COTTON-TOP TAMARIN SSP© HUSBANDRY MANUAL

The purpose of this husbandry manual is to provide useful guidelines for maintaining and
exhibiting cotton-top tamarins in captivity. We have provided the most current
information on cotton-top tamarins that spans the extensive literature on tamarins in the
wild, in research institutions, and in zoos. As new information becomes available, we will
be sending updated chapters for your manual. Please feel free to provide us with any
additional information or comments that may be useful for future revisions. Address
questions and comments to:

Rebecca Sellin
Cotton-top Tamarin SSP Coordinator
Disney’s Animal Kingdom
PO Box 10, 000
Lake Buena Vista, FL 32830

Acknowledgements

This manual was written in part by the members of the Cotton-top Tamarin
SSP Management Group. Special thanks to Linda Pastorello, Stacey Johnson, Bill
Langbauer, Candy McMahon, Ron Cline, Mike Quick, Mike Coker, Anne Dottore, Gerry
Aquilina, Anthony Brownie, Ingrid Porton for their valuable information and reviews of
this manual. Additional material for the chapters was provided by Dara Zirofsky, Parviez
Hosseini, Julie DeCubellis, Nicolette Zarday, and Yvonne Federowitz. The veterinary
chapter was written by Melinda Franceschini, with helpful information and reviews by
Vincent Seccareccia, D.V.M., David Lee-Parritz, D.V.M., James Cooley, D.V.M., and
Charles Sedgwick, D.V.M. The cover design was provided by Michael Stone. Dara
Zirofsky deserves our heartfelt thanks for providing invaluable assistance and patience in
writing, editing and coordinating the completion of this manual. Thanks to the staff of the
Roger Williams Park Zoo for their continued support of the cotton-top tamarin
conservation program. This project was funded by an Institute of Museum Services
General Operating Support grant to the Roger Williams Park Zoo.

Heartfelt thanks for providing invaluable assistance and patience in writing, editing and
coordinating the completion of this manual. Thanks to the staff of the Roger Williams
Park Zoo for their continued support of the cotton-top tamarin conservation program.
This project was funded by an Institute of Museum Services General Operating Support
grant to the Roger Williams Park Zoo.

I Natural History
Chapter Summary
 Cotton-top tamarins are small monkeys weighing between 400-700g and are approximately 23.07cm
long (including tail).
  The cotton-top tamarin is a highly endangered species, endemic to the northwest region of Colombia.
 Major threats to the cotton-top tamarin’s existence in the wild include , but are not limited to, habitat
destruction, hunting, and live capture.
 The cotton-top tamarin has been an important model for the biomedical research since it is the only
primate that spontaneously develops colonic adenocarcinoma in captivity.

Introduction

Although the cotton-top tamarin is abundant in captivity with populations found in

both zoos and research institutions throughout the world (Tardif, 1989), it is one of the
most endangered primates in its native habitat of Colombia. Found only in northwestern
Colombia, the cotton-top tamarin is continually threatened by the destruction of its
habitat, live capture for local and international pet markets and the biomedical industry
(Mast & Patiiio, 1988). During the late 1960's and early 1970's between 20,000-40,000
cotton-top tamarins were imported into the U.S. for use in biomedical research
(Hernandez Camacho & Cooper, 1976). In 1973, the species was declared endangered
and exportation was banned. The cotton-top tamarin is one of the most important primate
models for biomedical research and has been used in studies from Epstein-Barr virus to
colitis and colon cancer. However, it's primary use in the biomedical community has been
the study of colon adenocarcinoma, as it is the only primate model which, like humans,
spontaneously develops colitis and/or colon cancer (Clapp, 1993).

The cotton-top tamarin is just one of the many endangered species found in the country of
Colombia. Highlighting such an important species in education and public awareness
campaigns can generate support for the conservation of Colombia's natural resources.

Taxonomy

The Callitrichidae comprise the most diverse family of New World monkeys, with 32
species. Callitrichids are the smallest of the New World monkeys, have nonprehensile
tails, possess claws instead of nails, and move quadrupedally (Hershkovitz, 1977). All
callitrichids lack a set of paired molars that are typically present in other New World
primate species. In addition, Callithrix and Cebuella can be distinguished on the basis of
dentition from Saguinus and Leontopithecus. Only Callithrix and Cebuella have "short
tusked" lower anterior dentition allowing them to perforate tree bark and induce the flow
of exudates (gum and sap) which are important food sources. In contrast, Saguinus and
Leontopithecus have the "long-tusked" dental configuration in which the canines are
much longer than the incisors.

Of the 12 tamarin species within the genus Saguinus (NEttermeier et al., 1992;
Mittermeier & Coimbra-Filho, 1981), Snowdon and Soini (1988) have divided the
tamarins into two groups, the Hylaen (or Amazonian) and the extra-Amazonian. The
latter group of trans-Andean tamarins comprise three taxa (S. geoffroyi, S. oedipus, and S.
leucopus), all of which are found in Colombia.
There has been considerably discrepancy regarding the taxonomy of S. oedipus and S.
geoffroyi. Hershkovitz (1977) describes both the cotton-top tamarin and the Panamanian
tamarin as subspecies ofSaguinus oedipus (S. o. oedipus and S. o. geoffroyi respectively),
and Hernandez Camacho and Defler (1983; 1985) have also suggested that these two taxa
fall beneath a single superspecies. However, reports by Skinner (1991) and Rosenberger
(1992) have suggested the more widely accepted view that both of these taxa are full
species (see Mast et al., 1993 for a complete review). Skinner (1991) suggests that when
the geographic distribution and ecology of related varieties is poorly known, as in the
case of the cotton-top tamarin and the Panamanian tamarin, taxonomists must resort to
other methods, such as morphological comparisons. Skinner (1991) compared the
morphological traits for 17 characteristics among S. geoffroyi, S. leucopus, and S.
oedipus. She found that S. leucopus and S. oedipuswere more closely related than either
species were to S. geoffroyi. Therefore, she concluded that S. oedipus and S.
geoffroyi were two separate species. It is also important to note that only S.
oedipusspontaneously develops colon cancer.

Physical Description

The large shock of white fur on its head gives the cotton-top tamarin its most appropriate
name. Males and females are not sexually dimorphic weighing approximately 404-417 g
in the wild to 565-700 g in captivity (Savage, 1990; Savage et al., 1993). Knee-to-heel
length (M=7.26 cm) and head to tail length (M=23.07 cm) appear to be similar for both
wild and captive cotton-top taimarins (see Savage, 1990 for a complete review). The face
of the cotton-top tamarin is black, temples and sides of head are covered with short
adpressed silvery hairs. The face is adorned with grayish or whitish supraorbital band,
with a grayish fringe across the muzzle to each comer of the mouth. There is a wedge-
shaped midfrontal white crest. The dorsal surface of the body is primarily black or brown,
while the underparts of the body, arms, and legs are predominantly white (Hershkovitz,
1977).

Scent Gland Morphology

Female cotton-top tamarins have highly developed anogenital and suprapubic scent
glands. Females have larger scent glands than males. Perkins (1969) reported that the
sebaceous glands, apocrine secretary coils, and the secretary ducts associated with these
units were more extensive and more highly developed in females. The thickness of
glandular skin also differs between the sexes, with sebaceous glands observed up to
approximately 1.6 mm below the skin surface in females but only to a depth of 0.4 mm
below skin surface in males. Total area of the scent glands in female cotton-top tamarins
range from 7.89-8.31 CM2 (Savage et al., 1988). Use of the anogenital and suprapubic
glands differ between males and females.

Distribution
Cotton-top tamarins are found only in Colombia, from the eastern bank of the Atrato
River to the western bank of the Cauca and lower Magdalena Rivers, bounded by the
Colombian Caribbean coast to the north. To the south, the distributional range proposed
by Mast et al., (1993) follows the 1500-m contour from east to west beginning at the
Cauca River and crossing the Serranfa de Ayapel and the Serranfa de San Jer6nimo
(Hernandez-Camacho and Defler, 1983; 1985; Hershkovitz, 1977) (Figure 1).

Threats to the Survival of Wild Cotton-top Tamarins

Colombia is one of the most biologically diverse countries and is second only to Brazil in
overall numbers of plants and animal species. Given its size (one seventh that of Brazil),
Colombia harbors greater concentrations of species per unit area than any other country
on the planet (Alderman, 1989; Mast et al., 1993; Mittermeier & Mast, 1990). One of the
biggest threats to the cotton-top tamarin, and to Colombian biodiversity in general, is
forest destruction. Colombia is among the top ten countries worldwide in terms of
deforestation, and is surpassed only by Brazil, in the Western Hemisphere, in terms of
numbers of hectares deforested. Each year more than 4000 km' of tropical habitat is
destroyed (Myers, 1989).

Threats to wild cotton-top tamarins and many of the primates in Colombia, can be
characterized as direct pressures to the animals themselves (e.g. hunting and

Figure 1. From Mast et al., 1993.

live capture) or dangers associated with the loss of habitat (Mast et al., 1993; Mittermeier
et al., 1989). In the northern part of the cotton-top tamarin's range, the majority of the
forest that has been destroyed has been for large-scale clearance for agriculture or
ranching purposes. The remaining forest patches in this part of the country generally lie
atop agriculturally useless land (e.g. limestone outcropping, seasonally flooded river
margins) (Mast et al., 1993).

The portion of the cotton-top tamarin's habitat that lie in the foothills of the northern
termini of the western and central Andean cordilleras face fuelwood collection and small-
scale agricultural encroachment threats of unknown intensity. However, the most
damaging imminent threat comes from flooding of forest for hydroelectric projects (see
Mast et al., 1993 for a complete review).

Colombia's electric power is approximately 70% hydroelectric, yet only about 6% of the
country's hydroelectric potential has been exploited to date. Planned hydroelectric
projects for Colombia, if completed, would flood thousands of hectares of the country's
high diversity ecosystems. One proposed hydroelectric project alone, URRA (comprised
of LTRRA I and URRA 11) could flood over 60,000 ha in the upper Sin-6 river basin.
This area included more than 54,000 ha of primary and secondary forest lying inside the
Parramillo National Park and its buffer zone, one of the last major strongholds for the
cotton-top tamarin (Mast & Cubberly, 1987; Mast & Patiiio, 1988; Mast et al., 1993;
Ramirez Cerquera, 1985).

Fortunately, Colombia's power sector has avoided any major negative environmental and
social impacts resulting from hydroelectric compared to other countries. In recent years
under the terms of the World Bank's power sector adjustment loan (loan 2889-CO) the
Colombian central power agency (ISA) and its eight regional affiliates have undertaken a
program to minimize the environmental impact of hydroelectric expansion under the
National Power Expansion Plan (Mast et al., 1993). Efforts have been made to develop
methodologies for more effectively prioritizing projects to minimize their adverse
environmental and socioeconomic impacts, to provide environmental training for power
sector staff, and to develop more stringent environmental standards for hydroelectric and
thermal projects (Mast et al., 1993). Mast et al., (1993) provides a detailed description of
the proposed hydroelectric projects and their probably impact on the natural resources of
Colombia.

In addition, to the dramatic impact forest destruction has on the future survival of this
species, capture for the pet trade and/or exportation has and will continue to have, an
impact on the survival of cotton-top tamarins. Between 1968 and 1972 as many as 14,000
cotton-tops were imported to the U.S. and between 30,000-40,000 were exported from
Barranquilla, Colombia between 1960-1975 along (Heernandez Camacho & Cooper,
1976). The actual numbers of cotton-top tamarins captured from the wild during this
period is likely to be much higher given the high number of animals that died during
capture and/or export. Despite the 1973 Colombian ban and the listing of Saguinus
oedipus in Appendix I of CITES, importation of cotton-top tarnarins to the U.S.
continued in small numbers, most shipped through countries such as, Panama (Mack &
Mittermeier, 1984; Mittermeier & Coirnbra-Filho, 1983; Thorington, 1972). There is still
an active local market for cotton-top tainarins within Colombia (Mast & Cubberly, 1987;
Mast & Patifio, 1988). Wildlife dealers in Colombia are constantly selling cotton-top
tamarins as pets and may be smuggled to other countries (Barbosa et al., 1988). As Mast
et al., 1993 states "Notwithstanding laws to the contrary, if there is money to made
through the capture and sale of wild species, there will be someone willing to take the risk
to earn that money. The best way to curtail the threat posed by live captive is to eliminate
all demand for wild-captured animals." (p. 37)

II Social Organization
Chapter Summary

 Cotton-top tamarins should be housed as monogamous breeding pairs and

their offspring.
 Aggression is common in large family groups between the eldest siblings.
 Affiliative behavior and copulations are more frequent in newly paired
animals than established breeding pairs.
  Scent marking is common in both males and females.
 However, female scent marking is positively correlated with estrogen
activity.
 Cotton-top tamarins have a complex vocal repertoire with at least 38 distinct
vocalizations.

Social Structure

Although there is much debate about callitrichid social organization (Price & McGrew,
1991; Savage & Baker, 1996), cotton-top tamarins are successfully housed as
monogamous breeding pairs and their offspring in captivity. This choice of social
structure is the result of many years of investigating reproductive strategies of wild and
captive callitrichids (see Snowdon, 1989). Studies attempting to integrate adult animals
into existing stable families have failed since intruding animals are met with intense
aggression by resident animals (de la Ossa et al., 1988; French et al., 1984). However,
evidence of deviations from monogamy in captivity (Price & McGrew, 1991) and in the
field (Savage et al., 1996) have been observed. Multiple breeding females within groups
are common when their is some disruption within the breeding pair or group (death of a
mate, introduction of a step-parent, immigrating adult male) (Price & McGrew, 1991;
Savage, 1990; Savage et al., 1996).

Alternative Housing Options

Due to breeding recommendations and the variation found in the population, cotton-top
tamarins can be housed in a variety of social conditions other than the standard breeding
pair/family group.

Father + offspring (e.g. after the death or removal of the breeding female). This social
grouping generally remains stable. Most daughters remain reproductively suppressed
under these conditions, however, there have been noted exceptions. Daughters over 14
months of age should be contracepted if they appear to have 1) a highly active scent gland
(darkly pigmented and secreting sebum); 2) are actively scent marking their environment;
3) are observed copulating with a male.

Mother + offspring (e.g. after the death or removal of the breeding male). This social
grouping generally remains stable. The breeding female will continue to cycle and it is
rare that copulations are observed. However, if copulations between mother and sons are
observed, the female should be contracepted.

Iso-sexual groupings Housing same sex pairs of animals is fairly routine for animals that
have been reared in family groups. Hand-reared or improperly socialized animals may not
be appropriate for this type of grouping. In general, do not pair more than two unrelated
animals. However, sibling groups larger than two animals are generally successful.
Single sex-mixed callitrichid group A single cotton-top tamarin can usually be
successfully housed with a single individual of another callitrichid species. A common
marmoset (C. jacchus), golden-head lion tamarin (L. chrysomelas), and Goeldi's
marmoset (Callimico goeldii) have been successfully housed with a single cotton-top
tamarin (L. Pastorello, pers. comm.). Individuals of the same sex are recommended for
pairing.

Within Group Aggression

Fighting within groups resulting in the removal of individuals is not atypical for cotton-
top tamarins. Typically, in family groups aggression tends to be directed toward natal
rather than breeding individuals; aggressors are usually the same-sex parent or siblings
(McGrew & McLuckie, 1986). Fights between same-sex twins have been observed,
although the majority of aggression in stable family groups tends to be between the eldest
male siblings (S. Evans, pers. comm.; A. Savage, pers. comm.). Most of the aggression
between individuals begins slowly, but has been known to rapidly escalate and culminate
in death. The age at which aggression and resulting eviction of natal individuals from the
group occurs is variable and unpredictable.

Aggression between Eldest Male Siblings is most common in stable family groups. As
group size increases due to high birth rates in this species, fighting between the two eldest
male siblings is common. Interestingly, the rest of the group members appear to ignore
the tension between the two animals. Low levels of aggression are most common initially,
(displacement at the food dish, rough play, chasing, mounting) but generally escalates to
one individual dominating the other. The subordinate sibling emits submissive
vocalizations constantly (squawks, see Cleveland & Snowdon, 1982) and typically avoids
contact with the dominant sibling. The victim may also show fearful behavior upon being
approached by the dominant individual and often stays lower dm normal in the exhibit. It
is recommended that the sibling harassing the subordinate sibling be removed from the
family when this is observed before any severe fighting develops. Do not attempt to
reintroduce this animal to the group.

Aggression between Father and Male Offspring-occurs in stable family groups, but is
most often observed when there has been some change in the environment. Moving
animals to new exhibits or introducing another species to residents can often result in
group disruption. Fathers can behave very aggressively toward their offspring, often
resulting in severe fighting. The offspring should be removed and no attempts to
reintroduce the offspring to the group should be made.

Aggression between Females is relatively rare and most commonly occurs when there is a
disruption in the environment (see above). Daughters have been observed to challenge
their mothers (mounting, harassing, displacing) but, unless the mother is old or impaired,
she will usually defend her position in the group. Daughters should be removed from the
family group only if the mother is becoming aggressive. Most daughters can live in stable
family groups for many years. Evictions of sons are much more frequent than daughters
in most captive cotton-top tamarin groups.

Social Behavior

There have been extensive studies of the behavior of cotton-top tamarins in captivity and
in most recently in the wild. Studies have shown that most captive cotton-top tamarins
live in monogamous pairs. Newly formed pairs of cotton-top tamarin show increased
affiliative behavior and are observed to engage in sexual activity more frequently than do
established breeding pairs (French et al., 1984; Savage et al., 1988; Tardif, 1984a;
Widowski et al., 1990). This increase in affiliative behavior occuring when the female
was removed from the family and paired with a male appears to be important in
establishing the pair bond in this species. However, as the duration of the pair bond
increases, affiliative behavior and scent marking decreases (Savage et al., 1988). This
decrease has been attributed to the addition of offspring to the group. Established
breeding pairs often spend less time in affiliative behavior with one another and direct
more of their attention toward their offspring (Savage et al., 1988). Nonetheless, the pair
bond appears to be strong in these animals as intruders are attacked (French & Snowdon,
1981) and territorial displays between cages in large colony rooms of tamarins are
frequent when visual contact between groups is allowed.

Scent Marking Cotton-top tamarins have highly developed anogenital and suprapubic
scent glands (see French & Cleveland, 1984 for a complete review). Both males and
females are observed to scent mark, however, females scent mark significantly more than
their male counterparts. The function of scent marking has been widely debated. Studies
have suggested that scent marking does have a communicatory function in callitrichids
(see Epple, 1975; Ziegler & Bercovitch, 1990). Rates of scent marking differ between
cycling and non-cycling females. Newly paired cotton-top tamarin females showed a
dramatic increase in rates of scent marking, rates much higher than those observed when
females lived with their families or in isolation (French et al., 1984; Savage et al., 1988).
Savage et al., (1 988) and Widowski et al., (I 990) found a positive correlation between
estrogen activity and frequency of scent marking. Increases in scent marking paralleled
increased in estrogen activity, with the highest frequency of scent marking occurring
when the female was cycling. However, the highest frequency of scent marking occurred
when the female was paired with a male.

The increase in scent marking also parallels the similar changes in the apparent amount of
sebum produced by the scent glands. Although the total area of the scent gland does not
change, it appears to produce more sebum after the female was removed from her family
and paired with a male (French, 1982; Savage et al., 1989). Thus, it appears that the scent
glands are fully developed in females by the age of 20 months but require the stimulation
of elevated levels of estrogen to produce sebum and a darkening of the pigment (Savage
et al., 1989).
Vocalizations Cotton-top tamarins have a highly developed vocal repertoire (Cleveland &
Snowdon, 1982) with at least 38 distinct vocalizations. They have specific vocalizations
for alarm, food, levels of aggression, and submission. Tamarins possess a rudimentary
syntax and grammar and it has been suggested that infant cotton-top tamarins go through
a "babbling" or practice stage as they learn the appropriate vocalizations (C. Snowdon,
pers. comm.). A copy of the "Vocal Repertoire of the Cotton-top Tamarin" is available on
loan from the Wisconsin Regional Primate Research Center Library (1223 Capitol Ct.,
Madison, WI 537151299 phone 608 263 3512).

III Reproduction
Chapter Summary

 Average inter-birth interval in captivity: 29 weeks

 Gestation length: 183 days
 Length of ovarian cycle: 18-20 days
 Each family consists of one reproductively active male and female and their
offspring.
 Fertility of daughters is suppressed while they remain in their natal group.
 Exposure to a novel male is necessary to release a female from reproductive
suppression.
 Experience caring for at least one, but preferably two litters of younger
siblings is necessary before pairing with a mate for both males and females.

Reproductive Patterns

Cotton-top tamarins have a high capacity for rapid reproduction in captivity. There have been
extensive studies of female reproductive physiology but very little is known about male reproductive
physiology. Females generally give birth to twins (80%), although singletons are also frequent (18%,
Snowdon et al, 1985).

Occasionally, cotton-top tamarins give birth to triplets (2%, Snowdon et al., 1985), but they rarely
raise all three offspring without human intervention. The gestation length for this species is 183.7 ±
1.14 days (Ziegler et al., 1987a). The first postpartum ovulation occurs within 27.3 ± 0.51 days for
females that give birth to twins, and 16.0 ± 0.75 days for females that give birth to singletons
(Ziegler, 1987a). Unlike many other primates, the postpartum ovulation can, and often does yield a
successful pregnancy. Eighty percent of the first postpartum ovulations result in a new pregnancy
(Ziegler, 1987a). Thus, in successful captive breeding colonies of cotton-top tamarins the average
inter-birth interval is 29 weeks (Snowdon et al., 1985).

