) in a semi-naturalistic
captive colony. American Journal of Primatology 20: 1-12.

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Rothe, H., K. Darms, and A. Koenig. 1992. Sex ratio and mortality in a laboratory colony of the common
marmoset (Callithrix jacchus). Laboratory Animals 26: 88-99.

Rothe, H., A. Koenig, and K. Darms. 1993. Infant survival and number of helpers in captive groups of
common marmoset (Callithrix jacchus). American Journal of Primatology 30: 131-137.

Saltzman, W., N.J. Schultz-Darken, and D.H. Abbott. 1997. Familial influences on ovulatory function in
common marmosets (Callithrix jacchus). American Journal of Primatology 41: 159-178.

Saltzman, W., N.J. Schultz-Darken, G. Scheffler, F.H. Wegner, and D.H. Abbott 1994. Social and
reproductive influences on plasma cortisol in female marmoset monkeys. Physiology and Behavior 56:
801-810.

Saltzman, W., J.M. Severin, N.J. Schultz-Darken, and D.H. Abbott. 1997. Behavioral and social correlates
of escape from suppression of ovulation in female common marmosets housed with the natal family.
American Journal of Primatology 41: 1-22.

Smith, T.E., C.M. Schaffner, and J.A. French. 1997. Social and developmental influences on reproductive
function in female Wied’s black tufted-ear marmosets (Callithrix kuhli). Hormones and Behavior 31:
159-168.

Snowdon, C.T., A. Savage, and P.B. McConnell. 1985. A breeding colony of cotton-top tamarins (Saguinus
oedipus). Laboratory Animal Science 35: 477-480.

Tardif, S.D., and C.E. Jaquish. 1994. The common marmoset as a model for nutritional impacts upon
reproduction. Annals of the New York Academy of Science 709: 214-215.

. 1997. Number of ovulations in the marmoset monkey (Callithrix jacchus): relation to body weight,
age and repeatability. American Journal of Primatology 42: 323-329.

Tardif, S.D., C.B. Richter, and R.L. Carson. 1984a. Effects of sibling rearing experience on future
reproductive success in two species of callitrichidae. American Journal of Primatology 6: 377-380.

. 1984b. Reproductive performance of three species of callitrichidae. Laboratory Animal Science
34: 272-275.

Van Elsaker, L., M. Heistermann, J.K. Hodges, A. de Laet, and R.F. Verheyen. 1994. Preliminary results
on the evaluation of contraceptive implants in golden-headed lion tamarins, Leontopithecus
chrysomelas. Neotropical Primates 2: 30-32.

Widowski, T.M., T.E. Ziegler, A.M. Elowson, and C.T. Snowdon, C.T. 1990. The role of males in
stimulating reproductive function in female cotton-top tamarins Saguinus o. oedipus. Animal
Behaviour 40: 731-741.

Ziegler, T.E., W.E. Bridson, C.T. Snowdon, and S. Eman. 1987a. Urinary gonadotropin and estrogen
excretion during the postpartum estrus, conception, and pregnancy in the cotton-top tamarin (Saguinus
oedipus oedipus). American Journal of Primatology 12: 127-140.

. 1987b. The endovrinology of puberty and reproductive functioning in female cotton-top tamarins
(Saguinus oedipus oedipus) under varying social conditions. Biology of Reproduction 36: 327-342.

Ziegler, T.E., C.T. Snowdon, and W.E. Bridson. 1990a. Reproductive performance and excretion of urinary
estrogens and gonadotropins in the female pygmy marmoset (Cebuella pygmaea). American Journal of
Primatology 22: 191-204.

51
Ziegler, T.E., T.M. Widowski, M.L. Larson, and C.T. Snowdon. 1990b. Nursing does affect the duration of
the post-partum to ovulation interval in cotton-top tamarins (Saguinus oedipus). Journal of
Reproduction and Fertility 90: 563-570.

52
DIETS FOR CALLITRICHIDS—MANAGEMENT GUIDELINES
Sue Crissey, Ph.D., Barbara Lintzenich, and Kerri Slifka

Meeting the nutritional needs of Callitrichids is essential if they are to survive and reproduce in captivity. It
is appropriate to offer animals in captivity a diet that best matches their nutritional requirements. Any
efforts to develop appropriate dietary guidelines must consider the following:
1) information from feeding-ecology data,
2) information from published nutrient-requirement data (which often includes laboratory primate
requirements),
3) foods available to zoos, and
4) the animals’ food preferences.
In this chapter, we will provide a general overview for feeding callitrichids. Several SSPs are establishing
or have published husbandry manuals for individual species that include species-specific nutritional and
feeding recommendations. Please refer to those documents for additional and, sometimes, more specific
nutritional information and feeding guidelines.

FEEDING ECOLOGY

Information on feeding ecology of callitrichids varies substantially. Much more qualitative data are
available on the types of foods consumed in the wild than quantitative data detailing the nutritional content
of the foods selected. Despite this lack of quantitative information, several generalizations about callitrichid
diets can be applied to captive-feeding regimens.

FOOD SELECTION
Reports indicate that, in the wild, food selection differs among callitrichid species from fruits and insects in
the larger species to exudates (gums, saps, and latex) and insects in the smaller species. Their primary
feeding strategies encompasses insect foraging for all (Garber 1992).

Emperor tamarins (Saguinus imperator) primarily are frugivorous and insectivorous. Grasshoppers are the
favorite food item. The diet also may include exudates, nectar, flowers, and other plant parts. In the dry
season when fruits are scarce, emperor tamarins may become intense nectar feeders (Terborgh 1983).
Rosenberger (1992) noted that they may lose as much as 15% of their body weight when consuming large
quantities of nectar.

Moustached (Saguinus mystax) and saddlebacked (Saguinus fuscicollis) tamarins spend up to 31% of
feeding time on nectar during the dry season (Garber 1988). The diet of moustached tamarins (S. mystax)
includes about 14% insects as determined by feeding time. Both saddlebacked (S. mystax) and moustached
(S. fuscicollis) tamarins consume water and prey from bromilliads (Nickel and Heymann 1996) as do
golden lion tamarins (Leontopithecus rosalia) (Garber 1992). Some may consume up to 38 species of
insects, including insects weighing over 8.5 grams (Nickel and Heymann 1996). Moustached tamarins (S.
mystax) also consume fruit seeds and pass these undigested (Heymann 1992).

Pygmy marmosets (Cebuella pygmaea) are arboreal, rarely coming to the ground. The pygmy marmoset
(C. pygmaea) is classified as an exudate feeder and insectivore. They feed on exudates by gouging holes in
the major branches of trees and the stems of vines with lower incisors (Kinzey et al. 1975; Ramirez et al.
1977). Preferred insects are grasshoppers, spiders, and butterflies. Ramirez et al (1977) noted that pygmy
marmosets (C. pygmaea) spend 67% of their total feeding time investigating and procuring exudates and
33% of feeding time foraging for insects. Fruit, buds, flowers, and nectar also are consumed, but constitute
a minor portion of the diet.

In terms of types of foods consumed (i.e., fruits, exudates, and insects), diets may vary considerably within
a species as well as among species. Diet variability may be a consequence of seasonal changes in food

53
availability and distribution. Saguinus species have been grouped as to foraging strategy. Groupings
include: 1) seasonal exudates feeding occasionally from tree trunks; 2) insects taken from bark surface and
tree trunks used as platforms for terrestrial prey; 3) bark stripping for insects and small vertebrates; and 4)
tree gouging year-round for exudates (Garber 1992). Interestingly, some moustached tamarins (S. mystax)
may consume soil, presumably for mineral content (Hartmann and Hartmann 1991).

ROLE OF GUT MORPHOLOGY IN FEEDING STRATEGY

The body size of callitrichids is classified as small compared to other New World primates. Body mass
generally ranges from 105 to 700 g (Garber 1992). Claw-like nails allow clinging while foraging. Garber
(1992) provides a table of body mass for callitrichids.

Gastrointestinal-tract morphology of callitrichids has been associated with the extent to which a species
consumes exudates, specifically gums. It is thought that, for increased digestion of gums, a more complex
GI tract is beneficial. Common marmosets, which are largely exudate feeders, possess a large complex
cecum with internal ribbon-like structures (Garber 1992). C. emiliae have a large complex cecum to help
process gums (Ferrari and Martins 1992). These GI-tract structures are less developed in the golden lion
tamarin (L. rosalia) (Garber 1992).

Dentition of callitrichids is combined into two categories: short-tusked dentition for gouging bark
(marmosets), and long-tusked dentition like other primates (tamarins) (Ferrari and Martins 1992). Dentition
is correlated with feeding strategy. Thus, it appears that these animals are well adapted for their specific
diets.

PUBLISHED NUTRIENT REQUIREMENT DATA

A few studies have established some basic nutrient requirements for a number of callitrichid species. The
National Research Council (1978) attempted to describe the nutrient requirements of nonhuman primates.
Although the NRC requirements are outdated and are under revision, they remain the main source of
compiled scientific information on nutrient requirements in nonhuman primates. Unfortunately, limited
species were examined and only 24 nutrients are presented in the NRC publication, while primates may
require considerably more (up to 47 nutrients).

ENERGY REQUIREMENTS
Energy requirements for marmosets and tamarins may be higher than for other New World primates. Morin
(1980) published energy requirements at 150-160 Kcal/kg body mass/day. However, the quantity of energy
needed is directly related to the digestibility of the foods consumed. The digestible energy of one artificial
diet fed to a variety of callitrichids ranged from 71% to 86%. Power (1991) indicated that the change in
digestible energy was correlated to body size. The smaller the body size, the less well energy was digested.
The larger the body size the better energy was digested. The exception was the pygmy marmoset, which
had the smallest body size but a high level of digested energy at 84%.

PROTEIN REQUIREMENTS
The NRC (1978) proposed that New World primates need a higher level of protein than their Old World
counterparts. New evidence shows that this may not exactly be true for all New World primates (Oftedal
1995). However, an increased level of dietary protein should not be deleterious to healthy animals. Flurer
and Zucker (1988) found that marmosets consumed their feces when fed diets less than 6% protein or when
lacking in one or more amino acids. Protein requirements for small primate species are published as 3.5 g -
4.5 g/kg body mass/day of high-quality protein (NRC 1978). No study has determined the protein
requirements of pregnant or lactating callitrichids. The protein requirement is linked to the array and
quantity of essential amino acids, the digestibility of protein in the diet, and the presence of secondary plant
compounds such as tannins. An amino acid associated with taurine is needed for proper development of
young primates, but its requirement as a dietary essential is unknown (Sturman 1993).

54
VITAMIN AND MINERAL REQUIREMENTS
New World primates are able to use dietary vitamin D 3, while Old World primates can use both vitamin D2
and vitamin D3. Studies have shown that marmosets and tamarins may require higher levels of vitamin D 3
than other New World primates because of a target organ receptor resistance to the active form of the
vitamin (Takahashi et al. 1985; Ausman et al. 1985). Vitamin D3 requirement is stated as 110 IU/100 g
body mass/day (Takahashi et al. 1985).

Vitamin C is a proven dietary essential in common marmosets and no less than 15 to 20 mg ascorbic
acid/kg body mass is required (Flurer et al. 1987; Flurer and Zucker 1989). In one study (Flurer et al.
1987), the animals were fed 500 ppm concentration in the diet. The authors concluded that the requirement
is higher than human requirements. However, when compared to common marmosets on the same diet,
saddlebacked tamarins had significantly lower circulating levels than the common marmosets, intimating
that there is a species difference in need (Flurer and Zucker 1987) and possibly a higher requirement in
some callitrichid species (Flurer and Zucker 1989).

Zinc deficiency was noted in moustached marmosets when fed less than 150 ppm of dietary zinc. When the
levels were increased by 40 ppm the deficiency symptoms were alleviated (Chadwick et al. 1979).

Nutritional deficiencies can cause a number of anemias in nonhuman primates (Wixson and Griffith 1986).
A deficiency of riboflavin causes normocytic normochromic anemia. Deficiencies of vitamin B 12 and/or
folic acid can cause macrocytic anemia. Wixson and Griffith (1986) suggested that New World primates
would be a good model for folate-induced anemia. Hypochromic iron deficiency can result from blood loss
from bleeding or intestinal parasites. While they did not report this specific to callitrichids, callitrichids
probably are susceptible to a number of anemias and other deficiency diseases if not provided a diet that
meets nutritional needs.

As mentioned previously, very few studies have been undertaken to define the nutrient requirements of
callitrichids. Other than the nutrients discussed above, the guidelines for New World primates are
recommended for use in feeding captive callitrichids.

FOOD AVAILABILITY TO ZOOS

Knowing which types of food callitrichids consume is important when developing a captive diet, but it is
more important to know the quantity of nutrients consumed. For the most part, these data are not available.
Clapp and Tardif (1985) reported that a variety of foods have been offered in marmoset research colonies.
Most facilities fed some type of commercial diet supplemented with insects, small vertebrates, and produce.

Protein requirements to feed adequately have been reported at 20% (dry-matter basis), but this may be
above true requirement levels. Adequate fat levels have been reported at about 7% and carbohydrates at
about 5.3% (both dry-matter basis). Diets now fed at laboratory colonies nearly have eliminated the
problem of marmoset wasting syndrome (Clapp and Tardif 1985).

In his study to examine a captive diet in Geoffroy’s marmosets, Price (1992) calculated the nutrient content
of a mixed diet to assess possible nutritional problems found in the collection. Because the animals were
housed singly and in groups, data were not easily applied to the adequacy of the diet. The diet met the
recommended levels for New World primates (NRC 1978) and appeared adequate for other species. Price
(1992) suspected protein level and some mineral levels were inadequate for these particular animals. It
appears possible to maintain and breed callitrichids in captivity on a manufactured diet supplemented with
other commonly fed items.

In developing a captive diet, zoos should consider which categories of foods are consumed by callitrichids
in the wild and which foods from the same categories are available to institutions. They should also
consider studies that indicate that the nutritional content of foods consumed by free-range primates may be
considerably different from the nutritional content of foods from the same botanical classification available
in captivity. Multiple reasons for this anomaly exist. Generally, fruits consumed in the wild are higher in

55
fiber and lower in sugars than those items cultivated for human use (Calvert 1985). Also, fruits consumed
by callitrichids in the wild may be primarily unripe, while those available to zoos are usually very ripe.
Ripening increases the sugar level in the fruit and may help explain why fresh fruit fed in zoos can causes
loose stool in callitrichids. Finally, free-ranging callitrichids consume a variety of insects and exudates,
food items not commercially available to institutions. Zoos must acknowledge that, in captivity, animals are
limited in dietary intake and, consequently, in nutrient intake by the foods which are offered.

FOOD PREFERENCE

As mentioned before, the foods comprising most of the diet of free-ranging animals may not be that most
sought, but that most available. Differences in food choice also may be based on physiological condition.
Hence, day-to-day fluctuations in food consumed may vary dramatically within species and among
individuals.

Types and variety of food items offered artificially limit captive callitrichid diets. Studies with a variety of
laboratory mammals have shown that an animal does not necessarily select food items based on the item’s
nutrient content (Price 1992). Therefore, it can safely be assumed that captive callitrichids, given a limited
variety of succulent food items, will not necessarily select food items of adequacy in nutrient content.
Instead, animals may select items based on sugar content, fat content and even novelty. Thus, it is
important that zoos offer foods that compliment each other nutritionally.

Pennington (1993) lists the nutrient content of commonly fed food items, such as produce. Allen (1989) has
published information about less commonly fed food items, such as insects. The nutritional content label on
manufactured products presents the guaranteed analyses of the packaged product, but does not show levels
of vitamins and minerals. Many times, manufacturers will provide these to zoos upon request. If not, the
product can be chemically analyzed.

Using published research on nutritional requirements, the NRC guidelines, and data on wild-callitrichid
feeding and nutrient content of food items available in zoos, it is possible to formulate appropriate diets for
captive callitrichids.

FORMULATION OF APPROPRIATE DIETS

Zoos must be flexible when formulating diets for captive callitrichids. They must take into account animal
preferences, weight, exercise, physical condition, environment, behavioral considerations, and food
availability. Therefore, it is more appropriate here for the authors to offer guidelines for nutrient content
and food categories rather than recommending specific food items in set quantities. Guidelines allow for
flexibility in diet formulation while assuring a nutritious diet is consumed.

Nutrients presented in the next section provide only target levels and food items are presented as food
groups. The entire diet (as well as the animals’ enclosure) should be viewed as potential enrichment and, as
long as the target nutrient levels are met within the diet consumed, food presentation can be altered to
accommodate behavioral and enrichment needs.

Consider the feeding strategy in offering the diet. Feeding tubes, fashioned like bromeliads, or “flaky”
substrates can simulate picking and bark-gouging. Gums, while limited, can provide substantial activity
(Kelly 1993). Take care that all ingested food items are considered as diet contributors.

56
CALLITRICHID MANAGEMENT GUIDELINES—DIET RECOMMENDATIONS

FOOD AND WATER


Food—Adults
Schedule
1. Animals should be fed at least twice per day. The interval between morning and
afternoon feeding should fall between 4.5 to 6.5 hours. Since marmosets spend much
time foraging, feeding times may be scattered throughout the day.
2. The morning (or activity period) feeding should consist of more food than the
afternoon or evening (inactivity period) feeding, though the same categories of foods
should be offered. If possible, food should be available throughout the day and
scattered to encourage foraging.
Nutrient Content
If consumed in its entirety, the proper diet contains the nutrients listed in Table 1 on a
dry-matter basis (based on calculated analysis). These should be considered target
nutrient levels until more specific nutrient levels are defined (adapted from published
literature and New World monkey NRC requirements). Levels are expressed in quantity
per unit of diet.

TABLE 1. TARGET NUTRIENT LEVELS

Nutrient Concentration in diet* Nutrient Concentration in diet*


Energy (kcal/g) ** Choline (mg/kg) —
Crude protein (%) ** Biotin (mg/kg) 0.1
Fat (%) — Vitamin C (mg/kg) 500 or more
Fiber (%) — Calcium (%) 0.6
Linoleic acid (%) 1 Phosphorous (%) 0.4
Vitamin A (IU/g) 14 Magnesium (%) 0.2
Vitamin D (IU/g) 2.2 or less Potassium (%) 0.9
Vitamin E (mg/kg) 56 Sodium (%) 0.3
Thiamin (mg/kg) 5.6 Iron (mg/kg) 200 or less (80-200)
Riboflavin (mg/kg) 5.6 Zinc (mg/kg) 11.1
Niacin (mg/kg) 55.6 Copper (mg/kg) 1.5
Pyridoxine (mg/kg) 2.8 Manganese (mg/kg) 44.4
Folacin (mg/kg) 0.2 Selenium (mg/kg) —
Vitamin B12 (mg/kg) 0.6 Iodine (mg/kg) 2***
Pantothenic acid (mg/kg) 16.7

See explanations on previous pages for justification of nutrient levels.


* Probable requirements for New World primates. Depending on the interpretation of the NRC (1978), the
requirements for magnesium, iron, and manganese may be overestimated.
** The requirements for these nutrients are higher for marmosets and tamarins than for other New World
primates. Energy required is 150-160 Kcal/Kg body mass/day (d) (Morin 1980); protein for small primate
species is 3.5- 4.5 g/Kg body mass/day of high-quality protein (NRC 1978); vitamin D3 required is 110
IU/d/100 g body mass (Takahashi et al. 1985).
***NRC may have overestimated the quantity needed. For most other animals the requirement is about 0.1.
—No NRC requirement stated for this nutrient. This does not mean there is no requirement, just that studies
have not been performed. For selenium, the level in many mammals is about 0.1 ppm.

Daily Diet
Food Items
Zoos can achieve the nutrient levels outlined above by offering a diet consisting
of the food items listed in Table 2. Note: food items or food groups are
expressed as percentages, by weight, of total diet fed. Percentages were derived
from free-ranging data and food-item, nutrient-content information.

57
For flexibility, three diets are represented. Each meets or exceeds the target
nutrient levels outlined above. Food groups are presented in Appendix A. It is
assumed that the insects fed are crickets and mealworms. Mealworms contain
substantially more fat and energy than crickets, therefore, a higher percentage of
crickets to mealworms should be used for overweight animals. Invertebrates
must be fed an 8% calcium diet for at least 4 days prior to being fed to the
animals (Ward and Crissey 1997).

The vegetables and starches offered should be cooked (steamed or microwaved)


to enhance digestibility. Nectar, if the animals consume nectar in the wild, may
be fed (diluted 50:50 with water) and mixed with the diet. This is not in addition
to the diet. Fruit must be decreased by weight as nectar is offered. If, for
logistical or cost reasons, the use of insects must be decreased, increase the
nutritionally complete portion of the diet (by weight).

TABLE 2. SAMPLE DIETS


DIET #1
% IN DIET
FOODS (by WEIGHT as fed)
Commercial Marmoset Diet 70
Fruit 10
Vegetables 5
Starches 5
Insects 8

Nutrient Content of Diet #1


The commercial marmoset diet that compliments the diet above is one with the following specifications.
This particular product is a canned product (hence the higher moisture content). With the use of this
product, the diet must contain a source of vitamin C. (This can be obtained from the fruit, if a good source
is used.) This product contains the following nutrients as stated on the label and/or in the informational
literature:
Crude Protein minimum % 9.30 Ash maximum % 2.50
Crude Fat minimum % 3.20 Calcium minimum % 0.33
Crude Fiber maximum % 0.80 Phosphorous minimum % 0.24
Moisture maximum % 60.00 Vitamin D3 min IU/g 9.90

DIET #2
% IN DIET
FOODS (by WEIGHT as fed)
Commercial Primate Diet 50
Fruit 12
Vegetables 10
Starches 10
Insects 18

Nutrient Content of Diet #2


The commercial primate diet that compliments the diet above is one with the following specifications. This
product contains the following nutrients as stated on the label and/or in the informational literature:
Crude Protein minimum % 25.0 Calcium minimum % 1.0
Crude Fat minimum % 5.0 Phosphorous minimum % 0.6
Crude Fiber maximum % 4.0 Vitamin D3 IU/g 6.6
Moisture maximum % 10.0
Ash maximum % 6.1

58
DIET #3

% IN DIET
FOODS (by WEIGHT as fed)
Commercial Primate Diet A 47
Commercial Marmoset Diet B 10
Water 3
Fruit 10
Vegetables 10
Starches 10
Insects 10

Nutrient Content of Diet #3a


The commercial primate diet that compliments the diet above is one with the following specifications. This
product contains the following nutrients as stated on the label and/or in the informational literature:
Crude Protein minimum % 25 Ash maximum % 6.1
Crude Fat minimum % 5 Calcium minimum % 1
Crude Fiber maximum % 4 Phosphorous minimum % 0.6
Moisture maximum % 10 Vitamin D3 IU/g 6.6

Nutrient Content of Diet #3b


The commercial marmoset diet that compliments the diet above is one with the following specifications.
This is a powdered product formulated to be mixed with water and heated to a gel. Thus water was added
as part of the diet. It also is stated that it should be used with another manufactured primate diet (such as
used in this example). This product contains the following nutrients as stated on the label and/or in the
informational literature:
Crude Protein minimum % 33 Ash maximum % 5
Crude Fat minimum % 14 Calcium minimum % 0.85
Crude Fiber maximum % 6 Phosphorous minimum % 0.67
Moisture maximum % 2 or 0 Vitamin D3 IU/g 30

Quantity of food per day


How much to feed per day may be difficult to determine. Optimally, quality of food should be based on
accurate measurements of the animal’s body mass (or body weight). Charting an animal’s body mass over
time will provide an indication of optimum weight and normal fluctuations for that individual. This
information can be extremely valuable as a predictor of possible problems associated with weight changes,
including disease.

An average, active adult animal will consume approximately 5% of body weight per day (dry-matter basis);
or somewhere between 16 to 24% of body weight on an as-fed basis (depending on the moisture content of
the diet). However, this depends on exercise and physiological state. If the animal is lactating, intake
increases to 1.5 times usual. If the animal is in a period of decreased activity, it will consume less. In a
large colony of animals where there is high competition or animals of differing age/sex groupings, or where
there is the possibility of pest infestation, the animals should be fed so that there is a small quantity of food
remaining after the feeding period. However, there should not be so much food remaining as to allow
sorting and rejection of food items to occur. The challenge for animals’ caregivers is to assure that each
animal receives its prescribed diet, especially the nutritionally complete manufactured portion.

Remember, the quantity of food to be consumed depends on the nutrient density of the diet and the
digestibility of the food items. In callitrichids, the requirements for energy and protein are calculated
according to the body mass of the animal. Again, monitoring body mass will help determine intake.

To convert the percentages provided in the diets in Table 2 to actual quantity of foods to feed, the following
formula can be used: TOTAL g diet per day x percent food item in the diet/100

59
Size of food items
An individual should easily handle food items. Sizes and shapes should be varied for behavioral
enrichment.

Feeding behavior
Food sharing and stealing is common within family groups and serves to teach the young about important
food items. However, feeding the quantities as outlined above should circumvent the problem of an
individual in a group not receiving enough food because of competition.

Food—Handreared young
Feeding regimes for handreared young are available from the studbook keeper and the Infant Diet/Care
Notebook (AZA 1993, currently being updated and revised). Zoos have handreared a number of infants
successfully and reintroduced them after weaning to a family group for socialization and to learn parental-
care techniques.

Water—Adults
Fresh water should be available at all times. Food and water dishes should be disinfected daily to prevent
bacterial build-up, especially Pseudomonas.

ADDITIONAL COMMENTS ON FOOD AND FEEDING

Certain foods (like excessive quantities of fruit) may periodically cause diarrhea in some animals. The
literature for the gel diet states that loose stool may be associated with it, if fed in large quantities.
Temporarily restricting affected individuals to only the nutritionally complete primate biscuit/canned diet
may clear up the problem. Reducing the quantity of fruit in the diet may also produce desired results. The
importance of including the nutritionally complete primate diet cannot be overemphasized; its consumption
is critical to proper dietary management of these animals. The nutrient content of the diet should be
reassessed if one nutritionally complete food item is substituted for another. A drop or increase in food
intake must be carefully monitored and body weight should be maintained. Oral medication may be
handfed to individuals in favorite food items.

