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.

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

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

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.

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)

Day of Life	Amount of Formula/Food Offering per Feeding	Duration between Feedings	Number of 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
34-36	5.8 ml Primilac, 1.0-1.5 ml yogurt/ Gerber high-protein baby cereal	4 Hours	4
37-39	5.8 ml Primilac, 1.5-2.5 ml yogurt/Gerber high protein baby cereal/egg or fruit mash (banana, applesauce, apples, pears)	4 Hours	4
40-46	7.0 ml Primilac, 2.5-3.5 ml  Gerber high-protein baby cereal/yogurt/ fruit and egg mash	4-5 Hours	3
47-53	5.0 ml Primilac, 3.5-4.0 ml yogurt/Gerber high-protein baby cereal/fruit and end egg mash	8 Hours	2
54-60	Primilac gradually decreased by 1.0ml each day.   Hill's ZuPreem Marmoset diet starts on day 54.  Gradually solid foods   increased.	8 Hours	2
60-90	Supplemental feeds of 1/4 cup yogurt, Gerber high-protein baby cereal/egg mash		2

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).