Cotton-top tamarins do not exhibit seasonal patterns of reproduction in most captive colonies housed
under artificial lighting and temperature conditions. In wild populations, there is usually a seasonal
birth peak associated with the onset of the rainy season (Savage, 1990; Savage et al., 1996).
However, wild-caught captive groups kept in outdoor enclosures in their native habitat have inter-
birth intervals similar to the 29 weeks found in the captive colonies suggesting that diet may regulate
fertility in the wild (Savage, 1990).

Ovarian Cycle

The ovarian cycle of the cotton-top tamarin is approximately 20 days in length (Brand,
1981; French et al., 1983; Ziegler et al., 1993). There are no physical signs of ovulation
that are readily detectable by human observers, however studies have shown that there are
olfactory cues in the scent secretions and urine of female cotton-top tamarins that are
readily detectable by their mates (Ziegler et al., 1993). Copulations are not restricted to
the time of ovulation, as evidenced by the continuous receptivity of females to males
throughout the entire reproductive cycle (French, 1984; Savage et al., 1988).

Puberty and Puberty Acceleration

Although the onset of puberty is between 15-17 months in cotton-top females that remain
in their natal group, it can be accelerated by exposure to a novel male to as early as 10
months (Ziegler, 1987b). Females removed from their natal group at an early age and
paired with an unfamiliar adult male will exhibit an acceleration of puberty and the rapid
onset of ovarian cycles (French et al., 1983; Ziegler, 1987b). However, at this early age,
most females have not had sufficient infant caretaking experience to successfully raise
their own offspring. Thus, although a cotton-top female may be physiologically mature at
10 months of age, she lacks the social experience necessary to successfully rear her
offspring.

Suppression of Fertility

The reproductive biology of the female cotton-top tainarin is significantly influenced by

her social environment. As long as a female (daughter) remains in her natal group, her
ovarian cycles will be suppressed. Suppression of fertility in the natal group has been
observed in cotton-top females as old as 44 months (French et al., 1984). Although
suppressed females do have detectable levels of estrogen and luteinizing hormone,
indicating that they are reproductively mature, their hormones are at unusually low levels
and are acyclic. Removal from the family and pairing with an unfamiliar male is
necessary to initiate normal ovarian cycles in cotton-top females. Although isolation from
the natal group elevates hormone levels, normal ovarian cycles are not established until
the female is paired with a novel male (Savage et al., 1988; Widowski et al., 1992;
Ziegler, 1987b). Although close (within 15 cm) exposure to a novel male, including a
combination of auditory, olfactory and particularly visual contact may be enough to
stimulate ovulation in most cotton-top females, auditory and olfactory contact alone are
not enough to stimulate ovulation (Widowski et al., 1990; 1992). Scent secretions mixed
with urine from the natal group will delay the initiation of normal ovarian cycles (Savage
et al., 1988). However, once normal cycles are established, they cannot be suppressed by
exposure to scent secretions (Savage et al., 1988).
Reproductive Senescence

Older (14-16 years) cotton-top tamarin females may experience some irregularity of
cycles, yet true reproductive senescence does not begin until approximately 17 years of
age (Tardif & Ziegler, 1992). Although cotton-tops over 17 years are anovulatory,
hormone levels are moderate and the steroidogenic luteal cells are still functional, despite
a lack of follicular development (Tardif & Ziegler, 1992). This is substantially different
from the pattern in Old World primates, where the cessation of follicular development in
reproductive senescence is associated with substantial decrease in steriodogensis (Tardif
& Ziegler, 1992). Although testosterone levels and sperm counts have not been
systematically evaluated in this species, males appear to be capable of siring offspring
throughout their lifetime, with little evidence of reduced fertility with age.

Contraception

The Cotton-top Tamarin SSP in coordination with the AZA Contraception Advisory
Group have recommended certain methods for contracepting cotton-top tamarin females.
Development and testing of effective means of contraception for this endangered species
continues to occur. Cooperation in providing information that allows the evaluation of the
current contraceptive recommendations is desperately needed. Please refer to Appendix 1
in the Veterinary Care chapter.

Any cotton-top tamarin female who is to be contracepted should receive the MGA
implant available from Dr. Ed Plotka (for order form, refer to Appendix 2 in the
Veterinary Care chapter). If the female recommended for contraception is pregnant, she
should be given 10 mg/kg DepoProvera within 10 days postpartum. Once the infants are
weaned (14-16 weeks), an MGA implant can be inserted. If an adult female is in a family
group that contains daughters and must be contracepted, do not remove her from the
group for more than 24 hours, as daughters may compete with their mother for the
breeding position upon her return. Daughters greater than 14 months of age who are in
groups containing an unrelated breeding adult male should receive an MGA implant for
as long as they remain in the group.

IV Infant Development
Chapter Summary

 Average birth weight of infants in captivity:40-50g.

 Daytime birth usually indicates distress.
 Parental care is learned in cotton-top tamarins. Both males and females
should have early infant caretaking experience with at least two litters of
siblings prior to their own reproduction.
Parturition

Parturition in cotton-top tamarins usually occurs in the evening between 1730-2040 hr

(Adler, 1988; Price, 1990) and lasts one to two hours. Females have been found to give
birth regardless of whether or not a light is on in the enclosure area. A litter typically
consists of twins, although singletons and triplets are born on occasion. An average
newborn weighs approximately 40-50 g (Dronzek et al., 1986).

The five stages of birth designated by Price (1 990) and Stevenson (I 976) are as follows:

Stage 0: The mother appears restless immediately before abdominal contractions begin,
frequently changing her position and sometimes reacting irritably to other family
members. This stage is reported to last for at least 20 minutes.

Stage 1: Contractions begin and the first infant appears. Primiparous females may seem
more distressed during this time than multiparous mothers. Females usually remain in or
near the nest box but sometimes move around the enclosure, not engaging in social
interactions. Characteristic postures include a quadrupedal stance with hind legs splayed,
or semi-upright squatting position, sometimes with hands on a support. Just before labor a
female raises her tail, as if about to defecate; this position is a reliable indicator of the
onset of delivery. This stage typically lasts about one hour.

Stage 2: The infants are expelled completely. This stage typically lasts for 2 to 9 minutes,
depending on the number of infants born. A breech birth will considerably prolong this
period of delivery and frequently results in suffocation of the infant.

Stage 3: This is the interval between the expulsion of the infants and the delivery of the
placenta, lasting about 5 minutes.

Stage 4: The placenta is consumed, usually by the mother. Frequently the father
participates, and occasionally the offspring may eat small pieces. This stage last
approximately 12 minutes.

It is rare that females give birth during the day or within public view. Most labors
observed during daylight hours signify a female in distress. If a female is observed in
labor for greater than I hour, it is likely that she will not be able to deliver her infants
vaginally. Consult a veterinarian to determine whether a cesarean section is necessary. In
most cases, a female that has had a cesarean section can deliver future infants vaginally.

During the first hour after birth infants are generally carried dorsally by mothers,
although fathers sometimes assist in carrying. Occasionally an infant falls after delivery;
so it is wise to cover the floor of the cage with a soft substrate such as a mat, shavings, or
some straw. Any member of the family may retrieve the fallen infant. Usually several
group members will investigate the newborn until one of them succeeds in retrieving the
infant (Price, 1990). Occasionally, an infant will be rejected by the family group during
the first few days of life. Factors resulting in rejection of offspring will be discussed
below.

Postnatal Care

Parity and Sibling-Rearing Experience of Parents

Parental care is not instinctual in cotton-top tamarins, it is learned. Thus, to ensure a

self-sustaining captive breeding population, young tamarins must be provided with
opportunities to assist in the rearing of their siblings. Animals denied the opportunity of
carrying an infant on their back prior to their own reproduction, will be incompetent
parents. Both males and females must be provided with early infant caretaking experience
to ensure reproductive success (Cleveland & Snowdon, 1984; Snowdon et al., 1985;
Tardif et al., 1986; 1990; 1992).

Since parental care is shared by all group members, non-reproductive cotton-top tamarins
develop parenting skills, while in their natal family group, by carrying and interacting
with younger siblings. In order to gain this experience, an individual should remain with
its family group for at least two litters. Studies have shown that animals 7-14 months are
the primary play partners for the new infants. Animals greater than 14 months are more
involved in carrying infants (Cleveland & Snowdon, 1984).

Infant rejection is most common in animals not properly socialized. Both males and
females denied early infant caretaking experience have the highest probability of
rejecting and/or killing their offspring. Efforts to increase the likelihood of parental care
has not met with much success. Males with early infant caretaking experience have been
paired with inexperienced females and visa versa. Neither of these pairings, based on
previous infant caretaking experience, have led to a high probability of rearing their own
offspring, but such a combination may result in a higher success rate than two
inexperienced parents together.

The Role of Non-reproductive Helpers, Fathers, and Mothers in Infant Care

While mothers seem to be the primary caregivers during the early weeks of life, fathers
and older offspring play an important role in infant rearing as development proceeds
(Cleveland & Snowdon, 1984). Not only is it important for siblings to gain experience in
caring for infants, but it is believed that the mother relies on these non-reproductive
helpers, as well as on fathers, to share the burden of infant care. The frequency of
twinning, a high infant to adult body weight ratio for this species, as well as, the energetic
costs of pregnancy and lactation may be responsible for the active role of siblings and
fathers in infant care (Cleveland & Snowdon, 1984; Tardif et al., 1986).

Figure 1 illustrates the differences in the rate of carrying infants for all groups members
(see Tardif et al., 1990 for a complete review). Mothers and fathers are the primary
carriers of the infants in the first two weeks of life, but then the mothers' participation in
carrying drops off, while fathers continue to carry as much or more. As the breeding
female carries her infants less, non-reproductive helpers carry more, until the infants gain
independence at about 10-15 weeks. Furthermore, carrying time increases with the age of
the carrier. Offspring over the age of 14 months carry the most, while those offspring less
than 7 months of age rarely carry the new infants.

The size of the family group appears to affect the amount of time that parents spend
carrying infants. One study reported that as group size increased, mothers spent less time
carrying (Cleveland &Snowdon, 1984), although other studies report a different finding;
more helpers resulted in a decrease in paternal carrying, but not maternal carrying (Tardif
et al., 1990; Price, 1992). Price (1992) also found that singletons spent less time off
carriers than twins, starting at week 5, but this difference

Figure 1. Carrying rates of individuals in a family- From Tardif et al., 1990.

disappeared by week 10, as both singletons and twins became more

independent. While the gender of the infants does not affect how much they were carried
by any family member, Cleveland & Snowdon (I 984) found males to participate in
carrying infants more than females.

Infant Development

Cotton-top tamarin infants develop quite rapidly (Figure 2). Infants nurse throughout the day in the
first weeks of life. Infant status (singleton or twin) and gender have no effect on the amount of time
spent suckling (Price, 1990). Predictably, as nursing decreases over time (reaching minimal levels
around week 20), food begging increases. Cotton-top tamarin infants take their first steps away from
their caregivers between weeks 4-5 and the first intake of solid food occurs during week 6
CLE LAND & SNOWDON: TAMARIN SOCIAL DEVELOPMENT

Figure 2. Temporal changes in behavior over the first 20 weeks of life: (A) Carry and Contact behavior, (B)

Solid Food Intake and Nursing, (C) Time off from group members, (D) Solitary, Social, Wrestle and Other

Play. From Cleveland & Snowdon, 1984.

(Cleveland & Snowdon, 1984). Typically, infants beg for and receive food from all
family members. Parents share more food items than offspring, and younger siblings
share less than older siblings. In general, males tend to share food with infants more
frequently than females (Cleveland & Snowdon, 1984: Price 1990). Overall infants in
larger family groups receive more food than those in smaller groups (Price, 1992).

Non-reproductive helpers are also responsible for playing with new offspring. Social
play consists of wrestling, hang-wrestling, back-hugging, chasing, batting, biting, mutual
investigation, and vocal play. This is in contrast to solitary play, which is "any
exploratory behavior involving manual or oral investigation of an object that can be
performed alone (e.g. swinging on rope, chasing tail, chewing wood and twine)"
(Cleveland & Snowdon, 1984). Both forms of play begin at around 6-8 weeks and
increase as the infant develops.

In one study, parents and adult offspring were rarely observed playing with infants, while
subadults, juveniles, and twin partners spent respectively greater amounts of time
engaged in social play. Most of this play consisted of wrestle play. Twins spent more time
engaged in all forms of play than singletons (Cleveland & Snowdon, 1984).

Hand-rearing and Reintroducing Rejected Infants

(For a complete review of hand-rearing techniques, see Dronzek et al., 1986)

Due to a fairly high rejection rate, especially among first litters, hand-rearing techniques
have been developed for cotton-top tamarin infants which have been abused or neglected
by their original family groups. The methods described below consist primarily of using a
mechanical surrogate, a non-human primate infant formula, and, most importantly, a
gradual process to reintroduce the infant to a social group.

Usually rejection occurs within the first few days postpartum; family members will either
ignore or harass an infant until it dies or is removed. If an infant has been abandoned or
rejected within the first 3 days of life, it is imperative that the infant be removed from the
social group. Infants rejected during this time have not nursed and are often dehydrated. It
is also important during the hand-rearing process to minimize human contact with the
infant. A hand-reared infant which is accustomed to being in contact with and cared for
by humans will be hindered in its normal social development.

Surrogates: A candidate for hand-rearing is placed on a suspended surrogate in an

incubator with a constant temperature of 32.2'C for two days. The temperature is
decreased gradually to 26.7'C during the first week. Relative humidity is maintained at
70-80%. The surrogates are constructed from a 23 cm x 13 cm piece of 1/4" mesh
hardware cloth which is formed into a cylinder. A 50 cm heating cable is attached in
loops to the interior, while the exterior is covered with artificial brown fur. The heating
cable provides heat to the infant, although the main source of heat is from the incubator.
In the case of an adult tamarin death, the skin is saved, treated non-toxically, and sewn
directly onto the artificial fur. Surrogates are made mobile by attaching them to the top of
the incubator with 30 cm elastic bands. This provides a bouncing movement when the
infant moves. A rocker is also used for additional motion. The rocker's motor has a
reciprocating arm with a 1 1/4" throwing distance. The motor is mounted outside the
incubator on a piece of plywood, and a piece of plastic-insulated wire is run from the
reciprocating arm to the elastic band of the surrogate.

SURROGATE DIAGRAM
Figure 3. The diagram illustrates the construction of the mobile surrogate. The heating cable is looped inside the wire mesh, and the wire mesh is completely
covered by artificial fur and tamarin fur. From Dronzek, et al., 1986.

A feeding surrogate is made from a 13 cm x 17 cm piece of 1/4" mesh hardware cloth

which is covered with artificial fur and formed into an arc of diameter 6 cm. A 2 cm hole
is cut near one end which allowed the insertion of a nipple through to the front of the
surrogate. The infant is encouraged to climb onto the feeding surrogate and search for the
nipple.

Nipple construction: Formula is fed to infants through a nipple attached to a 3 cc

syringe. Nipple construction was based on the design of Dr. James Ogden, Rush
Presbyterian-St. Lukes Medical Center, Chicago, EL. A 25 gauge disposable needle cut to
a length of 0.5 cm is attached to a 3 cc disposable syringe. The needle and syringe
together are dipped alternately in glacial acetic acid and latex. This is done two or three
times, always beginning and ending with acetic acid, so that the nipple will be strong and
thin enough. After dipping, the needles are dried upright for one hour and then submerged
in water for 24 hours. They are then removed from water, dried, and small holes are
formed at the tips.

Feeding Procedure: The diet consists of a non-human primate formula (Primilac,

Bioserve, Inc., Frenchtown, NJ) which is prepared fresh daily in the amount needed. See
Table 1 for feeding schedule described in Dronzek et al., (1986). During the first two
days of life, formula is diluted to 50% to allow the digestive system a slow introduction to
the formula. After that, formula is given at full strength. Before feeding, the formula is
warmed to 37'C, and any bubbles are expelled from the syringe. The infant is fed on the
feeding surrogate described previously. The formula is expelled slowly from the nipple so
that the infant can nurse at its own rate. It is important that the formula be administered
slowly to avoid aspiration of the fluid in the lungs. After feeding, the infant's anogenital
region is wiped with a warm water soaked gauze pad to stimulate urination and
defecation. This procedure is discontinued after 20 days, when the infant can defecate and
urinate spontaneously. The mechanical rocker is switched on for short intervals after
feeding to simulate carrying motion as well as to prevent bloating.
Gradually the infant is weaned from formula and introduced to solid foods, beginning
with yogurt which is added to the formula. The infant is then encouraged to lap
formula/yogurt mixture from a bowl. By day 33, only the bowl is used, and gradually
other solid foods are introduced. Once the infant is able to eat independently,
reintroduction into a family group begins. After the infant is integrated to the family
group, supplemental feedings of yogurt, Iiigh-protein Gerber baby cereal, mashed egg or
fruit (bananas, applesauce, apples, pears), and a vitamin supplement (Hi Vit, FYSCO
Pharmaceutical Corp, Buena, NJ) are continued twice daily until the infant is three
months of age.

Treatment: An infant with lacerations or bite wounds receives a treatment of 3 ug/kg

body weight of long-acting penicillin (Longicil, Fort-Dodge Laboratories, Inc. Fort
Dodge, IA). Lacerations or bite wounds are cleaned and treated with a topical

Table 1. Feeding Schedule (from Dronzek et al., 1986)

Duration Number of
Amount of Formula/Food Offering per
Day of Life between Feedings
Feeding
Feedings per Day

1-4 1.0-1.4 ml Primilac 2 Hours 9

5-8 1.501.9 ml Primilac 2 Hours 9

9-16 2.0-2.4 ml Primilac 2 Hours 7-8

17-20 2.5-2.9 ml Primilac 2.5 Hours 6

21-24 3.0-3.5 ml Primilac 3 Hours 6

25-30 3.7-4.4 ml Primilac 3.5 Hours 5

31-33 4.6-5.7 ml Primilac, 1.0ml yogurt 4 Hours 4

5.8 ml Primilac, 1.0-1.5 ml yogurt/ Gerber

34-36 4 Hours 4
high-protein baby cereal

5.8 ml Primilac, 1.5-2.5 ml yogurt/Gerber

37-39 high protein baby cereal/egg or fruit mash 4 Hours 4
(banana, applesauce, apples, pears)

7.0 ml Primilac, 2.5-3.5 ml Gerber high-

4-5
40-46 protein baby cereal/yogurt/ fruit and egg 3
Hours
mash

5.0 ml Primilac, 3.5-4.0 ml yogurt/Gerber

47-53 high-protein baby cereal/fruit and end egg 8 Hours 2
mash

Primilac gradually decreased by 1.0ml

each day. Hill's ZuPreem Marmoset diet
54-60 8 Hours 2
starts on day 54. Gradually solid foods
increased.

60-90 Supplemental feeds of 1/4 cup yogurt, 2

 Gerber high-protein baby cereal/egg mash

antiseptic. If an infant is dehydrated, an injection is given of equal parts 10% dextrose and
electrolyte solution at a volume equal to 10% of the infant's body weight. Any infant who
experiences bloating or diarrhea is put on a formula which consists of equal parts oral
electrolyte solution and Primilac.

Reintroduction: Generally infants are not reintroduced to their natal family group, but
into another family that can provide both social and infant care experience. While still in
an incubator (2-3 weeks), the infant is exposed to its adoptive family for 2-3 hours daily.
The incubator should be placed in front of the adoptive family so the infant and family
can have visual and auditory contact.

When the infant can thermoregulate, at about 3-4 weeks, it is placed on a surrogate in a
reintroduction cage outside the adoptive family's cage. The reintroduction cage, which
maximizes visual contact, is constructed from 1/4" mesh hardware cloth and wood, and
measured 41 cm x 43 cm x 41 cm. The cage should contain a variety of branches and
runways so that the infant can locomote freely. In the beginning, the infant should spend
one hour each day in the cage. Gradually the time spent in the cage is increased to 8-9
hours daily, but the infant should always be returned to the incubator in the early evening.

During the fourth week of life, the reintroduction cage is placed inside the adoptive
family cage, approximately 1.0-1.5 m above the floor. Family cages should range from a
minimum size of 0.85 m W x 1.5 m L x 2.3 m H to a maximum size of 1.8 m W x 3.0 m
L x 2.3 m H (Dronzek et al., 1986). Branches and runways are added to allow the family
to approach the infant in the reintroduction cage. Thus, the family is able to investigate
the infant without having direct contact. The infant remains in the reintroduction cage
with its surrogate and is no longer returned to the incubator.

During weeks 5 and 6, the infant with its surrogate is removed from the reintroduction
cage and placed on top of the nest box in the adoptive family cage during the day, but
returned to the reintroduction cage at night. The infant is observed continuously for the
first day, and then if the family shows no aggression toward the infant, and the infant
does not appear distressed, observation time is gradually reduced to once every 30
minutes. At first, the infant spends a few hours out of the reintroduction cage, but by
week 6, it spends the entire day on the nest box. During weeks 6-8, if the infant does not
voluntarily leave the surrogate, the surrogate is removed for short periods of time (10
minutes). As the infant becomes less anxious, the surrogate is removed for longer periods
of time, until the infant spends most of its day without the surrogate. The surrogate is
replaced in the evening until the infant rejects the surrogate (8-10 weeks) and sleeps with
the family. If by week 10 the infant has not rejected the surrogate, the surrogate is
removed permanently. The infant is generally observed sleeping with the family the same
night.
The most important part of any hand-rearing program is the reintroduction to a
family. Infants should not be reintroduced to parents that do not have early infant
caretaking experience. Typically, if parents denied early infant caretaking experience
rejected their own infants at birth, they will do so again, if you reintroduce their offspring
to them. It is rare that incompetent parents can be rehabilitated. Therefore, a hand-raised
infant must be incorporated into a stable, reproductively active, family if it is to have a
normal social development. This is crucial so that the infant can gain sibling-rearing
experience. The best results are obtained when the infant and adoptive family are
introduced to each other gradually, allowing time for mutual habituation. The infant
should be housed near the adoptive family while in the incubator as early as possible.
Furthermore, reintroductions appear to be most successful when the adoptive families
consist of subadult siblings and at least one juvenile older than ten months. The older
siblings are important because they carry and share food with the introduced infant, and
the juvenile is influential in initiating play. Dronzek et al., (I 986) found that if an infant
younger than ten months was present in the family group, it tried to initiate play with the
hand-reared infant, who often became distressed. At that point the family sometimes
acted as if the hand-reared infant was a threat to their infant and became aggressive. If a
family does not accept a hand-reared infant, it is possible to reintroduce it to another
family, or, as a last resort, to a single adult.

