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Breeding performance of captive-born cotton-top tamarin (Saguinus oedipus) females Proposed explanations for colony differences.

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American Journal of Primatology 11271-275 (1986)
Breeding Performance of Captive-Born Cotton-Top Tamarin
(Saguinus oedipus) Females: Proposed Explanations
for Colony Differences
Marmoset Research Center, Oak Ridge Associated Uniuersities, Oak Ridge, Tennessee
Successful breeding by captive-born Saguinus oedipus females has now been
reported from several colonies, but a marked parity effect (ie, differences in
infant survival with the number of litters produced) is usually observed;
survival of infants of primiparous females is extremely low but increases
with subsequent litters. This parity effect was not observed in the captiveborn breeding females in the Oak Ridge Associated Universities colony,
with survival of offspring of primiparous females a t 58.6%. Two explanations are proposed for this difference: (1)pairing with a male having previous experience in siring and rearing offspring may improve infant survival
for primiparous females; and (2) postponing mating to a later age may
increase infant survival for primiparous mothers.
Key words: tamarin, reproduction, husbandry, parental behavior
Successful captive breeding of the cotton-top tamarin (Saguinus oedipus) is
critical to the species’ continued use in research and to its conservation. S. oedipus
represents a unique research resource for the study of spontaneous colon cancer
[Clapp et al, 19851and EBV-induced lymphoproliferative disease [Hanto et al, 19851.
However, the species is critically endangered in the wild [Cerquera, 1985; Mittermeier & Coimbra-Filho, 1983; Tardif, 19851. Extensive efforts have gone into improving the captive breeding performance of this species, and in the past 10 years,
survival of offspring of wild-caught animals has increased from 25-35% to 50-70%
in most large colonies [Gengozian e t al, 1978; Hampton et al, 1978; Kilborn et al,
1983; Kirkwood et al, 1983; Tardif et al, 1984al.
Until recently, the breeding performance of captive-born animals (particularly
females) was frequently reported to be far inferior to that of wild-caught animals
[Kilborn et al, 1983; Tardif et al, 1984al. Breeding performance of captive-born
females equivalent to that previously reported for wild-caught mothers has recently
been reported by Kirkwood et a1 [1985] for the colony a t the University of Bristol,
and by Snowdon et a1 [1985] for the University of Wisconsin colony. Reports from
Received March 3, 1986; revision accepted June 20, 1986.
Address reprint requests to Suzette D. Tardif, Marmoset Research Center, Oak Ridge Associated Universities, Oak Ridge, TN 37831.
0 1986 Alan R. Liss, Inc.
272 1 Tardif, Carson, and Clapp
both colonies indicate similar pronounced parity effects: infant survival for primiparous females is low (9-18%) but increases as females produce subsequent litters
(to 60-70%). In both colonies, the majority of infant losses is attributed to inadequate
parental behavior.
The following is a report on the reproductive performance of colony-born S.
oedipus females in the colony a t Oak Ridge Associated Universities. These results
are compared with those of other colonies, and explanations for differences in
breeding success between the colonies are proposed.
Details on the husbandry, diet, and management of the Oak Ridge breeding
colony have been published previously [see Richter, 1984; Clapp & Tardif, 19851.
Briefly, all breeding animals were housed as mated pairs with up to three litters of
offspring in 127 x 153 x 153-cm cages. All pairs were visually isolated but could
hear and probably smell other animals.
Between September 1979 and December 1985, 17 colony-born females had produced a total of 81 young in 42 deliveries. All females had experience with infant
siblings prior to being mated (experience is defined here as being present during the
rearing of infant siblings). The following parameters were compiled for comparison
with other published reports: (1) percent of births that were abortions or stillbirths;
(2) percent survival of live-born offspring for first, second, and t h i d f o u r t h deliveries;
(3) mean age at mating; and (4) mean age a t first delivery. A chi-square test was
used to determine whether there was a significant association between parity and
infant survival. In addition, infant survival in pairs with proven (ie, having previously sired offspring and reared them to weaning) versus unproven or previously
unsuccessful males was compared using a chi-square test. Both the proven and the
unprovedunsuccessful groups contained wild-caught and captive-born males. There
was one wild-caught male who had not previously bred in captivity. He was considered unproven.