IMPORTANCE OF MEASURING DIETARY INTAKE AND METHODOLOGY

Ultimately, it is the diet (food items) actually consumed by each animal that will determine its nutrient
status. The diet offered must allow the animal to consume the nutrients needed. If the animal does not
consume the diet or certain portions of the diet, it may not receive the nutrients it requires. Therefore, it is
important to assess diet consumption periodically.

One method to determine diet consumption follows. Over a period of at least five days, keepers collect data
on diet offered and consumed. Different keepers should collect data to determine variation in individual
food preparation. Calculate consumption by measuring the quantity (by weight) of food items offered and
subtracting the quantity of food remaining. Each keeper apportions food according to normal procedures.
Weigh each item on a digital scale before adding to food pan. Orts (leftover food) are collected at the end
of the feeding time or before the next feeding time and weighed. Enrichment food items are included and
should be accounted for in the same manner.

Some foods dehydrate, so desiccation should be considered. Likewise, addition of water (i.e., rain or
misting) should be estimated. One simple way to avoid this is to determine intake by dry matter. If a drying
oven is unavailable, to determine food-weight changes, a weighed sample pan should be placed near a cage
(where the animals are housed) in an area free from pests. The pan should be left for the same period of
time as the diet and subjected to similar environmental conditions. The percentage of water gain or loss
should be determined and a correction factor calculated. This "factor" can then be used to determine the
actual quantity of diet consumed without the conflicting problem of moisture. A computer analysis (one
example: Animal Nutritionist software by N-squared Inc, Silverton, OR) can be used to calculate nutrient

60
content of the diet offered and consumed. For nutritional advice, please consult your nutritionist or obtain a
name of a professional nutritionist from the AZA Nutrition Advisory Group.

Special considerations:
1. Overweight Animals—If the diet is adequate in nutrients, the diet can be decreased in total
(beginning with a 5% decrease). Other options include decreasing the calorically dense food
items and/or increasing the lower calorie items. The importance of monitoring body mass can
not be overemphasized.
2. Seasonality—An occurrence in the wild, animals in captivity may occasionally undergo
seasonal fluctuations in intake and body mass. If these are determined to be normal for the
species or particular animal, changes in food offered can be made. The importance of
determining animal body weight and food consumption can not be overemphasized.
3. Periodontal disease—Animals that consume primarily soft foods that do not abrade the tarter
from teeth may have an increased susceptibility to dental disease. A nutritionally balanced
diet is important in maintaining oral health. Also, care should be taken to periodically offer
crunchy or hard foods that may help keep teeth clean.
4. Vitamin D—Tamarins require more vitamin D than other New World primates (Ausman et al.
1985; Takahash et al. 1985). The requirement for vitamin D for tamarins is 110 IU/day
(d)/100 g body weight (BW) on an as-fed basis (Takahashi et al. 1985). If animals are housed
indoors only, they must rely totally on diet for their vitamin D: if outdoors, they have the
opportunity to convert a vitamin D precursor in the skin to vitamin D upon exposure to
ultraviolet light. Much work is currently being performed with respect to vitamin D
deficiency and primates housed indoors (Meehan et al. 1996).
5. Wasting disease—Protein and calories are very important to callitrichids to prevent the
occurrence of protein/calorie malnutrition, which could lead to Marmoset Wasting Syndrome
(Barnard et al. 1988). Research has shown that tamarins require 150-160 Kcal/Kg body
mass/day (Morin 1980). The NRC (1978) recommends 3.5-4.5 g/Kg body mass/day high
quality protein for small primate species.
6. Species specific concerns—Cotton-top tamarins provide a model for studying colitis and
colon cancer. It is thought that this may be congenital. There also have been reports of high
blood pressure and heart disease in pygmy marmosets. The relationship to diet is unknown.
Taxonomically, callimicos appear slightly different than marmosets and tamarins and may
handle certain nutrients such as vitamin D differently (Crissey et al. 1996). The animal
manager should consult individual SSP manuals for details on species-specific differences.

APPENDIX A. FOOD CATEGORIES


Items listed in this appendix are examples with respect to availability. For additional information about
food categories and exchanging one item within a food group with another, consult the American Dietetic
Association (1995).

Fruit Veggies Starches


apples carrots sweet potato
bananas green beans white potato
grapes cucumber peas
oranges green pepper acorn squash
papayas zucchini cooked rice
blueberries cauliflower cooked pasta
strawberries cooked/canned beans corn
pineapple
grapefruit
pears

61
REFERENCES

Allen, M. E. 1989. Nutritional Aspects of Insectivory. Ph. D. thesis. E. Lansing: Michigan State University.
American Dietetic Association and American Diabetes Association. 1995. Exchange Lists for Meal
Planning. Chicago: American Dietetic Association.
Ausman, L. M., D. L. Gallina and R. J. Nicolosi. 1985. Nutrition and metabolism of the squirrel monkey.
In: Handbook of Squirrel Monkey Research, eds. A. L. Rosenblum and C. L. Coe, pp. 349-378. New
York: Plenum Press.
American Zoo and Aquarium Association (AZA). 1993. Infant Diet/Care Notebook. Wheeling, WV: AZA.
Barnard, D., J. Knapka and D. Renquist. 1988. The apparent reversal of a wasting syndrome by nutritional
intervention in Saguinus mystax. Laboratory Animal Science 38(3):282-288.
Calvert, J. J. 1985. Food selection by western gorillas (G. gorilla gorilla) in relation to food chemistry.
Oecologia 65:236-246.
Chadwick, D. P., J. C. May and D. Lorenz. 1979. Spontaneous zinc deficiency in marmosets, Saguinus
mystax. Laboratory Animal Science 29(4):482-485.
Clapp, N. K., and S. D. Tardif. 1985. Marmoset husbandry and nutrition. Digestive Diseases and Sci.
30(12):17S-23S.
Crissey, S. D., T. Meehan, M. A. Pruett-Jones, A. Baker and L. Phillips. 1996. Vitamin D metabolites (1,25
dihydroxy D and 25 hydroxy D) in Goeldi monkeys (Callimico goeldii) and the incidence of renal
disease. Symp. Comp. Nutr. Soc. 1:33-36.
Ferrari, S. F., and E. S. Martins. 1992. Gummivory and gut morphology in two sympatric Callitrichids
(Callithrix emiliae and Saguinus fuscicollis weddelli) from Western Brazilian Amazonia. Am. J. Phys.
Anthrop. 88:97-103.
Flurer, C. I., M. Kern, W. A. Rambeck and H. Zucker. 1987. Ascorbic acid requirement and assessment of
ascorbate status in the common marmoset (Callithrix jaccus). Ann. Nutr. Metab. 31:245-252.
Flurer, C. I., and H. Zucker. 1989. Ascorbic acid in a New World monkey family: Species difference and
influence of stressors on ascorbic acid metabolism. Z Emahungswiss 28:49-55.
———. 1988. Coprophagy in marmosets due to insufficient protein (animo acid) intake. Laboratory
Animals 22:330-331.
———. 1987. Difference in serum ascorbate in two species of Callithricidae. Internat. J. Vit. Nutr. Res.
57:297-298.
Garber, P. A. 1992. Vertical clinging, small body size, and the evolution of feeding adaptations in the
Callitrichinae. Amer. J. Phys. Anthrop. 88:469-482.
———. 1988. Foraging decisions during nectar feeding by tamarin monkeys Saguinus mystax and
Saguinus fuscicollis Callithrichidae, Primates, in Amazonian Peru. Biotropica 20(2):100-108.
Hartmann, E. W., and J. Hartmann. 1991. Geophagy in moustached tamarins, Saguinus mystax (Platyrrhini:
Callithrichidae), at the Rio Blanco, Peruvian Amazonia. Primates 32(4):533-537.
Heymann, E. W. 1992. Seed ingestion and gastrointestinal health in tamarins. Lab. Primate Newsletter.
July: pp 15.
Kelly, K. 1993. Environmental enrichment for captive wildlife through the simulation of gum-feeding.
Anim. Welfare Info. Center Newsletter. 4(3):9.
Kinzey, W. G., A. L. Rosenburger and M. Ramirez. 1975. Vertical clinging and leaping in a neotropical
anthropoid. Nature 255:327-328.
Meehan, T. P., S. D. Crissey, C. D. Langman and D. E. Sailer. 1996. Vitamin D related disease in infant
primates. Proceed. AAZV Conf. 91-93.
Morin, M. L. 1980. Progress report #8 on “Wasting Marmoset Syndrome. Bethesda: Dept. HEW, PHS,
NIH.
Nickel, D. A., and E. W. Heymann. 1996. Predation on Orthoptera and other orders of insects by tamarin
monkeys, Saguinus mystax mystax and Saguinus fuscicollis nigrifrons (Primates: Callithrichidae), in
north-eastern Peru. J. Zool. Lond. 239:799-819.
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C.: National Academy of Sciences.
Oftedal, O. T. 1995. Comparative nutrition of New World primates. Symp Health Nutr. New World
Primates by AZA New World Primate Taxon Advisory Group:4-8.
Pennington, J. A. T. 1993. Bowes and Church’s Food Values of Portions Commonly Used. 16th ed.
Perennial Library: Harper & Roe.

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Power, M. L. 1991. Digestive Function, Energy Intake and The Response to Dietary Gum in Captive
Callithrichids. Ph.D. thesis, Berkeley: UC-Berkeley.
Price, E. C. 1992. The nutrition of Geoffroy’s marmoset Callithrix geoffroyi at the Jersey Wildlife
Preservation Trust. Dodo. J. Wildl. Preserv. Trusts 28:58-69.
Ramirez, M., C. H. Freese and J. Revilla. 1977. Feeding ecology of the pygmy marmoset, Cebuella
pygmaea in Northeastern Peru In: The Biology and Conservation of the Callithrichidae, ed. D. G.
Kleiman, pp. 91-104. Washington, D.C.: SI Press.
Rosenberger, A. L. 1992. Evolution of feeding niches in New World monkeys. Am. J. Phys. Anthrop.
88:525-562.
Sturman, J. A. 1993. Taurine in development. Physiological Reviews 73(1):119-147.
Takahashi, N., S. Suda, T. Shinki, N. Horiuchi, Y. Shiima, Y. Tankoka, H. Koisumi and T. Suda. 1985. The
mechanisms of end-organ resistance to 1-alpha, 25 dihydroxycholecalciferol in the common marmoset.
Biochem. J. 227:555-563.
Terborgh, J., ed. 1983. Five New World Primates. A Study of Comparative Ecology. Princeton: Princeton
University Press.
Ward, A. M. and S. D. Crissey. 1997. Practical Feeding of Reptiles. Regional Proc. Amer. Zoo Aquar.
Assoc. Phoenix, AZ.
Wixson, S. K., and J. W. Griffith. 1986. Nutritional deficiency anemias in nonhuman primates. Laboratory
Animal Science 36(3):231-236.

63
ENRICHMENT AND OPERANT CONDITIONING OF CALLITRICHIDS
Michelle Farmerie, Don Neiffer VMD, and Karen Vacco

The following chapter addresses enrichment and operative conditioning pertaining to callitrichids and
Callimico. Information presented comes from two principle sources: personal experiences at the authors’
institution, and the results of a comprehensive survey distributed in July 1997. Also, included at the end of
this chapter is a list of references for further information.

Forty of one hundred institutions holding callitrichids and/or Callimico responded to the survey. These
results are found throughout this chapter. Each institution that responded was assigned a number (Appendix
A). The first part of this chapter follows the survey (Appendix B) as closely as possible.

The goal of this chapter is to present a portion of the information presently available on enrichment and
operative conditioning in callitrichids and Callimico. The authors hope this information will stimulate
communication and an exchange of ideas between institutions.

There are some general guidelines to follow when designing enrichment and operative conditioning
programs for any animal. It is important that unnatural behaviors not be encouraged. It is also important to
regulate the quantity and variety of the treats used to avoid obesity. Enrichment and training programs need
to be approved by the appropriate supervisory personnel. The toxicity and safety of an item or training
method should be reviewed by a veterinarian and when appropriate a nutritionist and/or botanist. The
Pittsburgh Zoo requires all food items, and techniques to be discussed with the veterinarian. The
horticulture department is also consulted regarding issues of plant toxicity. If in doubt—keep it out!

Careful records must be kept of methods tried, items used, and results found so that others can use the
information gathered. One of the easiest ways to keep records is by using standardized forms for both
enrichment and training (Appendix C). Each institution, depending on its resources and policies, may need
to develop its own form.

One last point worth mentioning exists. The information provided in this chapter is not based on formal
scientific studies. In fact, little research has been undertaken to determine if enrichment and operative
conditioning imparts positive stress on animals. While benefits of both enrichment and operant
conditioning programs have been realized by a number of institutions, any benefit of a particular technique
or item is somewhat subjective. For example, we (the author’s) assume that placing callitrichids in view of
other primate species is enriching when this may, in fact , be imparting a negative stress on the animals.
The bottom line is to proceed with caution and consider all potential outcomes of any aspect of your
program.

ENRICHMENT

Enrichment is anything added to or already occurring in an animal's environment that potentially creates
mental stimulation, evokes the senses, or helps to produce naturally occurring behaviors in an animal.
Enrichment may take many forms.

Training programs that improve animal husbandry can promote mental stimulation. Many items can alert
the senses and some items may initiate problem-solving techniques that a species might perform in the
wild. Enrichment can also occur in an animal's environment as a result of daily circumstances.

When giving enrichment items, keep in mind that after repeated exposure to the same stimulus an animal
may become bored. To avoid boredom, vary the type, amount, and presentation of any enrichment item.
Keep enrichments random, as predictability can cause a once effective technique to lose its novelty. To

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avoid predictability, keep a calendar of scheduled enrichments. A schedule also promotes advance
preparation that can maximize staff involvement in enrichment activities.

Document events by keeping records. These records should include the particular successes and failures of
different items, devices, and techniques. Accurate records are useful in evaluating an existing program and
may aid others trying to create new programs.

The following pages list the different types of enrichment being used at forty institutions.

TABLE 1. CALLITRICHID SPECIES CURRENTLY HOUSED AT INSTITUTIONS RESPONDING TO THE SURVEY


Callitrichids Institution
1. Callimico goeldii 3, 7, 8, 10, 22, 29, 32, 33, 36, 39, 40
Goeldi’s monkey
2. Callithrix geoffroyi 7, 9, 19, 29, 36, 39, 40
Geoffroy’s marmoset
3. Callithrix jacchus 5, 7, 14, 18, 21, 36, 39, 40
Common marmoset
4. Callithrix penicillata 1, 19
Black-eared marmoset
5. Callithrix kuhli 1, 15, 20, 28, 39, 40
Black tufted-eared marmoset
6. Callithrix pygmaea 7, 14, 16, 17, 21, 22, 27, 29, 30, 36, 40
Pygmy marmoset
7. Leontopithecus chrysomelas 7, 8, 19, 22, 36, 39
Golden-headed lion tamarin
8. Leontopithecus rosalia 3, 7, 9, 10, 11, 12, 13, 15, 16, 19, 20, 21, 22, 23, 24, 25, 27, 28, 31,
Golden lion tamarin 32, 33, 34
9. Saguinus bicolor 2
Pied or bicolor tamarin
10. Saguinus fuscicollis 3, 21, 40
Saddle-back tamarin
11. Saguinus imperator imperator 19, 39
Emperor tamarin
12. Saguinus imperator subgrisescens 6, 19, 39
Emperor tamarin
13. Saguinus imperator & subgrisescens 19, 39
Emperor tamarin (hybrid)
14. Saguinus leucopus 40
Silvery marmoset
15. Saguinus midas midas 3, 9, 13, 21, 38, 40
Red-handed tamarin
16. Saguinus midas niger 1
Black-handed tamarin
17. Saguinus mytax 40
Mustached tamarin
18. Saguinus oedipus 1, 4, 7, 9, 10, 11, 12, 13, 15, 17, 18, 19, 20, 24, 26, 27, 30, 31, 35, 37,
Cotton-top tamarin 38, 39, 40

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GROUP COMPOSITION
Group size varied from a lone animal of one species to groups as large as seven individuals. Not
suprisingly, group interaction between breeding pairs and siblings appears to be more stimulating than an
animal left to entertain itself.

Of the forty institutions that responded to the survey, twenty housed other animals with their callitrichids.
Using the mixed-species concept not only diversifies the environment, but can stimulate the animals as
well. Table 2 includes a list of institutions that house mixed species. The name, number of the institution,
type of callithrichid, and species of animal they are housed with are included.

TABLE 2. MIXED-SPECIES GROUP COMPOSITION AT RESPONDENT INSTITUTIONS


Institution Mixed Species
(3) Baltimore Zoo SAGUINUS MIDAS MIDAS EUPHRACTUS SEXCINCTUS
Red handed-tamarin Six-banded armadillo
SAGUINUS FUSCIOLLIS DASYPUS NOVEMCINCTUS
Nine-banded armadillo
(4) Binder Park Zoo SAGUINUS OEDIPUS 1.2 Testudo carbonaria
Cotton-top tamarin Red-footed tortoise
0.1.1 Iguana iguana
Green iguana
(7) Denver Zoo CALLIMICO GOELDII 1.1.1 Pithecia pithecia
Goeldi’s monkey Pale-faced saki
1.1 Choloepus didactylus
Two-toed sloth
LEONTOPITHECUS ROSALIA 1.1 Dasyprocta agouti
Golden lion tamarin Brazilian agouti
CALLITHRIX PYGMAEA 1.1.2 Callicebus moloch
Pygmy marmoset Orabussu titi
CALLITHRIX JACCHUS 1.1 Myoprocta pratti
Common marmoset Acouchi
(8) Dickerson Park Zoo CALLIMICO GOELDII Leontopithecus rosalia
Goeldi’s monkey Golden lion tamarin
(10) Dreher Park Zoo SAGUINUS OEDIPUS Amazona ochrocephala
Cotton-top tamarin oratrix
Yellow-faced amazon
Iguana iguana
Green iguana
Rallus sp.
Slate-necked rails
Leontopithecus rosalia Callimico goeldii
Golden lion tamarin Goeldi’s monkey
(species not specified)
Sloth
Anas sp.
Teal
Iguana iguana
Green iguana
Ramphastos sp
Toucan
(species not specified)
Tortoise

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TABLE 2. MIXED-SPECIES GROUP COMPOSITION AT RESPONDENT INSTITUTIONS (CONT.)
Institution Mixed Species

(11) El Paso Zoo Leontopithecus rosalia Paroaria capitata


Golden lion tamarin yellow-billed cardinal
Pteroglossus sp.
Aracari
Lophospingus pusillus
Black-crested finch
Ramphocelus carbo
Silver-beaked tanagers
Cacicus haemmorrhous
Red-rumped caciques
Saguinus oedipus Geochelone denticulata
Cotton-top tamarin Yellow-footed tortoise
Cyanocorax chrysops
Plush-crested jay
(15) Henson Robinson Zoo CALLITHRIX KUHLI 0.1 Choloepus didactylus
Black tufted-eared marmoset Two-toed sloth
(16) Indianapolis Zoo LEONTOPITHECUS ROSALIA 2.0 Callithrix pygmaea
Golden lion tamarin Pygmy marmoset
Geochelone denticulata
Yellow-footed tortoise
1.0 Dasyprocta cristata
Orange-rumped agouti
1.1 Paroaria coronata
Red-crested cardinal
1.1 Sicalus flaveola
Saffron finch
(17) Lincoln Park Zoo SAGUINUS OEDIPUS 1.2 Podocnemis Sp.
Cotton-top tamarin Amazon river turtle
1.1 Anas leucophrys
Ringed teal
1.1 Choloepus hoffmanni
Hoffman’s sloth
SAGUINUS IMPERATOR Callithrix pygmaea
Emperor tamarin Pygmy marmoset
(18) Little Rock Zoo CALLITHRIX JACCHUS Pithecia pithecia
Common marmoset Pale-headed saki
(19) Los Angeles Zoo SAGUINUS OEDIPUS 1 Leontopithecus rosalia
Cotton-top tamarin Golden lion tamarin
Callithrix geoffroyi 1 Saguinus imperator
White-fronted marmoset Emperor tamarin
1 Leontopithecus rosalia
Golden lion tamarin
(24) Pittsburgh Zoo Leontopithecus rosalia Inia geoffrensis
Golden lion tamarin Amazon river dolphin
Saguinus oedipus Dasyprocta puncata
Cotton-top tamarin Central American agouti
(25) Potawatomi Zoo Leontopithecus rosalia Iguana iguana
Golden lion tamarin Green iguana

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TABLE 2. MIXED-SPECIES GROUP COMPOSITION AT RESPONDENT INSTITUTIONS (CONT.)
Institution Mixed Species
(27) Roger Williams Park Zoo Callithrix pygmaea 0.1 Leontopithecus r. rosalia
Pygmy marmoset Golden lion tamarin
0.1 Choloepus didactylus
Two-toed sloth
Saguinus oedipus Coendou prehensilis
Cotton-top tamarin Prehensile-tail porcupine
(29) San Diego Zoo Callimico goeldii 2.3 Dinomys branickii
Goeldi’s monkey Parcaranas
0.2 Aotus trivirgatus
Douroucouli
1.0 Pithecia pithecia
Pale-faced saki
(33) Sedgwick County Zoo Callimico goeldii 1.1 Pteroglossus sp.
Goeldi’s monkey Aracari
Deroptyus a. accipitrinus
Hawk-headed parrots
3.2 Geotrygon versicolor
Crested quail dove
(35) Staten Island Zoo Saguinus oedipus Choloepus hoffmanni
Cotton-top tamarin Hoffman’s sloth
(35) Staten Island Zoo (continued) Iguana iguana
Green iguana
Eurypyga helias
Sun bittern
(species not specified)
Toucanet
Psophia sp.
Trumpeter
(36) Sunset Zoo Saguinus imperator 2.0 Callithrix pygmaea
Emperor tamarin 2.1 Pygmy marmoset
Momotus momota
Blue-crowned motmot
(39) Virginia Park Zoo Callithrix jacchus Coendu prehensilis
Common marmoset Prehensile-tail porcupine
0.1 Myoprocta pratti
Green acouchi
(40) Wildlife Conservation Society Callimico goeldii Leontopithecus rosalia
Goeldi’s monkey Golden lion tamarin
Callithrix penicillata kuhli 2.1 Callicebus donacophilus
Black tufted-eared marmoset Dusky titi
Callithrix geoffroyi 1.1 Callicebus donacophilus
Geoffroy’s marmoset Dusky titi
Callithrix jacchus 1.0 Myoprocta acouchy
Common marmoset Acouchi
Saguinus m. midas 0.1 Callicebus donacophilus
Red-handed tamarin Dusky titi
Saguinus fuscicollis 1.1.1 Callicebus donacophilus
Saddle-back tamarin Dusky titi
Saguinus leucopus 0.1 Myoprocta acouchy
Silvery marmoset Acouchi

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HOUSING
The size of exhibit or holding areas varied from a 2’x 3’x 3’ wire-mesh cage to a tropical forest building in
which the animals are free ranging. Thirteen institutions also offered outdoor housing with obvious
physical and mental benefits. Table 3 incluees a list of substrates and “furniture” used in two or more
callitrichid exhibits or holding areas:

TABLE 3. SUBSTRATES AND/OR FURNITURE USED IN CALLITRICHID EXHIBITS OR HOLDING AREAS


Substrates Furniture
Concrete Bungee cords
Grass Nest boxes
Newspaper Platforms
Peat moss Rock ledges
Pine bark mulch Ropes
Pine shavings Tree limbs (artificial and real)
River rock Vines (artifical and real)
Sand Window ledges

PLANTINGS
In the housing section, the survey requested a brief description of the types of plantings used in callithrichid
exhibits and holding areas. Many institutions provided extensive botanical lists that the authors thought it
would be a useful addition to the chapter. Knowing what types of flora to use successfully and safely with
callitrichids can help make their environment more enriching. Table 4 includes a list of flora that has been
used at various institutions.