Social Structure

Although there is much debate about callitrichid social organization (Price & McGrew,
1991; Savage & Baker, 1996), cotton-top tamarins are successfully housed as
monogamous breeding pairs and their offspring in captivity. This choice of social
structure is the result of many years of investigating reproductive strategies of wild and
captive callitrichids (see Snowdon, 1989). Studies attempting to integrate adult animals
into existing stable families have failed since intruding animals are met with intense
aggression by resident animals (de la Ossa et al., 1988; French et al., 1984). However,
evidence of deviations from monogamy in captivity (Price & McGrew, 1991) and in the
field (Savage et al., 1996) have been observed. Multiple breeding females within groups
are common when their is some disruption within the breeding pair or group (death of a
mate, introduction of a step-parent, immigrating adult male) (Price & McGrew, 1991;
Savage, 1990; Savage et al., 1996).

Alternative Housing Options

Due to breeding recommendations and the variation found in the population, cotton-top
tamarins can be housed in a variety of social conditions other than the standard breeding
pair/family group.

Father + offspring (e.g. after the death or removal of the breeding female). This social
grouping generally remains stable. Most daughters remain reproductively suppressed
under these conditions, however, there have been noted exceptions. Daughters over 14
months of age should be contracepted if they appear to have 1) a highly active scent gland
(darkly pigmented and secreting sebum); 2) are actively scent marking their environment;
3) are observed copulating with a male.

Mother + offspring (e.g. after the death or removal of the breeding male). This
social grouping generally remains stable. The breeding female will continue to cycle and it is rare that copulations are
observed. However, if copulations between mother and sons are observed, the female should be contracepted.

Iso-sexual groupings Housing same sex pairs of animals is fairly routine for animals that have
been reared in family groups. Hand-reared or improperly socialized animals may not be
appropriate for this type of grouping. In general, do not pair more than two unrelated
animals. However, sibling groups larger than two animals are generally successful.

Single sex-mixed callitrichid group A single cotton-top tamarin can usually be

successfully housed with a single individual of another callitrichid species. A common
marmoset (C. jacchus), golden-head lion tamarin (L. chrysomelas), and Goeldi's
marmoset (Callimico goeldii) have been successfully housed with a single cotton-top
tamarin (L. Pastorello, pers. comm.). Individuals of the same sex are recommended for
pairing.

Within Group Aggression

Fighting within groups resulting in the removal of individuals is not atypical for cotton-
top tamarins. Typically, in family groups aggression tends to be directed toward natal
rather than breeding individuals; aggressors are usually the same-sex parent or siblings
(McGrew & McLuckie, 1986). Fights between same-sex twins have been observed,
although the majority of aggression in stable family groups tends to be between the eldest
male siblings (S. Evans, pers. comm.; A. Savage, pers. comm.). Most of the aggression
between individuals begins slowly, but has been known to rapidly escalate and culminate
in death. The age at which aggression and resulting eviction of natal individuals from the
group occurs is variable and unpredictable.

Aggression between Eldest Male Siblings is most common in stable family groups. As
group size increases due to high birth rates in this species, fighting between the two eldest
male siblings is common. Interestingly, the rest of the group members appear to ignore
the tension between the two animals. Low levels of aggression are most common initially,
(displacement at the food dish, rough play, chasing, mounting) but generally escalates to
one individual dominating the other. The subordinate sibling emits submissive
vocalizations constantly (squawks, see Cleveland & Snowdon, 1982) and typically avoids
contact with the dominant sibling. The victim may also show fearful behavior upon being
approached by the dominant individual and often stays lower than normal in the exhibit.
It is recommended that the sibling harassing the subordinate sibling be removed from the
family when this is observed before any severe fighting develops. Do not attempt to
reintroduce this animal to the group.
Aggression between Father and Male Offspring-occurs m stable family groups, but is
most often observed when there has been some change in the environment. Moving
animals to new exhibits or introducing another species to residents can often result in
group disruption. Fathers can behave very aggressively toward their offspring, often
resulting in severe fighting. The offspring should be removed and no attempts to
reintroduce the offspring to the group should be made.

Aggression between Females is relatively rare and most commonly occurs when there is
a disruption in the environment (see above). Daughters have been observed to challenge
their mothers (mounting, harassing, displacing) but, unless the mother is old or impaired,
she will usually defend her position in the group. Daughters should be removed from the
family group only if the mother is becoming aggressive. Most daughters can live in stable
family groups for many years. Evictions of sons are much more frequent than daughters
in most captive cotton-top tamarin groups.

Social Behavior

There have been extensive studies of the behavior of cotton-top tamarins in captivity and
in most recently in the wild. Studies have shown that most captive cotton-top tamarins
live in monogamous pairs. Newly formed pairs of cotton-top tamarin show increased
affiliative behavior and are observed to engage in sexual activity more frequently than do
established breeding pairs (French et al., 1984; Savage et al., 1988; Tardif, 1984a;
Widowski et al., 1990). This increase in affiliative behavior occuring when the female
was removed from the family and paired with a male appears to be important in
establishing the pair bond in this species. However, as the duration of the pair bond
increases, affiliative behavior and scent marking decreases (Savage et al., 1988). This
decrease has been attributed to the addition of offspring to the group. Established
breeding pairs often spend less time in affiliative behavior with one another and direct
more of their attention toward their offspring (Savage et al., 1988). Nonetheless, the pair
bond appears to be strong in these animals as intruders are attacked (French & Snowdon,
1981) and territorial displays between cages in large colony rooms of tamarins are
frequent when visual contact between groups is allowed.

Scent Marking Cotton-top tamarins have highly developed anogenital and suprapubic
scent glands (see French & Cleveland, 1984 for a complete review). Both males and
females are observed to scent mark, however, females scent mark significantly more than
their male counterparts. The function of scent marking has been widely debated. Studies
have suggested that scent marking does have a communicatory function in callitrichids
(see Epple, 1975; Ziegler & Bercovitch, 1990). Rates of scent marking differ between
cycling and non-cycling females. Newly paired cotton-top tamarin females showed a
dramatic increase in rates of scent marking, rates much higher than those observed when
females lived with their families or in isolation (French et al., 1984; Savage et al., 1988).
Savage et al., (1988) and Widowski et al., (1990) found a positive correlation between
estrogen activity and frequency of scent marking. Increases in scent marking paralleled
increased in estrogen activity, with the highest frequency of scent marking occurring
when the female was cycling. However, the highest frequency of scent marking occurred
when the female was paired with a male.

The increase in scent marking also parallels the similar changes in the apparent amount of
sebum produced by the scent glands. Although the total area of the scent gland does not
change, it appears to produce more sebum after the female was removed from her family
and paired with a male (French, 1982; Savage et al., 1989). Thus, it appears that the scent
glands are fully developed in females by the age of 20 months but require the stimulation
of elevated levels of estrogen to produce sebum and a darkening of the pigment (Savage
et al., 1989).

Vocalizations Cotton-top tamarins have a highly developed vocal repertoire (Cleveland

& Snowdon, 1982) with at least 38 distinct vocalizations. They have specific
vocalizations for alarm, food, levels of aggression, and submission. Tamarins possess a
rudimentary syntax and grammar and it has been suggested that infant cotton-top
tamarins go through a "babbling" or practice stage as they learn the appropriate
vocalizations (C. Snowdon, pers. comm.). A copy of the "Vocal Repertoire of the Cotton-
top Tamarin" is available on loan from the Wisconsin Regional Primate Research Center
Library (1223 Capitol Ct., Madison, WI 537151299 phone 608 263 3512).

V Captive Management
Chapter Summary

 Only one group of tamarins should be housed in an exhibit. If there a re

more than one group of tamarins in your facility they should be visually
isolated from one another.
 Cotton-top tamarins in naturalistic, mixed species exhibits provide an
exciting education experience for the visitors.
 Cotton-top tamarins should be maintained at 25-29 C (76-85 F) with 50-
70% humidity and on a 12L:12D light cycle.
 Providing enriched environments where animals can acquire and retain the
behavioral skills they would need to survive in the wild should be strongly
encouraged.
 A list of live plants for use in cotton-top tamarin exhibits and toxic plants to
avoid using is provided.

Housing in Captivity

Cotton-top tamarins have been housed in research institutions and zoos for several
decades. Considerable information is currently available on techniques for maintaining
cotton-top tamarins in captivity that considers not only the physical but psychological
well-being of this endangered species.
Caging In research institutions, cotton-top tamarins have been housed in cages that range
in size from 0.2 m'- 12m' (Evans, 1983; Gengozian et al., 1978; Hampton et al., 1978;
Kilborn et al., 1983; Kirkwood et al., 1983; Ogden et al., 1978; Snowdon et al., 1985;
Tardif et al., 1984a;b). Variability in reproduction and infant survival has been seen in
most research colonies. The most successful colonies have large complex cages and
animals that have been properly socialized (see Snowdon et al., 1985 for a complete
review).

In zoos, cotton-top tamarins have been housed in cages that range in size. The smallest
recommended cage for a family group of tamarins is at least 3L x 2W x 2.5Hm. It should
be noted however, the larger the cage or exhibit, the greater probability of housing large
families with minimal disruption in the group.

Only one pair/family should be housed in a cage/exhibit. If more than one group of
tamarins is present in your facility, it is critical that they are visually isolated from one
another. If pairs/families can see their neighbors, territorial behavior (vocalizing,
piloerection, displaced aggression) will follow. Since the groups cannot resolve the
encounter appropriately, it is very common to see displaced aggression in the group. One
animal, usually the adult male, will begin to chase or attack another conspecific in his
group, while repeatedly directing his attention to the neighboring group. Placing opaque
barriers (heavy curtains, kalite, etc.) between groups is sufficient to inhibit this behavior.
However, it is critical that the barriers are monitored to ensure that the tamarins cannot
see one another. Olfactory and auditory contact with neighboring groups does not cause
significant disruption in the behavior or reproduction of cotton-top tamarins in captivity.

Construction Materials Cages should be constructed on non-toxic materials and either

glass or wire fronted. Naturalistic exhibits have tremendous educational benefit for
maintaining and displaying natural behavior to the public.

Substrate The use of soil, wood shavings, or other natural absorbent materials such as
bark or mulch that can be removed for appropriate hygiene is most appropriate. A solid
substrate is not recommended since infants and young animals may be injured in a fall.
Animals should not be encouraged to forage on the floor of the exhibit since they will
likely be exposed to more pathogens. Encouraging foraging on the exhibit floor is not
recommended since wild tamarins are rarely, if ever, observed foraging on the forest
floor.

Cage Furnishings Cages should be filled with a high density of natural branches and vines
or ropes. The branches and vines/ropes provide a surface on which the claws can get a
good grip and should be arranged to give the animals a variety of textures, diameters and
degrees of firmness. Some branches may be quite solid and do not move when an animal
lands, other branches may move. Branches should be placed at least one meter or more
above ground level to simulate an arboreal environment. Branches, nest boxes, etc.
should be cleaned occasionally to allow retention of odors and scent marks in the cage.
However, changing the structure of the environment by adding new branches or
rearranging old branches is suggested every 4-6 months to force animals to plan new
travel routes.

Plants Developing a naturalistic exhibit for the tamarins is encouraged whenever possible.
Exhibits filled with lush plantings are beneficial for the visitors and also the tamarins.
However, please be aware that some plants are toxic to primates. Table I lists plants that
have toxic properties and should be avoided. (For additional information on toxic plants
see AZH & AAZV 1992 Toxic Plant Survey; Fowler, 1981).

Nest boxes Each cage should have a minimum of one nest box measuring at least 30 x 30
x 30 cm with a 10 x 15 cm hole cut in the middle of the box. The hole is large enough to
accommodate an adult animal carrying an infant on its back to enter with ease. In
addition, a hinged top is suggested to facilitate ease of cleaning the nest box. Wooden
nest boxes with simple sliding doors may allow for easy capture when the animals have
gone to sleep for the night. Place the nest box at least 1.5 m from the ground. There
should be several branches leading to and from the nest box.

Feeding and Watering Stations At least one, but preferably two feeding stations are
recommended, especially for large groups of tamarins. Feeding stations should be placed
at least 1.5 m from the ground. Tamarins should be fed at least twice a day (see nutrition
section for more details.) Avoid placing branches directly above feeding and watering
stations to avoid contamination by feces and urine. Food and water dishes/bottles should
be sanitized daily to prevent a bacterial buildup.

Water should be provided ad lib. Tamarins can easily adapt to drinking out of a water
bottle. There are several benefits to using water bottles such as ease of administration of
medication, less contamination of the water, and monitoring water intake of pregnant
females. Pregnant females are known to consume large quantities of water when
pregnant. Although pregnancy may be difficult to detect in some females, an increase in
group water consumption in most family cages will usually indicate pregnancy.

Lighting and Photoperiod The light cycle should be maintained at 12L: 12D throughout
the year since there is little daily variation in the light cycle in the equatorial region of
Colombia. For those animals that do not receive Vitamin D3 in their diet, between 30-60
minutes daily of ultraviolet light is recommended. UV lights should be placed 1-2 m
above favored resting places, but not accessible to direct physical contact. Longer
exposure to UV lights may be harmful. However, access to direct sunlight is the preferred
method of obtaining Vitamin D3-

Temperature The temperature should be between 25-29'C (76-85'F) with between 5070%
humidity (Kilborn et al., 1983; Letcher et al., 1992; Scullion et al., 1987).

Outdoor Exhibits Cotton-top tamarins tend to thrive in outdoor exhibits as long as the
temperature remains within the suggested range. Supplemental heating can be provided
near the nest box on cooler days. However, the tamarins should not remain outdoors
without access to a ready heat source (i.e., indoor heated enclosure) for extended periods
if the temperature falls below the recommended range.

Free-ranging cotton-top tamarin exhibits have been quite popular and

successful in zoos (see Price, 1992 and Savage, In press) A group of tamarins has been
released at the Jersey Wildlife Preservation Trust and at the Roger Williams Park Zoo.
Although this is a very popular exhibit for the zoo visitors, and undoubtedly an enriching
experience for the animals, it requires a significant amount of staff time and should only
be considered if there are individuals that can dedicate themselves full-time to this
project. For additional information on the support material and release program of the
Roger Williams Park Zoo contact Anne Savage.

Mixed Species Exhibits Cotton-top tamarins can be housed in mixed species exhibits with
some bird species, reptiles or amphibians and/or mammals. Mixed species are encouraged
as a way to display animals as you would find them in the wild and to conserve exhibit
space. Cotton-top tamarins have been successfully housed with sloths, prehensile tailed
porcupines, iguanas, tortoises, and agoutis. However, it should be noted that cotton-top
tamarins have been known to catch small birds in or near their exhibit.

Because of the potential transmission of Herpesvirus by squirrel

monkeys (Samiri), cotton-top tamarins should be housed at different sites and handled by
different keepers. For additional information see the Veterinary Care chapter of this
manual.

Environmental Enrichment Concern for the psychological well-being of captive cotton-

top tamarins is an important component in any animal management plan. In the wild,
cotton-top tamarins live in very complex environments requiring animals to locomote
through complex forest environments, learn how to acquire and process food, and avoid
predators. Simulating similar situations in captivity is of utmost importance (Snowdon &
Savage, 1989). The ideal captive environment is one where animals could acquire and
retain the behavioral skills they would need to cope successfully with their natural
environment were they ever to be released to the wild. Foraging devices are probably the
most effective means of enriching the lives of captive tamarins. Wild tamarins spend
more the 60% of their day foraging for food (A.Savage, pers. comm.).

Designing foraging devices that mimic the natural foraging habitats of wild tamarins is
most desirable. Feeders with small holes that allow crickets or mealworms to escape at
unpredictable times are an inexpensive, yet enriching option for these small primates. The
materials necessary for a feeder are a small piece of hollowed tree (e.g. Oak) about 4
inches in diameter, 1/2 inch dowel rod that is 8 inches long, PVC tube with twist cap and
approximately 18 inches of thin rope. The hollow of the tree should be me made large
enough to accommodate the PVC tube. Do not hollow out the tree so that it is open ended
on both sides, leave one side closed. When the PVC tube is secured within the log, drill
two 1/2 inch holes through the diameter of the cylinder. These holes should be made a
few inches from the closed end and the dowel should be inserted so that equal amounts of
it extend on either side. Additional small holes should be drilled through both the log and
the PVC tube. Drill a small hole through the twist cap of the PVC tube in which the thin
rope will be drawn through. Put crickets into the hollow space and secure twist top.
Suspend the feeder from the roof of the enclosure to simulate swinging tree branches.

Hanging baskets filled with shavings and small pieces of food or insects provide tamarins
with the opportunity to forage for much longer periods than if food was presented in a
food dish. Presenting whole food items (apple, orange, banana) attached to a stand/stick
will allow the animals to manipulate the large items into manageable sizes for
consumption.

It should be noted that all foraging devices or opportunities should be at least 1.5 m from
the ground. The tamarins should never be encouraged to forage on the floor of the exhibit,
since it is likely that they would quickly become prey items in the wild. Moreover, gum
feeding devices are designed for marmosets that have the appropriate dentition to gouge
holes. Cotton-top tamarins do not have the proper dentition to gouge holes and in the wild
tend to feed on sap opportunistically. They will feed on sap from a tree tapped by another
species.

There are many interesting articles on appropriate primate enrichment techniques. The
Shape of Enrichment, Laboratory Primate Newsletter, and Zoo Biology frequently
publish articles on enrichment opportunities for primates. For additional information or a
bibliographic listing of primate enrichment options contact the Primate Information
Center, Regional Primate Research Center, SJ-50, University of Washington, Seattle, WA
98195 or the Wisconsin Regional Primate Research Center Library, 1223 Capitol Ct.,
Madison, WI 53715-1299.

Pest Control Pest (rodents, cockroaches, feral domestic animals, etc.) should be
adequately controlled or eliminated since they are potentially a major cause of mortality
through predation or disease transmission.

Identification of Individuals Permanent identification of animals is strongly

recommended. Whenever possible, please use the recommended transponder chip
(Trovan, Infopet Identification System, Burnsville, MN). Tattooing with the
INTERNATIONAL STUDBOOK number is also appropriate. Animals should be
tattooed on the inner thigh. Hair dye can be used as a temporary means of identifying
animals when needed.

Sexing Individuals Sexing adult animals is a simple procedure. The male's scrotum and
penis and the female's large clitoris are easily distinguishable in adult animals. Correctly
sexing prepubescent animals can be confusing. When examining the genitals of an
animal, a female can be identified by examining the slit in the genital area. If there is only
a small slit at the tip, it is a male, if the slit runs nearly the length of the ventral surface it
is a female. Patterns of urination may also assist in correctly sexing individuals. Young
males tend to urinate a stream that may be slightly arced, while females urinate in small,
but frequent drops.

Capture Methods The easiest and least stressful method of capturing cotton-top tamarins
is to lock them in their nest box at night or early in the morning before daylight.
However, if a particular individual needs to be captured, the following methods can be
employed. If the exhibit is not densely furnished with branches and vegetation, most
animals can be easily netted. Using a fine mesh net (0.5 cm or less) is recommended to
prevent the tamarin’s claws from becoming entangled in the net.

However, in lush exhibits, using a net is problematic since it tends to get caught

on the branches in the cage. The animals also become very stressed as they are chased
through the exhibit. A second method has been developed to alleviate some of the
common stress associated with capture. A keeper can enter the cage wearing thick
leather/suede gloves (welding gloves purchased from local hardware stores are
appropriate). Tamarins not habituated to this method of capture, will approach the keeper.
Using the element of surprise, the keeper can then quickly grab the tail of the animal with
one hand and use the other hand to grab the animal's body. Quickly release the tail, and
use both hands to secure the tamarin. Never attempt to hold the animal by the tail because
it is quite probable that you may injure the animal as well as receive numerous bites from
a very agile, angry tamarin! Also, make sure you are gently holding the animal with both
hands and supporting its body at all times.

Shipping Procedures

Animal shipment guidelines have been established by CIT'ES (Convention on

International Trade in Endangered Species), IATA (International Air Transport
Association), USDA (United States Department of Agriculture) and USFWS (United
States Fish and Wildlife Service).

General guidelines for shipping cotton-top tamarins are similar to those for golden lion
tamarins (Golden Lion Tamarin Management Committee, 1990)

Container Specifications Use a plastic airline approved shipping kennel (Skykennel) or a

non-toxic treated wooden crate. The size of the crate should be at least 50 cm wide by one
meter in length. Use screws, but make sure they do not protrude to the inside of the box.
Do not use nails.