Losses that were due to abortion and stillbirth of full-term young accounted for
9.4%of the 85 young born. The loss is less than the 20% previously reported for the
wild-caught Oak Ridge breeding population [Tardif et al, 1984al or the 29.0%
reported by Kirkwood et a1 [1985] for the captive-born Bristol breeding colony. The
5% loss reported by Snowdon et a1 [1985] for the captive-born Wisconsin colony is
outstandingly low.
Table I shows the number of infants born and the number and percent surviving
to 6 months for first, second, and third/fourth deliveries. There was a tendency for
infant survival to decrease with increasing parity, but the effect was not significant
(x2 = 0.96, P < 5).While the small sample size makes conclusions tenuous, this
trend may be due to the fact that triplet births were more frequent in later deliveries. In the present sample, infant survival was significantly lower in triplet litters
(33.0%)than in singleton or twin litters (62.5%)(x2 = 6.66, P < .Ol), with infants
from triplet litters frequently having low birth weights ( < 40g). When infant survival of singleton and twin litters only was compared, there was a tendency for
infant survival to increase with increasing parity (54.5%, 66.7%, and 72.7% for
deliveries 1,2, and 314, respectively), but again the effect was not significant (x2 =
1.12, P < 5).While Kirkwood et a1 [1985] do not list litter size ratio by delivery, the
overall percent of triplet litters born in the Bristol colony was similar to that
observed at Oak Ridge (24% vs 30%). Snowdon et a1 [1985] reported a much lower
overall occurrence of triplets (2%) a t Wisconsin, which probably contributed to
higher overall infant survival.
Breeding by Captive-Born Suguinus oedipus Females I 273
TABLE I. Relation of Parity to Reproductive Performance for Captive-Born S. oedipus
Females in Oak Ridge Colony, September 1979 to December 1985
No. deliveries
Litter size ratio, %
(singletons: twins: triplets)
No. abortions and
stillborn young
No. live-born young
No. surviving (%)
Delivery No.
In comparing the breeding performance of these three colonies, two factors may
explain the differences in effect of parity. The first factor is the previous breeding
experience of the father. Previous reports on S. fuscicollis [Epple, 1978, Epple &
Katz, 19801 and S. oedipus [Tardif et al, 1984133 indicated that infant survival was
greatest for those pairs in which at least one parent had previous experience with
infants, either from helping with infant siblings or rearing its own offspring. However, for both species, experience of the female seemed to be more crucial, since pairs
containing a n experienced female and a male with no previous exposure to infants
displayed adequate parental care. For the Bristol, Wisconsin and Oak Ridge colonies, most of the captive-born primiparous females had some exposure to infant
siblings, although the extent of their involvement in care of those siblings may have
varied considerably [Kirkwood et al, 1985; Snowdon et al, 19851.
Likewise, the males in each colony appeared to have had exposure to infant
siblings; however, the previous breeding experience of the males was different across
colonies. In the Bristol colony, 28 of the 31 captive-born females were mated to
captive-born males who had not previously sired and reared their own offspring
[Kirkwood et al, 19851. The report from the Wisconsin colony also appears to include
primarily pairings of captive-born animals neither of whom had previously sired or
delivered offspring [Snowdon et al, 19851. In the Oak Ridge colony, for the females
producing a live first delivery, six were mated to proven males (ie, males who had
successfully sired and reared offspring), whereas ten were mated to either unproven
or unsuccessful males (ie, males who had never sired offspring or had sired but never
successfully reared offspring; however, all unproven males who were captive-born
had experience with infant siblings). Survival of live-born offspring of primiparous
females mated to proven males was higher (69.2%) than survival of offspring of
primiparous females mated to unprovedunsuccessful males (36.8%). This difference
was not related to the origin of the male (see Table II). This difference (x2 = 3.24, df
= 1, .05 < P < .1)suggests that male experience at siring and rearing offspring
may be important. Further evidence is provided by comparing instances of abuse or
neglect in different pairs. There were six observed cases of abuse or neglect of
infants of a first litter. Five of these were in pairs in which the male was unproved
unsuccessful. While a previous report on the Oak Ridge colony indicated that
experience of males with infant siblings did not affect infant survival in pairs in
which the female was a n experienced mother [Tardif et al, 1984b1, the present data
suggest that for inexperienced, primiparous females, pairing with a proven male
may improve infant survival.