TABLE 4. FLORA USED IN CALLITHRICID EXHIBITS AND HOLDING AREAS IN SELECTED INSTITUTIONS
Institution Species Common Name
Discovery Island Fiscus benjamina Weeping fig
Magnolia (species not specified) Magnolia
Murraya paniculata Orange jessamine
Bromeliaceae (species not specified) Bromeliad
Lagerstroemia Cape myrtle
Ulmus parvifolia Evergreen elm, Chinese elm
Impatiens walleriana Busy lizzie
Dreher Park Zoo Ficus sp. Ficus, Fig
Eugenia uniflora Surinam cherry
Musa x paradisiaca Banana
Species not specified Ferns
Greater Baton Rouge Zoo Ficus Ficus, Fig
Neomarica bicolor Walking iris
Scindapsus aureus Pothos, Devil’s ivy
Bromeliad sp. Bromeliad
Species not specified Palm Trees
Greenville Zoo Liriope Lily turf, Mondo grass
Ligastrum japonicum ‘variegatum’ Variegated privet
Liagstrum sp. Common privet
Ilex sp. Holly
Aspidistra elatior (lurida) Cast-iron plant
Eleagnus pungens Thorny eleagnus
Nandia domestica Nandina, Heavenly bamboo
Henry Doorly Zoo Sabal palmetto Cabbage palm, Palmetto plant
Busica buceras Black olive
Bougainvillea sp. Paper flower
Ficus aurea Strangler fig

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Institution Species Common Name
Thuja (species not specified) Arborvitae
Indianapolis Zoo Aechmea ‘Bert’ Bromeliad, Vase plant
Aechmea muricata Bromeliad, Vase plant
Aechmea pendulifora Bromeliad, Vast plant
Anthurium affine Flamingo flower
Arecastrum romanzoffianum Queen palm
Billbergia muriel waterman Bromeliad
Carica papaya Papaya, Melon tree
Cattleytonia jamaica red No reference
Cereus sp. Cactus
Cestrum nocturnum x diurnum Night-blooming jessamine
Chamaedorea elegans Parlor palm
Nephrolepis ealta ‘Kimberly Queen’ Boston fern, Lace fern
Philodendron (species not specified) Philodendron
Philodendron goeldii No reference
Portea petropolitana extensa Bromeliad
Spathiphyllum ‘Sensation’ Peace lily
Lincoln Park Zoo Dracaena deremensis ‘Janet Craig’ Dracaena, Fountain plant
Spathiphyllum ‘Sensation’ Sensation peace lily
Livistona chinesis Chinese fan palm
Ravenea rivularis Majestic palm
Strelitzia nicolai White Bird of paradise
Philodendron pertusum Split-leaf philodendron
Topeka Zoo Acacis farnesiana Popinac
Acalypha hispida Chenille plant
Aglaonema ‘Malay beauty’ or ‘Pewter’ Chinese evergreen
Aglaonema nitidum ‘Curtisii’ Chinese evergreen
Alocasia macrorrhiza Giant elephant’s ear
Amomum cardamomum Cardamon
Aspidistra elatior (lurida) Cast-iron plant
Bambusa ventricosa Buddha’s belly bamboo
Bougainvillea glabra Paper flower
Brassaia actinophylla Queensland umbrella tree
Bromeliad sp. Bromeliad
Canna generalis striatus Bengal-tiger canna
Carissa grandiflora Natal plum
Caryota mitis Fishtail palm
Chlorophytum cosmosum Spider plant tree
Chlorophytum cosmosum ‘Variegatum’ Variegated spider plant
Chysalidocarpus lutescens Butterfly palm, Areca palm
Citrus x paradisi Grapefruit
Codiaeum variegatum pictum ‘Appleleaf’ Apple-leaf croton
Codiaeum variegatum pictum ‘LM’ L.M. Rutherford croton
Cordyline australis Grasss palm, Cabbage tree
Cordyline terminalis Ti plant
Cordyline terminalis var. Ti Tree of kinds
Crinum giganteum Giant spider lily
Cycas revoluta Sago palm
Cyperus alternifolius Umbrella plant
Dendrocalamus giganteus Giant bamboo
Dieffenbachia amoena Dumbcane
Dieffenbachia amoena ‘Tropic Show’ Dumbcane variety
Dracaena deremensis ‘Bausei’ Bausei dracaena
Dracaena deremensis ‘Janet Craig’ Janet Craig dracaena
Dracaena deremensis sp. ‘Warneckii’ Warneckei dracaena

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Institution Species Common Name
Dracaena fragrans massangeana Corn plant
Dracaena marginata (gracilis) Madagascar dragon tree
Duranta repens Skyflower, Pigeonberry
Eriobotrya japonica Chinese loquat, Japanese plum
Ficus benghalensis Banyan Tree
Ficus benjamina Weeping fig
Ficus benhamina ‘variegata’ Variegated weeping fig
Ficus carica Common fig
Ficus elastica ‘variegata’ Rubber plant–variegated form
Ficus lyrata Fiddle-lead fig
Ficus pumila Creeping fig
Ficus religiosa Bo-tree
Hedera helix English ivy
Hibiscus sp. Hibiscus
Jacaranda mimosaefolia (acutifolia) Mimosa-leaved ebody
Kalanchoe blossfeldiana (hybrid) Kalanchoe, Flaming katy
Livistona chinesis Chinese fan palm
Monstera deliciosa Swiss-cheese plant
Musa x paradisiaca Common banana
Nephrolepis exaltata ‘Bostoniensis’ Boston fern, Fishbone fern
Ophiopogon japonicus ‘Kyoto dwarf’ Kyota dwarf, Snake’s beard
Pandanus utilis Screw pine
Passiflora edulis Purpose granadilla vine
Philodendron cordatum (true species) Heart-leafed philodendron
Philodendron lehmunnii No reference
Philodendron selloum Lacy tree philodendron
Philodendron williamsii Esperito santo philodendron
Phoenix dactylifera Date palm
Pheonix roebelenii Pygmy date palm
Pleomele reflexa Malaysian dracaena
Podocarpus macrophyllus Chinese yew, Buddhist pine
Polyscias fruticosa Ming Aralia
Pseuderanthemum atropurpureum Purple false eranthemum
Rhaphidophora celatocaulis Single plant
Sansevieria trifasciata ‘Hahnii’ Bird’s nest sansevieria
Sansevieria cylindrica Spear sansevieria
Sansevieria trifasciata ‘Laurentii’ Snake plant
Scheffler venulosa Hawaiian schefflera, Starleaf
Scindapsus aureus Pothos, Devil’s ivy
Spathiphyllum sp. Peace lily
Strelitzia alba Giant bird of paradise
Strelitzia reginae Bird of paradise
Syngonium podophyllum Arrow-head vine, Nephthytis
Syngonium podophyllum ‘Emerald Gem’ Arow-head vine green
Syngonium podophyllum albo – virens Arrow-head vine variegated
Trachycarpus fortunei Windmill palm
Vriesa splendens Flaming-sword bromeliad

Institution numbers 1, 11, 18-21, 23-31, 34-36, and 38-40 all have live plantings in their callithrichid areas
but did not list the specific types.

FOOD AS ENRICHMENT
One of the simplest enrichment techniques is to vary the type and size of food given to animals in their
daily diets. Substitutions given a couple of times throughout the course of a week can break up the
monotony of an unchanging diet. Alternating between whole and cut food can add to the complexity of an

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animal’s meal. Exotic food given occasionally can also add variety. However, the veterinarian should
always be consulted regarding any alteration in an animal’s diet before substitutions or additions are made.
Besides type and size, presentation of food items can have enriching properties. Table 5 includes a list of
different types of puzzle feeders used to dispense food at the corresponding institutions:

TABLE 5. TYPES OF FOOD DISPENSERS BY INSTITUTION


Food Despensers Institution

Bird feeders 24
Ferret logs 24
Foraging baskets 11, 24
Plastic feeder tubes 2
Puzzle feeder 16, 33
Soda bottle feeder
Treat logs 8, 11, 34
Wood feeder tubes 2

INSECTS
The presentation of insects is another source of enrichment. A nutritional supplement, live insects can elicit
many of the natural foraging behaviors seen in wild callitrichids. Almost every institution that responded to
the survey provides some type of insect. The most commonly used insects are mealworms, crickets and
waxworms, which are usually presented as part of the total diet. Increased enrichment has been obtained by
scattering insects in exhibits, dispensing them in various feeders, and using them as rewards in training.

ENRICHMENT OTHER THAN FOOD


There are many physical objects that can be used to enrich an animal’s environment. Table 6 includes a list
of “enrichment other than food” given at different institutions. Keep in mind that these have not been tested
for safety and the appropriate staff should be consulted before using any item. Questions about the
following list should be directed to the corresponding institution. Not all of these items may be appropriate
for “on exhibit” use.

TABLE 6. NON-FOOD ENRICHMENT ITEMS BY INSTITUTION


Enrichment Institution

Bags 17
Balls (wiffle, boomer, cat) 2, 4, 7, 25, 26, 29, 40
Bells 15, 24
Bird toys 1, 5, 17, 19, 24, 29, 39
Blankets 39
Boxes 16, 17, 22, 32
Bungee cords 14, 24, 27, 40
Burlap 2
Children’s toys 15
Egg cartons 2
Feathers 2
Hammocks 12, 29, 39, 40
Hay 2, 12, 38
Keys 19
Mirrors 1, 40
Mobiles 3
Motorized dancing balls 9
Paper 2, 22
Paper rolls 2, 16, 17

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Enrichment Institution
PVC pipes 1, 4, 22
Shoes 2
Snowballs 2
Squeak toys 2
Stuffed animals 14
Swings 3, 27
Tire swings 29
Yogurt cups 3

SENSORY ENRICHMENT
Certain types of enrichment can be given specifically to enhance the senses. Table 7 includes the most
common methods reported.

TABLE 7. SENSORY ENRICHMENT ITEMS BY INSTITUTION


Sensory Enrichment Institution

Extracts 24
Fresh and dry herbs 28, 31, 39
Jungle sounds 2, 32, 27
Junk CD’s (Hung in cage) 2
Mirrors 7, 9, 22, 24
Music 1, 2, 7, 9, 24, 28, 39
Perfumes 2, 28, 39
Videos (Tamarins and tamarin calls) 22

Types of sensory enrichment that may occur in an animal’s daily life but are not necessarily provided by
the caretaker for that reason include:

Views of other animals


Keeper interaction
Misters
Mixed-species exhibit
Transient insects and animals
Visitors
Vocalizations of other animals
Waterfalls
Weather (i.e., rain, wind, sunlight, and snow)

EXHIBIT MANIPULATION
Changing or rearranging existing limbs or vines in an animal’s exhibit or holding area is another technique
to enrich its environment. Falling water or streams may also be useful.

BROWSE
When considering browse for enrichment, callitrichids may not immediately come to mind. Although many
callitrichids may not consume large quantities of browse, they do use it in many different ways. Individuals
in the Pittsburgh collection have been observed chewing and stripping bark, biting off the leaves, and
running while another member of the group tries to take it from them. This enables them to use all of their
senses in addition to exercising. Browse may be nothing more then a temporary change in their
environment for them to explore. Although callitrichids may not eat it, browse is still a useful form of
enrichment.

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Table 8 was compiled from approved browse lists provided by several institutions and primate husbandry
manuals. Appropriate institution numbers accompanies browse species reportedly used with callitrichids
specifically. The authors do not guarantee the non-toxicity of these plants but have supplied them as a
source of information. In general, browse is presented as cuttings added to the exhibit or holding area.

TABLE 8. BROWSE LIST


SCIENTIFIC NAME COMMON NAME INSTITUTION
Acacia sp. Acacia 19, 20, 31, 34
Acer sp. Maple 1, 28, 38
Acer saccharium Silver maple
Acer saccharum Sugar maple 2, 4, 24
Acer negundo Box elder
Acer nigrum Black maple
Acer platanoides Norway maple
Alnus spp. Alder
Amelanchier sp. Serviceberry 4
Amelanchier sp. Juneberry
Amelanchier sp. Shadebush
Bambusa sp. Bamboo 2, 10, 11, 14, 20, 24, 27, 28, 29, 30, 32, 39
Betula allegheniensis Yellow birch
Betula papyrifera White birch
Bromeliad sp. Bromeliads
Celtis Hackberry
Cercis canadensis Redbud
Cercis siliquastrum Judastree (European redbud)
Cornus florida Flowering dogwood
Crataegus spp. Hawthorn
Elaeagnus umbellata Autumn olive 4
Fagus grandifolia American beech
Ficus sp. Ficus 10, 11, 17,24, 29, 30
Gleditisia triacanthos Honey locust
Hemerocallis fulva Daylily flower heads 2
Hibiscus sp. Hibiscus 10, 29, 31
Jacaranda acutifolia Mimosa 20
Jasminom sp. Jasmine 39
Lagerstroemia indica Grape myrtle 39
Liquidambur styraciflua Sweet gum
Malus sp. Crabapple
Morus sp. Mulberry 2, 11, 14, 24
Morus alba White mulberry 27, 39
Morus ruba Red mulberry 4, 27
Musa sp. Banana 24
Neomarica Walking iris
Populus sp. Poplar 1
Populus alba E. white poplar
Populus balsamifera Balsam poplar
Populus nigra Lomberdy poplar
Populus grandidentata Bigtooth poplar
Populus tremutoides Quaking aspen
Populus deltoides Cottonwood
Prunus sp. Cherry bush 34
Pueraria lobata Kudzu
Pyrus calleryana Gallery pear
Rosa sp. Rose petals 31, 39

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Scientific Name Common Name Institution
Salix sp. Willow 17, 24, 25
Salix amygdaloides Peachleaf willow
Salix babylonica Weeping willow
Salix fragilis Crack willow
Salix nigra Black willow
Thuga occidentalis Cedar 4
Ulmus sp. Elm 8, 24
Vitis sp. Wild grape 20, 24
Zea mays Cornstalks (green) 1

OPERANT CONDITIONING

To maintain a healthy population of callitrichids, monitor their health on a daily basis. The authors have
found that the best way to achieve this is through operant conditioning. Operant conditioning can help train
behaviors that will decrease animals’ stress levels. For example, a callithrichid trained to enter a portable
nest box avoids the stress of being netted for transport to the veterinary hospital. Additionally, certain
aspects of medical management, such as weighing and abdominal palpation, can be simplified and
performed more regularly without the use of manual or chemical restraint. In addition, training itself is
often considered enriching.

Before initiating a training program, perform a literature search to familiarize yourself with operant
condition information. Specific information on callithrichid training may be impossible to obtain. However,
general information can be modified to fit any training program. With hope, this chapter will provide a
foundation your callitrichid training program.

After completing the research, discuss the methods that will be used and the long-term goals of your
program with the appropriate supervisor and the staff veterinarian. Talk to other keepers/trainers at your
institution who are already training other species (i.e., sea lions, dolphins, elephants).

It is also important to consider relevant factors before beginning any training program. For example, a large
amount of trust develops between trainers and their subjects, and it is highly probable that the animal will
become less afraid of people over time. This may be problematic if primate/visitor interaction is possible in
free-ranging environments. In such situations, limit the scope of your training. Individuals who will be
training the callitrichids at your institution should be comfortable working “hand’s on” with the animals.
As animals lose their fear of trainers, they will likely become more comfortable and may initiate physical
contact even when it is not part of the training routine (i.e., jumping on trainers, pulling fingers, grooming
trainer’s hair). This has been observed with animals born into groups where a training program is already
established. While such contact may not be a problem, informing staff of such possibilities is important.
This physical contact can be shaped into behaviors that may prove to be very beneficial.

Following is a description of what the authors have found to be the most successful methods of training
callitrichids, specifically cotton-top tamarins. Included are definitions that have been found to be the most
important in understanding operant conditioning. Also included are step-by-step explanations of what
worked best for the authors. This is by no means the only way to approach callitrichid training, but is
instead a description of one successful program already in place. A list of other references can be found at
the end of this chapter.

DEFINITIONS

Operant conditioning: A type of learning in which behaviors are altered primarily by regulating the
consequences that follow them. The frequency of behaviors is altered by the consequences that they
produce (Scarpuzzi et al. 1991).

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Positive reinforcement: Anything that, occurring in conjunction with an act, tends to increase the
probability that the act will occur again (Pryor 1984).

Primary reinforcer: A reinforcing event that does not depend on learning to achieve its reinforcing
properties (food, water, and sex) (Havemann and Kagan 1976; Whittaker 1977; Kazdin 1989).

Secondary reinforcer (Conditioned reinforcer or bridge): An event that becomes reinforcing after it has
been paired or associated with a primary reinforcer (Havemann and Kagan 1976; Whittaker 1977; Baron,
Byrne and Kantowitz 1977; Kazdin 1989)

Variable reinforcement schedule: To maintain learned behavior with some degree of reliability, it is not
only not necessary to reinforce it every time. Indeed, it is vital that you do not reinforce it on a regular
basis. Switch to reinforcement only occasionally, and on a random or unpredictable basis (Pryor 1984).

Shaping (Successive approximation): Taking a very small tendency in the right direction and shifting it one
small step at a time towards the ultimate goal (Pryor 1984).

Jackpot: A reward that is much bigger than the normal reinforcement, and one that comes as a surprise to
the subject (Pryor 1984).

Wrong: Means “I’m not going to reinforce that but try again.” It is another technique to tell the animal what
you want, wrong is not “No” (Wilkes 1995).

No: Means that a behavior is not acceptable, and if it occurs again it will be followed by a time out.

Time out: A temporary stop in a session initiated by the trainer as a result of an inappropriate behavior by
the animal. The break in the session usually depends on the amount of time the trainer feels is necessary to
get the animal back on track. During this time the trainer does not react in any way, positively or
negatively, to the subject.

TABLE 9. TOOLS NECESSARY TO BEGIN OPERANT CONDITIONING PROGRAM


Tools Examples
Bridge Clicker, whistle, designated word
Target Drumstick, trainer’s finger
Reward Cheerios™, mealworms, grapes, raisins
Station Coasters of different colors and shapes unique to each one, individually colored clips, designated
branches

INITIAL TRAINING PROGRAM

Following is a list of some of the most important behaviors to train when beginning a callitrichid-training
program. These behaviors have been taught to a single cotton-top tamarin as well as a family group
comprised of seven of cotton-top tamarins. Remember that individuals differ and approaches to teaching a
behavior may have to be modified to best suit certain individuals or situations. For example the age, sex,
temperament or status of an individual within a group may all play a role in the animal’s progress in
learning. Behaviors can be considered learned when they become reliable upon command.

The first step in establishing a positive relationship between the trainer and animal is conditioning the
reinforcer. This can be accomplished by handing the animal a highly regarded food item and clicking
immediately before the animal takes the treat from the trainer. If the animal is too timid to take the treat
directly from the trainer, try clicking the animal for taking a treat from any other surface. Slowly decrease
the space between trainer and animal until the treat is accepted from the trainer’s hand. Initially the click
may frighten the animal but it usually gets used to the sound very quickly. After the trainer feels reasonably

76
confident that the animal has made the association between the click and the treat the trainer has
“conditioned the reinforcer.” Initial conditioning should begin with name recognition, target, and station.

NAME RECOGNITION
Results in the animal giving the trainer its attention.
Name recognition is very useful when working in a group. Because the complexity of the training will only
increase, it is very important that the animals know which animal the trainer wants to work. This is
accomplished by saying their name and clicking and treating when the animal gives the trainer their
attention. Initially eye contact with the trainer can be considered attention. As the callitrichid learns other
behaviors their name recognition can be reinforced by saying their name before a command and only
reinforcing the animal that was asked to perform the given behavior. It is not necessary to have name
recognition mastered before teaching other initial behaviors.

TARGET
Plain drumstick—animal touches its nose to the tip of a drumstick
To encourage the animal to come to the target, raisins can be smeared on the tip of a drumstick. When the
animal touches their nose to the tip a click is given immediately before they take the raisin. This usually
requires approximately a dozen repetitions before the raisin is no longer necessary. After the behavior is
predictable, the verbal cue “target” should be introduced just prior to the animal touching the target.

Finger—animal touches the trainer’s outstretched index with its nose.


The introduction of the trainer’s finger as a target can eventually enable the trainers to manipulate the
animals’ bodies for medical examinations. The use of the trainer’s finger as a target can prove to be the
single most important behavior taught. Not only is it a segue to physical manipulation, but when a finger is
presented in conjunction with the command “target” the callitrichid knows its time for training and not a
negative advancement towards them.

STATION
Animal identifies their designated station by touching it with its nose.
Cork beverage coasters of assorted shapes and colors have been found to be durable and safe to use. The
goal is to have each individual recognize their station. The introduction of coasters may elicit a very strong
flight reaction. To desensitize them, try visually exposing them to the coasters outside of their holding area.
This may take longer for some individuals, but eventually the animal will not consider the coaster a threat.
When training groups, a coaster can be assigned to the animal that shows the most interest in a particular
color. When the animal’s nose touches the station they should receive a click and then a reward. If the same
individual investigates other coasters do not reward it. It does not take long to elicit only the touching of
their station.

The use of the animal’s name is an integral part of teaching “station” to a group. Stations should not be
rearranged until a consistent response to the station command in the same location is achieved. It may be
desirable to shape this behavior so the animal places the majority of their body on the station when given
the command. The final test is then to rearrange the stations and ask each individual to station.

INTERMEDIATE TRAINING PROGRAM

When initial behaviors are consistently repeated, it is then possible to expand the training program.
Behaviors learned initially will act as building blocks that will increase the chances of success when
teaching more complicated tasks.

NESTBOX
Animal enters a nestbox
Training a callithrichid to enter a nestbox is one of the most useful behaviors that can be taught. Placing
treats on top of a nestbox is one of the easiest ways to get them accustomed to it. Once the animal is
comfortable on top of the box, a target can be inserted through a hole in the side. It may be necessary to
place a treat on the target to encourage the animal to enter the box. By giving the animal access to the front

77
and back of the box they tend to be less intimidated. After they are comfortable going into the box, the back
can then be closed leaving the front as the only way in. Eventually the treat on the target will no longer be
needed. This behavior is shaped by first rewarding them for placing any part of their body in the box while
targeting. The final step is when their whole body is in the box, their nose is on the target, and they allow
the door to be shut behind them. The diagram of the box used for training this technique can be found in
Appendix D.

OTHER TARGETS
Colored drumstick—animal identifies its designated color drumstick by touching it with its nose
The use of color-coded drumsticks assigned to each animal is useful when dealing with multiple and overly
eager animals. It is beneficial to coordinate the color of an animal’s drumstick with the color of their
station. By this point, target should be a learned behavior. This behavior is taught by only rewarding the
animal if they target their designated color drumstick. This technique can be cumbersome when dealing
with more than four animals.

Laser pointer—animal targets the beam of light


A laser pointer can be introduced when close contact with a callithrichid is not an option. The beam of a
laser pointer serves the same purpose as a target but without actual contact with the trainer. Due to the
chance of eye injuries from direct contact with the beam, it is advisable not to use a laser pointer in close
quarters or if the callithrichid can come in actual contact with the pointer while the beam is activated.

Colored clips—animal identifies its color clip by touching it with its nose
Colored clips are used in the same manner as a station or a colored drumstick but with two major
advantages—the clips can be placed on any surface including branches, ropes, and mesh, and they free up
the trainer’s hands. This behavior can be taught by following the same steps as station or target and can
function as both.

HOLD/STAY
Animal continues to hold a behavior or stay at a specific location.
Hold or stay can be added to all learned behaviors and can be extremely helpful. The hold/stay can be
elicited by rewarding longer variations of the original behavior or by gradually increasing the time between
the completion of the behavior and the delivery of the treat. The verbal command “hold/stay” can be added
when the trainer is consistently getting the length of the approximations they desire.

ON
Animal places its body on the trainer’s hand or other surface
The more trusting the subject, the easier this behavior is to train. The trainer places his or her hand—palm
side up—and lures the animal across it with a treat. First, click when one limb is on the trainer’s hand, then
two and so on. Eventually, the animal will place all four limbs onto the trainer’s hand. Individuals can even
be trained to jump directly onto the trainer’s hand from a distance. The “on” behavior may also be easily
captured in young animals who may already jump from a trainer’s shoulder or back. The “on” behavior
may prove to be useful not only by greatly enhancing physical manipulations, but also in the event of an
emergency when the need to get an individual in hand may be immediate.

UP
Animal stands up on its hind legs, making its underbelly accessible.
The “up” behavior can be achieved by holding the target above the animal’s head and then asking it to
target. This requires it to stand up on its hind legs to reach the target, exposing its underbelly. After this
behavior is shaped the verbal cue “up” can be added. It may be helpful to ask for this behavior in an area
where the animal can brace himself or herself on something (i.e. a branch, a wall, or a trainer’s hand)
especially if any pressure is going to be applied to the animal’s underbelly.

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ADVANCED TRAINING PROGRAM

When the initial and intermediate training program objectives have been achieved, the trainer can condition
callitrichids to allow routine medical examinations such as obtaining weights and temperature, physical
manipulations including implant detection, heart rates, chest sounds, detection of fetal heartbeats, and oral
examination. The collection of biological samples such as vaginal cytology and urine is also possible.
Accomplishing these tasks greatly minimizes the need for capture.

MEDICAL
Weighing—animal completely on the scale until a weight registers
The use of stations can provide an easy transition to the scale. Once the animal feels comfortable with the
scale in its territory, it will easily follow a target or its station onto the scale. After numerous repetitions for
each animal, the trainer can then add the verbal cue “scale”. At that point, the target or station is usually no
longer needed. In some cases it may be necessary to bring the less enthusiastic individuals to the scale with
the actual food reward.

Administration of medicine—animal takes the contents of a syringe orally.


Jelly or other desirable treats can be a good way to get callitrichids to take liquids from a syringe. The
purpose of this is to desensitize them to a syringe in the event that oral medication is required.

Biological samples—the free catch of urine or fecal matter


The collection of biological samples from callitrichids is not very difficult. Collecting first thing in the
morning before lights are turned on can ensure a successful free catch of urine or stool. By establishing a
positive relationship with the animal, it is relatively simple to coordinate entering their holding and
collecting the samples. It will not take long to attach a verbal cue “go” to the excretion of wastes to make
the behavior consistent on command.

Physical manipulation—animal permits the manipulation of its body without resistance


Before this is possible, the callitrichid must first be comfortable with the trainer’s touch—without the touch
eliciting the flight response. This is accomplished by only touching the animal on their terms. Gradually,
the animal should permit full-body manipulation when requested by the trainer. This conditioning is most
obviously beneficial when veterinarians are able to do manipulations themselves. This will require regular
participation from the veterinary staff for the callitrichid to become comfortable with them.

Vaginal cytology—animal permits a sterile cotton swab to be inserted into her vagina
Veterinary staff should be consulted before proceeding with this training. Although invasive, this procedure
can be very useful in the diagnosis of uterine pathology such as metritis and pyometra, and in gauging
estrus cycles. Begin by showing the female a cotton swab so she is familiar with it before training. Start the
training by having the female station at her colored clip, which should be positioned in a way that allows
access to her vagina. Begin touching her vaginal area very lightly with the sterile cotton swab and reward
her for any touch that she allows. As she becomes more comfortable with this, longer touches will be
tolerated. Initially, it is possible to coordinate the offering of the treat by one trainer as a second trainer
takes a mock sample. After the callitrichid is familiar with this, a sterile cotton swab can be inserted into
her vagina and secretions for analysis and/or cultures can be obtained.

Manipulation of a contraceptive implant—animal permits manipulation of her back until a


contraceptive implant is detected
Many times it is essential to have females in a callitrichid group receive contraceptive implants. Usually
implanted between the shoulder blades, the implant may be difficult to visually check. Being able to check
the implant site for abscesses, migration, or removal is important. At this stage, trainers should be able to
manipulate their subject’s body on a daily basis. The trainer can accomplish this in one of two ways: 1)
have her target in a manner that causes her to lower her head, or 2) hold a treat between the trainer’s fingers
and coax the animal to lower her head. Either method will expose her implant site for easy manipulation.
This examination should be incorporated into the animal’s daily routine.

79
Abdominal palpation—animal permits the manipulation of its abdomen
While the animal is performing the “up” behavior, hold a treat to steady it and apply light pressure to its
abdomen. Another approach is to have the animal stretch across the trainer’s hand for a treat while using
the other hand to palpate.