All shipping containers need good ventilation. Make several 0.5 cm holes on both sides
and front of box. A second option requires 1/3 of the front and sides to be covered with 2
layers of 0.5 cm fine mesh, which will allow for good ventilation and prevent the
tamarins from probing their hands through the holes of the mesh. The wire mesh should
be covered with burlap to give the animals' privacy.
Attach handles on the side to carry the crate. The advantage to having the handles on the
side is it provides extra space for ventilation in case two crates are placed close to one
another. A device to create space for ventilation is mandatory when shipping animals.

All skykennels have swinging doors made of mesh. Make sure to cover the door with fine
mesh (0.5 cm) and burlap. When designing doors for wooden crates, it is best to use a
sliding door.

A second slatted, wood floor should be fastened to the original floor. Allow 0.5 cm
between the slats for urine and feces to drop through to the floor below. This spacing
decreased the chance of an animal getting its hand or foot caught. Please note that the
IATA regulations specifically require a removable dropping tray. Cover the floor with
absorbent material such as wood shavings. Attach a dowel 1 cm in diameter to the sides
of the crate for perching.

The shipping container must be labeled on the sides and top as to which side is up (use
arrows to indicate direction), note the content of the crate (i.e., number of animals,
species), and consignor and consignee addresses and phone numbers.

Shipping Animals If more than one animal needs to be shipped, the following is
recommended. Two animals can be sent in the same container or compartment if they are
familiar with one another and have been paired or in a family prior to shipment. A pair
with young infants or juvenile offspring less than 8 months of age should be shipped in
the same compartment. If you are shipping a large family, a single large crate should be
divided into several compartments. The interior walls between compartments should
allow cross-ventilation and auditory/olfactory contact. Allowing all members of a large
family to share a single compartment of crate, even a large one, can result in overheating
or death. Shipping pregnant females is always a risk since it is quite likely that she will
abort early in her pregnancy.

Shipment Timing and Regulations Deciding when to ship animals is a critical factor.
Remember mail takes precedence over animals and animals can be left sitting in a cargo
area during busy, holiday seasons. When possible, schedule departure and arrival for
Tuesday through Thursday (to avoid weekends) and during normal business hours to
ensure that the cargo office is open for pickup.

It is best to ship animals during the spring or fall to avoid extreme

temperatures. Tamarins are easily chilled or overheated. If sky kennels are used,
ventilation is rarely a problem, however, it is often difficult to keep the animals warm.
Providing a nest box for animals shipped in cooler weather can assist animals in coping
with temperature stress. Please note that a certain amount of container modification may
be required to meet the prevailing environmental conditions. The USDA Animal Welfare
regulations for birds and mammals prohibit shipment of animals if the temperature is
below 7.2'C (45'F) for more than 45 minutes during handling (i.e., being transported)
unless accompanied by a certificate of acclimation to lower temperatures. Shipments of
animals are also prohibited when the temperature exceeds 29.5'C (85'F) in any animal
holding facility at the terminal or over 23.9'C (75'F) for more than 4 hours at the terminal,
or over 29.5'C (85'F) for more than 45 minutes during handling.

A representative from the zoo should stay with the tamarins until they are loaded to be
sure they are kept in as quiet an area as possible, are not disturbed by curious airport
personnel, are not left in drafts or direct sun, are not placed under or between other
freight, and are actually loaded on the correct flight. The animals do not need to be fed for
a short flight, if they were fed prior to being crated. If the trip exceeds five hours, some
food should be provided (fresh fruit, marmoset diet). Specimen reports, medical records,
and health certificates for each individual should accompany every shipment, in addition
to necessary permits that may be required by each state. All cotton-top tamarins are
shipped for noncommercial purposes and are to be used for education and exhibition
purposes only.

Upon arrival, animals should be released from the shipping crate and reunited with family
members if appropriate. Animals should be given a nest box, food and water immediately
upon release from the crate.

Table 1. List of toxic plants (R. McManamon, pers. comm.and Fowler, 198 1)

Deciduous trees that should not be planted in zoos or aviaries

Gymnoodadus dioica Kentucky coffee tree

Melia azedarach Chinaberry, pride of India, bead tree

Sapium sbiferum Chinese tallow tree

Deciduous trees that should be planted with caution in zoos and avaries*

Aesculus sp. Horse Chestnut

Cassiafistual Golden shower

castanea mollissima Chinese chestnut

Ginko biloba Ginko, maidenhair

Inglaus sp. Walnuts

Koelreuteria sp. Chinese flame, golden-rain tree

Laburnum sp. Golden-chain tree

Maclura pomifera Osage orange

Prunus sp. Cherry, plum, peach

Sophora japonica Japanese padodatree, chinese scholar tree

Robinia Pseudoacacia Tolseacacin, Black locust

Schinus molle Coffee Tree

Acer rubrum Red maple

*Trees in this group have been reported as poisonous to one or more species of animal.

Perhaps one growth stage (foilage, fruits, seeds) of the tree is poisonous.

Deciduous trees that may be used in zoos and avaries

Acer sp. except A. rubrum All species of maple, boxelder

Ailauthus altissima Tree of Heaven

Albizia sp. Silk tree

Alnus sp. Alder

Amelanchier sp. Serviceberry, Juneberry

Bauhinia varigata Bouhinia, Mt. Ebony, orchid tree

Betula sp. Birches

Carpinus sp. Hombeains

Carva illinoensis Pecan

Catalpa sp. Catalpa, Indian Bean

Celtis sp. Hackberry

Cercis sp. Redbud, Judastree

Cornus sp. Dogwood

Crataequs sp. Hawthorn

Davidia involucrata Dore tree

Diospyros sp. Persimmon

Elaeagnus augustifolia Russian Olive

Fagus sp. Beeches

Ficus sp. Fig trees

Fraxinus Ashes

Gleditsia sp. Honey locust

Jacaranda sp. Jacaranda, green ebony

Lagerstroemia indica Crape myrtle

Larix decidua Larch

Liquidambur styraciflua Sweet gum

Liriodendron tulipifera Tulip tree, tulips, poplar, yellow poplar

Magnolia sp. Magnolia, cucumber tree

Malus sp. Apple, crab apple

Morus sp. Mullberry

Nyssa sylvatica Pepperidge, black tupelo

Paulownia tomentosa Paulowia, emperess tree

Pistachio chinensis Chinese pistache

Plantanus sp. Plane tree, sycamore, buttonwood

Populus Sp. Poplars

Prosopis sp. Mesquito, honey mesquito

Pyrus calleryana Gallery pear

Quercus sp. Oaks

Salix sp. Willows

Sassafras albidum Sassafras

Sorbus sp. Mt. Ash

Syringa amurensis Tree lilac

Tilia sp. Linden, basswood

Ulmus Sp. Elms

Narrowleafed evergreen trees or shrubs that should not be planted in zoos or

aviaries.

Taxus sp. Yew

Nerium oleander Oleander

Narrowleafed evergreen trees and shrubs that may be used in zoos and aviaries.

Abies sp. Firs

Arauicaria heterophylla Norfolk pine

Cedrus sp. Cedars, deodar

Chamaecyparis Cypress

Cpressus sp. Cypress

Juniperus sp. Juniper, Pfitzers

Libocedrus decurreus Incense cedar

Metasequoia glyptostroboides Dawn redwood

Picea sp. Spruces

Pinus sp. Pines

Podocarpus sp. Yew podacarpus, fem, podcarpus

Pseudotsuga menziesii Douglas fir

Sequoiadendron giganterum Giant sequoia

Taxodium distachum Bald cypress

Thuja sp. Arboffitae

Tsuga sp. Semlocks

Broadleafed evergreen trees and shrubs that should never be planted in zoos or
aviaries.

Kalmia latifolia Mt. Laurel

Leucothoe sp. Leucothoe, black

Nerium oleander Oleander, rosebay

Pieris sp. Andromeda

Broadleafed evergreen trees or shrubs that should be planted with caution in zoos
and aviaries.

Acacia sp. Acacia, golden wattle

Aucuba japonica Japanese acuba

Buxus sp. Box, boxwood

Codiaeum variegatum Croton

Daphne sp. Daphne

Euphorbia sp. Euphorbias, spurges

Hypericum sp. St. John's-wort, gold flower, aaronsbeard

Ilex sp. Hollys

Ligiuestrum sp. Privet

Photinia sp. Photinia

Pittosporum sp. Pittosporum

Prunus sp. Cherries, peaches, plums, nectarines

Rhododendron sp. Rhododendron, azalea

Schinus molle Pepper tree

Broadleafed evergreen tree or shrubs that can be planted in zoo and aviaries.
Abelia sp. Abelia

Arbutus unedo Strawberry tree

Arctostaphylos sp. Bearberry, kinnikinnick, manzanita

Berberis sp. Barberry

Collistemon sp. Bottlebrush

Camellia sp. Camellia

Carissa graudiflora Natal plum

Casuarina equisetifolia Beefwood, Australian pine, She oak

Ceanothus sp. California lilac

Cinnamomum camphora Camphor tree

Citrus sp. Orange, lemon, lime, grapefruit

Cotoneaster sp. Cottoneaster

Erica sp. Heather

Eriobotrya japonica Loquat

Eucalyptus sp. Eucalyptus

Eugenia sp. Eugenia

Euonymus sp. Euonymus

Fatsiajaponica Aralia

Feijoa sellowiana Pineapple guava

Ficus sp. Fig, Indian laurel

Fraximus Shamel ash, Evergreen ash

Gardenia jasminoides Gardenia

Hibiscus rosa-sinensis Chinese hilrscus

Larus nobilis Laurel, Sweet bay

Mangolia grandiflorum Magnolia

Mhonia sp. Oregon grape, holly, grape

Nandia domestics Heavenly bamboo, Sacred bamboo

Olea european Olive

Pachistima sp. Pachistimas, Oregon boxwood

Pluanbago capensis Cape plumbago

Pyracantha sp. Firethom, Pyracanha

Quercus sp. Oak

Ulmus Sp. Evergreen elm

Viburnum sp. Virbumum

Xylosma Shiny xylosma

Vines that should not be planted near animal enclosures.

Clematis sp. Clematis

Hedera sp. Ivy

Ipomea sp. Morning glory

Lantana sp. Lantana

Lycium sp. Matrimony vine

Minisperum canadense Moonseed

Monstera sp. Monstera, Cheese plant, Ceriman

Parthenocissus sp. Creepers, Virginia creeper, Boston Ivy

Philodendron sp. Philodendron

Senecio sp. Mexican flairne vine

Soladra sp. Goldcup chalice vine, cup of gold

Solaum sp. Bittersweet, Potato vine, Paradise flower

Trachelospermum jasminoides Starjasmine

VI Nutrition
Chapter Summary

 Adult animals consume on average 152 kcal/g body weight (range 112-
253kcal/g body weight).
 Lactating female’s caloric intake increases to 260 kcal/g body weight; thus,
diets of lactating females should be adjusted to accommodate this increased
energetic demand.
 Diets should address both the physical and psychological needs of the
animals.

Diet Development

Developing a captive diet can be a complicated task. Barnard & Knapka (1993) have
presented an extensive review on callitrichid nutrition. They suggest that the nutritional
requirements for a wild animal should be based on information from four areas of study:
1) observation of the diet consumed by related species; 2) field observations of food
consumption by the species being studied; 3) anatomical features of the species that
influence nutritional requirements; and 4) controlled research of the nutritional
requirements of the species. Because of the extensive studies on callitrichids in both the
field and in the laboratory, the current knowledge of the nutritional requirements have
been established using these methods.

Field Observations

In the wild cotton-top tamarins have been observed feeding primarily on fruits and insects
(Hampton et al., 1966; Neyman, 1978; Savage, 1990). They have not been observed to eat
leaves, nor do they gouge holes in trees to obtain sap. Tree gouging to obtain exudates
has never been observed in captive or field studies of Saguinus
or Leontopithecus. However, cotton-top tamarins are opportunistic feeders of sap, using
holes gouged by birds, insects or rodents (Raimerez, 1985; Neyman, 1978; Savage,
1990). Cotton-top tamarins have also been observed to feed on other animals, including
small birds, lizards, and eggs (Neyinan, 1978; Savage, 1990).

A causal relationship has been suggested between the small body size of callitrichids and
their insectivous habitats (Temerin et al., 1984). Metabolic costs of maintenance and
locomotor activity are relatively high in small primates. Given the small size of
callitrichids, they have adapted to feeding on insects, a food source that is high in
calories.
Gut transit times are also decreased in small-bodied as compared to large bodied
primates. Milton (1984) advances a physiological explanation for this "as body size
increase, metabolic costs per unit body weight decrease exponentially while gut volume
remains proportionate to body mass." So, in small mammals, the size of the gut cannot
process the amount of food required for their disproportionately high energetic
requirements per unit body weight without decreased food transit time. Thus, the short
gut transit times seen in cotton-top tamarins and other callitrichids, explain field
observations that they seek out nutritionally concentrated food and rarely, if ever, eat
fibrous plants that require long transit times to digest. To date, the nutrient composition of
a wild cotton-top tamarin diet has not been completely determined.

Captive Diets

It is generally accepted that feeding cotton-top tamarins a commercial primate diet

supplemented with various foods and nutritional supplements is sufficient to prevent
deficiencies when nutritional requirements are not known. It has also been suggested that
a varied dietary regime satisfies the behavioral needs of the monkeys as well (Coimbra-
Filho et al., 1981; Epple, 1970; Kirkwood, 1983; Kirkwood et al., 1983; Snowdon &
Savage, 1989; Tardif et al., 1988).

Documentation of cotton-top tamarins responses to diets supplemented with various

foods has provided valuable information regarding the animals' taste preferences, as well
as insights into their nutritional requirements. King (1978) examined dry matter, energy,
protein, and fat intake collected from captive cotton-top tamarins and other callitrichids
given a commercial primate diet, plant products (vegetables and fruits), and animal
products (eggs, milk, insects, etc.). Daily voluntary dry matter intake was 52 g/kg body
weight. This consisted of approximately 16% primate diet, 77% plant products, and 7%
animal products. The protein intake consisted of approximately 38% primate diet, 42%
plant products, and 27% animal products. Fat intake was 13.6% of the total calories. The
sources of dietary fat consisted of approximately 15% primate diet, 55% plant products,
and 30% animal products.

Benirschke and Richart (1963) fed a colony of callitrichids a variety of fruits, nuts, and
animal protein food sources. They found that sweetened milk, fresh eggs, and insects
were readily consumed while vegetables, fish, meat, or cooked food was avoided. The
monkeys maintained constant body weight and had normal hair coats while on this diet.
In general, these studies suggest that callitrichids fed diets based on plant products,
insects, and animal products had a nutritional requirement for an animal protein source
and had a preference for fruits and insects.

Various diets have been developed that are composed primarily of a commercially
prepared diet appropriate for callitrichids and supplemented with fresh fruits, vegetables,
and insects, and animal products. However, problems have resulted when using
supplemented diets. There are numerous reports indicating that tamarins develop
preferences to fruit, which resulted in decrease consumption of the more nutritious foods
(see Bamard & Knapka, 1993 for a complete review; Kirkwood, 1983; Kirkwood et al.,
1983). In studies by Kirkwood and his colleagues (1983), cotton-top tamarins who were
fed a diet comprised of one-fourth apple, one-fourth banana, one-eighth orange, and ad
lib monkey pellets for 5 years, had a high incidence of diarrhea. The tamarins ate the fruit
prior to and in preference to the monkey pellets. When a change in the diet was made to
include one-fifth of an egg per monkey daily and fruit was reduced by one half, there was
an increased consumption of the commercial diet, resulting in a 50% increase in protein
intake. A decrease in the occurrence of chronic diarrhea was observed and an increase in
body weight, new hair growth on alopecic monkeys and an increase incidence of triplet
births was also noted.

Vitamin and Mineral Requirements

There is little published information regarding the vitamin and mineral requirements of
cotton-top tamarins. Most commercial callitrichid diets contain Vitamin D3. However,
care should be taken if you plan to administer Vitamin D3 since fat soluble vitamins are
toxic at high concentrations. Bamard & Knapka(1993)list the following values for
reference.

Source:

Vitamin D 32000 IU/kg body weight or a daily Flurer & Zucker, 1987
intake of 33 IU per 400 g body weight

Retinol 171 g/kg body weight King, 1978

Cholecalciferol 2.8 g/kg body weight King, 1978

Calcium 206 mg/kg body weight King, 1978

Phosphorous 194 mg/kg body weight King, 1978

Protein and Energy Requirements

Protein and energy requirements of smaller species are greater on a per unit body weight
basis than those of larger species (Clarke et al., 1977). Pregnancy, lactation, and growth
increase energy requirements. There have been several studies examining energy and
protein consumption in adult cotton-top tamarins.

Source:

Daily intake of 130 kcal/kg body weight Kirkwood et al.,1983

metabolized energy (ME)
 152 kcal/kg body weight Kirkwood &
Underwood, 1984

160 kcal/kg body weight Escajadillo et al.,1981

225 kcal/kg body weight Flurer et al., 1983

189-219 kcal/kg body weight Tardif et al., 1988

Daily intake of protein .6 g protein/kg body weight Kirkwood et al., 1983

9.75 g protein/kg body weight Flurer et al., 1983

It should be noted that the overall caloric density of the diet may affect protein
requirements. According to Bamard and Knapka (1993), a high caloric density partially
offsets protein needs, and this is likely to account for the extreme difference between the
values in Kirkwood et al., (1983) and Flurer et al., (1983) studies. Clapp and Tardif
(1985) and Escajadillo et al., (1981) report success in maintaining cotton-top tamarin with
an average dietary protein content of 20% and 22.5% respectively.

Of the three dietary energy sources (protein, carbohydrate, fat) the least necessary for
cotton-top tamarin health is fat. Escajadillo et al., (1981) and Clapp and Tardif (1 985)
report an average of 8.9% and 9.2% fat content respectively is sufficient for cotton-top
tamarins in captivity.

While comparatively little discussion in included in the literature about the carbohydrate
content of the diet, it is the largest single component and provides the bulk of the energy
readily accessible to the animal. Studies examining carbohydrate content suggest values
that range from 47.2-81.4% (Clapp & Tardif, 1985; Escajadillo et al., 198 1; Flurer et al.,
1983).

Fiber content in the diet of callitrichids is a subject of considerable discussion. The

percent of "undigestible" fiber in a number of diets studied ranged from 1.5-10% (Flurer
et al., 1983). Protein digestiability began to decrease as fiber content exceeded 4% (Flurer
et al., 1983).

Krombach et al., (I 984) found that chitin (specifically shrimp meal), used as a fiber
source, is at least partially digestible by callitrichids. How this is accomplished is not
exactly clear, but may either be the result of microbial action in the gut or of chitinolytic
enzymes produced by the monkeys (Barnard & Knapka, 1993). Although not clinically
proven, the latter possibility points to insects (with their chitinous exoskeletons) as an
even more important nutritional component than previously thought.
Kirkwood and Underwood (1984) examined the food intake of cotton-top tamarins at
various stages of the life cycle. They determined that the energy intake required for
maintaining adult cotton-top tamarins was approximately 152 kcal/kg body weight/day
with a range of 112-253 kcal/kg body weight/day. The mean intake for pregnant females
in the last 7 weeks of pregnancy was approximately 139 kcal/kg body weight/day, which
was not significantly different from that of non-pregnant monkeys. However, during
lactation the daily caloric intake increased significantly to 260 kcal/kg body weight/day.
It was suggested that the ME provided by the breast milk was 17.8 kcal/day. Thus, this
suggests that captive diets must be modified to accommodate the high energetic demands
of lactation.

Suggested Diet

ZuPreem Marmoset (Hill's) diet is basically a nutritious diet for cotton-top tamarins. Additional
items in conjunction with ZuPreem Marmoset diet however, will allow for a complete
diet that addresses not only the physical but psychological needs of the tamarins. Cotton-
top tamarins have been observed to consume between 30-40 g/kg/day (Escajadillo et al.,
1981; Flurer et al., 1983).

Rather than provide a listing of each institutions diet, we have provided sample diets that
meet the current nutritional standards for callitrichids. The diets of the Brookfield Zoo
and Central Park Wildlife Center have been prepared by their respective nutritionists and
represent a completely well balanced diet for cotton-top tamarins.

Brookfield Zoo Cotton-top Tamarin Diet (per animal)

Diet provides approximately 184 kcal/kg/day

Divide this amount into two feedings.

Item Amount

Hill's ZuPreem Canned Marmoset Diet 46 g

Frugi Fruit' 24 g

Sweet Potato l0 g

Crickets 2.15 g (10, 3d/wk)

Mealworms 0.34 g (10, 3d/wk)

Marmoset Protein Supplement² 0.06 g

1. Frugi Fruit is of 54.5% apple, 11.4% grape, 17% banana, 5.7% raisins, 5.7% currants, 5.7%
blueberries)
2. Marmoset Protein Supplement consists of 16.3% spray dried eye whites, 24.5% high
nitrogen casein, 40.8% soybean protein, 16% magnesium oxide, 2% iron sulfate, 0.4%
manganese sulfate)

Note: The Marmoset Protein Supplement is spread over the frugi fruits

Central Park Wildlife Center Cotton-top Tamarin Diet (12er animal)

Diet provides approximately 175 kcal/kg/day

Item Amount

AM Diet

Hill's ZuPreem Marmoset Diet 50 g

Spectrum Primate Pro-Plus 6g

Bird salad 25 g

PM Diet

Spectrum Primate Pro-Plus 6g

Bird Salad' 50 g

One treat per day can be given, including: apple, banana, greens, orange, mealworms, or
crickets.

If needed, orange juice can be used on the high fiber primate biscuit to entice animals to
eat; otherwise there is no need for orange juice.