Differential male experience does not provide a complete explanation for the
colony differences since the infant survival for primiparous females with unproven
274 I Tardif, Carson, and Clapp
TABLE 11. Percent and Total Number (in Parentheses)of Infants Survivingto 6 Months
Relative to Source and Previous Breeding Experience of Father
Infant survival
71.4 (5)
40.0 (4)
66.7 (4)
33.3 (3)
males in the Oak Ridge colony was still higher (36.8%) than the overall first litter
survival observed in the Bristol and Wisconsin colonies (9-18%). A second factor
that may explain the differences between the Bristol and Oak Ridge colonies is the
age at which females are mated. Kirkwood et a1 [1985] reported a n average age a t
first mating of 19 months. The average age at first mating in our colony was
substantially older, at 27.8 months (+ 2.5 SE). While the difference in age at mating
was 9 months, the difference in age at first delivery in these two colonies was only 3
months (31.0 vs 34.0 months). Kirkwood et a1 [1985] observed a high incidence of
abortions in females delivering before 29 months of age, suggesting one difficulty
associated with mating at a n early age. Even for females producing live-born offspring, the low survival of young mothers’ infants suggests that females mated a t
early ages may display deficiencies in maternal care. Kirkwood et a1 [1985] report
that infant death was frequently due to parental abuse or neglect. These deficiencies
may be due to insufficient experience with infant siblings. It has frequently been
reported that experience with infant siblings is critical for the development of
adequate parental care in tamarins [Epple, 1975; Hoage, 1978; Snowdon et al, 1985;
Tardif et al, 1984b]. The age a t which S. oedipus is exposed to infant siblings
determines the extent to which the animal participates in infant care [Cleveland &
Snowdon, 1984; Tardif, unpublished data]. Perhaps relatively early removal of animals from their natal family groups does not allow for adequate experience with
infants. It may also be that early mating influences the relation of the mated pair
in a manner detrimental to infant survival [Epple & Katz, 19801. Data on the age of
the fathers was not included for the Bristol or Wisconsin colonies, but this factor
might also affect breeding performance.
1. Infant survival of primiparous captive-born S. oedipus females was equal to
that of multiparous females in the Oak Ridge colony. This result contrasts with
reports from other colonies of marked parity effects.
2. Two factors are suggested to explain these colony differences: (1)the use of
proven males (ie, have previously sired and reared offspring) mated to the primiparous females a t Oak Ridge; and (2) a n older age of mating.
This research was supported by NIH grant R24 RR02022-02, NCI Contract N01CP-51006, NIH grant 2 SO7 RR05746-13, Oak Ridge Associated Universities Corporation, and by contract DE-AC05-760R00033between the U.S. Department of Energy and Oak Ridge Associated Universities. The efforts of J. Kirkwood, C.
Lushbaugh, C. Snowdon, and R. Tardif in reviewing the manuscript are gratefully
acknowledged. The submitted manuscript has been authored by a contractor of the
U.S. Government under contract DE-AC05-760R00033.Accordingly, the U.S. Government retains a nonexclusive, royalty-free license to publish or reproduce the
Breeding by Captive-Born Suguinus oedipus Females / 275
published form of this contribution, o r allow others to do so for U.S. Government
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