Conditioning for the detection of fetal heartbeats—useful for detecting pregnancies and viable
fetuses
The stethoscope should first be presented to the animal as a target. Have the animal touch the stethoscope
with its nose and reward it with a treat. Using this technique, touch different parts of its body with the
stethoscope until the animal is comfortable with the feel of the instrument. The “up” behavior is used to
obtain access to the individual’s abdomen. Once their underbelly is accessible, the stethoscope can be
placed for auscultation. Conditioning an animal to remain steady should permit the trainer to hear fetal
heartbeats.

Heart rates—animal allows a stethoscope to be positioned on its chest


Once the animal is acclimated to the touch of the stethoscope on their abdomen, it should be no problem to
place it on its chest. The “up” behavior again provides the easiest access to the necessary area. The animal
needs to “hold” the “up” position so the trainer can listen to the animal’s uninterrupted heart rate for a
minimum of six, and preferably fifteen seconds. Multiply the resulting number by ten or four respectively
to provide an accurate heart rate.

Chest sounds—animal allows a stethoscope to be positioned on its chest and back


No additional training should be required to monitor chest sounds since the animal should already be
accustomed to the stethoscope on that part of their body.

Temperature—a complete body temperature registers through the use of a rectal thermometer
Veterinary staff should be consulted before proceeding with this training. Follow the same techniques
described in the section on “vaginal cytology” except substitute a clean lubricated thermometer for the
cotton swab. Because the animal must remain in place until a complete reading of their body temperature
registers the Hold/Stay portion of this behavior must be mastered before this procedure can be successful.
This procedure is invasive and may not be permitted by every animal.

Oral examination—animal opens its mouth for oral examination


This behavior can be very useful in monitoring callitrichid dental health. One of the easiest ways is to take
advantage of a callitrichid’s natural response to investigate “new objects” with their mouth. Sometimes a
penlight may elicit this behavior, if so you are in luck. Penlights are the perfect size and very helpful when
examining teeth, mouth, and gums. Because it is a new item it will not take long for the animal to associate
the penlight with the mouth-opening behavior. After the behavior becomes predictable the verbal cue
“open” can be added. Initially, the trainer may need to allow the animal to make contact with the penlight
to continue to produce the “open” behavior. Often, this does not provide enough space between the penlight
and the animal’s mouth for a satisfactory examination. This problem can be rectified by incrementally
putting more space between the individual’s mouth and the light.

If the introduction of the penlight does not produce any type of mouth opening, try different objects until
one does. Perhaps a small twig of browse will work. After the verbal cue has been successfully attached to
the behavior, the trainer can introduce the penlight in addition to the “new object”. Gradually shift to only
the penlight. If you are unable to produce any mouth-opening behavior through the use of new items, it is
possible to capture this behavior by waiting for it to occur on its own. This will, however, take considerably
longer.

One result of teaching “open” can be the animal’s misunderstanding that this behavior is also acceptable in
conjunction with the “target” behavior. The “open” can be easily extinguished in the “target” behavior by
strictly reinforcing only the targeting which occurs with a closed mouth. The author’s have had no
experience with “open” leading to biting.

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PROBLEMS AND SOLUTIONS

PROBLEM: TRAINING MULTIPLE ANIMALS TOGETHER


It is very difficult to provide equal training time to each individual without interference from more
dominant members of the group. Because separating individuals is not always possible or advisable, other
alternatives must be examined as solutions.

Station
The teaching of the station behavior is one way to counteract this problem. It provides each animal with a
place to be and therefore allows time to work with the less dominant animals.

Increase the size of the treat


To keep the dominant animals busy for longer periods of time, try increasing the size of the treat. For
example, it takes longer for an animal to eat a square of bread then a Cherrio™. Sometimes the animal will
work without food rewards so this is not always a solution.

Increase the complexity of the treat


Another approach to solving this problem is to give an animal a more difficult and much more time-
consuming treat to eat. The treat that may best meet this need is a peanut. Peanuts also make excellent
jackpots.

Increase the length of the session


Increasing the length of the session allows more time to work with all of the animals, including the less
dominant individuals. Be aware of all individual attention spans and make sure you are the one who
determines the conclusion of each session. It is possible to end an individual animal’s training session while
continuing to work with other members of the group. This is most successful when the more dominant
animals in a group are focused on first.

Add another trainer


A solution that is recommended but not always an option is to add another trainer. At first this may make
the animals suspicious if they are not used to two people in their area at the same time. Once the animals
realize that two trainers are not a threat, dividing the group between trainers is very useful. Trainers should
only reinforce the animals they are responsible for in any given session.

PROBLEM: VERY CAUTIOUS ANIMALS


Although some animals may be more hesitant then others, they, too, can be proficiently trained. Often
smaller steps may work better with the less dominant individuals. Any progress, no matter how minor,
should be rewarded.

PROBLEM: ELICITING A SKILL AFTER A NEGATIVE OUTCOME


There is often a drop in the performance of a skill when a negative outcome is the result. One example of
this is when an animal goes into their nestbox and the outcome is a trip to the hospital. The amount of time
it takes to make any behavior reliable again varies depending on the intensity of the event and the
individual animal. Sometimes it is necessary to repeat the beginning steps of the behavior to produce the
complete behavior again.

PROBLEM: “WHAT WORKED FOR EVERYONE ELSE ISN’T WORKING HERE”


Some individuals may not readily learn a behavior that other group members pick up easily. Trainer
creativity may result in the best solution. Sometimes, an “off the wall” idea about leading an animal
through a behavior is the best one. Don’t be afraid to try something different to initially produce a behavior
that you want to capture.

PROBLEM: DISTRACTIONS
Initially, the smallest distraction can disrupt a training session. Any loud noises, activity in front of the
animals area, or anything out of the ordinary may cause a chain reaction of alarm calls and flight responses
that brings the training session to an end. The solution to this comes with time. The more comfortable the

81
animals become with their trainer and training, the easier it is to bring their attention back to the trainer and
the session.

PROBLEM: CONSISTENCY AMONG TRAINERS


Maintain consistency between trainers because using different training techniques will only confuse the
animals and be counter-productive for everyone. Daily record keeping and good communication between
trainers helps ensure consistency in a training program.

PROBLEM: TIME FOR TRAINING


Since many trainers are also keepers and have multiple responsibilities, it can sometimes be difficult to find
as much time as desired for training. However, as little as five minutes a day will keep the program moving
forward.

PROBLEM: OFF DAYS


Sometimes, for no apparent reason, an animal may not be interested in training. At that point the session for
that animal should be ended.

CONCLUSION

Teaching the behaviors in this chapter may significantly aid in many husbandry and medical situations
involving callitrichids. Additionally, the authors have found that training has been a very valid enrichment
technique for callitrichids. The tamarins at the authors’ institution are extremely interested in their training
sessions and seem to become excited while training preparations are being made. The development of a
training program has been rewarding for all individuals involved from tamarin to trainer. The authors
believe that the same benefits will be reaped at other institutions that establish callitrichid-training
programs of their own.

The behaviors that callitrichids can learn are not limited to the ones mentioned in this chapter. The use of
operant conditioning as a tool in their management is full of potential. It is the authors’ hope that the
publication of this chapter will initiate a network of communication and discussion between callitrichid
keepers. In addition, the authors are interested in the results of any callitrichid training program and
welcome any information about this subject. Such correspondence can be sent to the address below.

For more information, feel free to contact Michelle Farmerie or Karen Vacco at The Pittsburgh Zoo, One
Wild Place, Pittsburgh, PA 15206. Phone: (412) 365-2385. FAX: (412) 365-2583.

APPENDIX A. INSTITUTIONS THAT RESPONDED TO THE SURVEY


Institution Address Contact
African Safari Wildlife Park 267 Lightner Road Bill Coburn
Port Clinton, OH 43452-3851 Fax (419) 734-1919
Tele (419) 732-3606
Akron Zoological Park 500 Edgewood Avenue Michelle Studer
Akron, OH 44307-2199 Fax (330) 375-2575
Tele (330) 375-2250
Baltimore Zoo Druid Hill Park Gwen Mullen
Baltimore, MD 21217-9973 Fax (410) 396-6464
Tele (410) 396-7102
Binder Park Zoo 7400 Division Drive Jenny Barnett
Battle Creek, MI 49017 Fax (616) 979-8834
Tele (616) 979-1351, ext. 158
Brandywine Zoo 1001 N. Park Drive Yvonne Maurer
Wilminton, DE 19802 Fax (302) 571-7787
Tele (302) 571-7604
Como Zoo Midway Parkway & Kaufman Drive Lou Distano
Saint Paul, MN 55103 Fax (612) 487-8203

82
Institution Address Contact
Tele (612) 487-8201
Denver Zoo City Park Bruce Kane
Denver, CO 80205-4899 Fax (303) 376-4901
Tele (303) 376-4900
Dickerson Park Zoo 3043 N. Fort Misty Mitchell
Springfield, MO 65803 Fax (417) 833-4459
Tele (417) 833-1570
Discovery Island P.O. Box 10000 Dawn Safranek-Leonard
Lake Buena Vista, FL 32830-1000 Fax (407) 824-3467
Tele (407) 824-2875
Dreher Park Zoo 1301 Summit Boulevard Dr. Randy McCormick
West Palm Beach, FL 33405 Fax (561) 533-6085
Tele (561) 585-0887
El Paso Zoo 4001 D. Paisano Yvonne Carbis
El Paso, TX 79905 Fax (915) 521-1857
Tele (915) 521-1850
Greater Baton Rouge Zoo P.O. Box 60 Talon Thornton
Baker, LA 70704 Fax (504) 775-3931
Tele (504) 775-3877
Greenville Zoo 150 Cleveland Park Drive
Greenville, SC 29601 Fax (864) 467-4314
Tele (864) 467-4300
Henry Doorly Zoo 3701 S. 10th Street Cathy Socha
Omaha, NE 68107-2200 Fax (402) 733-4415
Tele (402) 73-8401
Henson Robinson Zoo 1100 E. Lake Drive Colleen Wirrick
Springfield, IL 62707 Fax (217) 529-8748
Tele (217) 753-6217
Indianapolis Zoo 1200 W. Washington Street Lynn Villers
Indianapolis, IN 46222 Fax (317) 630-5153
Tele (317) 630-2034
Lincoln Park Zoo 2200 N. Cannon Drive Lynn Tupa
Chicago, IL 60614` Fax (312) 742-2137
Tele (312) 742-7716
Alt Tele (312) 742-7732
Little Rock Zoo #1 Jonesboro Drive Sydney Tanner
Little Rock, AR 72205-5401 Fax (501) 666-7040
Tele (501) 666-2406
Los Angeles Zoo 5333 Zoo Drive
Los Angeles, CA 90027 Fax (213) 662-9786
Tele (213) 666-4650
Micke Grove Zoo 11793 N. Micke Grove Road Susan Wier, Lucy Jones, Jeff Holland
Lodi, CA 95240-9499 Fax (209) 331-7271
Tele (209) 953-8840
Monkey Jungle 14805 SW 216 Street Julio C. Perla
Miami, FL 33170 Fax (305) 235-4352
Tele (305) 235-1611
National Zoological Park Smithsonian Institution Cathy Morrison
Washington, D.C. 20008-2598 Fax (202) 673-5686
Tele (202) 673-4753
New England Science Center Harrinton Way Don Winans
Worcester, MA 01603 Fax (508) 752-6879
Tele (508) 791-9211
Pittsburgh Zoo 1 Hill Road Michelle Farmerie, Karen Vacco
Pittsburgh, PA 15206 Fax (412) 365-2385

83
Institution Address Contact
Tele (412) 668-3794
Potawatomi Zoo 500 S. Greenlawn Betsy Singleton
South Bend, IN 46615 Fax (219) 235-9080
Tele (219) 235-9800
Prospect Park Wildlife Center 450 Flatbush Avenue Donna Fernandes, Marian Glick-Baurer
Brookyn, NY 11225-3707 Fax (718) 399-7337
Tele (718) 399-7312
Roger Williams Park Zoo 1000 Elmwood Paul Guidetti, Joel M. Hamilton
Providence, RI 02907 Fax (401) 941-3988
Tele (401) 785-3510
Ross Park Zoo 185 Park Avenue Deidre Flaherty
San Diego, CA 92112-0551 Fax (607) 724-5454
Tele (607) 724-5461
San Diego Zoo P.O. Box 551 Sue Averill
San Diego, CA 92112-0551 Fax (619) 231-0249
Tele (619) 231-1515
San Francisco Zoo 1 Zoo Road Eve Watts Lyon
San Francisco, CA 94132--1098 Fax (415) 681-4749
Tele (415) 753-7144
Santa Ana Zoo 1801 E. Chestnut Avenue Connie Sweet
Santa Ana, CA 92701 Fax (714) 953-4701
Tele (714) 647-6575
Santa Barbara Zoo 500 Niños Drive Susan Hoegeman
Santa Barbara, CA 93103 Fax (805) 962-1673
Tele (805) 962-5339
5555 Zoo Boulevard Mike Quick
Sedgewick County Zoo
Wichita, KS 67212 Fax (316) 942-3781
Tele (316) 942-2213
Sequoia Park Zoo 531 K Street
Eureka, CA 95501-1165 Fax (707) 441-3247
Tele (707) 441-4227
Staten Island Zoo 614 Broadway Mark Rich
Staten Island, NY 10310 Fax (718) 981-8711
Tele (718) 442-3101
Sunset Zoo 2333 Oak Street Ryan Gulker
Manhattan, KS 66502-3824 Fax (785) 587-2730
Tele (785) 587-2737
Topeka Zoo 635 SW Gage Boulevard Mike Coker
Topeka KS 66606-2066 Fax (785) 272-2539
Tele (785) 271-0523
Utica Zoo Steele Hill Road Gary Zalocha
Utica, NY 13501 Fax (315) 738-0475
Tele (315) 738-0472
Virginia Zoological Park 3500 Granby Street Lisa Behm
Norfolk, VA 23504 Fax (757) 441-5408
Tele (757) 441-5227
Wildlife Conservation Society Bronx, NY 10460 Coleen McCann
Tele (718) 220-5161

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APPENDIX B. CALLITRICHID ENRICHMENT AND OPERATIVE CONDITIONING SURVEY

The purpose of this survey is to obtain information for the callitrichid husbandry manual and more
specifically, the chapter on operative conditioning and enrichment. The results of this survey will hopefully
serve as a guide for institutions housing callitrichids so that the lives of these species may be improved in
captivity. We realize that multiple types of housing and social groupings may be in use for callitrichids at
any one institution, depending on the resources available and that institution’s goals. For this reason, we
request that you make copies of this survey and complete one for each situation existing at your institution.
We realize that time is at a premium and we gladly accept any information, no matter how general. Where
possible, however, detailed descriptions are preferred. Feel free to contact Karen Vacco, Michelle
Farmerie, or Don Neiffer at (412) 365-2385, Fax: (412) 365-2583, if you have any questions regarding this
survey. Thanks!

Historical information:

1. What species of callitrichids are housed at your institution?

2. Group composition: Total number in group __________

Adults M _____ F _____


Juveniles M _____ F _____
Infants M _____ F _____

3. Housed (Check appropriate) _____ on exhibit _____ off exhibit


_____ inside _____ outside

4. Brief description of holding area/exhibit (including, but not limited to dimensions, substrate, furniture,
plantings):

5. Mixed species? Yes _____ No ______

Enrichment (Please fill in all that apply):


1. Browse
Types (Latin names if possible)
Presentation

2. Insects
Types
Presentation

3. Other food items


Presentation

4. Enrichment items other than food (ex. balls, bird toys)


Types

5. Other types of enrichment


Sensory (i.e., music, oils, spices, mirrors)

Exhibit manipulation (i.e., changing limbs or vines, adding falling water or streams)

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Operative conditioning/training goals (Please comment on all that apply):

1. Medical procedures on unrestrained animals (e.g., routine weighing, medication, urine and fecal
collection, fetal heartbeat detection, vaginal cytology)

2. Do you provide training as a source of enrichment (e.g., attention given to animals serves as a positive
stimulus in itself)

3. If yes, please describe method.

4. Crate training (i.e., for exhibit/holding maintenance or for transport to veterinary hospital).

Types of positive conditioning/training used and brief description

1. Have you used operative conditioning to elicit any of the following behaviors? If so, please provide a
brief description where necessary.

A. Name Recognition

B. Target
i) types (e.g., drumstick, laser pointer, finger)

C. Station
i) types (e.g., coasters, platforms, perches)

D. Physical Manipulation
i) types (e.g., keeper’s fingers, dowel, swab)

E. Other

2. What secondary reinforcers do you use (e.g., clickers whistles, voice)?

3. Please list types of primary reinforcers (i.e., types of treats, other)

4. Do you use?
A. Voice Commands __________
B. Physical Cues __________
C. Both __________
D. Other __________

We welcome any additional information on enrichment or training techniques not presented in this survey.

86
APPENDIX C. EL PASO ZOO ENRICHMENT SHEET: ENRICHMENT PROGRAM
SPECIES: Golden Lion Tamarin
EXHIBIT: South American Pavilion
Center Exhibit
EXHIBIT MATES: Yellow-billed cardinal, aracari, black-crested finch, silver-beaked
tanagers, and red-rumped caciques

The social group for the golden lion tamarins should be a family group if possible, but juvenile groups,
non-breeding pairs, same sex groups, etc., may be displayed also. A minimum of one nest box that can
accommodate all group members will be available. The furnishings should include both rigid and flexible
vertical and horizontal supports of different diameters. Nest boxes and elevated feeding and water stations
should be located at or above average public eye levels.

If the golden lion tamarins must be housed singly, then when possible it will be housed with visual, audible,
and tactile contact with the members of the group unless the veterinarian determines an exemption for
health reasons.

Approved Enrichment Devices:


1. Free-spinning feeder logs on ropes
(Logs are filled with raisins, small chop, peanut butter, or mealworms.)
2. Hanging fruit on a string or thick line (such as weed-eater line)
3. Foraging holes in cork bark
4. Foraging baskets
5. Passive mealworm dispensers
6. Passive cricket dispensers
7. Yogurt dispensers (not yet approved)
8. Dry cereal and or pasta (not yet approved)
9. Coconut mealworm dispenser
10. Foraging log (need to discuss)
11. Addition of different forage items (bamboo, leafy branches, etc.)
12. Changing branches or vines
13. Addition of scents and spices to branches or leaves in exhibit
14. Jell-O™ cubes made with fruit juice (not yet approved)

Each approved enrichment device will be randomly scheduled at the first of the month and written on a
monthly calendar. Each day after the enrichment has been implemented, the keeper will initial the calendar
square indicating that the enrichment has been done. The calendars will be located in a centralized area in
the South American Pavilion. Additional comments or the animal’s response to a new enrichment item will
be noted in daily log sheets and on the animal enrichment response/evaluation form. The success of the
scheduled enrichment items will be reviewed monthly. Additions or subtractions of new or unsuccessful
enrichment devices will be noted on the enrichment program as needed.

87
PITTSBURGH ZOO TRAINING WORKSHEET
DAILY BEHAVIORS WORKED
Date: Total number of sessions: Treats/rewards: Trainer:

Environmental Factors:
Allegra Dunkin Piglet Vincent Jules Hector Harley Ceres Sadie
Name Recognition
Targets:
Drumstick
Colored Drumstick
Finger
Laser Pointer
Hold/Stay
Station ( coaster )
Station ( colored clip )
Implant Manipulation
Abdominal Manipulation
General Body Manipulation
Stethoscope ( touch w/any body part )
Heart Rate
Chest Sounds
Abdominal Sounds / Fetal Heartbeats
Nestbox
On
Open
Scale
Syringe ( oral meds )
Temperature
Up
Vaginal Swab
New:
Comments/Notes:

Allegra-
Dunkin-
Piglet-
Vincent-
Jules-
Hector-
Harley-
Ceres-
Sadie-

88
REFERENCES

Baron, Bryne, and Kantowtiz. 1977. Psychology: Understanding Behavior. Philadelphia: Saunders.
Farmerie, M. R., and K. L. Vacco. 1997. Turning a negative into a positive for cotton-top tamarins through
operant conditioning. In Proc. 3rd International Environmental Enrichment Conference, Orlando, FL,
October 1997.
Havemann and Kagan. 1976. Psychology; An Introduction, Harcourt Brace Javanovich, Inc.
Kazdin, Alan E. 1989. Behavior modifications in applied settings; 4th edition. Pacific Grove: Brooks/Cole.
Pryor, Karen. 1985. Don’t Shoot The Dog, Bantam Books.
Savage, A. Ph.D, ed.. 1995. Cotton-top tamarin (Saguinus oedipus) AZA SSP Husbandry Manual.
Providence: Roger Williams Park Zoo.
Scarpuzzi, Michael R., Clinton T. Lacinak, Ted N. Turner, Charles D. Tompkins and David L. Force
(1991). Operant Conditioning, Sea World, Inc.
The Shape Of Enrichment: A Quarterly Source Of Ideas For Environmental And Behavioral Enrichment.
Current and back issues.
Whittaker, James O. 1977. Introduction To Psychology, 3rd edition; Philadelphia: Saunders.
Wilkes, Gary. 1995. Click And Treat Training Kit, Version 1.1, Wiles Publishing.

89
Handrearing Callitrichids and Callimico in Zoological Parks
Vince Sodaro and Sue Crissey, Ph.D

INTRODUCTION

Techniques for handrearing callitrichids were first developed in biomedical laboratories in the 1960s. The
earliest reported successes occurred at the University of Texas Institute for Dental Science where seven
Saguinus oedipus were handreared in 1964 (Hampton et al. 1967). A procedure similar to that described by
Hampton et al. was used in 1965 to handrear Saguinus nigricollis and Saguinus fuscicollis in a biomedical
laboratory established for viral oncogenesis studies (Wolfe et al. 1972). These efforts were followed by
successes with Leontopithecus (Rohrer 1979), Saguinus (Pook 1974), Callithrix (Pook 1976), and Callimico
(Beck et al. 1982) in zoological institutions in the 1970s. Cebuella was not successfully handreared until the
1980s (Albers 1990) but the handrearing of other species had by then become a fairly common occurrence.

While callitrichids in laboratories were often handreared for experimental purposes or to derive specified
pathogen-free animals for biomedical studies (Hobbs et al. 1977), zoological institutions strive to promote
parental rearing of offspring whenever possible. Handrearing is avoided unless warranted by problems. Parental
incompetence, neglect, or rejection of offspring is perhaps the problem that most frequently necessitates
handrearing. Poor parental care and rejection of offspring by animals lacking prior experience with infant care
has been documented for several callitrichid species (Hoage 1977; Dronzek et al. 1986; Pook 1974; Epple
1970).

For some species, handrearing may be warranted by the occurrence of triplets. While Leontopithecus rosalia
triplets have been successfully parent-reared in captivity, Stevenson (1976) found that Callithrix jacchus in her
colony were unsuccessful in rearing triplets. One pair succeeded in rearing two infants from a set of triplets,
while the third infant died on day three. In two other cases of Callithrix jacchus triplets, Stevenson found it
necessary to remove one of the infants for handrearing. Similarly, Callimico, which normally have single births,
may have difficulty raising twins. A multiparous, wild-caught female that gave birth to twins at Brookfield Zoo
succeeded in raising only one of the infants; the other died on day four. In a second case of Callimico twinning
at Brookfield, a male infant was removed for handrearing when the dam appeared to be having trouble carrying
and positioning the two infants for nursing.

A variety of medical problems affecting either callitrichid dams or neonates may also necessitate handrearing.
A case of mastitis in a multiparous Callimico dam at Brookfield Zoo necessitated removing a two-day-old
infant for handrearing after the dam repeatedly prevented the infant from nursing. Hampton et al. (1967)
handreared an unusually small and possibly premature Saguinus oedipus triplet that was found to be in a
weakened condition at one day of age. Infants born by Caesarian section may require handrearing as a result of
the inability of a recuperating dam to rear the infants.

INCUBATORS AND THERMOREGULATION

Newborn callitrichids are unable to thermoregulate and must be housed in incubators until several weeks old. In
some of the early successes with handrearing, infants were kept in incubators until ages ranging from six to
eight weeks for Saguinus species (Wolfe et al. 1972), to as long as ten to twelve weeks for Saguinus and
Callithrix species (Ogden 1979). Several species have since been found to tolerate removal from incubators at
much earlier ages if provided with heating pads, heated surrogates, or heat lamps. Leontopithecus rosalia
infants handreared at Oklahoma City Zoo were removed from incubators at two to three weeks and housed in
glass-fronted boxes with a heating pad that covered approximately one third of the bottom of the box (Rohrer
1979). Dronzek et al. (1986) found that Saguinus oedipus infants could thermoregulate at three to four weeks
and could then be transferred from an incubator to a reintroduction cage. Callimico have also been found to be
able to thermoregulate at three to four weeks and can be removed from incubators at twenty-three to twenty-
five days (Sodaro et al. 1994).

90
Standard incubators designed for human infants are commonly used to house newborn callitrichids (Wolfe et al.
1972; Ogden 1979; and Dronzek et al. 1986). Various authors have reported a range of recommended
temperatures and relative humidity for infants in incubators, along with schedules for reduction of temperature
and humidity before and after removal of the infant from the incubator (Table 1).

DIET

Ideally, a handrearing formula would be developed to imitate mother's milk. However, limited information is
available on the nutrient composition of the milk of the various species of callitrichids. Published reports that
include the handrearing formulas successfully used for callitrichids are also limited. In 1993, the American Zoo
and Aquarium Association published the Infant Diet/Care notebook. A chapter on the handrearing of small
prosimians and callitrichids was included in this publication (Crissey 1993). Information included in that
chapter originated from published literature, information available on the commercially available milk
replacers, and from a handrearing questionnaire circulated at that time. Data collected on 34 animals in six
institutions were taken from the survey. The information in this section is drawn mainly from the pertinent
sections of that document.

MILK COMPOSITION

Milk output and composition will change over time. A single sample is not necessarily a good indication of true
milk composition thoughout the lactation period (Ausman 1995). There are, however, trends and for example
callitrichid milk can be considered more concentrated than human milk. Saguinus oedipus milk was reported to
contain 3.8% protein, 3.1% fat, 5.8% carbohydrate (lactose) and 0.4% ash, on a fresh weight basis (Hafes
1971). From these data, tamarin milk can be calculated to be approximately 86.9% water and contain 0.66
kcal/gram. It was reported that milk composition of Callithrix jacchus was more dilute (Ausman 1995).