1. BIRD SALAD RECIPE (Provides: 700 kcal/kg)

Mix for 2 kg:

fruit 1000 g

mixed vegetables 500 g

greens 400 g

avi-powder 100 g
oyster shell 4g

dicalcium phosphate (powder) 2g

vitamin E powder (Rovimix) 0.1 g

PREPARATION: Chop fruits and greens (kale) finely, add mixed vegetables and coat

all with dry ingredients.

FRUIT: 4 apples (500g), 3 cups blueberries (350g), 1 cup grapes (150g)

VEGETABLES: frozen mixed vegetables - 4 cups (500g)

ROVINUX 40%: vitamin E supplement, Hoffinann-LaRoche, Inc.

VII Veterinary Care

Chapter Summary

 Cotton-top tamarins are the only non-human primate that spontaneously

develops colon cancer.
 Diagnostic and treatment options for a variety of cotton-top tamarin diseases
are discussed.

Veterinary Care

The following is a detailed chapter describing some of the major clinical diseases found
in cotton-top tamarins. Much of this information has been derived from studies of
tamarins in research laboratories and is a valuable reference for managing cotton-top
tamarins in zoos.

I. NORMAL REFERENCE VALUES

Adult body weight (wild) 400-430 g (Savage et al., 1993)

Adult body weight (captive) 500-700 g

Hemogram 5.20-7.01 x106ml

Red blood cells 5.4-16.7 x103ml

White blood cells 12.3-17.6 g/dl

Hemoglobin 38.3-55.8 %

Hematocrit 70.0-84.0 fl

mcv 22.1-27.0 g

MCH 30.5-33.3 %

MCHC 150-721 x103ml

Platelets 0.0-0.1x103ml

Bands 1.5-12.2 x103ml

Segmented neutrophils 0.8-5.7 x103ml

Lymphocytes 0.0-1.6 x103ml

Monocytes 0.0-0.5 x103ml

Eosinophils

* Values are from The New England Regional Primate Research Center

Clinical Chemistry

GLUHK 75-169 mg/dl

BUN 10-32 mg/dl

Creatinine 0.5-0.9 mg/dl

Total protein 5.5-7.9 g/dl

Albumin 3.2-5.2 g/dl

Calcium 6.0-10.3 mg/dl

Phosphorous 1.8-8.0 mg/dl

Globulin 2.7 g/dl

Alkaline phosphatase 0.0-476 nlEq/1

GGT 0.0-37.7 IU/dl

AST (SGOT) 0.0-322 m/1

LDH 0.0-585 mg/l

Cholesterol 52-204 mg/dl

Total bilirubin 0.00-0.57 mg/dl

ALT(SGPT) 0.0-70 m/1

Amylase 148-639 m/1

CPK 0.0-2325 m/1

C02 0.0-30 mEq/1

Direct bilirubin 0.0-0.30 mg/dl

Triglycerides 0.0-147 mg/dl

Sodium 146-160 mEq/1

Potassium 2.8-4.6 mEq/1

Chloride 78-122 mEq/1

Globulin 1.5-3.5 g/dl

Albumin/Globulin 0.862-2.602

Anion gap 15-55

Indirect bilirubin 0.0-0.49 mg/dl

*Values are from The New England Regional Primate Research Center

II. EXAMINATION AND PROCEDURES

The health of all tamarins should be monitored on a daily basis by zoo keepers with
follow up care by a veterinarian. The tamarins should undergo periodic physical
examinations to facilitate early diagnosis and treatment of serious diseases. Periodic
examinations and procedures should at least include the following:

History (abnormalities in health or behavior, changes in diet or environment, etc.)

 Thorough physical examination (including dental exam, palpation for abdominal
masses and pregnancy)

Weighing

Tattooing/Transponder implant for identification

Tuberculosis testing (annually)

Depending on the environmental conditions and protocol of the individual institutions,

the following may be indicated:

Serum banking

Vaccinations (measles and rabies; based on the specific risk factors at each institution)

Prophylactic antiparasitic drugs (dependent on history of parasitic disease and risk

factors)

Additional procedures that may be warranted depending on the specific situation are:

CBC, clinical chemistry

urinalysis

cultures

serology

III. INFECTIOS DISEASES

Infectious diseases are common problems in callitrichids. A review of the most

common infectious diseases in callitrichids is presented, with special emphasis on the

diseases affecting cotton-top tamarins.

A. Bacterial

Tamarins are susceptible to infection by a large number of bacterial organisms.

Significant clinical disease may occur secondary to concurrent viral or parasitic infection,
prior debilitation, decreased immunity or the extensive use of antibiotics. The more
significant pathogens are reviewed here. Readers are referred to Potkay (1992) for a
detailed discussion of documented cases of infections in callitrichids.
Campylobacter jejuni

Campylobacter is the most frequently isolated organism from nonhuman primates with
diarrhea. C. coli is not considered pathogenic. C. jejuni is a common cause of diarrhea
and enterocolitis in cotton-top tamarins. Campylobacter sp. are often isolated from
asymptomatic animals (Paul-Murphy, 1993). This organism may be an enzootic and
opportunistic infectious agent in many colonies. The fecal-oral route is the primary mode
of transmission. The diseased state involves a secretary diarrhea. It is uncommon to find
frank blood and mucus in the feces (Paul-Murphy, 1993). Soft mucoid feces are
produced. Feces are fluid, yellowish and may contain occult blood in cases of greater
severity (Russell, 1993). Whether diarrhea is due to the invasiveness of the organism or to
the production of an enterotoxin is unclear. A cytotoxin may be involved in the
pathogenesis of disease.

It is common to find gas-filled loops of bowel (Paul-Murphy, 1993). On histologic

examination in macaques, there are no pathologic changes observed in the jejunum or
ileum (Russell, 1993). There are changes associated with colitis observed 48-72 hours
following infection. The lamina propria is moderately infiltrated with inflammatory cells,
mainly neutrophils along with lymphocytes and plasma cells. There is neutrophilic
infiltration between crypt epithelial cells and many neutrophils are found in gland lumens
(crypt abscesses). In more serious cases, necrosis leads to flattening of the luminal
epithelium and replacement with squamous cells. Dilated lymphatics containing
mononuclear cell infiltrates are seen in the submucosa. The comma-shaped organisms
may be observed in the lamina propria and on the surface epithelium. Goblet cells are lost
from the luminal epithelium, cuboidal and flattened cells replace the columnar
epithelium, and the lumen of the colon contains necrotic and degenerating epithelial cells
and red blood cells (Russell, 1993).

It is difficult to distinguish diarrhea caused by Campylobacter from other bacterial

causes. Animals with C. jejuni infection may show abdominal discomfort but do not have
anorexia as seen with other enteric pathogens and signs are usually limited to a soft to
fluid diarrhea (Russell, 1993). Early presumptive diagnosis of Campylobacter enteritis
may be attempted through the identification of comma-shaped Gram-negative rods on
Gram stained fecal smears (McClure et al., 1986). Definitive diagnosis requires isolation
of the organism. Cultures should be made from fresh stool or a rectal swab. The presence
of erythrocytes and leukocytes on fecal smears stained with methylene blue is highly
variable. Blood chemistry findings are nonspecific. The leukocyte count may range from
a normal leukocyte count to leukocytosis with a toxic left shift and the fibrinogen level is
frequently increased (Paul-Murphy, 1993).

Administration of appropriate fluid and electrolyte replacement therapy is very important.

Antimotility drugs interfere with intestinal motility and are contraindicated. Some
antimicrobials which are successful in susceptible strains are aininoglycosides,
clindamycin, chloramphenicol, furazolidine, erythromycin, ciprofloxacin and
enrofloxacin. The current drug of choice for the treatment of Campylobacter enteritis is
oral erythromycin but some resistant strains exist. Enrofloxacin is a suitable second
choice for strains not sensitive to erythromycin. Antibiotic sensitivity tests are not
routinely done but are indicated in those cases where animals do not respond to
erythromycin or enrofloxacin (D. Lee-Parritz, pers. comm.).

Prognosis is good provided antibiotics, fluids and other supportive care are administered
properly (D. Lee-Partitz, pers. comm.). Reinfection from the affected individuals' own
feces or from feces of animals housed in the area can interfere with recovery.

Klebsiella pneumoniae

This organism is generally an opportunistic pathogen infecting sick or debilitated animals

(Richter, 1984). It is one of the more common bacteria currently associated with clinical
disease in callitrichids. Clinical disease is usually associated with serotype 1 (Richter,
1984). Animals often present with acute death lacking prior clinical signs (D. Lee-Panitz,
pers. comm.) The main manifestation of disease is lobar pneumonia. This organism may
also cause septicemia and enteritis. Signs frequently observed are seizures, opisthotonos
and abortion (D. Lee-Parritz, pers. comm.). Clinical signs may also include coughing,
sneezing, dyspnea, nasal discharge, diarrhea, hypothennia, anorexia and lethargy.

Post mortem findings may include gaseous distension and congestion of the small
intestine. The liver may be enlarged with diffuse yellow areas on the surface. Lesions
show intense congestion and contain mono- and poly-morphonuclear leukocytes
suggesting the cause of death to be septicemia (Potkay, 1992).

Isolation and identification of the organism can be made following culturing of samples
from pharyngeal swabs or transtracheal lavage. Antibiotic sensitivity should be
determined and appropriate therapy administered. Cephalosporins, chosen to penetrate
into the meninges, may be an effective treatment (D. Lee-Parritz, pers. comm.).
Supportive fluid and oxygen therapy may be necessary. Prognosis is generally poor with
death occurring due to lobar pneumonia, meningitis or septicemia (D. Lee-Parritz, pers.
comm.).

Salmonella sp.

This organism is of special importance because of its zoonotic potential. Clinical disease in
nonhuman primates is generally associated with the overall health of the population.
Disease caused by Salmonella in New World monkeys is infrequently reported (Paul-
Murphy, 1993). The fecal-oral route is the most common mode of transmission. Oral
route infection may also occur when contaminated food items such as raw meat fed as a
dietary supplement are consumed. Asymptomatic chronic carriers are common and may
serve as sources of infection. Rodents and small birds may also be potential sources of
infection. Insects have also been implicated as possible mechanical vectors. The potential
for exposure may be high in zoos since the organism may be carried by a number of
different species. Incidence appears to be higher in zoos than in primate research facilities
(Paul-Murphy, 1993).

One manifestation of clinical disease seen with Salmonella in nonhuman primates is

gastroenteritis. This disease is associated with a watery diarrhea due to net secretion of
fluids throughout the intestinal tract following invasion of the mucosa by the organisms.
Signs occur rapidly and may include anorexia, depression and fever. Dehydration can be
severe. Sometimes stools may contain blood and mucus (Paul-Murphy, 1993).

There is congestion and edema in the ileum, cecum and colon. Superficial ulcerations and
petechial hemorrhages may be found. The intestinal epithelium shows degeneration and
desquarnation. Infiltration of the epithelium can occur with spread to the lymph nodes
resulting in subsequent systentic infection. This organism sometimes causes fatal
septicemias. Serositis and focal necrosis of the liver and lungs characterize fatal cases
(Richter, 1984).

Isolation of the infectious agent is required for definitive diagnosis. Isolation may be
difficult during the recovery phase of the illness. It is very difficult to isolate organisms
from asymptomatic carriers which can present problems in terms of preventing the spread
of the disease. Cultures should be made from fresh feces or rectal swabs. More
mononuclear cells are found in fecal smears stained with methylene blue relative to the
numbers found in cases of shigellosis. The percentage of mononuclear cells in the blood
also tends to be higher in cases of salmonellosis when compared to shigellosis (Paul-
Murphy, 1993).

Appropriate fluid and electrolyte replacement therapy are of primary importance.

Antimotility drugs affect intestinal motility and are contraindicated.

Treatment with antibiotics is not indicated unless sepsis is evident (Richter, 1984)
because of the risk of inducing a carrier state. Animals should be isolated and supportive
therapy administered. The animal's own immune system is likely to resolve the disease
(D. Lee-Parritz, pers. comm.) Resistance can pose a problem in the treatment of
salmonellosis. Antibiotic sensitivity tests should be used to determine appropriate
therapy. Some of the currently used drugs for the treatment of Salmonella gastroenteritis
are cephalothin, cefazolin, trimethoprim-sulfamethoxazole, ciprofloxacin and
norfloxacin. Many strains have shown resistance to arnpicillin, erythromycin,
chloramphenicol, tetracycline, kanamycin and dihydrostreptomycin (Paul-Murphy, 1993).
Reinoculation by the fecal-oral route from the animal's own feces or from the feces of
animals housed together is a potential complication of successful treatment (Paul-
Murphy, 1993).

Shigella sp.

According to Potkay (1992), this organism is an important pathogen in callitrichids and

may be seen in concurrent infections with Salmonella. However, incidence of disease
may be low to nonexistent (D. Lee-Parritz, pers. comm.) and there are few reports in New
World primates (Paul-Murphy, 1993). Clinical disease is usually correlated with the
overall health of the population. Transmission is mainly by the fecal-oral route. Isolation
of this organism from the feces in callitrichids may occur without the presence of clinical
disease (Richter, 1984).

Signs associated with clinical disease in nonhuman primates may occur abruptly and
include watery stools containing blood and mucus, colitis, anorexia, depression, lethargy,
fever, dehydration, abdominal discomfort, painful and ineffectual straining during
defecation and death. Stools often have a characteristic odor (Paul-Murphy, 1993).
Diarrhea is caused by invasion of the intestinal epithelium and subsequent intracellular
multiplication in the submucosa or lamina propria. It is uncommon for this organism to
invade beyond the lamina propria and enter the bloodstream. The site most affected is the
colon where the luminal surface may be roughened. It may also be purulent or
hemorrphagic. Shigella sp. can produce an exotoxin with both cytotoxic and enterotoxic
effects. There is an acute inflammatory response of the intestinal tract which may result in
the release of mediators that increase intestinal secretion and decrease absorption leading
to fluid loss (Paul-Murphy, 1993).

Postmortem investigation may show petechia and erosions of the large intestine. Enlarged
mesenteric lymph nodes are often associated with disease. Epithelial cell loss and
infiltration of the lamina propria with polymorphonuclear leukocytes is seen. Crypt
abscesses may occur (Paul-Murphy, 1993).

In order to obtain a definitive diagnosis, the organism must be isolated using fresh fecal
specimens or rectal swabs. It may be difficult to isolate this organism during the recovery
phase of the disease. Large numbers of polymorphonuclear leukocytes with many band
forms are often found on examination of fecal smears stained with methylene blue. Blood
chemistry tests may show a pronounced leukocytosis with a marked left shift and the
presence of large numbers of toxic neutrophils and band forms. Fibrinogen levels are
frequently elevated (Paul-Murphy, 1993).

Appropriate fluid and electrolyte replacement therapy are of the utmost importance.
Antimotility drugs interfere with intestinal motility and are contraindicated.
Antimicrobial resistance should be considered in implementing appropriate antimicrobial
therapy. Shigella sp. have a strong potential for developing multiple resistance. Some
effective antibiotics include ftimethoprim-sulfamethoxazole, arnpicillin, tetracyclines and
fluoroquinolones. Many strains show resistance to ampicillin. Trimethoprim-
sulfainethoxazole administered orally or parenterally is the recommended choice. For the
initial treatment of dysentery, enrofloxacin may be a good option. Antibiotics may prove
useful in decreasing the shedding period of this organism. Therapy may be complicated
by reinfection from the animal's own feces and from the feces of infected individuals
housed in the vicinity (Paul-Murphy, 1993).

Yersinia sp.
This organism can be a cause of gastroenteritis in callitrichids. Infection may occur
through contaminated food or water. There is increasing evidence that wild rodents may
serve as a source of infection for nonhuman primates (McClure et al., 1986). Diarrhea
which may contain blood is often observed. Pathologic findings include ulcerative
enterocolitis of varying degrees and inflammation of the mesenteric lymph nodes.
Necrosis of the spleen and liver are also common findings (McClure et al., 1986).
Microscopic examination of imprint smears and lesion sections show numerous grain
negative rods.

Tuberculosis

This disease is very uncommon in callitrichids and New World monkeys are relatively
resistant. Mycobacterium tuberculosis may cause a slowly progressive respiratory
disease. Disease may also involve visceral organs and the spinal column (Ott-Joslin,
1993). Transmission is through aerosolization and inhalation. Clinical signs are unreliable
in indicating the extent of disease. Debilitation may only appear shortly prior to death.

Diagnosis is based on tuberculin hypersensitivity testing. Old tuberculin (1,500 units or 0.

1 ml) is injected intradermally into the upper eyelid and the area is subsequently
examined at 24, 48 and 72 hour intervals for the presence of edema, induration or
erythema. All nonhuman primates should be tested systematically on an annual basis and
more frequently if warranted by the risk of exposure. On occasion, radiographs may aid
in the diagnosis of well-developed cases by the identification of lesions. Euthanasia is
generally the recommended procedure for positive individuals except in the case of
extremely rare or valuable animals and clinicians should use appropriate judgment in
determining mode of action. Regulations may vary and state or federal institutions should
be consulted. Isoniazid is the common form of treatment for tuberculosis in humans and
multiple agent therapy may be advised.

Pseudomonas

Pseudomonas is considered to be an important pathogen of callitrichids.

Bronchopneumonia is the most common presentation. Debilitated animals are especially
susceptible to disease caused by this organism. In callitrichid populations with enzootic
infections, successful elimination of this organism is extremely difficult (Cicmanec,
1977; Deinhardt et al., 1967). Associated conditions include vegetative endocarditis,
pericarditis, myocarditis, empyema and septicemia (Deinhardt et al., 1967).

Infraorbital abscesses

Infraorbital abscesses commonly result from chronic dental disease or from sinus
abscesses. Attempts should be made to determine the cause of infraorbital abscesses when
they occur. The oral cavity should be examined for cracking, splitting and looseness of
teeth, exposed pulp cavities, and periodontal disease. Radiographs may aid in diagnosis.
The underlying cause should be appropriately addressed. Drainage and irrigation are
important for successful treatment and should be implemented initially (D. Lee-Panitz,
pers. comm.). Abscesses should be cultured and antibiotic sensitivity determined.
Appropriate antibiotics should be administered systemically. These lesions may require
long periods of time to heal (Richter, 1984).

Osteomyelitis

Osteomyelitis may occur following puncture wounds and is frequently seen locally in
bitten digits. Systemic antibiotics are recommended and it is important to be aware that
healing may take long periods of time. Amputation of digits is often warranted.

Osteomyelitis may also occur on the tail tip following fecolith formation. Dermatitis,
necrosis and exposure of the coccygeal vertebra occur subsequent to fecolith formation
followed by osteomyelitis. The occurrence of fecolith formation may be prevented by
increasing the distance between perches and the cage floor (Richter, 1984). In institutions
with good husbandry practices, this problem should not occur.

Treatment involves bathing of the tail tip and local treatment with antibiotics. Systemic
antibiotic use may be advisable. Wounds inflicted during fighting may lead to systemic
osteomyelitis. Systemic antibiotics should be administered immediately. Repeated
cultures should be made from infected sites and antibiotic sensitivity determined. Oral
broad spectrum antibiotics such as cephalexin are the appropriate method of treatment
pending receipt of sensitivity testing results (D. Lee-Parritz, pers. comm.). Radiography is
useful in the diagnosis of osteomyelitis.

B. Mycotic

Little information is available concerning mycotic infections in callitrichids.

Candida sp.

Candida sp. appears to be a normal inhabitant of the mucous membranes, genital tracts
and skin of nonhuman primates (Migaki, 1986). Candidiasis occurs infrequently in
debilitated animals or in animals which have received long-term antibiotic therapy. The
most common agent is C. albicans. Manifestations in nonhuman primates include
glossitis, usually seen as a thickened gray-white coat on the margins or tip of the tongue,
esophagitis, and less frequently, gastritis. The creamy white plaque-like lesions form
pseudomembranes and are due to heavy growth of the organism (Migaki, 1986).
Ulcerations may be seen on the tongue or mouth. Signs often disappear if the underlying
cause of debilitation is cured. Oral nystatin is generally effective in the treatment of
gastrointestinal tract candidiasis in animals.

C. Parasitic

Protozoa
Giardia sp.

According to Wolff (1990), infections with these organisms seem to be rare in New
World monkeys and Giardia sp. are not included in her description of the parasites of
callitfichids.

Trypanosoma cruzi

While disease is infrequent, infections with Trypanosoma sp. are common. Most trypanosomes are
not zoonotic. The only trypanosome known to be pathogenic in New World monkeys is T.
cruzi which is also a significant human pathogen responsible for Chagas' disease. Caution should be
exercised when working with feral animals and in endemic areas. The distribution of the organism is
South and Central America and may occur in some areas of the southern and southwestern United
States (Toft, 1986). Insect vectors from the family Reduviidae serve as the intermediate hosts.

The trypanosomal form of the organism is found in the bloodstream. The leishmanial
form is seen in cells of the skeletal muscle, cardiac muscle, reticuloendothelial system, as
well as other tissues. When clinical disease does occur in New World primates, it is
frequently associated with generalized edema and myocarditis. Other signs include
anemia, splenomegaly, hepatomegaly and lymphadenitis. lestopathologic findings include
the presence of pseudocysts in areas of the infected myocardium. These pseudocysts
contain the organisms which have a central nucleus and a prominent kinetoplast shaped
like a bar. The kinetoplast is diagnostic for this organism and helps in distinguishing it
from Sarcocystis and Toxoplasma (Toft, 1986). With heavy infections in tamarins,
monocytic infiltrations in the liver may be observed (Deinhardt et al., 1967).

Diagnosis is based on the identification of the organisms in thick and thin blood smears
stained with Giemsa stain or by examination of organ smears or sections. Serological
tests may also aid in diagnosis. There is no treatment available but attempts to control the
insect vector may decrease the incidence.

Entamoeba histolytica

According to Wolff (1990), natural infection in New World monkeys is uncommon but
when it occurs the pathogenic effects tend to be relatively more severe than those seen in
Old World monkeys. However, Richter (1984) states that E. histolytica appears to be
fairly common in callitrichids. Several non-pathogenic Entamoeba sp. occur in New
World monkeys so obtaining a definitive diagnosis of E.histolytica is important (Wolff,
1990). Cysts are infective and may be transmitted through ingestion of contaminated
food, water, insects and fomites.

Ordinarily, the organism lives in the lumen of the intestinal tract causing no pathologic
signs. It can become pathogenic when it enters the intestinal mucosa (Levine, 1970). The
severity of clinical signs varies with the strain of organism, the nutritional and health
status of the individual and the individual's gastrointestinal tract flora. When clinical
disease occurs, it manifests as amebic dysentery. Clinical signs include severe diarrhea,
dehydration, weakness, anorexia and vomiting. Diarrhea may or may not contain mucus
and blood.

Post mortem examination shows colitis with necrosis and ulcerations. Histopathological
findings include the presence of characteristic flask-shaped ulcers in the colon.
Trophozoites may be seen around or in the ulcers (Toft, 1986).

Diagnosis is made by the identification of the organism in the feces. Fresh, wet mount,
fecal preparations in a saline solution can be examined for the presence of motile
trophozoites. Lugol's iodine may aid in the recognition of organisms. There is a non-
pathogenic form of E. histolytica, as well, that has smaller trophozoites. The finding of
erythrocytes within trophozoites is a method of diagnosing the pathogenic form because
only the pathogenic type ingests red blood cells (Toft, 1986).

Metronidazole and paromomycin can be used for treatment of this disease (Wolff, 1990).

Toxoplasma gondii

New World monkeys are highly sensitive to disease caused by this organism and death
may ensue in 5-6 days (Wolff, 1990). Toxoplasma gondii is distributed around the world.
Failure to identify seropositive callitrichids in the wild could be explained by their high
susceptibility to the disease (Potkay, 1992) or possibly by their lack of exposure to
infected rodents. The most likely form of transmission in captive animals is through
ingestion of bradyzoites in animal tissues but infection may also occur following
ingestion of sporulated oocysts which are shed by the definitive hosts belonging to the
family Felidae or through transplacental transmission (Potkay, 1992). Insect vectors can
aid in the spread of this organism by serving as transport hosts.

Signs associated with disease are nonspecific and may include decreased appetite
progressing to anorexia, diarrhea, vomiting, weakness, sluggishness, depression,
crouched posture, fever, cough, discharge from the nose and eyes, leukopenia, dyspnea,
pale mucous membranes, abortion, coma and death.

Post mortem findings may include pulmonary edema, cardiomegaly, necrosis of the
myocardium, hemorrhagic lymphadenopathy, enlargement and hyperplasia of the spleen,
hepatic congestion and hepatocellular necrosis. Histopathological findings include
interstitial and fibrinous pneumonia, focal myocarditis, focal hepatic necrosis, necrotic
lymphadenitis, necrotic splenitis and intestinal lesions. Intracellular and/or extracellular
tachyzoites are often seen in association with inflammatory lesions (Toft,1986).

Diagnosis is based on examination of histological sections and smear preparations for the
identification of the parasites. Serological tests are available for identification of this
organism. Monitoring of felid fecal samples for the presence of oocysts in a zoological
setting may aid in the prevention of the spread to tamarins, however, oocysts are only
shed for a very brief period of time, so their absence in the feces does not indicate
absence of infection. Felid feces should be disposed of properly in order to avoid the
possibility of sporulated oocysts contacting vectors and fomites (Flynn, 1973).
Sulfadiazine, pyrimethamine and clindamycin have been used somewhat successfully to
treat this disease in people and dogs (Wolff, 1990).

Pneumocystis carinii

According to Wolff (1990), natural infection with this organism has not been found to
occur naturally in callitrichids, but has been observed in colonies and may cause
significant disease in immunocompromised individuals. Organisms are located in the
bronchioles and alveoli. The main disease manifestation is interstitial pneumonia.
Diagnosis is based on examination of pulmonary secretions and histological sections.
Treatment of disease involves the use of trimethoprim and sulfa-methoxazole (Wolff,
1990).

Helminths

Nematoda

Many nematode species occur in callitrichids. Some of the more significant pathogens are
described here. For a detailed account of documented cases, see Potkay (1992).

Oxyurata

Callitrichids may be infected by a number of pinworm species. However, morbidity is

extremely low. Infection by the human pinworm Enterobius vermicularis may occur in
captive populations of callitrichids (Wolff, 1990). To date, there do not appear to be any
reports of infection with E. vermicularis in cotton-top tamarins. Humans may serve as
sources of infection for primates who can then act as reservoirs and reinfect humans
(Flynn, 1973). Organisms inhabit the large intestine. Irritation and perianal pruritis may
occur resulting in self-mutilation, increased irritability and restlessness. Hemorrhagic
enteritis and abdominal discomfort may be observed.

Diagnosis can be made by visualization of adults in the anal area. Celophane tape may be
used in order to obtain eggs from the anus for identification. Pyrantel painoate can be
used to treat pinworm infections (Wolff, 1990).

Trichospirura leptostoma

This spirurid nematode is a common parasite of the pancreas in callitrichids. This

organism requires an intermediate arthropod host. Cockroaches may be capable of
serving as intermediate hosts (Potkay, 1992). Acute chronic pancreatitis may result from
infection (Wolff, 1990). Massive infections may be responsible for a wasting disease type
syndrome in C. jacchus. Periductal fibrosis, proliferation of ducts and exocrine pancreatic
atrophy may be observed (Potkay, 1992). Diagnosis is made at necropsy and it is often an
incidental finding on histologic examination. It may be possible to diagnose infection
through fecal flotation. There is no reported treatment but ivermectin may be effective
(Wolff, 1990). Fenbendazole may also be a potential treatment.

Pterygodermatites nycticebi (Rictularia nycticebi)

This organism has been associated with morbidity and mortality in Leontopithecus
rosalia (Montali et al., 1983). Cockroaches, crickets or other insects serve as intermediate
hosts for this organism (Potkay, 1992). Clinical signs include watery diarrhea which may
contain adult wom-is, anorexia, weakness, anemia, hypoproteinemia and leukopenia.

Post mortem findings have included the presence of numerous parasites in the
gastrointestinal tract. Histologic exam demonstrated the anterior ends of the adult
organisms embedded in the small intestinal mucosa. A necrotic pseudomembrane and
clubbing of the small intestinal villi were also seen (Montali et al., 1983).

Diagnosis is generally based on the identification of eggs, worins or larvae in the feces.
Prophylactic wonnings with ivermectin and mebendazole, as well as cockroach
population control measures, can decrease the possibility of infection (Wolff, 1990).

Physaloptera sp.

Physaloptera dilatata can cause infection in callitrichids. The organism attaches to the
gastric mucosa and can cause gastritis and hyperplastic gastric lesions with heavy
infections (Wolff, 1990). Diagnosis is made by fecal Rotation. The use of high doses of
mebendazole has proven effective in some Physaloptera species (Wolff, 1 990).

Filariasis

Infection with several species of filarial worins is a common occurrence in wild-caught callitrichids.
Wild cotton-top tamarins have been observed with a filarial worm parasite belonging to the
genusMansonella. Typical of this parasite, the adult lives in the body cavity of the host and produces
living microfilaria that circulate in the peripheral blood. They are not pathogenic (Savage, 1990).

Filarial worms inhabit the thoracic or abdominal cavities, or the subcutaneous tissues. Transmission
occurs by way of blood sucking insects. However, there have not been any reports of clinical signs
associated with infection (Potkay, 1992). Diagnosis is made by the identification of microfilariae in
smears of the peripheral blood, or by demonstration of adults in subcutaneous tissue or in the
peritoneal cavity on necropsy. According to Potkay (I 992), no treatments have been evaluated or
reported.

Trematodes

Trematodes are often encountered in New World monkeys. Only some of the more
important species are discussed here. For a synopsis of prior reports of trematode
infections in callitrichids, see Potkay (1992).
Asthemiafoxi

This organism is a fairly common, moderately pathogenic fluke that resides in the bile
duct. The mode of infection appears to be unknown. Mollusks serve as obligatory
intermediate hosts. Generally, infection is asymptomatic, but various degrees of
pathogenicity may be observed depending on the parasite level. Heavy infections can lead
to an inflammatory reaction and thickening of the bile ducts, resulting in mechanical
blockage. Fecal sedimentation may allow for identification of the characteristic eggs. Post
mortem diagnosis can be made based on the presence of adult flukes in the bile duct.
Praziquantel can be used to treat infection (Wolff, 1990).

Cestodes

Cestodes do not seem to be a serious cause of disease in callitrichids. Clinical disease or

enteric pathology are rarely observed with tapeworm infections in nonhuman primates
(Toft, 1986). Nonhuman primates may act as inter-mediate hosts developing larval forms
in somatic tissues (Toft, 1986). The reader is referred to Potkay (1992) for a listing of
reported cases of cestode infections in callitrichids.

Diphyllobothrium erinacci and Spirometra reptans

Infection is generally asymptomatic and the presence of spargana is usually an incidental

finding at necropsy. Spargana are the pleurocercoid larval form of these organisms and
the term for infection is sparganosis. Infection probably occurs following ingestion of
crustacean intermediate hosts (Wolff, 1990).

Spargana may occur in just about any part of the body. They are usually found in
subcutaneous, muscle and connective tissues as well as in the abdominal or pleural
cavities. Inflammation and edema may occur following migration through the tissues or
as a result of degeneration following the death of the organisms. Calcification of chronic
lesions may occur allowing for radiographic visualization. Subcutaneous tissue nodules
may be palpable in the live animal. There is no known treatment for infection but if
necessary, organisms may be removed surgically (Wolff, 1990).

Acanthocephalans

Prosthenorchis elegans and P. spirula

The acanthocephalans, thomy-headed wonns, are probably the most significant parasites
of callitrichids. Insects, most commonly German cockroaches, serve as intermediate
hosts. Infection with P. elegans is more common than with P. spirula (Potkay, 1992).
These organisms frequently inhabit the distal ileum, cecum and proximal colon. Parasites
are often found at the ileocecal valve (Richter, 1984). Toft (1986) lists several references
and states that P. spirula generally inhabits the terminal ileum while P. elegans tends to
be found in the cecum or colon.
The worm attaches its proboscis to the intestinal mucosa which results in pronounced
inflammation, necrosis, fibrosis and the formation of nodules. The worms invade the
intestinal walls leading to abscessation, peritonitis, and sepsis. Fatal peritonitis and
septicemia can result when the intestinal wall is perforated.

There are no distinctive symptoms associated with infection (Potkay, 1992; Toft, 1986).
Clinical signs of Prosthenorchis infection may include diarrhea, anorexia, cachexia, pain,
depression, debilitation and death. Infection by secondary pathogens which are able to
colonize the lesions produced by the parasites are usually responsible for fatal cases. The
passage of bloody and scanty stools may be seen in severe cases. Mesenteric
lymphadenitis and splenomegaly may be associated with infection (Potkay, 1992).
Intussusception, mechanical blockage or rectal prolapse may occur with severe infections.
Histologic findings include inflammation, mucosal ulcers, and granuloma and abscess
formation in the intestinal wall (Toft, 1986).

Diagnosis is based on the demonstration of eggs in concentrated fecal samples and, less
commonly, on the presence of worms. Fecal flotations are inadequate for the
identification of eggs and direct smears or sedimentation methods must be employed
(Toft, 1986). The presence of the characteristic thorny-headed worms found at necropsy
are diagnostic. There appear to be no consistent and confirmed reports of successful drug
therapy. Drugs like ivermectin have not been evaluated as potential treatments (Potkay,
1992). Worms may persist in healthy hosts so supportive nutrition and the administration
of antibiotic therapy, when necessary, are important for preventing clinical disease
(Richter, 1984). Surgical excision of worms may be an appropriate therapeutic approach.
Cockroach control is an important aspect of preventing acanthocephalan infection.

Arthropoda

Arthropods don't appear to be a serious cause of disease in callitrichids. As previously

described, several insects may transmit viruses and parasites. See Potkay (1992) for a
listing of reported cases of infection in calfitrichids.

Pentastomes

Porocephalus clavatus nymphs are frequently found in Saguinus sp., although there do
not appear to be any reports in S. oedipus to date (Potkay, 1992). The nymphs may be
observed in a coiled "C" position, encapsulated in the peritoneal and thoracic cavities
(Richter, 1984). Nymphs may be located within cysts in the lungs, liver and meninges,
and beneath the parietal peritoneum and pleura (Potkay, 1992). Dead nymphs may result
in chronic inflammation (Cosgrove et al., 1970). There have not been any reports of
clinical signs and there are currently no treatments (Potkay, 1992).

Mites
Acariasis is seldom seen in callitrichids, even though they are parasitized by several
species of mites (Potkay, 1992). Demodex sp. have been found on the skin and in the hair
follicles and may cause dermatitis. Reported clinical signs in S. geoffroyi included
cutaneous erythema, alopecia, and the formation of papules on the head, tail and limbs
(Hickey et al., 1983). Focal inflammation and degeneration were observed in areas
surrounding infected hair follicles. Diagnosis is made by the identification of the
organisms following a deep skin scrape. Successful treatment in the above case involved
the use of ronnel and rotenone ointment.

D. Viral

The Regional Reference Center for Simian Viruses of the Southwest Foundation for
Research and Education located in San Antonio, Texas has been established for the
investigation of nonhuman primate viruses and may be a useful resource for the
identification of viral agents.

Herpesviridae

Herpesvirus tamarinus (Herpesvirus-T or Herpesvirus platyrrhinae)

Infection with this virus frequently results in a systemic fatal disease in callitrichids. The
squirrel monkey (Saimiri sciureus) serves as the natural host for this organism. Infection
is often latent in the natural host but may cause mild herpetic lingual ulcers and
stomatitis. The virus is shed in oral secretions and oral lesions. Spread of the organism
occurs through aerosols, direct contact or fomites. If the virus occurs in a susceptible
monkey colony, it can reach epizootic levels by spreading rapidly, resulting in high
mortality rates (Melendez, 1976).

Infection in tamarins is generally fatal. Common signs of disease include anorexia,

weakness, depression, emaciation, rhinitis, conjunctivitis, sneezing, serous nasal
discharge, ulcerative dermatitis, and vesicles and ulcers on the oral and labial surfaces.
Hyperesthesia and pruritus with frequent scratching may be seen (Richter, 1984).

Post mortem findings include gastrointestinal tract ulcerations and hemorrhage,

splenomegaly, bronchitis and focal pneumonia. Often hemorrhage and focal necrosis in
the adrenal cortex and lymph nodes are seen. Gray-white focal necrosis of the liver and
other organs may be found (Richter, 1984).

Intranuclear inclusion bodies are seen in neural, visceral and mesenchymal cells. The
characteristic inclusion bodies are useful for differentiating this disease from other viral
causes of hepatitis. Intranuclear inclusion bodies may be basophilic or eosinophilic.
Multinucleated giant cells containing intranuclear inclusions may be found around areas
of visceral necrosis or in mucosal cells. Histopathological findings include encephalitis,
focal demyelination, proliferation of glial cells and neuronal degeneration. There is
monocytic infiltration of the liver, spleen and lymph nodes (Richter, 1984).
Prevention involves avoiding contact with species that may be reservoirs for the virus
which includes Saimiri, Ateles, Cebus, and Lagothrix. It is very important to house
tamarins separately from these animals. There is a protective vaccine available for this
disease. The vaccine is an attenuated variant of Herpesvirus T and is called T-SPV. This
vaccine prevents disease in tamarins, with vaccinated animals demonstrating high levels
of antibodies in 21 days following administration without showing any clinical signs of
illness (Melendez, 1976).

Herpesvirus saimiri, Herpesvirus ateles and Epstein-Barr virus (EBV)

Experimental infection with these viruses can be oncogenic in S. oedipus. Following

innoculation, they may lead to an aggressive neoplasm bearing a strong resemblance to
lymphoma. It is important to keep tamarins at a safe distance from cebids in zoos because
of the potential for infection. Callitrichids have been used extensively in the research of
EBV. For a summarized account of experimental studies with these viruses in
callitrichids, the reader is referred to Potkay (1992).

Human herpesvirus (Herpesvirus hominis or Herpes simplex)

There are no reports of natural infection with herpesvirus type 2 in callitrichids. Type 1
has been isolated from Saguinus sp. (Murphy et al., 1972). Experimental infection can
lead to fatality so it is recommended to avoid contact between the tamarins and humans
with active herpes fever blisters even though not much is known about the natural
potential for pathogenicity.

Cytomegalovirus (CMV)

CMV has been isolated from the salivary glands of S..fuscicollis without any signs of
clinical disease (Nigida et al., 1979). The presence of this virus in nonhuman primates is
usually an incidental finding at necropsy. In debilitated animals, it is important to be
aware of the possibility of clinical disease as a result of latent viral infections (Richter,
1984).

Varicella virus (Chickenpox)

There do not appear to be any reported cases of natural infection with this organism in
callitrichids.

Poxviridae

Monkeypox

Monkeypox resembles smallpox and is therefore a reportable disease (Ott, 1980).

Although uncommon in humans, it is a zoonotic disease. HI titers to monkeypox have
been identified in S. oedipus but the significance of this finding is unknown (Kalter et al.,
1974). The disease can be fatal in marmosets (Ott-Joslin, 1993). Transmission occurs
through direct contact with viral entry by way of skin abrasions or through the respiratory
route (Ott, 1980; Ott-Joslin, 1993).

Ott-Joslin (1993) describes lesions in nonhuman primates as occurring on the hands, feet,
hind limbs, buttocks, tongue, and the pharyngeal, laryngeal and tracheal mucosa. Lesions
involve small papules which coalesce resulting in the formation of vesicles which
develop reddish-brown crusts and slough after several days (Ott, 1980). Cellular
proliferation, epidermal cell degeneration and necrosis, and eosinophilic intranuclear and
intracytoplasmic inclusion bodies are seen on histological examination of lesions (Ott,
1980). Evaluation of lesions, histologic examination, and isolation of the viral agent are
useful for diagnosing infection. Serology is not very useful in diagnosing the disease
because antibodies are produced in low concentrations (Ott, 1980).

Paramyxoviridae

Parainfluenza

Disease caused by parainfluenza virus type I (Sendai strain) has been documented in
callitrichids with various degrees of clinical sips and disease. Fever, nasal and ocular
discharge, sneezing, coughing, tachypnea, dyspnea, conjunctivitis, piloerection,
depression and weight loss are some of the clinical signs that have been observed
(Murphy, et al., 1972; Flecknell et al., 1991). Pulmonary lesions may be seen at necropsy
(Murphy et al., 1972).

Parainfluenza virus types 2 and 3 (HA-1 strain) have been isolated from Saguinus
sp. without the presence of clinical signs (Murphy et al., 1972). Types 1 and 3 were
isolated from the lungs of affected animals in an epidemic viral infection of a callitrichid
population (Richter, 1984). Parainfluenza virus types 1 and 3 are frequent causes of
childhood respiratory disease and care should be exercised in keeping infected individuals
at an adequate distance from the tamarins (Richter, 1984).

Paramyxovirus saguinus

Gastroenterocolitis caused by a paramyxovirus was described in a colony

of S. oedipus (Fraser et al., 1978). This disease was associated with a high level of
mortality. Clinical sips included inappetance, anorexia, diarrhea and dehydration. Post
mortem findings included congestion and hemorrhage of the gastrointestinal tract. Colitis,
gastritis, enteritis and cholangitis were seen. Epithelial syncytia with intranuclear
inclusion bodies were associated with the colitis and cholangitis. In addition,
intracytoplasmic inclusion bodies were observed in the bile duct syncytial cells.

Morbillivirus

Measles (rubeola) is a highly contagious virus which is spread through aerosolization,

entering the host through respiratory or conjunctival mucosa. Fatal infection and clinical
disease associated with high morbidity has been reported in S. oedipus (Levy and
Mirkovic, 1971). This outbreak in a callitrichid colony resulted in 326 deaths. Clinical
signs included lethargy, swollen eyelids, mucous nasal discharge, rhinorrhea, facial
edema and maculopapular exanthema on the lips and skin. Death occurred within 8-18
hours following initial signs of disease. Yyule clinical signs and histopathology can aid in
the diagnosis of rubeola, isolation of the virus, serology or immunocytochemistry are
necessary for ruling out other paramyxoviruses and making a definitive diagnosis
(Potkay, 1992; Lowenstine, 1993).

There were not any significant gross post mortem findings. The main histopathological
finding observed at necropsy was interstitial pneumonia. Giant cells containing
eosinophilic intranuclear inclusion bodies were observed. Large monocytes were seen in
the lung parenchyma, some containing intranuclear inclusion bodies. Warthin-Finkeldey
(W-K) type giant cells were present in the mesenteric lymph nodes, spleen, lungs and
colonic lymphoid tissue. Animals surviving the infection were shown to have significant
levels of hemagglutination inhibition antibody (HIA) against measles. Tamarins that were
not exposed to the virus were negative for viral antibodies. See Lowenstine (1993) for an
in depth discussion of measles virus infection in nonhuman primates.

Both human measles vaccine and human gamma globulin, which is generally high in
rubeola antibodies, can be used prophylactically. Richter(1984)states that the use of
inactivated vaccine and human IgG are recommended for use in callitrichid colonies.
Vaccinating for measles does not appear to be standard protocol at zoological parks.
However, clinicians in many laboratory institutions choose to vaccinate callitrichid
colonies based on risk of exposure (D. Lee-Parritz, pers. comm.).