HANDREARING FORMULA

A compilation of published data and the survey of holding institutions that performed successful handrearing
shows that a combination of a human-infant milk replacer and a high-protein nutritional supplement is an
effective formula for callitrichid handrearing (Beck et al. 1982; Crissey 1993). The formulation suggested as
appropriate contained 8.4 grams of human-infant formula (powder) with 2.4 grams of Sustagen™, a protein
powder, and 60.0 ml boiled water. There also was a high-protein primate formula (Primilac™) available which
was used by one of the surveyed institutions.

Human-infant formulas are very similar. In fact, law mandates the nutrient levels contained in them. Averaged
values were used in minimum allowable standards. These nutrients must be present in the formula at the time of
use and many manufacturers add extra nutrients to ensure that all nutrients are presented at the mandated levels
(Benton 1989). Thus, the formulas Similac™, SMA™, Enfamil™, and Isomil™ are similar (Typlin 1986; PDR
1989). Isomil™ is a soy-based formula and unless there is an allergy to milk protein or the animal is lactose
intolerant, there is no need for the use of the soy-based formula (Ausman 1995). These allergies/intolerances
have not been published with respect to callitrichids so it is assumed that there is no problem. In the survey,
SMA™ was the product used most often in addition to Sustagen™, the high-protein supplement (Crissey
1993).

Sustagen™ contains milk protein and lactose. Table 2 provides the nutrient breakdown of the suggested
formula

91
TABLE 1. Recommended incubator temperatures, relative humidity (RH), and schedules for reduction of temperature and humidity before and after removal of
callitrichid infants from incubators.

Incubator
Author Species Temp. RH Comments
Hampton et al 1967 Saguinus oedipus 82-86F 85% for 1 week; At 5 weeks, infant put in wire cage 24” x 30” x 15”
50% thereafter
Wolfe et al. 1972 Saguinus oedipus 88-90F 50% or above Isolette infant incubator (Air Shields Inc., Hatboro, PA 19040 USA). At 6-8
Saguinus nigricollis weeks, infants are transferred to modified rabbit cages in rooms with
Saguinus fuscicollis temperatures of 78-82F, RH 50-60%
Pook 1974 Saguinus fuscicollis 89F Oxygenaire human incubator used. Temperature reduced to 83F at 5 weeks.
Infant placed in “small cage” on day 40.
Stevenson 1976 Callthrix jacchus 25-28C An incubator was not used. Infants were kept in a wooden nestbox on a
toweling mattress with a small piece of toweling for the infants to cling to.
Cicmanec et al. 1979 Saguinus spp. 88-90F 50%
Callithrix jacchus
Hearn et al. 1979 Callithrix jacchus 25-30C 80% Initially, a higher ambient temperature of 30-35 C may be preferable, but
should not exceed this. Ambient temperature should be gradually reduced to
room temperature of 25 C.
Ogden 1979 Saguinus spp. 90F 70-80% Isolette incubator (Air Shields, Inc.) Incubator temperature is maintained at
90F with 80-90% RH for four weeks. Temperature and RH are gradually
reduced to room conditions of 80F and RH of 50%. Infants remain in
incubator until weight of 150 g is reached at approximately 10-12 weeks.
Infants are then transferred to modified rabbit cages.
Rohrer 1979 Leontopithecus 85-90F Armstrong X-4 Baby Incubator used. A heating pad with rheostat control is
used for heating and is covered with bedding. Infants are removed from
incubator at 2-3 weeks and moved to a 37” x 22” x 22” glass-fronted box. A
heating pad is used as the heat source and covers 1/3 of the bottom of the box
so that the infant can move away from the heat if necessary.
Dronzek et al. 1986 Sanguinus oedipus 32.2C 70-80% Isolette Infant Incubator, Model No. C-86. Temperature maintained at 32.2 C
for first two days, then gradually decreased to 26.7 C during the first week.
Removed from incubator at 3-4 weeks.

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TABLE 2. MILK REPLACERS FOR CALLITRICHIDS. NUTRIENT CONTENT, AS FED
Nutrient SMA/Sustagen/Water Primilac
Water, % 84.75 85.9
Energ, ME kcal/g 0.96 0.25
Protein, % 2.65 3.58
Carbohydrate (lactose), % 11.15 8.11
Fat,% 4.75 3.79
Linoleic acid, % 0.9 -
Vitamin A, IU/g 2.71 3
Vitamin D3, IU/g 0.5 0.55
Vitamin E, ppm 28.4 20
Thiamin, ppm 1.10 0.81
Riboflavin, ppm 1.64 1.62
Niacin, ppm 9.91 8
Pyridoxin, ppm 0.89 0.81
Folic acid, ppm 0.09 8
Vitamin B12, ppm 0.003 0.03
Pantothenic acid, ppm 4.45 5
Choline, ppm 160.7 405
Biotin, ppm 22.4 0.4
Vitamin C, ppm 90.36 120
Calcium, % 0.076 0.075
Phosphorous, % 0.053 0.045
Magnesium, % 0.009 0.017
Potassium, % 0.093 0.087
Sodium, % 0.027 0.038
Iron, ppm 26.02 13
Zinc, ppm 7.67 2.8
Copper, ppm 0.72 0.68
Manganese, ppm 0.56 2.62
Iodine, ppm 0.09 0.35
SMA/Sustagen/Water formula=Human infant formula (powder) 8.4 grams; Sustagen (powder) 2.4 grams; Water 60 grams. Primilac formula
at manufacturers suggested dilution. (Crissey 1993)

FEEDING SCHEDULES AND QUANTITIES


Many institutions use just a pediatric electrolyte solution or a dextrose solution for the first day. Diluting with
this solution and slow conversion over several days may allow easy conversion to full formula. The final
formula need not contain the solution and diluting with boiled water is recommended (Crissey 1993).

It is suggested that an appropriate quantity to feed callitrichids is from 20-27% of their body weight per 24
hours. Of the institutions answering the survey, a range of 12-27% of body weight was fed. In the beginning of
handrearing, a more diluted formula, fed at 10-12% of body weight, may help avoid potential problems with
diarrhea (Crissey 1993).

Most infants were fed on demand or 2-3 hour intervals. By two to three weeks of age, the number of feedings
per day can be decreased to three to four times daily, as consumption of solid foods increased. Monitoring

93
daily body weight fluctuations is an appropriate method to determine infant needs and subsequent success. A
growth curve for a particular species is important for comparison. Figures 1 and 2 illustrate growth curves for
callimicos and tamarins, respectively.

FEEDING APPARATUS
Some institutions used a latex nipple formed on 3 cc syringe (Dronzek et al. 1986). Others simply used syringes
to drop formula into the infant's mouth.

WEANING

Callitrichids have teeth at least by three weeks of age. They can bite and swallow soft foods at four weeks.
These infants will play with food at a very early age and solid foods should be offered to provide familiarity
with the items (Ruppenthal 1979). Diluted baby cereal can be fed with the formula (either separate or mixed
with formula) beginning at two weeks. Soft, steamed, or canned foods (primate and/or marmoset canned foods)
can follow soon thereafter. Considerable consumption of soft foods should be seen by one month and
sometimes, formula offerings should be limited to encourage consumption of these foods. Most callitrichids are
weaned to an adult diet by about 3 to 4 months of age.

SURROGATES

Callitrichids, like all nonhuman primates, cling to the bodies of older animals during infancy and should be
provided with surrogates during handrearing. The surrogates used for handrearing callitrichids are often as
simple as a rolled up towel, a stocking stuffed with cotton, or a plush "stuffed animal" toy. Surrogates of this
type provide infants with security and a soft surface for clinging but may do little to prepare them for
reintroduction to conspecifics. Infants that have been handreared for several weeks may become irreversibly
imprinted on artificial surrogates and upon reintroduction fail to recognize a conspecific as something to which
they may cling. As a result, the valuable socialization experience of being carried is lost. Although little data
exists to correlate surrogate types with successful reintroductions of handreared infants to conspecifics, it may
be reasonable to assume that more realistic surrogates may aid in the transition from the handrearing
environment.

Surrogates of more sophisticated design have also been used. Dronzek et al. (1986) provided handreared
Saguinus oedipus infants with heated surrogates constructed from a piece of ¼-inch hardware cloth that was
formed into a cylinder enclosing a looped heating coil. These surrogates were covered with artificial fur to
which non-toxically tanned real tamarin fur was sewn. The surrogates were then suspended to the top of an
incubator by elastic bands to provide a bouncing motion that simulated the sensation of being carried by a
conspecific. Further movement was provided by a small motor with a reciprocating arm with a 1-¼ inch
throwing distance. This motor was mounted on plywood outside of the incubator and had a piece of plastic
coated wire that connected the reciprocating arm to the elastic band of the surrogate.

Surrogates of this type were first developed at the Bielefeld Callitrichid Station, Bielfeld, West Germany
(Wolters, unpublished). Surrogates developed there were fabricated to be the approximate shape and size of
adult Saguinus oedipus with proportionate limbs and head, and covered with artificial fur. These surrogates
were also heated and suspended by elastic bands. Infants were provided with two surrogates during the
handrearing process, one of which was designed to represent a lactating female, and which had a nursing unit
consisting of a specially designed silicon nipple mounted on a short tube. A removable tube filled with enough
formula for one feeding fit into the tube, which was attached near the armpits of the "mother" surrogate.
Initially, infants were transferred to the feeding surrogate only during formula feedings, and afterwards
transferred back to the "father" surrogate. Infants were capable of transferring between surrogates without
assistance beginning at ages of seven to ten days. During weaning, a small bowl for solid food was attached to
the chest of the "father" surrogate, while the amount of formula available from the "mother" surrogate was
gradually reduced.

94
Feeding surrogates can be beneficial to a handrearing process insofar as they may allow an infant to associate
feedings with the surrogate, rather than with a human caretaker, thereby reducing some of the inprinting on
humans that commonly occurs with handreared callitrichids.

Surrogates should continue to be provided for infants until after reintroduction to a family group. They can be
removed if group members begin to carry the infant. If this does not occur, the surrogate should be removed
when the infant begins to huddle and sleep with other group members or seems to be showing confidence in
spending time away from it.

REINTRODUCTION

The ultimate goal of any handrearing endeavor should be the reintroduction of the infant to its natal group or
integration into a suitable foster group.

Similar methods for the initial stage of reintroduction have been described in several published accounts of
handrearing. This consists of housing the infant with its surrogate in an interim or "howdy" cage that is placed
near or within the cage of the group to which the infant will be introduced. This allows the infant and its
prospective family visual, auditory, and olfactory contact with each other prior to the actual introduction, and
offers caretakers and managers opportunities to observe and assess the reactions of the infant and group
members to each other. This method has been used for Callithrix jacchus (Kuster 1978), Leontopithecus rosalia
(Rohrer 1979), and Callimico goeldii (Beck et al. 1982; Sodaro et al. 1994). After a period of acclimation,
infants are allowed to leave the interim cage and given direct access to the group to which they are being
introduced. Initially, infants may be returned to their interim cage at night or whenever observers are not
present until they appear to be well integrated into the group.

Pook (1978) reintroduced Callithrix and Saguinus infants directly to family groups without the use of interim
cages. Infants of six to seven weeks of age were placed, on their surrogates, in a warm spot in a fairly well used
part of the cage with observers present to assess the reactions of the infant and the group to each other. Initially,
infants were left in the groups' cage for short periods of time. These sessions were gradually extended over a
period of ten to fifteen days until the infants were being removed only at night. When weaning was complete
and the infants were engaging in positive social interactions, they were allowed to remain in the group cage
overnight.

Dronzek et al. (1986) exposed handreared Saguinus oedipus to the families to which they would later be
introduced at two to three weeks of age while the infants were still in the incubator. The incubator was placed in
front of the family group for two to three hours daily to give the infant and group members visual and auditory
contact with each other. Callimico goeldii infants at Brookfield Zoo were handreared in incubators that were
placed inside of the cage of the group to which the infants were later reintroduced (Sodaro et al. 1994). This
method provided the infant and the group with visual, auditory, and olfactory contact with each other from day
one. Infants were removed from the incubator for each feeding and fed in the cage. Group members were
allowed to approach, sniff, and touch the infant. This, in turn, allowed the infants to become familiar with the
group members before actually being reintroduced to them.

Stevenson (1976) used five-month-old handreared Callithrix jacchus infants to aid in the socialization process
of a newborn female of the same species that was being handreared. This infant was first exposed to these
juveniles on day two, with the older animals being allowed to lick and nuzzle her face. Beginning at two weeks
of age, the infant was allowed to spend thirty minutes per day with them, during which time both carried her.
The apparently tame nature of the older animals allowed easy retrieval of the infant for bottle-feeding.

The ages at which infants have been first removed from incubators and transferred to interim cages or to the
cages of family groups varied from as young as twenty-three days for Callimico goeldii (Sodaro et al. 1994), to
as long as sixty-three days for Callithrix jacchus (Kuster 1978). The older an infant is prior to reintroduction to
a family group, the greater the loss of the normal socialization process that a parent-reared infant experiences. It
is therefore extremely important to attempt reintroduction at as early an age as possible. This is limited only by
the earliest age at which the infant can thermoregulate and be removed from an incubator, and the earliest age at

95
which the infant can locomote independently. Although it is highly desirable that an infant be carried by
members of the group to which it is introduced, this should not be allowed to happen to an unweaned infant that
is not capable of dismounting from a carrier to return to caretakers for bottle feeding. Stevenson's case (1976) is
exceptional in this regard because the handreared juveniles to which the Callithrix jacchus infant was
introduced were apparently tame individuals that allowed themselves to be handled for removal of the infant.
Retrieval of a dependent infant from a normal adult conspecific is difficult, if not impossible, without capture
and manual restraint.

In general, the outcomes of reintroduction attempts are often unpredictable and not always successful. Pook
(1976) reported that an attempt to reintroduce a pair of Saguinus oedipus infants to their parents at the age of six
weeks failed when the sire chewed off the leg and part of the tail of one of the infants. This occurred the first
time the infants were left unattended in the group after a week of supervised introductions ranging from one-
half hour to one hour long. Kuster (1978) reported that an attempt to reintroduce a female Callithrix jacchus
infant to a family group failed when the infant avoided any approach or physical contact by the members of the
group. She exhibited intense fear of conspecifics, biting and running frantically when approached. This
behavior did not diminish after four days and the reintroduction attempt was stopped. The family had shown
little interest in the infant after all had touched and sniffed her. This infant had been reared in complete isolation
from conspecifics until sixty-three days old and was not given direct access to the group until fourteen weeks
old.

Kuster (1978) found that two infants with an age difference of four days fared much better when introduced to
the same family to which the previously mentioned infant had been introduced at the ages of forty-four and
forty-eight days, respectively. These infants integrated well into this group and later participated in the carrying
of offspring subsequently born into the group.

In certain situations, managers may opt for attempting to integrate handreared infants into a foster family rather
than to return it to its natal group. If a particular dam has a history of rejecting offspring, there may be little to
gain in terms of a normal socialization experience for handreared offspring that are reintroduced to her. Infants
returned to such a dam are less likely to have opportunities to gain infant experience if subsequent siblings are
likely to be rejected and also handreared. Handreared Saguinus oedipus in a colony at the University of
Wisconsin were generally not reintroduced to natal groups, but into foster families that were more likely to
provide social and infant-care experience (Dronzek et al. 1986).

Fostering of newborn or very young infants to adult pairs in which the female is lactating has also been
successful. Collier et al. (1986) successfully introduced a five day old Saguinus oedipus infant to an adult pair
to which stillborn infants had been born twenty-four hours earlier. The foster parents cared for the infant
through weaning and handrearing was thereby avoided.

SOCIALIZATION PROBLEMS OF HANDREARED CALLITRICHIDS

Handrearing, by its very nature, creates an abnormal socialization experience for callitrichid infants. A
handreared individual is unlikely to become a competent parent unless successfully integrated into a group that
can provide a positive social environment for learning species-specific behaviors and social skills. Nevertheless,
apparently successful integration into such groups often fails to compensate for the earlier loss of normal
socialization incurred during handrearing. Handreared individuals that have been reintroduced to normal social
groups may still exhibit aberrant behaviors and fail to rear offspring. In some cases, socialization problems
resulting from handrearing are immediately apparent at the time of reintroduction. This is evident in situations
in which reintroduced infants exhibit fear of conspecifics and resist their attempts to approach or carry them.
Several aspects of handrearing may be responsible for this behavior, including unfamiliarity with conspecifics
caused by isolation of the infant during handrearing, a strong psychological attachment to an artificial surrogate,
and imprinting on human caretakers. This results in the loss of the normal socialization experience that parent-
reared infants receive by being carried.

In the earliest efforts to handrear Callimico at Brookfield Zoo, infants were reared in isolation from
conspecifics. The majority of these infants were not carried by conspecifics after reintroduction (Sodaro et al.

96
1994). Many of these infants exhibited fear of conspecifics, but in several of these cases, the members of the
groups to which they were introduced showed indifference to their presence and did not attempt to carry them
or demonstrate other solicitous parental behavior towards them. The handrearing techniques used there were
substantially changed in the early 1990s, with infants being handreared in incubators that were located within
the enclosure of the groups to which they were later introduced. These infants were thus exposed to group
members from day one. All of these individuals were carried by group members following reintroduction and,
in general, became better integrated into groups than the infants that had been handreared in isolation.

Kuster (1978) reported that a female Callithrix jacchus that had been handreared in isolation was met with a
mixture of aggression and indifference when introduced to a family group. In this case, a female juvenile in the
group bit the infant several times during the introduction while other group members paid little attention. The
rejection of offspring by handreared callitrichids is a common occurrence. Many handreared individuals do not
receive infant experience prior to becoming parents, but the rejection of offspring by such individuals is more
likely to be a result of the failure of the handrearing process to provide a normal socialization experience rather
than lack of infant experience. This is not to suggest that infant experience is not important. On the contrary, it
has been well documented that callitrichids that have had infant experience have a greater success rate at
rearing offspring than those that lack prior experience (Snowden et al. 1986; Rettberg-Beck and Ballou 1997).
Nevertheless, Rettberg-Beck et al. reported a survival rate of approximately fifty per cent for Leontopithecus
rosalia that were born to parent-reared females that lacked prior infant experience. Similarly, five of eight
parent-reared female Callimico at Brookfield Zoo that lacked infant experience successfully reared offspring.
The key in these cases is that these individuals were parent reared and were well socialized.

No handrearing effort can be considered truly successful if the handreared individual does not ultimately
participate in the rearing of its own offspring. Moreover, no single handrearing technique can guarantee such an
outcome. Nevertheless, much can be learned from the published accounts of handrearing efforts that resulted in
well socialized, as well as poorly socialized individuals. Clearly, the best approach may be one that aims for
reintroduction as early as possible while allowing infants and the groups to which they will be reintroduced to
be in close visual, olfactory, and auditory contact throughout the handrearing process. If such an approach is
combined with the use of realistic surrogates, and the handling of the infant is minimized to prevent imprinting
on humans, there may be hope for rearing of individuals that will later rear their own offspring.

APPENDIX 1. PRODUCT LISTING

Enfamil® SMA®
Mead-Johnson Wyeth-Ayerst Laboratories
Bristol Meyers Squibb Division of American Home Products Corp.
2400 W. Lloyd Expressway PO Box 8299
Evansville, IN 4772 Philadelphia, PA. 19101

Isomil®/Similac® Sustagen®
Ross Products Division Mead Johnson Nutritional Division
Abbott Laboratories Mead Johnson
Columbus, OH 43215-1724 Evansville, IN 47721
Bristol Myers Squibb
Primalac®
BioServe, Inc.
PO Box 450 Frenchtown NJ 08825

97
REFERENCES

Albers, Koen B. M. 1990. International Studbook for the Pygmy Marmoset Cebuella pygmaea. Second Edition.
Apenheul Zoo: The Netherlands.
Ausman, L. 1995. Nutritional needs of the neonate and growing young monkey. In: Symposium on Health and
Nutrition of New World Primates, 12 March. New World Primate Taxon Advisory Group of the American
Zoo and Aquarium Association.
Beck, B. B., D. Anderson, J. Ogden, B. Rettberg, C. Brejla, R. Scola and M. Warneke. 1982. Breeding the
Goeldi's Monkey Callimico goeldii at Brookfield Zoo, Chicago. International Zoo Yearbook 22:106-114.
Benton, D. 1989. Personal Communication.
Collier, C, S. Kaida and J. Brody. 1981. Fostering techniques with cotton-top tamarins Saguinus oedipus
oedipus at Los Angeles Zoo. International Zoo Yearbook 21:224-5.
Crissey, S. 1993. Infant Diet/Care Notebook. Wheeling, WV: American Zoo and Aquarium Association.
Dronzek, L. A., A. Savage, C. T. Snowdon, C. S. Whaling and T. E. Ziegler. 1986. Technique for hand-rearing
and reintroduction of rejected cotton-top tamarin infants. Laboratory Animal Science 36:243-7.
Epple, G. 1970. Maintenance, breeding, and development of marmoset monkeys (Callitrichidae) in captivity.
Folia Primatologica 12:56-76.
Hafez, E. ed.. 1971. Comparative Reproduction of Non-Human Primates. Springfield, IL: Thomas Publishing.
Hampton, S. H., and J. K. Hampton, Jr. 1967. Rearing marmosets from birth by artificial laboratory techniques.
Laboratory Animal Care 17:1-10.
Hearn, J. P., and F. J. Burden. 1979. "Collaborative" rearing of marmoset triplets. Laboratory Animals 13:131-
3.
Hoage, R. J. 1977. Parental care in Leontopithecus rosalia: Sex and age differences in carrying behavior and
the role of prior experience. In: The Biology and Behavior of the Callitrichidae, ed., D. Kleiman, pp. 293-
305. Washington D.C.: Smithsonian Press.
Hobbs, K. R., G. Clough and J. Bleby. 1977. The establishment of specified-pathogen-free marmosets
(Callithrix jacchus). Lab. Anim. 11:29-34.
Kuster, J. 1978. Preliminary investigations on the integration/reintroduction of hand reared common marmosets
(Callithrix jacchus) into family groups. In: Biology and Behavior of Marmosets, eds. H. Rothe, H-J.
Wolters, and J. Hearn, pp. 149-152. Gottingen:Eigenverlag.
Ogden, J. 1979. Handrrearing Saguinus and Callithrix genera of marmosets. In: Nursery Care of Nonhuman
Primates. G. C. Ruppenthal, ed., pp. 313-10. New York: Plenum Press.
PDR, Physicians Desk Reference for Non Prescription Drugs. 1989. Oradell, NJ: Medical Economics Co.
Pook, A. G. 1974. Handrearing and reintroduction to its parents of a saddleback tamarin. Jersey Wildlife
Preservation Trust Annual Report 11:35-59.
———. 1976. Some notes on the development of handreared infants of four species of marmosets
(Callitrichidae). Jersey Wildlife Preservation Trust Annual Report 13:38-46.
———. 1978. Some notes on the reintroduction into groups of six handreared marmosets of different species.
In: Biology and Behavior of Marmosets, eds. H. Rothe, H-J. Wolters, and J. Hearn, pp. 155-159.
Gottingen:Eigenverlag.
Rettberg-Beck, B., and J. Ballou. 1997. Personal Communication.
Rohrer, M. A. 1979. Handrearing golden lion marmosets, Leontopithecus rosalia at the Oklahoma City Zoo.
Anima Keepers' Forum 6:33-39.
Ruppenthal, G.C., ed. 1979. Handrearing infant callitrichids, (Saguinus spp and Callithrix jacchus), owl
monkeys (Aotus trivirgatus), and capuchins (Cebus albifrons). In: Nursery care of nonhuman primates, pp.
307-312. New York: Plenum Press.
Sodaro, V., K. Pingry and K. Snyder. 1994. Changes in handrearing procedures for Callimico goeldii at
Brookfield Zoo. In: 1994 AZA Regional Conference Proceedings, pp. 404-407. Wheeling, WV: AZA.
Snowdon, C. T., A. Savage and P. B. McConnell. 1985. A breeding colony of cotton-top tamarins (Saguinus
oedipus). Laboratory Animal Science 35:477-480.
Stevenson, M. 1976. Maintenance and breeding of the common marmoset. (Callithrix jacchus) with notes on
hand-rearing. International Zoo Yearbook 16:110-16.
Typalin, B. 1986. Human Milk Replaces. Dr. Scholl Nutrition Conference.
Wolfe, L. G., J. D. Ogden, J. B. Deinhardt, L. Fisher and F. Deinhardt. 1972. Breeding and handrearing
marmosets for viral oncogenesis studies. In: Primate Breeding, ed. W.I.B. Beveridge, Basel: Karger.

98
Wolters, J. Maintenance and breeding of callitrichids in captivity Part I. Artificial rearing techniques for the
cotton-top tamarin (Saguinus oedipus). Unpublished.

99
HANDREARING CALLIMICO GOELDII IN ZOOLOGICAL PARKS
Vince Sodaro

INTRODUCTION

Attempts to handrear callimico infants are most frequently necessitated by poor maternal care or actual
rejection or abandonment. The vast majority of callimico births occurs at night and is seldom observed by
keepers. At the first morning check of the animals, keepers typically discover abandoned infants. Such infants
may be found lying on the floor or shelves of the cage, or being carried by another member of the female's
group. Unlike Leontopithecus (Hoage 1977) and Saguinus (Price 1992) infants, which may be carried by other
members of a female's group in the first week of life, captive-born callimico infants are normally carried
exclusively by the dam until four or five weeks of age. A newborn callimico being carried by group members
other than the dam signals maternal rejection or other problems and requires an immediate response.

Competent, experienced females exhibiting good maternal care will appear to be comfortable carrying a
newborn infant, which is normally carried dorsally across the upper back and back of the neck when not being
nursed. Such females will facilitate nursing for the infant by raising their arm away from their body to allow a
rooting newborn to find the nipple easily, which is close to the armpit. Once the infant is in nursing position, the
female will appear to hold her upper arm close enough to the infant's head to block it from straying from the
nipple.