Clinicians should make an educated decision of whether or not to vaccinate tarnarins for
measles based on the conditions at each individual institution. Effective protection is
conferred by both killed and modified live vaccines (Lorenz & Albrecht, 1980). Ott (1
980), states that vaccination of marmosets with live vaccines is not recommended.

Arenaviridae

Callitrichid Hepatitis Virus (CHV)

This is a recently recognized, acute, fatal, epizootic disease of callitrichids. Epizootics

have only occurred in zoos and wild animal parks and have not been seen in laboratory
colonies (Montali, 1993). It has been determined that the agent responsible for this
disease is an arenavirus which is closely related to lyrnphocytic choriomeningitis virus
(Stephenson et al., 1991). Despite the fact that callitrichid hepatitis has not been
associated with human disease, appropriate care should be exercised when working with
infected monkeys (Montali, 1993). S. oedipus has been involved in prior outbreaks of this
disease (Ramsay et al., 1989). It is thought that rodents serve as reservoirs of this
organism (Ramsay & Montali, 1994; Ramsay et al., 1989). For this reason, the feeding of
mice to tamarins should be avoided and attempts should be made to minimize contact
with wild rodents. This disease is of serious concern due to the high incidence of sporadic
outbreaks with extremely high morbidity and mortality.

Clinical signs may include anorexia, depression, lethargy, dyspnea and adipsia. Death
often occurs without prior definitive signs. Mild lymphocytosis, and elevated levels of
serum aspartate arninotransferase (AST), alkaline phosphatase and bilirubin are seen
(Montali et al., 1989). These levels are indicative of hepatocyte injury and acute hepatitis.

Enlarged, sometimes mottled, yellow-tan livers are observed on post mortem examination
(Montali, 1993). Congested lungs, splenomegaly, jaundice, subcutaneous and
intramuscular hemorrhage, necrosis and inflammation in the spleen and lymph nodes, and
pleuropericardial effusion which can be sanguinous may be seen. In some recent cases,
nonsuppurative meningoencephalitis has also been observed (Montali, 1993). The liver
seems to be the primary organ targeted and extrahepatic lesions tend not to be severe
(Montali, 1993). All of these findings indicate that this disease is systen-iic but primarily
hepatotropic (Ramsay & Montali, 1994).

Histopathologic findings in both natural and experimental infection include swollen and
necrotic hepatocytes, and inflammation. Acidophilic bodies are found scattered
throughout the hepatic lobules. These represent remnants of hepatocytes which underwent
acidophilic degeneration (apoptosis) with the formation of acidophilic bodies (Montali et
al., 1989; Montali, 1993). In some cases, fatty change may occur in the liver and
lyinphoplasmacytic cellular infiltration may be present in the portal triads (Montali,
1993). Unlike with Herpesvirus T, there are no intranuclear inclusion bodies seen with
this disease (Montali, 1993). Characteristic histological changes can aid in the diagnosis
of this disease and definitive diagnosis can be made through serum and liver tissue
immunoblot assay evaluation.

Arboviruses

Yellow Fever

This disease is endemic in Central America, South America and Africa and is a potential cause of
mortality among captive tamarins in these areas. Transmission is via Aedes sp. and Haemagogus
sp.mosquito vectors. Mosquitos also act as reservoirs because once they are infected, they are
infectious for the remainder of their lives. Generally this disease is of little concern in non-endemic
areas. However, Aedes aegypti exists in the United States so this disease is potentially transmittable
in this country (Ott, 1980).

Rhabdoviridae

Lyssavirus (Rabies)

S. oedipus is susceptible to rabies and there is evidence to suggest that they may contract
the disease from modified live vaccines (Potkay, 1992). The form seen in monkeys is
usually of the paralytic type so they generally bite only if they are agitated and
transmission between monkeys and humans is very rare (Ott, 1980). The efficacy of
killed vaccines are not known and human vaccines are not effective in nonhuman
primates (Ott, 1980). However, INIRAB vaccine has been used successfully in a wide
variety of species which suggests that it would probably be effective in nonhuman
primates. Vaccination with killed vaccine is recommended for monkeys with high risk of
exposure. Clinicians must evaluate the situation at individual institutions where tamarins
are housed. Animals housed in open cages outdoors have more risk of being exposed.
Possibly the greatest potential for transmission is from bats which are small enough to
access open-bar cages. The prevalence of rabies in small rodents is extremely low so they
most likely do not pose a risk.

Retroviridae

There do not appear to be any significant reports of natural infections with retroviruses in
callitrichids. The reader is referred to Potkay (1992) for a summarized account of
numerous experimental studies in callitrichids. S. oedipus has been asymptomatically
infected with simian immunodeficiency virus (SIV) (Miura, 1989). However, there are no
reports of natural infection with this virus in callitrichids.

IV. OTHER DISEASES

Neoplastic

Colitis and adenocarcinoma of the large bowel

Colon cancer is one of the most deadly forms of cancer in humans. Cotton-top tamarins
are the only non-human primate known in which this type of tumor develops
spontaneously. In captive populations of cotton-tops with good nutritional practices, this
disease is the main cause of death. Other than those of the gastrointestinal system, the
incidence of spontaneous malignant neoplasms in cotton-top tamarins is very low.
Spontaneous colonic carcinoma occurs in about 35% of adult cotton-top tamarins in
captivity and is most likely to occur in animals 5-10 years old (Clapp & Henke, 1993).
Colitis and colon cancer either do not occur or are of relatively low incidence in natural
populations of S. oedipus (Wood et al., 1989).

Since cotton-top tamarins spontaneously develop colonic adenocarcinoma they are

considered an important model for the study of this disease. Colonic carcinoma has been
reported at several different institutions in widespread geographical locations (Clapp,
1993). This suggests that environmental factors may not play a major role in the etiology
of the disease, although they may exert some influence. A familial tendency is likely in
some cases.

Tamarins with colitis are often responsive to treatment with sulphasalazine. Diarrhea
usually resolves and the animal returns to its previous body weight. Histologic changes
often persist. Treatment is frequently given for one or two months and the status of the
animal is assessed by repeat colon biopsy. If severe changes persist, long-term therapy is
warranted. The animal should undergo regular examination because neoplasia is highly
likely in these animals, including palpation, biopsy, and contrast radiography when
available. Campylobacter is often present in tainarins with colitis (D. Lee-Parritz, pers.
comm.). However, the significance of Campylobacter is unknown at this time.

There is a strong link between colitis and colon cancer. The pattern frequently seen
involves the development of idiopathic ulcerative colitis observed prior to and during the
development of colon cancer. In S. oedipus, colon carcinoma develops either from
preexisting adenomas or more commonly from flat epithelium (Clapp & Henke, 1993). S.
oedipus colon cancer is considered to be multicentric in origin. Cancer probably
originates in flat mucosal areas changed by chronic colitis at the crypt base in the
reparative hyperplastic epithelium. Transformation of cells occurs, and the round,
pleiomorphic, transformed cells invade the lamina propria where they form poorly
defined colonies. Ulceration and erosion into the mucosal mass may occur resulting in a
malignant ulcer. There is often a sciffhous fibrous connective tissue response to
infiltrating neoplastic epithelial cells (J. Cooley, pers. comm). Metastasis occurs when
malignant cells enter the lymphatics of the mucosa and travel to the lymph nodes
(Lushbaugh et al., 1985). The neoplasm tends to metastasize to the regional lymph nodes,
less commonly to the pancreas and lungs, and infrequently to the liver.

Cachexia is commonly associated with the occurrence of disease. Currently, when weight
loss and chronic diarrhea occurs in this species, the most likely etiology is colitis and
possibly colon cancer. Acute colitic episodes may be asyrnptomatic. In symptomatic
cases, signs include loose stools, weight loss and lethargy.

Colonoscopy is useful in the evaluation and description of colitis. Colonoscopy and

biopsy are required for definitive diagnosis of colitis or colon cancer. The proper
procedure is well-documented (Clapp et al., 1993). A 5.0 mm fiberoptic pediatric
bronchoscope adapted for use in this species is used with simultaneous video image
display. Ulcers, nodules, hemorrhages and other abnormalities should be described and
biopsy samples collected from these lesions. Biopsy specimens are fixed in 10 % neutral
buffered formalin and histologic sections are prepared using routine techniques. Slides
should be routinely stained with Periodic Acid Schiff (PAS) stain and hematoxylin and
eosin. Histologic evaluation of colitis entails counting the number of inflammatory cells
in the lamina propria and epithelium, and describing the changes in crypt morphology.
Cases are considered chronic (inactive) when primarily mononuclear inflammatory cells
are present. Polymorphonuclear leukocytes are indicative of more acute (active) cases
(Clapp et al., 1993). Normal colons should not have elevated cellular infiltration of the
lamina propria. Mstopathological changes may include the presence of branched and/or
tortuous crypts and crypt atrophy.

Contrast radiography (barium enema) is helpful in the diagnosis of abdominal masses,

especially in the ileocecal region beyond the reach of the endoscope. Colon cancers often
appear as classic "apple-core" lesions. In an "apple-core" lesion, the bowel lumen is
constricted because of an intramural mass. The mucosal surface is often ragged because
of tumor gorwth. In a contrast radiograph, the barium column is contracted in the area of
the tumor and has the appearance of an apple core (D. Lee-Parritz, pers. comm.).

Appropriate postmortem examination initially involves culturing of samples from both

the ileum and colon and gross examination for plaque-like thickenings in colonic mucosa,
irregular plaques on serosa, and enlarged mesenteric lymph nodes, followed by collection
and fixation of tissue samples from all organs. The large and small intestines should be
laid flat and opened to facilitate the evaluation of the entire intestinal tract. Following
sampling for culture, the mesentery is cut adjacent to the intestine, the lumen is carefully
opened, avoiding wiping or rubbing the mucosal surface, and the entire remaining
intestine is immersed into fixative, usually 10 % neutral buffered fonnalin (J. Cooley,
pers. comm). This is followed by collection and fixation of tissue samples from all
organs.

Histopathological findings include effacement of normal colonic mucosal architecture

and PAS+ mucin-producing cancer cells which may be located in the submucosal
connective tissue and lymphatic spaces. Cancer extensions composed primarily of mucin
and malignant cells are visualized with the PAS stain, extending into the tunica
muscularis propria. Desmoplastic connective tissue is found around neoplastic cells. The
characteristic colonic cancer cells are easily recognized in metastases seen in other organs
(Lushbaugh et al., 1985).

Adrenal myelolipoma

Myelolipoma of adrenal origin has been identified in S. oedipus (Pearson et al., 1987;
Stein et al., 1982). The myelolipomas seem to occur in aged individuals. The juxtarenal
masses have not been considered to contribute seriously to clinical disease but may be
associated with some loss of body condition. The finding may be incidental at necropsy.

Necropsy findings from one of the cases describe a dark red, well-encapsulated, spherical
mass with some pale yellow areas. Histopathological findings included adipose tissue
containing hemopoietic tissue that resembled bone marrow and included megakaryocytes.
A thin rim of adrenal cortical cells and a connective tissue capsule were found in some
peripheral areas of the mass (Pearson et al., 1987).

Nutritional

Although understanding has greatly improved over the years, the nutritional needs of
callitrichids still remain poorly understood. For a list of references on current research in
the area of callitrichid nutrition, the reader can consult Potkay (1 992).

Hypoglycemia

Historically, hypoglycemia has been a problem in captive callitrichids and may be related to their
high metabolic rates (Cicmanec, 1977). Early clinical signs included muscle tremors and
unsteadiness. Fruits fed immediately following the onset were able to reverse early signs. For more
serious cases, 20% dextrose administered through a stomach tube along with insulin given
intraperitoneally were suggested. Alleviation or elimination of disease may be achieved by feeding
sugar in small amounts of feed many times throughout the day and by ensuring provision of
palatable feed.

Vitamin deficiencies

Tamarins require adequate vitamin C to avoid the onset of scurvy. Citrus fruits or
alternative supplements are appropriate supplemental sources of vitamin C. However,
citrus fruits may cause gastrointestinal distress so care should be exercised.

Vitamin D3deficiency used to be a widespread problem in callitrichid colonies resulting

in osteodystrophia fibrosa (rickets and osteomalacia). Vitamin D3 is required by New
World primates for normal bone metabolism. Vitamin D3 is more efficient at increasing
calcium absorption than vitamin D2(Hunt et al., 1967). New World monkeys are unable
to metabolize vitamin D2. Callitrichids have an even higher vitamin D requirement than
cebids because of a decreased sensitivity of the 1, 25 OH-D receptor. Now that the need
for D3 versus D2is understood, appropriate diets are usually formulated but it is
important to be aware of the possibility of faulty diet preparation (Richter, 1984).
Excessive feeding of insects should be avoided because these dietary components are
high in phosphorous and feedings may exacerbate marginal vitamin D nutrition by
inducing nutritional secondary hyperparathyroidism (D. Lee-Parritz, pers. comm.). The
suggested daily dietary value is 500 IU D3/monkey/week to prevent
hypovitaminosis D3(Hunt et al., 1967).

See Potkay (1992) for a discussion of other vitamin deficiencies observed in callitrichids,
both natural and experimentally induced.

Behavioral

Trauma caused by conspecifics

Physical conflicts between conspecifics may pose a serious health threat. Early detection
of injuries is vital to prevent abscess formation, septicemia, osteomyelitis and fatality.
Bacterial infection of wounds following fights in group-housed monkeys are common.
Bacterial culturing, antibiotic sensitivity testing and treatment should be undertaken
immediately but may not be necessary. Suturing of wounds is often successful if animals
are consistently monitored to prevent premature removal of sutures. Systemic and local
antibiotics should be administered in suitable cases.

Self-induced trauma

Self-mutilation has been known to occur. This may involve biting or hair pulling. Self-
inflicted alopecia can result. Attempts to increase the psychological well-being of the
animals by providing a diverse environment with suitable climbing structures, nest-boxes
and opportunities to hide from aggressive cage-mates is advised to minimize the
incidence of self-induced trauma.

Congenital

Congenital anomalies do not appear to be a common occurrence in cotton-top tamarins.

Achondroplastic dwarfism, polydactyly, and syndactyly have been observed in a newborn
male cotton-top tamarin. See Chalifoux (1993) for a description of the case.

Miscellaneous

Diarrhea

Diarrheal disease can be a very significant problem in captive tamarin populations.

According to Richter (1984), it is the largest cause of morbidity in tamarin colonies. The
cause in most of these cases goes undetermined. Some cases can be linked to bacterial or
viral causes while in other cases nutrition, behavior or other unknowns may play a role.
As previously discussed, chronic colitis has been linked in a causal relationship to colon
cancer in cotton-top tamarins whereas other Saguinus species may have clinically similar
colitis with the absence of colon cancer.

Signs include atony, megacolon and large quantities of feces. The feces often contain a
large amount of mucus. Coprophagy may occur in cases of diarrhea (Richter, 1984).

On postmortem examination, the large intestine is often enlarged and filled with gas or
ingesta. Histopathological findings include atrophy of crypts, inflammatory cell
infiltration of the mucosa and hyperplasia of residual crypts. Supportive therapy is
recommended for treatment of affected individuals. A slow recovery may occur in some
cases, while in others death may result (Richter, 1984).

Wasting Disease

This disease, which is known by several names, is an extremely significant disease of

poorly understood etiology. Since there may be many variable factors involved in each
individual case, it probably should not be considered a disease in itself but rather a
clinical syndrome. Potential causative factors may include stress, poor diet, heavy
parasitism, chronic bacterial infection and colitis.

Marmoset wasting disease is clinically characterized by rapid and persistent weight loss
with skeletal muscle atrophy especially seen in the legs. When a drop in body weight is
seen, this disease should be considered. Anemia and hypoproteinemia with associated
cervical or ventral edema commonly occur (Richter, 1984). Alopecia is often observed,
especially on the tail. Weakness or paralysis of the hind legs, intermittent diarrhea and a
wet or greasy appearance to the fur may be seen (Potkay, 1992). Affected animals are
particularly prone to acute episodes of hypoglycemia with associated hypothermia. Rectal
temperatures may drop as low as 300C and blood glucose levels may decrease to as low
as 40 mg/dI. Attempts should be made to increase body temperature and blood glucose
levels and to avoid the onset of Gram negative shock (Richter, 1984).

Post mortem findings include emaciation, muscle mass reduction and almost complete
absence of body fat. Other possible findings include colon or other gastrointestinal or
pancreatic lesions, Prosthenorchis, and Trichospirura. The nutritional and parasite
control program should be carefully evaluated in colonies with a high incidence of
marmoset wasting disease. Sporadic cases are likely the result of colitis or chronic
metabolic illness (D. Lee-Parritz, pers. comm.).

It appears that most treatments have been geared towards altering feeding and nutrition in
various ways. Treatment approaches should be tailored to the individual case based on
possible etiologies and necessary supportive therapies. Efforts should be made through a
problem oriented medical approach to narrow down the possibilities, and the original
cause treated appropriately.

Intussusception

Intussusception occurs relatively frequently in callitrichids. What leads to intussusception

is unclear but it probably involves increased gut motility following irritation due to
inflammation from infection, parasites, toxins or other causes. The occurrence of
intussusception and rectal prolapse are often associated.

Successful surgery in S. oedipus has been documented (Blampied & Allchurch, 1983).
This involved a case where the ileum had passed through the ileocecal valve and
telescoped into the anterior colon. Repeated episodes and treatment of rectal prolapse
occurred prior to identification of intussusception and surgery. In a prior case, a cotton-
top tamarin died following repeated episodes of rectal prolapse and replacement.
Intussusception was found on necropsy (Blampied & Allchurch, 1983).

The most common location for intussusceptions are the terminal ileum. It is very
uncommon for rectal prolapse to occur in the absence of intussusception, therefore rectal
prolapse should be treated by laparotomy and cecocolopexy rather than simple reduction
(Richter, 1984).

Acute shock is often seen with small intestine intussusception and this along with
palpation can be used to aid in diagnosis. Intussusceptions are serious emergencies
requiring immediate attention.

Mesangioproliferative Glomerulonephropathy

A retrospective study was carried out at the German Primate Center of all callitrichids,
including a number of S. oedipus, necropsied beginning in 1973 (Brack, 1988). The study
revealed that 91% of tamarins over 6 months old had spontaneous IgM-mediated
mesangioproliferative glomerulonephropathy. Inflammatory renal lesions were found to
be the most common organ lesions seen at necropsy. The disease is considered to be
involved in about 20 % of all the callitrichid deaths at the German Primate Center. The
destruction of increasing numbers of glomeruli influenced or resulted in the fatalities
observed. Genetics appeared not to play a role in the occurrence of this disease.

There were no distinct clinical signs but up to 88% had continuous or transient hematuria
and/or proteinuria, with urinary casts. Post mortem findings included mesangiosclerosis,
proliferation and sclerosis of Bowman's capsule, intraglomerular adhesions, and
glomerular sclerosis. IgM deposits were found in strong association with the mesangial
lesions along with Clq, C3 and C4 which is suggestive of classical complement pathway
involvement. This is similar to human IgM nephropathy. Nothing is known about the
origin and nature of the antigen causing the mesangial IgM deposits and resulting lesions
in callitrichids.

Toxicities

Inadvertant poisoning may occur and it is important to be careful of all substances that
may come in contact with tamarin populations.

V. ANESTHESIA

For brief restraint or phlebotomy, the injectable anesthetic, ketamine (10-20 mg/kg), is
safe and effective for adult tamarins (D. Lee-Parritz, pers. comm.). A combination of
ketamine (25 mg/kg) and midazolain Hcl (25 mg/kg) is effective for procedures that
require the animal's body to be less rigid (Savage et al., 1993). Isoflurane is the anesthetic
of choice for major surgical procedures. If gas anesthetics are not available, telazol or
pentobarbitol may be used but neither provides good analgesia and pentobarbitol has a
narrow therapeutic window (D. Lee-Panitz, pers. comm.). Pentobarbitol is a traditional
method of anesthesia requiring minimal equipment and little expense but it is important to
keep in mind that it does not provide good analgesia unless it is given at levels where it
depresses respiratory reflexes (C. Sedgwick, pers. comm.).

VI. ALLOMETRIC SCALING

For safe and effective administration of injectable drugs, it is important to allometrically

scale doses using specific minimum energy cost (SMEC) values. Theoretically, SMEC is
the energy per unit of body size (kcal/kg) that an animal uses to maintain bodily functions
at physiologic rest. SMEC = K(W kg0.75)/W kg = K(W kg-0.25) where K is 70 for
placental mammals and W is the animal's weight in kilograms. MEC = K(W kg0.75) so
SMEC is the MEC value divided by the animal's weight in kilograms. To determine the
SMEC-dose of a drug, the dose rate (mg/kg) of the control animal is divided by the
control animal's SMEC (C. Sedgwick, pers. comm.).

The proper doses of many drugs are unknown for tamarins so doses can be scaled using
the standard human pediatric dose. Attempts should be made to accurately deten-nine the
animal's weight in a triple beam balance prior to administration of the drug and the
following procedure using the example of ceftriaxone in a 500 g cotton-top tamarin
should be implemented to determine proper dosages.

According to the Physician's Desk Reference (1 995), the human pediatric daily dose rate
is 100 mg/kg. Using a weight of 20 kg for a human child:

SMEC = K(W kg-0.25= 70(20 kg-0.25) = 33

SMEC-dose = dose rate/SMEC = 100/33 =3

For a 500 g cotton-top tamarin:

SWC = 70(0.5 kg-0.25) = 83.2

Scaled dose rate = SMEC x SMEC-dose = 83.2 x 3 = 250 mg/kg

Scaled dose = 250 mg/kg x 0.5 kg = 125 mg

To illustrate the importance of scaling based on body weight, using the extreme example
of a 60 kg female gorilla, the scaled dose rate would be 75 mg/kg which is vastly
different from that of the cotton-top tamarin. This is because smaller animals have a
greater surface area to volume ratio. For a more in-depth discussion of scaling principles
and strategies, see Sedgwick (1993).

This principle of scaling does not need to be adhered to in the administration of inhalant
anesthetics. Inhalant anesthetics are effective at just about the same percent concentration
independent of the size of the animal because smaller sized animals have a greater
absorptive lung surface per unit of mass than larger animals. This is necessary due to their
higher metabolic rates (C. Sedgwick, pers. conun.).

VIII Research
Chapter Summary

 Evaluating our current captive management practices is a priority of the

Cotton-top Tamarin SSP Management Group.
 A series of projects for investigation are suggested for those individuals
wishing to pursue a research project.

Why conduct research?

From a husbandry perspective, the main function of research is to gather the information
needed to make good management decisions. In order to successfully maintains a healthy
population of cotton-top tamarins in captivity, we need to have a clear understanding of
their life in the wild. Using the information gathered from field studies we can begin to
develop management practices that will ensure that the species maintain the behavioral
characteristics found in wild animals. However, when implementing management
practices, it is critical that we evaluate whether these approaches really assist in
maintaining a desired behavior. Although, much information can be gathered through
informal observation, it is critical that we evaluate the success of our husbandry practices
using the scientific method.

Conducting Research: The Scientific Method

The steps to conducting a scientific study are as follows:

1. Conduct informal observations on your desired species.

2. Form a question based on your informal observations (Why do captive cotton-top

tamarins develop colon cancer and wild tamarins appear not to develop this disease?)

3. Conduct additional observations and an extensive literature search to assist in

refining your question.

4. Construct, if possible, mutually exclusive hypotheses (putative answers to your

question)

"Mutually exclusive" means that you attempt to frame your question so that one, and only
one, hypothesis is correct. This is not always possible, especially since many natural
phenomena have a plethora of interacting causes, but it makes for the strongest studies.
For example, possible hypotheses relating to colon cancer in cotton-top tamarins include:

i) The diet fed to cotton-top tamarins in captivity causes colon cancer.

ii) The stress of captivity causes colon cancer.

iii) Cotton-top tamarins are genetically predisposed to colon cancer.

iv) Wild cotton-top tamarins are consuming some item that prevents them
from developing colon cancer.

v) etc.

Note that these hypotheses may or may not be mutually exclusive (we may be feeding
them an inadequate diet and they may be genetically predisposed to colon cancer).
 5. Make testable predictions based on your hypotheses (for example, if cotton-top
tamarins were genetically predisposed to colon cancer, you would predict that the cancer
was heritable, and that tamarins who eventually develop colon cancer would tend to have
offspring that develop the same disease).

It is at this stage of the experimental design that you set up appropriate controls for
confounding variables. For example, to examine the hypothesis that animals may be
genetically predisposed to cancer, you would examine the occurrence of cancer in
offspring from animals of a specific genetic line that appear to develop cancer and
another genetic line that appear to be cancer-free. These animals would be housed under
the same environmental conditions (diet, type of habitat, enrichment opportunities etc.).
Thus, the cancer-free group of animals is the control group, and assures that any effect
you see is due to genetics, and not diet, habitat, etc.

6. Identify the behavior or other variables that are pertinent to your study and select
a sampling method.

How to select a sampling method and appropriate behavior depends on your hypothesis to
be tested. Two references to aid you in the development of your sampling method are:

-Martin, P. & Bateson, P. Measuring Behavior Cambridge University Press, Cambridge,

1996.

-A videotape and handbook entitled Research Methods for Studying Animal Behavior in a
Zoo Setting, produced jointly by the Washington Park Zoo and the Minnesota Zoological
Gardens.

7. Consult with a statistician before you collect data.

One of the most common mistakes people make in designing a study is the introduction
of a confounding variable or a procedural error that makes the data insufficient to answer
the question being asked.

8. Collect data.

9. Analyze the data.

You may need the help of a statistician to assist you in analyzing and interpreting your
data.

10. Interpret results and draw conclusions.

Remember when you interpret your results, science can only disprove hypotheses, it can
never prove them. A very simple example to illustrate this point: You could
easily eliminate ideas such as "Cotton-top tamarins tend to develop colon cancer because
they are a small New World Primate." We can reject this hypothesis, since there are many
other callitrichids that are the same size as cotton-top tamarins but do not develop colon
cancer. Therefore, size does not appear to be a feature important in the development of
this disease. However, you cannot say that "Because colon cancer in cotton-top tamarins
is heritable (if it is) that cancer is definitely caused by genetic factors", since apparently
heritable effects might have a non-genetic cause (such as individuals all housed in an
environment that contains some overlooked feature that predisposes occupants to colon
cancer ).

11. Disseminate results

It is critical that your results are published in peer-reviewed journals, newsletters, or

conference proceedings. Sharing your results at conferences will aid in developing a good
dialog with your colleagues and pen--nit others to implement your findings.

12. Form new research questions.

Continue to build on what you have already learned or develop new areas of
investigation.

Research Proposals

Completing a research proposal, even for a study conducted in-house, is a valuable

exercise, for it allows you to examine your research question and methodology. Many
zoos have their own research proposal application form. However, for those institutions
that do not currently have a protocol, the following outline, taken from a draft version of
the AZA research guide, gives the basic elements that should be included in as research
proposal.

A research proposal should let a reviewer determine:

I. The scientific validity and implication of the project.

II. The likelihood that the project will be successful.

III. The costs of the project.

Proposals should contain the following information:

I. Description of the Project

A. Title (concise but informative)

B. Project Summary or Abstract

C. Goals and Implications

D. Background Information (includes references to relevant studies)

E. Materials and Methods

a. Project Protocol

i. Sampling Methods

ii. Experimental Design and Manipulations

iii. Data Analysis

iv. Dissemination of Results

F. Reference List

II. Qualifications of Investigator(s)

A. Name

B. Institutional Affiliation

C. Address, Phone, Fax, Email

D. Attach Curriculum Vitae

a. Include relevant experience

b. Special skills appropriate to the project

c. List of publications

III. Budget (time and materials)

A. Zoo resources needed

a. Animals

i. Animals currently held

ii. Necessary acquisitions of animals

b. Staff Involvement

i. Number of staff

ii. Number of hours/week of staff time

 iii. Primary contact at the zoo

B. Resources supplied by the investigaton

a. Equipment

b. Supplies

c. Personnel

C. Schedule of Completion

Most zoos require the approval and permission of a research review committee and/or an
Institutional Animal Care and Use Committee.

Suggested Format

I.Cover Page

A. Title

B. Summary

C. Investigator Information

a. Name

b. Institutional Affiliation

c. Address, phone, fax, email

D. Primary zoo contact person, if any

II. Body of the Proposal

A. Goals and Implications

B. Background

C. Methods and Materials

D. References

III. Appendices

A. Budget
B. Schedule of Completion

C. Curriculum Vitaes

D. Other Pertinent Material

Resources Available to Aid You in Your Research

There are many resources available to assist you in the design and implementation of
meaningful research projects. These include:

* A videotape and handbook entitled Research Methods for Studying Animal Behavior in
a Zoo Setting, produced jointly by the Washington Park Zoo and the

Minnesota Zoological Gardens.

* The Experimental Design and Statistics Subcommittee of the AZA Behavior and
Husbandry Group, which offers the following services:

- Assistance with experimental design questions

sampling methods

controls

sample size

analysis tools

etc.

- Assistance and advice on statistics

assumptions

robustness

sensitivity

sample size

etc.

- Proposal Pre-review

For further information on these services contact:

Dr. William R. Langbauer Jr. Helena Fitch-Snyder
Research Director Animal Behavior Specialist
Pittsburgh Zoo C.R.E.S.
One Hill Road San Diego Zoo
Pittsburgh, PA 15206 P.O. Box 551
San Diego, CA 92112
(412) 665-3766 phone (619) 557-3954 phone
(412) 665-3661 fax (619) 557-3959 fax

Cotton-top Tamarin SSP Management Group Recommendations for Research Projects

Cotton-top tamarins have been extensively studied in research laboratories for the past
several decades. Moreover, recent field studies have aided our understanding of this
complex callitrichid. However, there is a vital need for studies of tamarins in zoo
populations, particularly in evaluating current management practices. The following are
some suggestions for research projects developed by the Cotton-top Tamarin
SSP Management Group:

1. Studies contrasting the reproductive success of parent-reared, hand-reared, and cross-

fostered cotton-top tamarins.

2. Studies of the long-term stability and optimal composition of step-parent (foster)

groups.

3. Studies examining the adaptability of cotton-top tamarins in free-ranging zoo

programs.

4. Studies of diet and nutrition.

5. Studies examining the occurrence of colon cancer in the zoo population using the
improved methods of detecting this disease (see veterinary care chapter).

6. Studies examining alternative means of contraception. Please note this should be in

conjunction with the AZA Contraception Advisory Group.

7. Studies examining the effectiveness of environmental enrichment programs.

We welcome any additional suggestions or ideas. Please contact Rebecca Sellin if you are
interested in pursuing any of the above projects.

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Appendix I

THE UNIVERSITY OF CALIFORNIA COLLEGE OF VETERINARY

MEDICINE November 15, 1999

Department of Pathology, Microbiology, Immunology

Haring Hall
University of California
Davis, CA 95616
phone: 530- 754-7567 FAX: 530-752- 3349

Dear Zoological Veterinarian,

Because of increasing concerns that contraceptives may be causing pathological effects in

the reproductive organs of many species, the AAZPA Contraceptive Committee
Pathology Survey will be extended to INCLUDE THE REPRODUCTIVE TRACTS OF
ALL FEMALE CARNIVORES AND PRIMATES. We will also be CONTINUING THE
SURVEY OF FELID REPRODUCTIVE TRACTS. I would be very grateful if you would
be willing to participate in the continuation of this study in felids and initiation of this
survey in carnivores and primates.

For this study, I need intact, fixed reproductive tracts (uterus and ovaries) from ANY
FEMALE CARNIVORE OR PRIMATE, REGARDLESS OF THE CONTRACEPTIVE
HISTORY. Reproductive tracts either from necropsies or ovariohysterectomies would be
appropriate. The tracts can be fixed in buffered formalin by emersion of the entire tract
for 72 hours if a small incision is made into the lumen of the uterus at each horn (ratio of
tissue to formalin = 1:10). Fixed tracts then can be wrapped in formalin-soaked paper
towels, enclosed in a leak-proof plastic bag and shipped by ground US mail (Federal
Express is not necessary). I have enclosed several mailing labels to make this more
convenient. For this study, it is essential that you also provide the INFORMATION
REQUESTED ON THE ENCLOSED FORM. This provides valuable data on the
duration and dose of contraceptive treatment and the effects of age and parity on the
lesions.
When the data is collated, I will send a brief report on the reproductive tract to you and
will be certain to acknowledge your contribution in any publication resulting from this
study.

I thank you in advance for contributing to this study. I am hoping that the results will
provide information that will allow us to use these contraceptives in regimes that will
minimize disease problems.

Sincerely yours,

Linda Munson, D.V.M., Ph.D.

THE UNIVERSITY OF CALIFORNIA COLLEGE OF VETERINARY

MEDICINE November 15, 1999

AZA CONTRACEPTIVE PATHOLOGY SURVEY

SUBI@MTTING VETERINARIAN:

ZOO:

ADDRESS:

ANIMAL ID: ISIS: ZOO ID: SB#: NAME:

SPECIES: DATE OF BIRTH:

DATE OF DEATH OR SPAY: WEIGHT:

BREEDING HISTORY:

HAS THIS ANIMAL BEEN CYCLING?

HAS THIS ANIMAL BEEN BRED?

NUMBER AND DATES OF PREGNANCIES:

FOR MELENGESTROL IMPLANTS:

HAS THIS ANIMAL SHOWN ESTRUS WHEN IMPLANTED?

IMPLANT# IMPLANT WEIGHT ANIMAL WEIGHT DATE INSERTED

DATE REMOVED

_____________ __________ ___________ ___________ ____________

_____________ __________ ___________ ___________ ____________

_____________ __________ ___________ ___________ ____________

_____________ __________ ___________ ___________ ____________

FOR OTHER CONTRACEPTIVES:

CONTRACEPTIVE TYPE:

DOSE OF CONTRACEPTIVE:

DATES OF TREATMENT:

Appendix II
DISEASE MONITORING IN CAPTIVE CALLITRICHIDS

The most effective and complete disease monitoring in captive callitrichids can be
accomplished through a centralized pathology database. ALL CAPTIVE
CALLITRICHIDS THAT DIE SHOULD RECEIVE A COMPLETE NECROPSY AND
ALL TISSUES SHOULD BE ANALYZED BY HISTOPATHOLOGY. Results of the
gross and histopathological examinations (Final necropsy report) should be submitted to
the Cotton-top Vet Advisor (Dr. Don Neiffer) for entry into the Callitrichid Disease
Database. The database then will be available to zoological veterinarians for developing
optimal medical management programs for specific species of callitrichids. The
Callitrichid Disease Database also will be available to monitor disease trends in the
captive population and to compare disease prevalences between free-ranging and captive
callitrichids.

Submit necropsy to:

Rebecca Sellin
PO Box 10,000
Lake Buena Vista, FL 32830-1000
Phone: (407) 938-1986
FAX: (407) 939-6391

POST MORTEM EXAMINATION OF CAPTIVE COTTON-TOP TAMARINS

A complete necropsy should be performed on any captive Cotton-top tamarin that dies. A thorough
necropsy provides data for the Cotton-top tamarin Disease Database on that species and is a means to
assess the success of captive management and preventative disease programs. The following is the
recommended protocol for Cotton-top tamarin, so that a complete data set can be collected on each
individual.

Upon death of a Cotton-top tamarin at your institution, please submit the complete medical record
(including details of the diet), results of the gross necropsy report, culture results, and results of
histopathologic examination to the Cotton-top Tamarin SSP coordinator. You are encouraged to
collect a duplicate tissue set in formalin to be submitted to the veterinary advisor. Assistance
with histopathology may be available through coordination with the veterinary advisor and an
associate pathologist.

SSP Coordinator Veterinary Advisor Associate Pathologist

Rebecca Sellin
Disney’s Animal Kingdom
1200 N Savannah Cir. E.
Bay Lake, FL 32830
Phone: (407) 938-1986
Fax (407) 939-6391
Dr. Don Neiffer
Disney’s Animal Kingdom
1200 N Savannah Cir. E.
Bay Lake, FL 32830
Phone: (407) 938-2719
Fax: (407 939-1909
Dr. Scott Terrell
Disney’s Animal Kingdom
1200 N Savannah Cir. E.
Bay Lake, FL 32830
Phone: (407) 938-2746
Fax: (407) 939-1909

Cotton-top tamarins have a high incidence of colon cancer (adenocarcinoma) and this species has
been used as an animal model for the study of colon cancer in humans. There is a strong link
between colitis and colon cancer. When providing the history of the animal, please include any
episodes of colitis or diarrhea prior to death. The distal ileum and colon should be examined
closely during the gross necropsy. The colonic tumors may be obvious or may present as a subtle
focal constriction or thickening of the colon wall. A large portion of the distal ileum and colon
should be collected in formalin for histologic examination (see collection techniques at end of
document, be sure to maintain the proper tissue/formalin ratio of 10:1). Dr. Scott Terrell is interested
in examining formalin fixed tissue from suspected or confirmed cases of cancer in Callitrichids.

A number of pathologists have noted on histopathology, a high incidence of iron pigment present in
the liver. In order to continue to track the incidence of iron pigment accumulation, the Neotropical
Primate TAG is requesting that all institutions include special stains for iron in their
histopathology protocols. Sections of liver measuring 1cm3 should be saved frozen (-70 to -80F)
as well.

Dr. Linda Munson at the University of California (Davis) is examining the reproductive tracts of
captive female carnivores and primates. Dr. Munson would like whole reproductive tracts
collected in formalin from necropsies or ovariohysterectomies. For details and submission form
please see Appendix I in the table of contents.

CALLITRICHID NECROPSY PROTOCOL

Institution/owner: Prosector:
Address:

Species: Animal ID: Studbook#:

Birthdate / age: Weight:

Date of death: Date of necropsy:

Manner of death: Spontaneous Euthanasia

History: (include clinical signs, circumstances of death, past history of diarrhea/colitis)

Blood or serum collected?: (Fresh or from carcass)

General condition: (Nutritional condition, physical condition)

Musculoskeletal system: (Bones, joints, muscles)

Body cavities: (Fat stores, abnormal fluids, serosal surfaces)

Hemolymphatic: (Spleen, lymph nodes, thymus)

Respiratory system: (Nasal cavity, larynx, trachea, lungs, regional lymph nodes)

Cardiovascular system: (Heart, pericardium, great vessels)

Digestive system: (Oral cavity, esophagus, small intestine, colon, liver, pancreas, mesenteric lymph
nodes)

Urinary system: (Kidneys, ureters, urinary bladder, urethra)

Reproductive system: (Testis/ovary, uterus, vagina, prepuse, accessory glands, mammary glands,
placenta)

Endocrine system: (Adrenal glands, thyroids, parathyroids, pituitary)

Nervous system: (Brain, spinal cord, peripheral nerves)

Sensory: (Eyes, ears)

Integument: (Skin)

FOR NEONATES

1. Fix umbilical stump and surrounding tissues

2. Look for congenital defects (cleft palate, atrial/ventricular septal defects, limbs)
3. Assess hydration and evidence of nursing (milk in stomach)
4. Determine if breathing occurred (do lungs float in formalin)
PRELIMINARY OBSERVATION / DIAGNOSES:

TISSUES SUBMITTED FOR HISTOPATHOLOGY (Yes/No?):

LABORATORY STUDIES: (List bacterial, fungal and viral cultures submitted)

ORGAN MEASUREMENTS / WEIGHTS:

Heart weight: _________________g

Left ventricular freewall thickness _________________mm

Right ventricular freewall thickness _________________mm

Interventricular septum thickness _________________mm

Liver weight: _________________g

Spleen weight: _________________g

Right kidney weight: _________________g

Left kidney weight: _________________g

Right adrenal weight: _________________g

Left adrenal weight: _________________g

Right thyroid weight: _________________g

Left thyroid weight: _________________g

Total brain weight: _________________g

Cerebellum weight: _________________g

TISSUE CHECK LIST

Preserve the following tissues in 10% neutral buffered formalin at a ratio of 1 part tissue to 10 parts
formalin. Tissues should be no thicker than 1cm. Include sections of all lesions and samples of all
tissue listed in this checklist. See additional tissues on neonatal checklist.

Heart ____ Trachea ____ Thyroid gland ____

Lung ____ Parathyroid ____ Thymus ____

Lymph nodes ____ Spleen ____ Liver ____

Esophagus ____ Stomach ____ Duodenum ____

Pancreas ____ Jejunum ____ Ileum ____

Cecum ____ Colon ____ Adrenal ____

Kidney ____ Urinary bladder ____ Testis/ovary ____

Uterus ____ Prostate ____ Brain ____

Skin ____ Skeletal muscle ____ Tongue ____

Diaphragm ____ Bone marrow, femur ____ Bone, rib ____

Spinal cord ____ Gall bladder ____

For neonates: Umbilical stump and associated tissues ____

ESSENTIAL FROZEN TISSUE (If organs are small, freeze what remains after collection of tissue
for histopathology. Freeze one half of lesions and place remaining tissue in formalin).

Heart ____ Lung ____ Liver ____

Spleen ____ Kidney ____ Skeletal muscle ____

Adipose tissue ____ Small intestine with contents ____

Brain ____ Any lesions or suspicious tissues ____

Serum ____ Whole blood ____

RECOMMENDED TISSUE SAMPLING PROCEDURES

Adrenal glands: If no visible lesions, submit 1 whole gland in formalin

Brain: Slice longitudinally along midline, ½ in formalin, ½ frozen

Gastrointestinal tract: Unopened cross section of esophagus, duodenum, jejunum, approximately
0.5cm in width. The duodenal cross section should include adjacent pancreas. A 5-10cm length of
jejunum should be tied off unopened with string and frozen whole for future toxin analysis. The
distal ileum and colon should be submitted whole. The entire distal ileum and colon should be
opened longitudinally along the anti-mesenteric border (swiss role technique). Be careful not to
touch or wipe the opened mucosa!

Heart: Long axis sections including atrium, valve and ventricle on both left and right

sides. Include a section of great vessels, aorta. Freeze remaining tissue.

Kidneys: Cut longitudinally and submit ½ of each kidney. Freeze remaining tissue.

Liver: Sections from 3 lobes with capsule and portion of gall bladder

Long bone / bone marrow: Submit distal femur split in ½, include growth plate

Lungs: Sections from cranial and caudal lobes on both left and right sides. Freeze 1 or more lobes.

Spleen: 1 transverse section

Lymph nodes: Cervical, mediastinal, bronchial, mesenteric, ileocecal

Pituitary: Entire gland

Reproductive tract: Entire uterus of female. One whole ovary. Entire testis cut transversely.

Sciatic nerve: 3mm section with adjacent muscle.

Tongue: Section from distal tip

Skeletal muscle: Section from thigh muscles, freeze tissue as well.

Spinal cord: Sections from cervical, thoracic, lumbar spine

Thymus: Section if present

Thyroid / parathyroid: Submit whole gland(s)

Urinary bladder: Submit whole