Poor maternal care or signs of rejection of an infant may not always be immediately apparent in situations in
which a female is found to be actually carrying a newborn infant but should be noticeable within two to three
hours of continuous observation.

Early indications of problems may include:


1) attempts by a female to dislodge an infant from her back by rubbing it against walls or substrates within the
cage;
2) pulling or holding the infant's head away from the breast during nursing attempts;
3) aggressive or defensive behaviors or obvious stress triggered by the approach of other group members; or
4) constant "fidgeting" with an infant.

If stress triggered by the presence or approaches of another group member seems to be the only factor affecting
the female's care of the infant, immediate removal of that group member is recommended to avoid the necessity
to handrear.

Infants should be removed for handrearing if poor maternal behaviors continue during continuous observations
on day one and no nursing has been seen.

An infant observed clinging low on a female's back, hindquarters, or carried ventrally for prolonged periods of
time is usually an indication of the infant's weakness due to lack of nursing or that the infant has other physical
problems. This situation requires immediate removal of the infant for evaluation and, most likely, handrearing.
Infants that have sustained bite wounds do not usually survive.

Twinning is a rare occurrence in Callimico (Altmann et al. 1988), with only six documented cases. Five of
these cases occurred at the Chicago Zoological Park, and in only two of these were both offspring born alive. In
one of these cases, a multiparous female appeared to be unable to handle the carrying and nursing of both
infants and one of the infants died on Day 3. In the second case, one of the infants was removed for handrearing
on Day 1 after the dam appeared to be experiencing similar difficulties. The occurrence of twinning in this
species should therefore be cause for concern to managers, even in cases in which the dam has previously
shown competent maternal skills. Removal of one of the infants for handrearing should be seriously considered
if observations suggest that the dam is having problems carrying or positioning the infants for nursing.

100
HANDREARING PROCEDURE

Eighteen callimico infants have been handreared at the Chicago Zoological Park using a protocol that has
evolved from one that was first developed at the Departments of Microbiology at Rush-Presbyterian St. Luke's
and University of Illinois Medical Centers in Chicago, Illinois (Wolfe et al. 1972). This protocol was first
successfully applied to callimico in 1978 (Beck et al. 1982). The handrearing process at the Chicago Zoological
Park has undergone many changes over the course of handrearing these infants and differs in certain aspects
from the protocol as described by Beck et al. (Sodaro et al. 1994).

INCUBATION AND THERMOREGULATION


If an infant is discovered abandoned, or is removed from the dam or other group members and appears to be
strong and warm to the touch, place in an incubator with the temperature set at between 89-90° F. If the infant
appears to be weak and is cold to the touch, the temperature of the incubator should be gradually increased to
89- 90° F over a period of several hours. This temperature range should be maintained for the infant through
Day 9 and decreased to 87° F on Day 10. The temperature should be decreased to 85° F on Day 14 and to 82° F
on Day 18.

Callimico have been found to be able to thermoregulate at ages ranging from 23 to 25 days and can then be
removed from incubators. Thereafter they should be placed in an interim cage within the enclosure of the group
to which the infant will be introduced. A supplemental heat lamp must be provided for warmth and the
temperature of the enclosure or room in which they are housed must be maintained at 78 to 80° F.

SURROGATES
Infants should be provided with a surrogate that approximates as closely as possible the size, shape, and color
of an adult animal. Ideally, a surrogate made from the preserved skin and fur of a callimico specimen would be
the best possible surrogate that could be provided, but if this is not possible, a small, black "stuffed animal"
made of soft artificial material can be used.

DIET AND FEEDING PROCEDURE


Nipples are made following a method developed by Dr. James Ogden (Ogden 1979). Formula is made from
60cc water, 1 tablespoon SMA (Wyeth Laboratories Inc.), and 1 teaspoon Sustagen (Mead Johnson & Co.)
(Beck et al. 1982).

Weak infants are first offered a 10% dextrose solution at a rate of 0.5cc every two hours. As the infant begins to
gain strength over the course of the first day, formula made with 10% dextrose solution instead of water should
be offered.

Strong, healthy infants are fed five times daily, with additional night feedings offered at two to three hour
intervals for the first eight to ten days. A schedule of five formula feedings daily should be continued through
Day 13, increasing the amount fed as the infant's demand increases. The initial amount fed should increase to
about 2cc per feeding at one week of age and to 3cc at two weeks of age.

Day 14: Increase number of feedings per day to six, offering Gerber Baby Cereal (Gerber Products Company)
at the second and the fourth feedings. The cereal is prepared by adding 1cc of formula to 1/4 teaspoon of dry
cereal. Mashed banana is added to the cereal on Day 18 and is gradually followed by other mashed fruits.

Day 25: Add a small amount of Zupreem Marmoset Diet (Premium Nutritional Products, Inc.) to the cereal.
Initial consumption of the science diet is usually poor but gradually improves as the infant becomes more
experienced with eating solids and approaches weaning.

Day 28: Decrease number of feedings per day to five, with the second and fourth being cereal feedings. Small
pieces of fruit, steamed sweet potato, and science diet are offered in addition to that mixed with the cereal.
Infants at this age typically consume between 5cc and 7cc of formula at each of their three formula feedings.

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Day 46: Decrease number of feedings to three, combining the first two and last two feedings such that formula
and cereal are fed simultaneously at these feedings. The midday feeding is formula. Infants at this age consume
between 8cc and 11cc of formula at each of the three feedings offered.

Day 70: the process of weaning the infant to the adult diet should begin by decreasing the amount of cereal
offered. This usually encourages the infant to begin to eat the fruits, steamed sweet potato, and science diet
more readily, although many infants at this age already do so.

Day 77: Discontinue cereal. Begin to gradually decrease the amount of formula offered per meal. Some infants
at this age may be consuming a maximum of 15cc of formula per feeding but many begin to show a preference
for solids before weaning has begun and will begin to refuse part of their formula ration. Infants should be
totally on the adult diet by Day 84.

BIRTH WEIGHTS AND WEIGHT GAIN


Only one of 18 infants that have been successfully handreared at the Chicago Zoological Park had a birth
weight of less than 53g. Thirteen infants with birth weights ranging from 37.5g to 50g died at ages ranging
from one to seven days despite handrearing efforts. Eleven of these weighed less than fifty grams. Two other
infants with weights of under 50g when handrearing attempts began at ages of four days and six days also died.
While infants in this weight range can be regarded as being of compromised and poor candidates for survival of
handrearing attempts, it is likely that a certain number of infants that are successfully reared by female
callimicos with good maternal skills fall within this weight range.

The majority of healthy handreared infants double their birth weight between weeks five and six, and triple
their birth weight at ages ranging from eight to ten weeks.

TABLE 1. BIRTH WEIGHTS AND WEEKLY WEIGHTS OF CALLIMICO HANDREARED AT CHICAGO


ZOOLOGICAL PARK
n=18 unless otherwise noted

Birth-weight range= 48-72.7g Mean= 58.7g


Males: n=8 Birth-weight range= 52.7-59g Mean= 57.47g
Females: n=10 Birth-weight range= 48-72.7g Mean= 59.69g

Weeks Of Age Range Mean


1 44-68g 59.24g
2 52-79.2g 65.71g
3 61-94g 77.18g
4 68-108.3g 90.13g
5 76-126g 105.31g (N=17)
6 94-145g 121.23g
7 96-153.6g 133.12g
8 118-177.5g 152.65g (N=16)
9 146-200.9g 171.63g (N=15)
10 160-219.3g 188.05g (N-14)

SOCIALIZATION PROBLEMS

Handreared callimico, like handreared marmosets and tamarins, frequently exhibit an array of socialization
problems, including imprinting on humans, poor parental skills and rejection of offspring, premature
peripheralization from foster groups, and incompatibility with conspecifics. The socialization process that
occurs through parental rearing of callimico infants within natal groups is a critical requirement for the social
and parental success of the individual upon reaching adulthood. After long periods of isolation from
conspecifics prior to reintroduction, most callimico infants do not recognize conspecifics as something to cling
to, or by which they might be carried. Adults in the groups to which they are reintroduced, whether the infants'
family or a foster family, seldom show solicitous parental behavior towards them.

102
It is therefore critical that all aspects of any handrearing endeavor focus on minimizing the social isolation from
conspecifics that often characterizes traditional "nursery" handrearing efforts, and promoting as close contact
between the infant and its family as is possible as early as possible.

REINTRODUCTION

While reintroduction to foster families rather than to natal groups has proven to work well for Saguinus oedipus
infants (Dronzek et al. 1986), nine callimico infants that were introduced to foster families at the Chicago
Zoological Park failed to become well integrated into these groups (Sodaro et al. 1994). Although they were
accepted and tolerated as group members while infants, all were harassed and peripheralized by one or both
foster parents at ages ranging from 3.5 to 13 months.

Contact between the infant and the other members of its family can be maximized from Day 1 by handrearing
the infant within the enclosure of the family. The following is a summary of the steps that can be taken to
accomplish this:

1. The incubator in which the infant is kept can be put inside of the family's enclosure. This allows extensive,
visual, auditory, and olfactory contact between the infant and the family from day one. The electrical cord
can be protected from possible chewing or biting by the group by a PVC pipe used as a conduit.
2. All feedings of the infant should take place in the groups' cage. Family members of three infants
handreared at the Chicago Zoological Park using this method seemed to maintain a high level of interest in
the infants and frequently directed protective or defensive behaviors at keepers who handled the infants.
This method also facilitated direct contact between the infants and group members as they crowded around
the infant. Keepers allowed infants and group members to touch and sniff each other during these feedings.
These three infants were provided with separate surrogates to which they were encouraged to transfer for
all feedings. The purpose of these surrogates was to establish a "bridge" that the infants eventually learned
to associate with food and which were used to lure them out of their interim cage into the vicinity of the
adults' food bowl. This, in turn, accelerated the process whereby the infants learned to locomote
independently as well as feed themselves from the families' bowl.
3. At the age of 35 days, infants should be removed from the interim cage during the day and allowed to have
direct contact with the group by attaching the surrogate to the top of the interim cage. A small branch
should be attached from the top of the interim cage to allow the infant a route to the food bowl or to return
to the inside of the interim cage.

If no negative interactions are observed between the infant and family members during two to three days of
observations of this situation, it is no longer necessary to return the infant to the interim cage at night.
Continued isolation of the infant in the interim cage at this stage would only serve as a further barrier to
socialization. If, and when, the infant begins to be carried by family members, the feeding surrogate can be used
to retrieve the infant for feedings. Once the infant has begun to sleep with family members, it can be regarded
as well-integrated into the family and the use of surrogates can be discontinued.

REFERENCES

Altmann, J., M. Warneke and J. Ramer. 1988. Twinning among Callimico goeldii. International Journal of
Primatology 9:165-168.
Beck, B. B., D. Anderson, J. Ogden, B. Rettberg, C. Brejla, R. Scola and M. Warneke. 1982. Breeding the
Goeldi's Monkey Callimico goeldii at Brookfield Zoo, Chicago. International Zoo Yearbook 22:106-114.
Dronzek, L., A. Savage, C. T. Snowden, C. S. Whaling and T. E. Zeigler. 1986. Technique for Handrearing and
Reintroducing Rejected Cotton-Top Tamarin Infants. Laboratory Animal Science 36:243-247.
Hoage, R. J. 1977. Parental care in Leontopithicus rosalia: sex and age differences in carrying behavior and the
role of prior experience. In: The Biology and Behavior of Callitrichidae, ed., D. Kleiman, pp. 293-305.
Washington, D.C.: Smithsonian Press.
Ogden, J. D. 1979. Hand-rearing Saguinus and Callithrix genera of marmosets. In: Nursery Care of Nonhuman
Primates, ed., G.C. Ruppenthal, pp. 313-319. New York: Plenum Press.

103
Price, E. C. 1992. Contributions to infant care in captive cotton-top tamarins Saguinus oedipus: the influence of
age, sex, and reproductive strategy. International Journal of Primates 13:2.
Sodaro, V., K. Pingry and K. Snyder. 1994. Changes in Handrearing Procedures for Callimico goeldii at
Brookfield Zoo. In: 1994 AZA Regional Conference Proceedings, pp. 404-407. Wheeling, WV: AZA.
Wolfe, L. G., J. D. Ogden, J. B. Deinhardt, L. Fisher and F. Deinhardt. 1972. Breeding and handrearing
marmosets for viral oncogenesis studies. In: Primate Breeding, ed. W.I.B. Beveridge, Basel: Karger.

104
PREVENTIVE MEDICINE
Jacqueline M. Zdziarski, D.V.M.

The best captive-animal management programs adopt multidisciplinary approaches. Management programs
that eliminate or minimize chronic stress through thoughtful enclosure design, behavioral enrichment,
population control, appropriate social groupings and breeding pairs, and balanced diets contribute to the
health and well being of the animals. Preventive health care is an essential part of any captive-management
program. A preventive medicine program includes:
 quarantine (physically separating new, incoming animals from the existing collection to prevent the
introduction and transmission of disease)
 routine examinations
 parasite detection and control
 immunizations
 tuberculin testing
 post-mortem examination
 balanced, high quality diet
 pest control program
To be successful, preventive medicine plans should be written, include education and training of all zoo
personnel responsible for carrying out the plan, and staff must be dedicated to carrying out the plan.

QUARANTINE

Quarantine prevents the introduction of disease into a stable collection, and identifies and prevents the
transmission of zoonotic diseases to zoo personnel or visitors. Zoonotic disease are those diseases that may
be transmitted from animals to man. Taxonomically, nonhuman primates are closely related to humans and
many diseases are transmissible between them, including parasites, bacterial agents, and viruses.
Transmission may occur via aerosol (coughing or sneezing), saliva (spitting), feces, or bodily fluids (blood,
urine, or wound exudates).

Exposure may occur while handling animals if caretakers are bitten, scratched, or if they come into contact
with bodily fluids. Humans may also be exposed while cleaning animal housing. Hoses often cause
infectious agents to become airborne where they may be inhaled or swallowed. To minimize the potential
for disease transmission, animals are held in a separate facility upon arrival until the health status of each
individual is determined.

Animals stressed by recent shipment are most likely to shed virus particles, bacterial agents, or intestinal
parasites. These pathogens may be latent or newly contracted during shipment. Since there is little control
over the animals' contacts during shipment in airports or dealers' trucks, adequate quarantine is necessary.
To prevent exposure to nonhuman primate-born disease of any type, zoo personnel must strictly adhere to
safety protocols. In all instances, animals held in quarantine should be accessible only to the personnel
providing routine maintenance and medical care. All other staff should not have access to these animals.

Employees working in nonhuman primate facilities should be required to wear protective clothing while
working with quarantined nonhuman primates. Protective clothing should prevent exposure to body fluids
and restrict their spread. When entering nonhuman primate quarantine areas, employees should wear long-
sleeved coveralls, boots, protective rubber gloves, and face protection. Face protection may consist of a
surgical mask and goggles, or, alternatively, a clear plastic face shield that covers the entire face.

Once duties in the quarantine rooms are completed, protective clothing should be removed and left in the
anteroom. Any biological samples (i.e., feces, blood) gathered for quarantine testing procedures should be
sealed in a container, double-bagged in plastic, and labeled "biohazard" before being removed from the

105
quarantine or treatment room. All cage debris, such as food, bedding, and excrement, should be double-
bagged in plastic and disposed of appropriately.

When the quarantine period ends, protective clothing should be decontaminated by chemical disinfecting
prior to machine washing, and the enclosure housing the animal should be disinfected with appropriate
agents.

Should a known exposure occur (e.g., bite wound, scratch, contamination with body fluid), the employee
should immediately report the incident. Immediate response may vary from written report of the incident to
immediate emergency medical care. A copy of the incident report should remain in the employee’s
permanent file.

QUARANTINE BASICS
1. The quarantine facility should be a separate facility, away from the collection. Ideally, the quarantine
facility should have its own dedicated quarantine staff. If staff must work elsewhere in the zoo,
caretakers should enter the quarantine area last so they are not servicing the animal collection after
coming into contact with the quarantined animals. Limit access to quarantine areas to necessary
personnel thoroughly trained in infection control.
2. Caretakers should wear protective clothing consisting of coveralls, rubber boots, gloves, face masks
and goggles, or face shields when servicing. Coveralls should be laundered when dirty and after the
animals are released from quarantine.
3. Clean animal caging daily. Use separate cleaning tools and food bowls for the quarantine area.
4. Institute adequate pest (vermin) control measures. Vermin serve as vectors for disease.
5. Perform complete physical examinations on all quarantined animals.
6. Establish a thorough and complete recordkeeping system. Record number of animals, source of
animals, date of shipment, and receipt into quarantine, TB test dates and results, history of health
problems, and diagnostic testing results.
7. Perform a complete post-mortem examination on any animal that dies in quarantine. Save
representative tissues in buffered 10% formalin and submit for histopathologic exam prior to releasing
other animals (housed in the same room) in quarantine.

OCCUPATIONAL HEALTH

Quarantine protects the health of not only the animal collection, but the veterinary staff, animal caretakers,
and the public. An ongoing, documented training program for the staff should be implemented to address
methods of husbandry and care, infectious disease hazards, and health precautions to prevent the spread of
infectious agents. Training should address protocols for reporting injury (bites, scratches) and unusual
illnesses. Good animal husbandry and management practices can reduce the risk of transmission of
zoonotic diseases.
1. Wear protective clothing when in direct contact with the animal or animal secretions (e.g., blood,
urine, feces, tissue infected or contaminated with microorganisms). Protective clothing includes
coveralls, lab coats, gowns, gloves, and face masks. Change protective clothing when it becomes
soiled. Soak the clothing in a chemical disinfectant after handling infectious material.
2. Strong personal hygiene practices are a must when working with nonhuman primates. Take care not to
touch the face, especially the mouth, nose, and eyes. Remember that inanimate objects, such as pens,
locks, and countertops, can harbor pathogens. Hand washing is considered one of the most important
preventive measures in reducing an individual’s risk of infection. Wash hands thoroughly after
handling an animal, an animal’s waste, soiled bedding and food, or tissues and diagnostic samples. Do
not eat, drink, or smoke in the animal areas. Use separate refrigerators to store animal food and human
food. Store animal bowls and utensils separately and do not use to prepare staff food.
3. Remove bedding, food, fecal matter, and other items in an animal’s enclosure before cleaning to
decrease the potential of aerosolizing infectious material and to improve the effectiveness of the
disinfectant agent. Wear protective clothing when cages are cleaned. Wear additional protective
devices, such as face shields, goggles, or respirators, when using high power hoses or steam cleaners.
4. Maintain an active pest control program.

106
5. Conduct a pre-employment physical examination on all employees and collect a baseline serum sample
at that time. The serum sample should be stored in an ultracold (-70oC) freezer.
6. Have employees report all bites and scratches to their supervisor and seek medical attention.
7. Employees with colds or cold sores should not work directly with nonhuman primates. If they must
work in the area, they should wear gloves and face masks. Employees with more serious illnesses
(diarrhea, fever, etc.) should seek medical attention and they should inform their physician that they
work with nonhuman primates.

PREVENTIVE PLAN

Perform complete physical examinations on New World primates routinely. Many zoos examine animals
annually; others perform routine exams every other year. I recommend regularly scheduling routine exams
rather than performing them opportunistically. A complete physical examination should include a
systematic evaluation of all body systems. Perform dental prophylaxis when needed. Collect a blood
sample for a complete blood count, serum chemistry profile, and freeze extra serum for future testing.

107
RESTRAINT AND ANESTHESIA OF NEW WORLD PRIMATES
Suzan Murray, D.V.M.

MANUAL RESTRAINT TECHNIQUES

Techniques for restraining and anesthetizing New World primates vary from species to species and depend
directly upon the animal’s size, temperament, and environment. In general, animals weighing less than 5 kg
can be restrained safely by one person, while larger animals often require either a second person or
chemical restraint.

The smallest New World monkeys, such as pygmy marmosets, Goeldi’s monkeys, and tamarins, can easily
be caught within a net and hand restrained for minor procedures, such as physical examination, blood
sample collection, vaccination, and tuberculin testing. Once the animal is within the net, the handler must
gain control of the head. The second hand can either control the hind legs or slip under the net and replace
the first hand. The free hand should then grasp and extend the rear legs. During this and all procedures,
handlers must remember that these animals are extremely dexterous and prone to escape. Handlers should
always wear leather gloves to prevent potential bite wounds. Remember: the teeth of primates can penetrate
the leather gloves.

Safely handling larger New World primates, such as howler and spider monkeys, requires chemical
restraint. If manual restraint is used, the monkey’s forearms should be grasped above the level of the
elbows and held behind the animal’s back. The rear legs and tail should then be extended by the second
hand.

CHEMICAL RESTRAINT

INJECTIONS
The type and route of administration of injectable anesthetics depends largely upon the animal’s size,
temperament, and immediate surroundings. The majority of small New World primates in captivity can
easily be restrained within a net and hand injected with an anesthetic. Simple procedures such as physical
examinations, tuberculin testing, and blood sample collection can be accomplished with intramuscular
ketamine hydrochloride (Fort Dodge Laboratories, Fort Dodge, Iowa) at 5-10 mg/kg. Ketamine is the drug
of choice due to its relatively quick onset of action, wide margin of safety, lack of respiratory and
cardiovascular depression, and fairly rapid recovery. For more prolonged procedures, supplemental
anesthesia may be achieved with additional ketamine, either intramuscularly or intravenously or via an
inhalation anesthetic agent. Although additional ketamine can provide adequate restraint, it is advisable to
use an inhalation agent for anesthetic maintenance.

Many veterinarians have also used Telazol (A. H. Robins, Richmond, Virginia) for short procedures in
New World primates. Prolonged recovery times and profuse salivation often accompany Telazol
administration, making this drug a less than ideal choice. When darting and/or in field situations where a
small injection volume and a short induction period is required, benefits of Telazol often outweigh these
side effects. Initial dosages of 3-4 mg/kg provides adequate restraint and muscle relaxation, while atropine
at a dose of 0.02-0.04 mg/kg IM can control the salivation. Although Telazol has a wide margin of safety,
and dosages of up to 30 mg/kg have been reported in some field studies, such high doses are invariably
accompanied by prolonged recovery times.

INHALATION ANESTHETICS
Fortunately, due to the relatively small size of most New World primates, inhalation anesthetics can be
used not only to maintain anesthesia, but to induce it as well. Small New World primates can be manually
restrained and induced using a facemask. Although both isoflurane (Aeranne, manufactured for Fort Dodge
Animal Health, Fort Dodge, IA by Ohmeda Caribe, Inc., Guayama, PR) and halothane (Fort Dodge Animal

108
Health, Fort Dodge, IA) have been used with great success as an anesthetic agent in many species,
isoflurane is generally preferred due to short recovery periods and a wide margin of safety. Gas anesthetics
may be supplied via an induction chamber, facemask, or endotracheal tube. The route of administration
depends largely upon the size of the animal and the length of the procedure. In general, all applicable sizes
of endotracheal tubes should be on hand for anesthetic emergencies.

New World primates are relatively easy to intubate. The animal can be placed in dorsal, ventral, or lateral
recumbency for intubation. The smaller the size of the animal (such as pygmy marmosets), the more
difficult the intubation procedure. With patience, practice, and small tools, it is possible to intubate most
animals. Required tools include a form of illumination (head lamp, laryngoscope, laparoscope, or assistant
with a light source) to identify the glottis; a moist cotton-tipped applicator to apply sight downward
pressure and partially extrude the tongue exposing the glottis; and various sizes of endotracheal tubes. If
small-gauge endotracheal tubes (size 2) are not readily available or do not fit, other small gauge tubing
such as intravenous catheters, rubber feeding catheters or shortened tom-cat catheters may be used. If
“homemade” endotracheal tubes are employed, take care to dull any rough edges that could damage the
oropharynx or trachea. Avoid applying a local anesthetic, such as lidocaine or cetacaine, on the glottis;
there is the potential for dosing and adverse side effects.

ANESTHETIC MONITORING

THERMOREGULATION
The loss of heat during anesthetic procedures is well documented and small animals are at a greater risk
than larger animals. Closely monitor body temperature and hydration status during the entire procedure.
Maintain all animals on a heated water blanket and, when possible, use a towel to cover the animal to
reduce exposure to the ambient environmental temperature. Exam gloves filled with warm water can be
placed alongside the animal to further retard heat loss. Alcohol and sterile preparation solutions should be
used judiciously to maximize antibacterial properties and minimize heat loss. Monitor core temperature
continuously to assess the efficacy of the thermoregulation techniques employed. When possible, place
intravenous catheters to help maintain adequate hydration status.

CATHETERIZATION TECHNIQUES
The femoral, jugular, saphenous, and antebrachial veins are all available for use in primates. The vessel
location is dependent upon the size of the animal, the length of time that the catheter will be left in place
and the status of the animal (moribund vs. alert and responsive).
 The jugular vein is located in the anterolateral aspect of the neck. The accessible portion of this vessel
is short, making it difficult to catheterize.
 The femoral vein lies close to the surface, parallel and medial to the femoral artery coursing distally
through the femoral triangle. This is a good location for central venous catheter placement in moribund
animals. Take care not to catheterize the femoral artery. If this occurs, the catheter should be removed
and digital pressure should be applied for approximately five minutes to prevent hematoma formation.
 The antebrachial veins are difficult to locate in smaller primates but often well developed in larger
animals. They course along the anterior surface of the antebrachium and along the medial elbow. If
prominent, these are ideal veins to catheterize for fluid administration.
 The lateral saphenous vein is located superficially on the posterior leg coursing along the flexor
surface of the tarsus caudally and proximally over the tibia.

109
HEMATOLOGY AND CLINICAL CHEMISTRIES
Noha Abou-Madi, D.V.M.

NORMAL VALUES

Normal values for New World primate hematology and clinical chemistries are summarized in the
following tables. Most of the information presented originates from data generated by ISIS. Table 1
summarizes the hematological values of members of the Callitrichidae family including the following
genera: Callithrix, Cebuella, Saguinus, Leontopithecus, and Callimico. Table 2 presents the hematological
values of members of the Cebidae family including the following genus: Aotus, Callicebus, Saimiri,
Pithecia, Cacajao, Cebus, Alouatta, Lagothrix, and Ateles. Tables 3 and 4 compile the data from clinical
chemistry values of the Callitrichidae and the Cebidae families respectively.

The blood values were not separated by sex or age. ISIS assumes normal status. The results appear
as mean values ± standard deviation, with the number of samples analyzed in parenthesis. Most of these
samples have been collected while the animals were under general anesthesia.

METHODS TO COLLECT AND PRESERVE BLOOD

Blood collection sites in New World primates include the femoral vein in the femoral triangle, the cubital
vein on the medial side of the elbow, the cephalic vein along the anterior surface of the antebrachium, and
the saphenous vein on the posterior aspect of the lower hind limb. In some species, the jugular vein is
accessible. Blood collection usually requires physical/manual restraint or chemical immobilization. Some
individuals operantly conditioned for medical procedures present their arm and will tolerate venipuncture
without restraint.

Depending on the size of the animal, a greater volume of blood should be collected than that required for
routine testing. This will allow banking of serum for future retrospective investigations. The samples
should be alliquoted and frozen (at -4° C or -70°C). A reliable identification system is necessary for each
retrieval of the samples. Blood smears should also be stained, fixed and stored for future references.

110
TABLE 1. HEMATOLOGY—CALLITRICHIDAE (MEAN ± SD (N))
Callithrix Callithrix Callithrix argentata Callithrix geoffroyi
jacchus pygmaea
Common Pygmy Marmoset Black-tailed White-fronted
Marmoset Marmoset Marmoset
3
WBC 10 /UL 6.1 ± 2.2 (30) 9.6 ± 8.5 (48) 8.2 ± 2.3 (4) 8.08 ± 3.6 (8)
6
RBC 10 /UL 5.6 ± 0.78 (25) 6.5 ± 1.2 (42) 6.1 ± 1.1 (2) 6.7 ± 0.89 (5)
HGB gm/dl 15.0 ± 1.4 (40) 13.6 ± 1.6 (19) 15.5 ± 1.2 (8) 16.7 ± 1.0 (4)
HCT % 44.6 ± 7.1 (45) 42.5 ± 4.9 (46) 46.4 ± 7.1 (11) 50.8 ± 3.8 (8)
MCH mg/dl 25.8 ± 2.7 (24) 66.8 ± 12.2 (42) 24.8 ± 0.4 (2) 23.6 ± 2.6 (3)
MCHC uug 34.2 ± 4.5 (39) 32.3 ± 2.2 (19) 34.1 ± 1.8 (8) 33.2 ± 3.6 (4)
MCV fl 74.3 ± 10.9 (24) 66.8 ± 12.2 (42) 74.3 ± 1.1 (2) 74.2 ± 8.5 (5)
SEGS 103/UL 3.2 ± 1.5 (24) 4.6 ± 3.7 (46) 3.3 ± 1.3 (3) 5.1 ± 2.1 (6)
3
BANDS 10 /UL 0.17 ± 0.08 (5) 0.26 ± 0.41 (7) --- ---
LYMPHS 3.0 ± 1.6 (24) 4.6 ± 4.7 (46) 4.3 ± 1.03 (3) 3.5 ± 4.1 (6)
103/UL
MONOS 0.25 ± 0.18 (15) 0.32 ± 0.47 (40) 0.47 ± 0.63 (3) 0.24 ± 0.12 (6)
103/UL
EOS 103/UL 0.23 ± 0.14 (15) 0.15 ± 0.19 (27) 0.20 ± 0.13 (2) 0.075 ± 0.015 (2)
BASOS 103/UL 0.16 ± 0.15 (7) 0.15 ± 0.13 (25) --- 0.085 ± 0.0 (1)
NRBC /100wbc 3.0 ± 2.0 (13) 2.0 ± 1.0 (22) 2.0 ± 0 (1) 18.0 ± 28.0 (3)
platelet cnt 609 ± 200 (6) --- --- ---
103/UL

TABLE 1 CONTINUED. HEMATOLOGY—CALLITRICHIDAE (MEAN ± SD (N))


Saguinus Saguinus Saguinus mystax Saguinus fuscicollis
oedipus imperator
Cotton-top Emperor Moustached Saddle-back
Tamarin Tamarin Tamarin Tamarin
WBC 103/UL 11.2 ± 5.2 (95) 9.5 ± 3.7 (54) 12.3 ± 2.8 (23) 8.7 ± 4.06 (12)
RBC 106/UL 6.3 ± 0.61 (76) 6.4 ± 0.90 (52) 6.06 ± 0.65 (10) 5.39 ± 1.02 (15)
HGB gm/dl 15.9 ± 1.7 (82) 14.1 ± 1.6 (47) 14.3 ± 1.9 (27) 14.0 ± 2.5 (20)
HCT % 47.9 ± 5.0 (99) 45.5 ± 5.6 (53) 48.2 ± 6.5 (36) 44.4 ± 6.6 (22)
MCH mg/dl 25.4 ± 1.5 (71) 22.6 ± 2.4 (46) 24.2 ± 0.7 (5) 26.4 ± 3.3 (15)
MCHC uug 33.1 ± 2.3 (81) 31.3 ± 1.9 (47) 30.1 ± 2.6 (27) 33.1 ± 3.9 (19)
MCV fl 76.3 ± 5.4 (74) 71.6 ± 8.0 (52) 78.2 ± 5.7 (10) 78.9 ± 7.6 (14)
SEGS 103/UL 7.03 ± 4.5 (90) 5.2 ± 2.4 (54) 5.1 ± 1.8 (17) 8.2 ± 4.5 (5)
BANDS 103/UL 0.33 ± 0.50 (20) 0.27 ± 0.34 (5) 0.08 ± 0.01 (2) ---
LYMPHS 103/UL 3.3 ± 1.7 (90) 3.6 ± 2.4 (54) 6.4 ± 2.5 (17) 1.9 ± 0.92 (5)
MONOS 103/UL 0.54 ± 0.44 (80) 0.51 ± 0.41 (49) 0.85 ± 0.52 (16) 0.30 ± 0.12 (3)
EOS 103/UL 0.21 ± 0.17 (47) 0.23 ± 0.16 (24) 0.39 ± 0.26 (12) 0.28 ± 0.17 (3)
BASOS 103/UL 0.10 ± 0.06 (24) 0.16 ± 0.10 (24) 0.22 ± 0.20 (5) 0.18 ± 0.08 (2)
NRBC /100wbc 1.0 ± 1.0 (22) 2.0 ± 4.0 (8) 3.0 ± 2.0 (15) 9.0 ± 19 (9)

Platelet cnt 103/UL 361 ± 74 (14) 626 ± 224 (5) 840 ± 142 (5) 546 ± 113 (3)
RETICS % --- 1 7.7± 0.0 (1) --- ---

111
TABLE 1 CONTINUED. HEMATOLOGY—CALLITRICHIDAE (MEAN ± SD (N))
Saguinus Saguinus labiatus Saguinus midas Saguinus nigricollis
geoffroyi
Geoffroy’s Red-bellied White- Red-handed Black-and-white
Tamarin lipped Tamarin Tamarin
3
WBC 10 /UL 13.5 ± 5.9 (14) 13.4 ± 4.4 (3) 15.6 ± 6.7 (48) 17.2 (1)
6
RBC 10 /UL 6.2 ± 0.73 (11) 5.8 ± 1.8 (3) 6.3 ± 0.56 (15) 6.0 (1)
HGB gm/dl 15.0 ± 1.2 (19) 14.1 ± 4.0 (3) 16. 1 ± 1.9 (47) 14.1 (1)
HCT % 46.3 ± 3.8 (20) 39.3 ± 11.7 (3) 49.5 ± 5.5 (61) 42.0 (1)
MCH mg/dl 24.6 ± 1.3 (9) 24.4 ± 1.5 (3) 26.5 ± 1.2 (15) 23.5 (1)
MCHC uug 32.0 ± 1.5 (18) 36.1 ± 0.80 (3) 32.9 ± 2.5 (46) 33.6 (1)
MCV fl 71.3 ± 9.8 (11) 67.5 ± 3.6 (3) 80.1 ± 3.6 (15) 70.0 (1)
SEGS 103/UL 8.5 ± 5.1 (14) 7.2 ± 3.2 (3) 8.7 ± 4.7 (37) 11.7 (1)
BANDS 0.11 ± 0.0 (1) 0.21 ± 0.23 (3) 1.05 ± 1.8 (11) ---
103/UL
LYMPHS 4.1 ± 1.3 (14) 5.2 ± 1.9 (3) 5.2 ± 3.2 (39) 4.3 (1)
103/UL
MONOS 0.73 ± 0.82 (14) 0.72 ± 0.21 (3) 1.1 ± 0.82 (35) 0.86 (1)
103/UL
EOS 103/UL 0.12 ± 0.10 (4) 0.0 ± 0.0 (1) 0.63 ± 0.67 (27) 0.344 (1)
3
BASOS 10 /UL 0. 11 ± 0.09 (5) 0.08 ± 0.0 (1) 0.18 ± 0.11 (12) ---
NRBC /100wbc 1.0 ± 1.0 (5) --- 7.0 ± 10.0 (15) ---
platelet cnt 386 ± 0 (1) --- 397 ± 132 (5) ---
103/UL
RETICS % --- --- 6.4 ± 3.5 (3) ---

112
TABLE 1 CONTINUED. HEMATOLOGY—CALLITRICHIDAE (MEAN ± SD (N))
Leontopithecus rosalia Callimico goeldi
Golden Tamarin Goeldi’s Monkey
WBC 103/UL 8.1 ± 3.7 (378) 6.2 ± 2.8 (262)
RBC 106/UL 6.2 ± 0.85 (305) 6.6 ± 0.71 (250)
HGB gm/dl 15.3 ± 1.9 (343) 14.3 ± 1.7 (261)
HCT % 45.6 ± 5.1 (375) 44.1 ± 5.0 (270)
MCH mg/dl 24.8 ± 2.8 (296) 21.5 ± 1.8 (250)
MCHC uug 33.7 ± 2.4 (323) 32.5 ± 2.3 (261)
MCV fl 74.0 ± 9.1 (302) 66.0 ± 5.2 (250)
SEGS 103/UL 5.3 ± 3.1 (338) 3.3 ± 2.09 (257)
BANDS 103/UL 0.14 ± 0.17 (99) 0.12 ± 0.11 (41)
LYMPHS 103/UL 2.4 ± 1.5 (339) 2.5 ± 1.5 (257)
MONOS 103/UL 0.30 ± 0.27 (272) 0.18 ± 0.15 (223)
EOS 103/UL 0.29 ± 0.30 (231) 0.16 ± 0.17 (154)
BASOS 103/UL 0.16 ± 0.16 (80) 0.04 ± 0.04 (15)
NRBC /100wbc 2.0 ± 2.0 (51) 2.0 ± 3.0 (40)
platelet cnt 103/UL 502 ± 165 (113) 8 72 ± 233 (108)
RETICS % --- 0.0 ± 0.0 (5)

113
TABLE 2. HEMATOLOGY—CEBIDAE (MEAN ± SD (N))
Saimiri sciureus Callicebus moloch Callicebus Cacajao
donacophilus rubicundus
Common Orabussu Titi Reed Titi Red Uakari
Squirrel Monkey
WBC 103/UL 8.6 ± 4.3 (131) 8.6 ± 4.9 ( 9) 8.54 ± 3.1 (55) 6.03 ± 3.3 (3)
RBC 106/UL 6.9 ± 0.82 (120) 6.1 ± 0.94 (9) 6.1 ± 1.09 (55) ---
HGB gm/dl 13.3 ± 1.6 (122) 15.3 ± 2.1 (9) 15.7 ± 2.3 (47) ---
HCT % 40.9 ± 4.5 (135) 47.9 ± 5.4 (9) 45.5 ± 6.5 (55) 51.0 ± 5.6 (3)
MCH mg/dl 19.1 ± 1.5 (115) 25.1 ± 1.1 (9) 26.7 ± 1.9 (47) ---
MCHC uug 32.7 ± 2.6 (121) 31.9 ± 2.7 (9) 34.8 ± 3.5 (47) ---
MCV fl 59.1 ± 5.5 (119) 79.2 ± 7.7 (9) 75.3 ± 8.8 (55) ---
SEGS 103/UL 4.4 ± 3.4 (114) 4.8 ± 3.9 (9) 5.2 ± 2.8 (55) 3.4 ± 2.05 (3)
BANDS 103/UL 0.07 ± 0.09 (20) 78 ± 17.4 (5) 7.4 ± 20.9 (16) ---
LYMPHS 103/UL 3.3 ± 2.2 (114) 3.4 ± 1.02 (9) 2.8 ± 1.3 (55) 2.4 ± 1.6 (3)
MONOS 103/UL 0.4 ± 0.46 (98) 0.21± 0.13 (8) 0.33 ± 0.23 (50) 0.13 ± 0.09 (3)
EOS 103/UL 0.25 ± 0.40 (76) 0.14 ± 0.16 (5) 0.22 ± 0.28 (33) ---
BASOS 103/UL 0.04 ± 0.05 (25) 0.0 ± 0.0 (4) 0.052 ± 0.072 (9) ---
NRBC /100wbc 0.0 ± 0.0 (16) 0.0 ± 0.0 (3) 1 ± 1 (11) ---
Platelet cnt 393 ± 89 (22) --- 499 ± 177 (3) ---
103/UL
RETICS % 0.0 ± 0.0 (1) --- --- ---

TABLE 2 CONTINUED. HEMATOLOGY—CEBIDAE (MEAN ± SD (N))


Ateles belzebuth Ateles fusciceps Ateles geoffroyi Ateles paniscus
Long-haired Brown-headed Black-handed Black Spider
Spider Monkey Spider Monkey Spider Monkey Monkey
WBC 103/UL 11.0 ± 2.2 (6) 17.8 ± 7.3 (49) 13.4 ± 7.2 (258) 17.5 ± 5.7 (13)
RBC 106/UL 5.3 ± 0.5 (7) 5.5 ± 0.8 (44) 5.4 ± 0.58 (200) 6.03 ± 1.1 (5)
HGB gm/dl 13.8 ± 1.1 (7) 14.3 ± 2.0 (45) 14.1 ± 3.4 (199) 15.8 ± 1.4 (6)
HCT % 41.3 ± 3.2 (7) 43.5 ± 6.4 (47) 42.6 ± 5.1 (254) 45.3 ± 7.9 (16)
MCH mg/dl 25.8 ± 0.7 (7) 26.0 ± 1.9 (44) 25.7 ± 1.7 (187) 24.8 ± 1.2 (4)
MCHC uug 33.3 ± 0.7 (7) 33.3 ± 1.3 (44) 33.7 ± 6.0 (195) 31.5 ± 1.4 (6)
MCV fl 77.4 ± 2.6 (7) 78.0 ± 5.9 (44) 76.9 ± 4.9 (190) 82.4 ± 10.4 (5)
SEGS 103/UL 7.6 ± 1.7 (6) 13.2 ± 6.2 (37) 8.8 ± 6.6 (223) 12.9 ± 6.2 (12)
BANDS 103/UL 0.39 ± 0.03 (6) 0.79 ±1.3 (33) 0.63 ± 1.1 (68) 0.63 ± 0.62 (9)
LYMPHS 103/UL 2.1 ± 0.45 (6) 2.9 ± 0.3 (37) 3.3 ± 1.9 (222) 3.07 ± 1.4 (12)
MONOS 103/UL 0.38 ± 0.19 (6) 0.92 ± 0.5 (36) 0.37 ± 0.35 (183) 0.52 ± 0.19 (11)
EOS 103/UL 0.43 ± 0.44 (6) 0.29 ± 0.32 (35) 0.27 ± 0.25 (148) 0.23 ± 0.06 (6)
BASOS 103/UL 0.11 ± 0.05 (5) 0.06 ± 0.1 (31) 0.08 ± 0.13 (60) 0.25 ± 0.0 (1)
NRBC /100wbc --- --- --- 4.0 ± 0 (1)
Platelet cnt 206 ± 64 (6) 385 ± 140 (18) 332 ± 91 (70) 240 ± 0 (1)
103/UL
RETICS % --- --- 0.0 ± 0.0 (5) ---

114
TABLE 2 CONTINUED. HEMATOLOGY—CEBIDAE (MEAN ± SD (N))
Aotus trivirgatus Alouatta caraya Alouatta palliata Lagothrix
agothricha
Douroucouli Black Howler Mantled Howler Wooly Monkey
Monkey Monkey
WBC 103/UL 12.0 ± 7.6 (90) 14.5 ± 5.2 (165) 8.7 ± 0.3 (3) 13.8 ± 6.03 (27)
RBC 106/UL 6.2 ± 1.1 (71) 4.76 ± 0.66 (135) --- 5.08 ± 0.79 (27)
HGB gm/dl 15.5 ± 1.7 (65) 14.2 ± 1.9 (150) --- 12.9 ± 1.3 (27)
HCT % 46.8 ± 6.2 (91) 43.0 ± 5.8 (164) 47.0 ± 6.1 (3) 39.1 ± 4.8 (32)
MCH mg/dl 27.1 ± 2.3 (55) 30.0 ± 1.6 (131) --- 25.7 ± 2.6 (27)
MCHC uug 34.0 ± 1.8 (65) 33.2 ± 1.6 (143) --- 33.8 ± 2.9 (27)
MCV fl 76.3 ± 10.9 (69) 89.8 ± 6.0 (134) --- 76.3 ± 7.8 (27)
SEGS 103/UL 4.3 ± 4.2 (80) 7.9 ± 4.7 (145) 4.3 ± 1.5 (3) 9.4 ± 5.0 (25)
BANDS 103/UL 0.1 ± 0.29 (17) 0.27 ± 0.25 (25) 0.09 ± 0.0 (1) 0.51 ± 0.52 (8)
LYMPHS 103/UL 5.7 ± 3.9 (80) 5.7 ± 2.4 (145) 3.4 ± 0.8 (3) 2.6 ± 1.1 (25)
MONOS 103/UL 0.3 ± 0.2 (66) 0.57 ± 0.39 (101) 0.52 ± 0.31 (3) 0.42 ± 0.37 (22)
EOS 103/UL 2.1 ± 2.4 (66) 0.57 ± 0.53 (121) 0.68 ± 0.2 (2) 0.55 ± 0.70 (20)
BASOS 103/UL 0.2 ± 0.1 (32) 0.17 ± 0.12 (36) --- 0.11 ± 0.01 (2)
NRBC /100wbc 3 ± 4 (25) 1 ± 2 (16) --- 1.0 ± 0.0 (1)
platelet cnt 103/UL 350 ± 99 (29) 347 ± 137 (90) --- ---
RETICS % --- 1.7 ± 0.6 (8) --- ---

115
TABLE 3. CLINICAL CHEMISTRIES—CALLITRICHIDAE
Callithrix jacchus Callithrix Callithrix Callithrix
pygmaea argentata geoffroyi
Common Pygmy Black-tailed White-fronted
Marmoset Marmoset Marmoset Marmoset
Glucose mg/dl 177 ± 65 (16) 161 ± 78 (43) 220 ± 85 (3) 243 ± 179 (4)
BUN mg/dl 19 ± 5 (15) 18 ± 8 (42) 11 ± 6 (3) 16 ± 1 (4)
Creatinine mg/dl 0.7 ± 0.2 (10) 0.5 ± 0.2 (28) --- 0.6 ± 0.2 (4)
Uric acid mg/dl 0.5 ± 0.2 (10) 3.6 ± 6.8 (11) --- 0.3 ± 0.4 (2)
Calcium mg/dl 9.5 ± 1.1 (17) 10.0 ± 2.0 (35) 9.0 ± 0.9 (6) 10.2 ± 0.4 (5)
Phosphorus mg/dl 5.3 ± 1.9 (15) 7.2 ± 4.3 (18) 7.2 ± 2.2 (6) 5.0 ± 0.5 (4)
Sodium mEq/L 147 ± 8 (12) 156 ± 6 (13) 153 ± 1 (2) 164 ± 0 (2)
Potassium mEq/L 4.9 ± 2.6 (12) 3.8 ± 1.5 (13) 3.4 ± 0.3 (2) 2.9 ± 1.7 (2)
Chloride mEq/L 103 ± 11 (10) 116 ± 8 (2) 96 ± 6 (2) 115 ± 1 (2)
Iron mcg/dl 129 ± 0 (1) --- --- 55± 51 (2)
Bicarbonate mMol/L --- 5.8 ± 1.0 (4) --- ---
Cholesterol mg/dl 176 ± 73 (7) 216 ± 95 (23) 88 ± 28 (2) 106 ± 81 (4)
Triglycerides mg/dl 160 ± 43 (2) 129 ± 43 (10) --- 290 ± 260 (2)
Total proteins gm/dl 6.8 ± 1.0 (17) 6.1 ± 0.9 (33) 7.5 ± 0.6 (3) 7.7 ± 0.7 (4)
Albumin gm/dl 5.1 ± 0.6 (4) 4.2 ± 0.8 (13) --- ---
Globulin gm/dl 1.7 ± 0.5 (4) 2.1 ± 0.7 (13) --- ---
AST (SGOT) IU/L 112 ± 112 (11) 64 ± 51 (35) 7 ± 1 (2) 109 ± 32 (3)
ALT (SGPT) IU/L 13 ± 24 (14) 15 ± 23 (30) 0 ± 0 (2) 14 ± 10 (4)
Tot. Bilirubin mg/dl 0.2 ± 0.3 (8) 0.3 ± 0.3 (13) --- 0.1 ± 0.1 (2)
Dir. Bilirubin mg/dl 0.0 ± 0.0 (1) 0.0 ± 0.0 (5) --- ---
Indir. Bilirubin mg/dl 0.1 ± 0.0 (1) 0.3 ± 0.3 (5) --- ---
Alk Phosp. IU/L 125 ± 64 (13) 322 ± 260 (31) 211 ± 29 (2) 97 ± 19 (4)
LDH IU/L 551 ± 429 (7) 354 ± 270 (13) 312 ± 8 (2) 414 ± 302 (3)
CPK IU/L 543 ± 0 (1) 768 ± 1055 (14) --- 180 ± 50 (2)
CO2 mMol/L --- 14.8 ± 8.3 (4) --- ---
GGT IU/L --- 5 ± 3 (7) --- ---
Lipase U/L --- 192 ± 188 (2) --- ---

116
TABLE 3 CONTINUED. CLINICAL CHEMISTRIES—CALLITRICHIDAE
Saguinus oedipus Saguinus Saguinus mystax Saguinus
imperator fuscicollis
Cotton-top Emperor Moustached Saddle-back
Tamarin Tamarin Tamarin Tamarin
Glucose mg/dl 179 ± 82 (62) 151 ± 58 (50) 117 ± 63 (18) 173 ± 66 (6)
BUN mg/dl 15 ± 8 (69) 14 ± 4 (49) 13 ± 5 (19) 14 ± 5 (4)
Creatinine mg/dl 0.7 ± 0.3 (60) 0.6 ± 0.2 (50) 0.7 ± 0.4 (3) 0.5 ± 0.2 (4)
Uric acid mg/dl 1.0 ± 0.7 (25) 0.2 ± 0.2 (17) --- 0.8 ± 0.1 (2)
Calcium mg/dl 8.9 ± 0.9 (67) 9.2 ± 0.8 (49) 8.7 ± 1.2 (24) 8.9 ± 0.9 (8)
Phosphorus mg/dl 4.8 ± 1.5 (61) 5.5 ± 1.8 (47) 8.0 ± 3.0 (20) 5.2 ± 1.1 (7)
Sodium mEq/L 150 ± 8 (52) 156 ± 8 (40) 154 ± 7 (13) 154 ± 1 (4)
Potassium mEq/L 4.0 ± 0.8 (55) 3.9 ± 0.9 (40) 4.9 ± 1.6 (13) 3.4 ± 0.7 (4)
Chloride mEq/L 104 ± 8 (51) 112 ± 5 (41) 104 ± 8 (13) 110 ± 1 (4)
Iron mcg/dl 127 ± 73 (5) --- --- ---
Magnesium mg/dl 2.4 ± 0 (1) --- --- ---
Bicarbonate mMol/L 20.5 ± 7.0 (4) 16.8 ± 5.4 (15) --- ---
Cholesterol mg/dl 121 ± 42 (60) 106 ± 45 (50) 106 ± 79 (13) 65 ± 12 (3)
Triglycerides mg/dl 69 ± 32 (30) 103 ± 71 (25) --- 80 ± 0 (1)
Total proteins gm/dl 6.6 ± 0.7 (64) 6.3 ± 0.7 (50) 6.5 ± 0.7 (15) 7.5 ± 1.0 (50
Albumin gm/dl 3.8 ± 0.5 (49) 3.5 ± 0.5 (43) 3.5 ± 1.0 (2) 4.2 ± 0.2 (2)
Globulin gm/dl 2.8 ± 0.5 (49) 2.8 ± 0.5 (43) 2.3 ± 1.3 (2) 2.5 ± 0.1 (2)
AST (SGOT) IU/L 157 ± 56 (57) 156 ± 69 (48) 56 ± 85 (14) 491 ± 892 (5)
ALT (SGPT) IU/L 38 ± 41 (63) 18 ± 15 (45) 7 ± 14 (15) 26 ± 32 (4)
Tot. Bilirubin mg/dl 0.2 ± 0.2 (58) 0.4 ± 0.3 (46) 0.1 ± 0.1 (6) 0.3 ± 0.4 (2)
Dir. Bilirubin mg/dl 0.0 ± 0.1 (13) 0.2 ± 0.2 (2) --- ---
Indir. Bilirubin mg/dl 0.2 ± 0.1 (12) 0.2 ± 0.1 (2) --- ---
Amylase SU 575 ± 400 (23) 1202 ± 354 (29) 496 ± 0 (1) ---
Alk Phosp. IU/L 184 ± 110 (57) 179 ± 119 (48) 358 ± 341 (14) 129 ± 68 (4)
LDH IU/L 460 ± 319 (32) 290 ± 92 (19) 594 ± 326 (13) 390 ± 226 (3)
CPK IU/L 645 ± 706 (26) 766 ± 574 (18) --- ---
CO2 mMol/L 18.1 ± 8.3 (26) 17.8 ± 3.9 (6) 24 ± 0 (1) 11.7 ± 3.5 (2)
GGT IU/L 21 ± 21 (26) 8 ± 5 (27) --- ---
Lipase U/L 40 ± 16 (9) 342 ± 609 (5) --- ---
Cortisol ug/dl 570 ± 0 (2) --- --- ---

117
TABLE 3 CONTINUED. CLINICAL CHEMISTRIES—CALLITRICHIDAE
Saguinus geoffroyi Saguinus labiatus Saguinus midas

Geoffroy’s Red-bellied Red-handed


Tamarin Tamarin Tamarin
Glucose mg/dl 199 ± 65 (9) 281 ± 47 (2) 186 ± 69 (29)
BUN mg/dl 15 ± 6 (9) 14 ± 2 (2) 15 ± 6 (25)
Creatinine mg/dl 0.7 ± 0.1 (8) 0.5 ± 0.0 (2) 0.6 ± 0.3 (18)
Uric acid mg/dl 0.3 ± 0.2 (4) --- 4.9 ± 0.0 (1)
Calcium mg/dl 8.9 ± 1.2 (11) 9.4 ± 0.3 (2) 7.7 ± 0.9 (38)
Phosphorus mg/dl 6.3 ± 3.1 (10) 2.5 ± 1.0 (2) 6.8 ± 2.5 (33)
Sodium mEq/L 149 ± 7 (6) --- 153 ± 4 (17)
Potassium mEq/L 4.3 ± 0.9 (6) --- 4.2 ± 1.7 (16)
Chloride mEq/L 103 ± 10 (6) --- 109 ± 6 (15)
Iron mcg/dl 136 ± 6 (2) --- ---
Bicarbonate mMol/L 18.5 ± 2.1 (2) --- ---
Cholesterol mg/dl 96 ± 40 (6) --- 136 ± 98 (14)
Triglycerides mg/dl 127 ± 31 (4) --- 73 ± 0 (1)
Total proteins gm/dl 6.4 ± 0.6 (11) 6.0 ± 0.0 (1) 6.3 ± 1.0 (26)
Albumin gm/dl 3.6 ± 0.7 (5) --- 3.8 ± 0.6 (8)
Globulin gm/dl 2.5 ± 0.5 (5) --- 2.4 ± 0.5 (8)
AST (SGOT) IU/L 287 ± 420 (9) --- 113 ± 79 (21)
ALT (SGPT) IU/L 54 ± 80 (9) 13 ± 4 (2) 8 ± 11 (21)
Tot. Bilirubin mg/dl 0.3 ± 0.3 (7) --- 0.7 ± 0.8 (13)
Dir. Bilirubin mg/dl 0.0 ± 0.0 (2) --- ---
Indir. Bilirubin mg/dl 0.2 ± 0.0 (2) --- ---
Amylase SU 649 ± 536 (5) --- ---
Alk Phosp. IU/L 180 ± 109 (9) --- 225 ± 197 (20)
LDH IU/L 316 ± 94 (5) --- 574 ± 427 (12)
CPK IU/L 968 ± 1179 (2) --- ---
CO2 mMol/L --- --- 13.9 ± 5.1 (5)
Fibrinogen gm/dl --- 200 ± 0 (1) ---

118
TABLE 3 CONTINUED. CLINICAL CHEMISTRIES—CALLITRICHIDAE
Leontopithecus rosalia Callimico goeldii
Golden-lion Tamarin Goeldi’s Monkey
Glucose mg/dl 156 ± 85 (309) 124 ± 44 (226)
BUN mg/dl 14 ± 6 (315) 23 ± 8 (216)
Creatinine mg/dl 0.5 ± 0.2 (263) 0.7 ± 0.4 (138)
Uric acid mg/dl 0.6 ± 0.5 (148) 0.6 ± 0.2 (123)
Calcium mg/dl 9.2 ± 0.9 (277) 9.8 ± 0.7 (181)
Phosphorus mg/dl 4.8 ± 2.1 (259) 5.4 ± 2.2 (167)
Sodium mEq/L 149 ± 4 (229) 150 ± 5 (162)
Potassium mEq/L 3.7 ± 0.9 (230) 4.4 ± 0.8 (166)
Chloride mEq/L 106 ± 5 (234) 108 ± 26 (156)
Iron mcg/dl 210 ± 75 (19) 100 ± 27 (6)
Magnesium mg/dl 1.52 ± 0.62 (19) 2.48 ± 0.27 (8)
Bicarbonate mMol/L 20 ± 7.4 (5) 18.3 ± 2.9 (3)
Cholesterol mg/dl 73 ± 30 (207) 108 ± 26 (156)
Triglycerides mg/dl 102 ± 86 (147) 84 ± 27 (6)
Total proteins gm/dl 6.6 ± 0.7 (304) 6.6 ± 0.6 (213)
Albumin gm/dl 3.7 ± 0.5 (199) 4.1 ± 0.6 (129)
Globulin gm/dl 2.9 ± 0.6 (197) 2.6 ± 0.5 (129)
AST (SGOT) IU/L 108 ± 53 (285) 120 ± 38 (224)
ALT (SGPT) IU/L 86 ± 81 (295) 70 ± 54 (226)
Tot. Bilirubin mg/dl 0.7 ± 0.8 (278) 0.4 ± 0.2 (208)
Dir. Bilirubin mg/dl 0.2 ± 0.4 (89) 0.1 ± 0.1 (12)
Indir. Bilirubin mg/dl 0.3 ± 0.3 (87) 0.2 ± 0.1 (12)
Amylase SU 917 ± 1065 (59) 349 ± 103 (6)
Alk Phosp. IU/L 73 ± 52 (259) 157 ± 68 (144)
LDH IU/L 439 ± 298 (179) 300 ± 163 (128)
CPK IU/L 704 ± 766 (169) 793 ± 1147 (111)
CO2 mMol/L 19.5 ± 6.0 (140) 19.8 ± 6.2 (119)
Fibrinogen gm/dl 167 ± 82 (6) 100 ± 0 (1)
GGT IU/L 53 ± 67 (143) 39 ± 35 (115)
Lipase U/L 25 ± 25 (40) 25 ± 13 (6)

119
TABLE 4. CLINICAL CHEMISTRIES—CEBIDAE
Saimiri sciureus Callicebus moloch Callicebus donacophilus
Common Squirrel Orabussu Titi Reed Titi
Monkey
Glucose mg/dl 92 ± 37 (93) 158 ± 73 (7) 128 ± 39 (49)
BUN mg/dl 30 ± 10 (94) 12 ± 4 (7) 16 ± 6 (50)
Creatinine mg/dl 0.9 ± 0.3 (91) 0.7 ± 0.2 (7) 0.7 ± 0.2 (43)
Uric acid mg/dl 0.4 ± 0.4 (37) 0.0 ± 0.0 (1) 0.1 ± 0.1 (15)
Calcium mg/dl 9.0 ± 0.6 (87) 9.6 ± 1.9 (7) 9.8 ± 0.5 (47)
Phosphorus mg/dl 5.7 ± 1.9 (82) 5.3 ± 1.8 (7) 3.9 ± 0.9 (40)
Sodium mEq/L 148 ± 4 (74) 148 ± 5 (6) 146 ± 4 (39)
Potassium mEq/L 4.3 ± 0.7 (73) 4.7 ± 0.7 (6) 4.1 ± 0.4 (40)
Chloride mEq/L 116 ± 5 (70) 112 ± 3 (6) 109 ± 3 (37)
Iron mcg/dl --- --- 195 ± 0 (1)
Magnesium mg/dl 0.2 ± 0.0 (1) --- 2.3 ± 0 (1)
Bicarbonate mMol/L 10.2 ± 2.7 (5) --- 21.4 ± 2.7 (5)
Cholesterol mg/dl 204 ± 67 (74) 238 ± 70 (5) 274 ± 94 (44)
Triglycerides mg/dl 80 ± 45 (47) --- 134 ± 54 (26)
Total proteins gm/dl 6.6 ± 0.6 (92) 8.0 ± 0.6 (8) 6.8 ± 0.5 (47)
Albumin gm/dl 3.8 ± 0.5 (75) 4.9 ± 0.5 (5) 4.4 ± 0.4 (31)
Globulin gm/dl 2.8 ± 0.8 (75) 2.7 ± 0.8 (5) 2.6 ± 0.4 (31)
AST (SGOT) IU/L 139 ± 70 (82) 41 ± 25 (6) 73 ± 91 (48)
ALT (SGPT) IU/L 104 ± 63 (89) 19 ± 9 (7) 35 ± 24 (47)
Tot. Bilirubin mg/dl 0.5 ± 0.4 (74) 0.5 ± 0.3 (7) 0.6 ± 0.3 (49)
Dir. Bilirubin mg/dl 0.0 ± 0.0 (7) 0.1 ± 0.0 (5) 0.1 ± 0.1 (12)
Indir. Bilirubin mg/dl 0.1 ± 0.0 (7) 0.4 ± 0.3 (5) 0.5 ± 0.2 (12)
Amylase SU 122 ± 132 (49) 285 ± 43 (3) 571 ± 345 (19)
Alk Phosp. IU/L 444 ± 290 (83) 116 ± 108 (7) 314 ± 365 (45)
LDH IU/L 596 ± 954 (34) 729 ± 293 (2) ---
CPK IU/L 1018 ± 1835 (16) 253 ± 29 (3) 1064 ± 1264 (13)
CO2 mMol/L 38.1 ± 1.3 (50) 6.3 ± 1.5 (3) 18.3 ± 6.8 (7)
Fibrinogen gm/dl --- 200 ± 141 (2) ---
GGT IU/L 28 ± 37 (52) 42 ± 38 (3) 249 ± 218 (29)
Lipase U/L 4 ± 2 (8) 27 ± 4 (3) 43 ± 27 (4)

120
TABLE 4 CONTINUED. CLINICAL CHEMISTRIES—CEBIDAE
Ateles belzebuth Ateles fusciceps Ateles geoffroyi Ateles paniscus
Mean ± SD (n) Long-haired Brown-headed Black-handed Black Spider
Spider Monkey Spider Monkey Spider Monkey Monkey
Glucose mg/dl 999 ± 37 (7) 88 ± 38 (43) 100 ± 38 (230) 143 ± 100 (2)
BUN mg/dl 12 ± 4 (7) 20 ± 8 (43) 17 ± 7 (242) 26 ± 16 (3)
Creatinine mg/dl 1.0 ± 0.1 (4) 1.0 ± 0.3 (43) 0.8 ± 0.3 (224) 4.6 ± 5.2 (2)
Uric acid mg/dl 2.5 ± 0.7 (7) 5.0 ± 1.3 (29) 5.6 ± 2.1 (133) ---
Calcium mg/dl 9.2 ± 0.3 (4) 9.5 ± 0.8 (44) 9.5 ± 0.9 (223) 10.2 ± 0.0 (1)
Phosphorus mg/dl 2.2 ± 1.2 (4) 4.8 ± 1.7 (43) 4.3 ± 1.8 (218) 1.8 ± 0.0 (1)
Sodium mEq/L 139 ± 2 (4) 143 ± 4 (44) 141 ± 3 (193) ---
Potassium mEq/L 4.2 ± 0.2 (4) 4.7 ± 0.9 (44) 4.2 ± 0.6 (198) ---
Chloride mEq/L 103 ± 3 (4) 104 ± 5 (36) 102 ± 4 (198) 94 ± 0 (1)
Iron mcg/dl 309 ± 321 (3) 110 ± 34 (2) 133 ± 31 (12) ---
Cholesterol mg/dl 211 ± 52 (4) 159 ± 49 (28) 175 ± 50 (222) 101 ± 0.0 (1)
Triglycerides 28 ± 0 (1) 84 ± 33 (26) 116 ± 63 (117) ---
mg/dl
Total proteins 6.4 ± 0 (1) 7.1 ± 0.8 (46) 7.4 ± 0.7 (224) 7.3 ± 1.3 (2)
gm/dl
Albumin gm/dl 4.4 ± 0 (1) 5.2 ± 1.0 (33) 5.4 ± 1.1 (179) 3.9 ± 0.0 (1)
Globulin gm/dl 2.0 ± 0 (1) 1.7 ± 0.8 (33) 2.1 ± 1.0 (179) 2.5 ± 0.0 (1)
AST (SGOT) 98 ± 16 (7) 111 ± 51 (43) 94 ± 34 (225) 51 ± 27 (2)
IU/L
ALT (SGPT) IU/L 26 ± 6 (7) 34 ± 22 (18) 30 ± 17 (188) 21 ± 0 (1)
Tot. Bilirubin 0.3 ± 0.1 (3) 0.5 ± 0.4 (44) 0.3 ± 0.2 (226) 0.4 ± 0.2 (2)
mg/dl
Dir. Bilirubin 0.1 ± 0.0 (3) 0.0 ± 0.0 (1) 0.0 ± 0.1 (64) ---
mg/dl
Indir. Bilirubin 0.3 ± 0.1 (3) 0.2 ± 0.0 (1) 0.3 ± 0.1 (63) ---
mg/dl
Amylase SU 308 ± 530 (3) 614 ± 345 (2) 820 ± 410 (51) 765 ± 0 (1)
Alk Phosp. IU/L 230 ± 173 (7) 315 ± 296 (44) 225 ± 265 (226) 99 ± 58 (2)
LDH IU/L 401 ± 268 (4) 730 ± 632 (30) 443 ± 326 (175) 281 ± 0 (1)
CPK IU/L 531 ± 169 (4) 296 ± 39 (4) 370 ± 371 (94) 194 ± 88 (2)
CO2 mMol/L 21.0 ± 0.0 (1) 22.2 ± 6.2 (26) 21.3 ± 4.8 (80) ---
GGT IU/L --- --- 17 ± 12 (52) ---
Lipase U/L --- --- 144 ± 104 (16) ---

121
TABLE 4 CONTINUED. CLINICAL CHEMISTRIES—CEBIDAE
Aotus trivirgatus Alouatta caraya Alouatta palliata Lagothrix
lagothricha
Douroucouli Black Howler Mantled Howler Wooly Monkey
Monkey Monkey
Glucose mg/dl 155 ± 82 (82) 113 ± 33 (2) 92 ± 13 (161) 92 ± 23 (28)
BUN mg/dl 18 ± 10 (82) 24 ± 8 (161) 25 ± 4 (2) 24 ± 9 (28)
Creatinine mg/dl 0.9 ± 0.3 (71) 1.2 ± 0.4 (160) 1.5 ± 0.1 (2) 0.8 ± 0.2 (27)
Uric acid mg/dl 0.5 ± 0.4 (16) 0.2 ± 0.2 (94) --- 5.0 ± 3.2 (18)
Calcium mg/dl 9.4 ± 1.0 (74) 9.6 ± 0.8 (156) 10.6 ± 0.6 (2) 10.1 ± 0.7 (27)
Phosphorus mg/dl 5.6 ± 1.8 (71) 4.7 ± 1.8 (156) 3.4 ± 0.4 (2) 4.0 ± 1.8 (27)
Sodium mEq/L 149 ± 5 (68) 140 ± 3 (151) --- 142 ± 3 (27)
Potassium mEq/L 3.8 ± 0.8 (70) 4.3 ± 0.6 (155) --- 4.1 ± 0.5 (28)
Chloride mEq/L 107 ± 6 (68) 102 ± 3 (147) --- 107 ± 3 (21)
Iron mcg/dl 98 ± 52 (6) 122 ± 41 (33) --- ---
Magnesium mg/dl 3.3 ± 0.0 (1) 1.9 ± 0.0 (1) --- ---
Bicarbonate mMol/L 15.6 ± 5.7 (9) 23.6 ± 1.7 (5) --- ---
Cholesterol mg/dl 169 ± 61 (71) 175 ± 46 (158) 147 ± 16 (2) 147 ± 46 (27)
Triglycerides mg/dl 139 ± 107 (36) 82 ± 35 (122) --- 42 ± 12 (17)
Total proteins gm/dl 7.3 ± 0.7 (79) 7.0 ± 0.6 (154) 6.7 ± 0.1 (2) 7.0 ± 0.5 (27)
Albumin gm/dl 61 ± 33 (60) 4.1 ± 0.6 (100) 2.9 ± 0.3 (2) 4.3 ± 0.5 (25)
Globulin gm/dl 3.2 ± 0.5 (49) 2.8 ± 0.6 (100) 3.8 ± 0.1 (2) 2.7 ± 0.6 (25)
AST (SGOT) IU/L 148 ± 64 (78) 121 ± 40 (158) 65 ± 19 (2) 59 ± 21 (26)
ALT (SGPT) IU/L 61 ± 33 (60) 26 ± 14 (134) 9 ± 4 (2) 35 ± 17 (25)
Tot. Bilirubin mg/dl 0.7 ± 0.4 (67) 0.4 ± 0.2 (154) 0.2 ± 0.0 (2) 0.7 ± 0.4 (27)
Dir. Bilirubin mg/dl 0.1 ± 0.1 (15) 0.1 ± 0.1 (46) --- 0.3 ± 0.2 (10)
Indir. Bilirubin mg/dl 0.3 ± 0.2 (15) 0.3 ± 0.2 (46) --- 0.3 ± 0.1 (10)
Amylase SU 1237 ± 1380 (14) 179 ± 85 (40) --- 445 ± 183 (18)
Alk Phosp. IU/L 245 ± 186 (76) 646 ± 1089 (152) 263 ± 48 (2) 257 ± 190 (28)
LDH IU/L 613 ± 607 (49) 543 ± 345 (131) --- 117 ± 48 (18)
CPK IU/L 940 ± 1859 (24) 597 ± 359 (59) 276 ± 207 (2) 400 ± 0 (1)
CO2 mMol/L 16.2 ± 5.4 (26) 19.6 ± 3.9 (54) --- 22.5 ± 1.3 (18)
Fibrinogen gm/dl --- 150 ± 71 (2) --- ---
GGT IU/L 14 ± 10 (16) 47 ± 21 (68) --- 41 ± 15 (19)
Lipase U/L 86 ± 110 (5) 17 ± 10 (2) --- 38 ± 36 (9)

122
WASTING MARMOSET SYNDROME
Donna M. Ialeggio, D.V.M.

Wasting Marmoset Syndrome (WMS) has been referred to in the literature as “marmoset wasting
syndrome,” “wasting,” and “wasting disease.” Despite its name, WMS may affect callitrichids other than
marmosets, and has been reported in species of Callithrix, Saguinus, Leontopithecus, and Cebuella.

A 1994 survey (Ialeggio and Baker 1995) indicates that WMS appears to be responsible for significant
morbidity in both zoologic and laboratory callitrichid collections. Many survey respondents were
unfamiliar with the full array of signs associated with WMS. Clinical signs associated with, but not limited
to WMS are decreased body weight (> 30%), alopecia, chronic diarrhea, chronic colitis, muscle atrophy,
and anemia. These clinical signs are non-specific and can be associated with a multitude of disease entities.
Not all animals suspected of having WMS will manifest all symptoms listed. Through thorough diagnostic
testing, known etiologies can be eliminated for each clinical symptom exhibited. A complete physical
examination should be performed including: hematology, serum or plasma biochemical analysis, fecal
examination, fecal/rectal culture for Salmonella, Shigella, Campylobacter, and Yersinia, tuberculin testing,
and radiography. Ultrasonography, electrocardiography, surgical or laproscopic exploration and/or
gastrointestinal biopsy may also be used to eliminate specific etiologic disease entities included in the
differential diagnosis.

It is probable that many factors contribute to the development of WMS in a given animal. At present, no
one specific etiology is known. Some of the factors that have been proposed as predisposing conditions or
causative agents include non-specific nutritional factors (i.e., protein deficiency, excessive fruit in the diet,
excessive dietary simple sugars, and conversely, insufficient simple sugars in the diet), stress, over
crowding, lack of social coprophagy, infectious agents, food allergies, inappropriate spectrum of natural
light, autoimmune disease, and anorexia.

As the cause or causes of WMS are unknown, supportive, symptomatic therapy for affected animals is
recommended. Exercise caution when using human enteral formulas, such as Ensure, since the osmolality
of undiluted preparations is too high for the diarrheic animal.

Published and anecdotal information suggest that when one or more of the proposed etiologies of WMS
have been addressed therapeutically, some improvement in or amelioration of clinical signs may occur. A
varied diet may encourage voluntary food consumption in some animals. Dietary factors may contribute to
the development of WMS, however the incidence of WMS in unrelated colonies feeding similar diets
varies considerably. Additional factors, such as the timing and frequency of feeding, diet presentation,
order of diet item presentation, variety of diet items, individual preferences, and social status should be
considered.

In the 1994 survey, the incidence of WMS was considerably higher in Callithrix and Saguinus spp. than in
Cebuella, Callimico, or Leontopithecus spp. This apparent difference in morbidity may reflect overall
collection bias (total number and number of species) toward the Callithrix and Saguinus spp. rather than a
predilection for WMS. In addition, the incidence of WMS in colonies containing more than 25 animals (of
one callitrichid species or in total) was appreciably greater than in smaller colonies. Whether this reflects a
true predisposition or is merely an increase in available at-risk animals and observational experiences is
unknown.

REFERENCES

Ialeggio, D. M., and A. J. Baker. 1995. Results of a preliminary survey into wasting marmoset syndrome in
callitrichid collections. In: Proceedings of the First Annual Conference of the Nutrition Advisory
Group of the American Zoo and Aquarium Association, pp. 148-158.

123
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ACKNOWLEDGMENT
We wish to thank The Primate Information Center for supplying a majority of these references.

INFECTIOUS DISEASES

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NEW WORLD PRIMATE NECROPSY PROCEDURE

1. Refrigerate the body if there will be a delay before necropsy (delays should be avoided since
autolysis proceeds rapidly). Do not freeze the body.
2. Record all relevant historical information.
3. Weigh the animal.
4. Perform an external exam - note any musculoskeletal abnormalities, ectoparasites, evidence of
trauma, skin lesions, etc.
5. Examine body orifices for patency, exudates, fecal staining around anus and tail, etc.
6. Evaluate nutritional condition based on fat stores and relative muscle mass.
7. Make a ventral midline incision from the mandible to the pelvis with a sharp scalpel or scissors.
Note any accumulations of fluid or exudate in the abdomen and obtain a swab for bacterial and/or
fungal culture and cytology if appropriate.
8. Note if diaphragm is intact and if there is negative pressure. Open the diaphragm with a scalpel
blade. Cut the ribs and open the thorax. Note any accumulations of fluid or exudate in the thorax
and obtain a swab for bacterial and/or fungal culture and cytology if appropriate.
9. Obtain a sterile blood sample for bacterial culture by direct heart puncture using a 1-3 cc syringe
with a 25-22 gauge needle.
10. Remove the internal organs and examine each systematically. Note the quantity and nature of
ingesta throughout the gastrointestinal tract.
11. Obtain samples for histopathology using the tissue list provided as a guide. Save samples of all
lesions.

TISSUE CHECK LIST

All of the following tissues may be placed together in a single container of 10% neutral buffered formalin.
The volume of formalin should be 10 times the volume of all tissues collected. The tissues should be no
thicker than 0.5cm to ensure proper fixation.
Skin Urinary bladder
Muscle (thigh) Ovary or testis
Sciatic nerve (with thigh muscle) Uterus
Tongue Lymph node
Esophagus Adrenal gland
Stomach Thyroid and parathyroid
Duodenum Thymus (if present)
Jejunum Trachea and lung
Ileum Heart (atrium & ventricular wall with great
Cecum vessels)
Colon Pituitary
Liver with gallbladder Brain
Pancreas Eye
Spleen Femoral bone marrow
Kidney

146
NEONATAL NECROPSY PROCEDURE
The follow procedures are in-addition to the general necropsy protocol for this species.

1. Examine and fix placenta and any fetal membranes that are available.
2. Determine degree of maturity/immaturity of fetus.
3. Determine crown-rump measurement.
4. Examine umbilicus (fix section of umbilical stump and surrounding skin in formalin).
5. Note any skeletal abnormalities (cleft palate, hare lip, facial/limb/trunk abnormality).
6. Note internal malformations (anomalies, diaphragmatic hernia).
7. Determine if the animal was stillborn. Place a section of lung tissue in 10% buffered formalin, if
the lung sinks, the animal probably did not breath. If the lung floated, the animal probably
breathed.
8. Examine stomach contents (milk, meconium, etc.).
9. Proceed with remainder of necropsy protocol for New World primates.

Freeze portions of the following tissues: Liver, Spleen, Lung, Brain, Heart, Kidney. Freeze each tissue
separately (at least 10g of each tissue if large enough). Store tissues in an ultra-low freezer (-70oC). If an
ultra-low freezer is not available, conventional freezing is acceptable. These tissues may be discarded after
a definitive diagnosis is established, but if possible, should be saved for future research purposes.

NECROPSY REPORT FORM

Institution:________________________________________________________
Address:__________________________________________________________
Date of Death:__________ ID#__________ Studbook #______________
Birth Date/Age:__________ Sex:__________ Weight (Kg):__________
Necropsy Date:__________ Necropsy Location:________________

History:
Enclosure mates:___________________________________________________
Indoor enclosure:_____ Outdoor enclosure:______
Weather/Indoor climate (approx. temp., windy, rainy, etc.):____________________
Movements or relocations:____________________________________________
Diet:_____________________________________________________________
Contraceptive implant type____________ Implant#________ Implant wt.______

Clinical history (include clinical signs, lab work, treatment and circumstances of death):

147
GROSS EXAMINATION

General external exam (nutritional condition, skin, body orifices, superficial lymph nodes)

Musculoskeletal system (bones, bone marrow, joints, skeletal muscle)

Respiratory system (nasal passages, trachea, bronchi, lungs, diaphragm, regional lymph nodes)

Cardiovascular system (heart, pericardial sac, great vessels, valves)

Digestive system (mouth, teeth, tongue, esophagus, stomach, intestines, regional lymph nodes)

Liver, gall bladder, pancreas, spleen (size, color, consistency)

Urinary system (kidneys, ureters, bladder, urethra)

Reproductive system (ovaries/testes, uterus, cervix, penis/vagina, accessory sex glands, mammary glands,
placenta)

Endocrine system (thyroid, parathyroid, adrenal and pituitary glands)

Central nervous system (brain, meninges, spinal cord)

Sensory organs (eyes, ears)

Laboratory results (microbiology, cytology, fluid analysis, etc.)

Prosector Date

148

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