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Comparison of infant care in family groups of the common marmoset (Callithrix jacchus) and the cotton-top tamarin (Saguinus oedipus).

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American Journal of Primatology 11:103-110 (1986)
Comparison of Infant Care in Family Groups of the
Common Marmoset (Callithrixjacchus) and the
Cotton-top Tamarin (Saguinus oedipus)
SUZE'ITE D. TARDIF, ROBERT L. CARSON AND BARBARA L. GANGAWARE
Marmoset Research Center, Oak Ridge Associated Universities, Oak Ridge, Tennessee
The involvement of parents and siblings in infant care in similarly composed groups of common marmosets (Callithrixjacchus) and cotton-top tamarins (Saguinus oedipus) was compared during the infants' first 8 weeks
of life. The results indicate an earlier infant independence in C. jacchus
than in S. oedipus due primarily to a more frequent rejection of carried
infants in C. jacchus. There was no species difference in extent of maternal
involvment in carrying infants. However, S. oedipus fathers carried infants
significantly more often during weeks 5-8 than did C. jacchus fathers.
Siblings were generally more involved in infant care at an earlier infant
age in C. jacchus than in S. oedipus.
Key words: parental behavior, behavioral ontogeny, weaning
INTRODUCTION
In all callitrichid species examined, various group members participate in the
care of infants. It is assumed that a callitrichid female would be unable to care for
infants alone due to high neonate-to-adult weight ratios, high frequency of twinning,
and high energy demands of pregnancy and lactation [Epple, 1975; Garber, 1984;
Tngram, 1977; Leutenegger, 1980; Hershkovitz, 19771.
The extent to which various group members participate in the care of infants is
highly variable. Some of this variation reflects probable species differences. Cleveland and Snowdon [1984], for example, suggest that male participation in infant
care is more important in tamarins than in marmosets [see also Box, 1975; Ingram,
19771. Hoage [1978] and Buchanan-Smith [1984] suggest that maturation rate may
differ between callitrichid species. Specifically, Hoage [19781 suggests that a slower
maturation rate, resulting in longer infant dependence, occurs in the larger callitrichid species in general. However, comparisons of infant care among different species
are usually hampered by variation in habitat or in colony environments, differing
group sizes and composition, and parity or experience of parents.
The present study compared infant care in family groups of the cotton-top
tamarin (Saguinus oedipus) and the common marmoset (Callithrixjacchus). Groups
were selected for similar composition and were housed and managed in an identical
fashion. With these extraneous factors controlled, the extent of parental and sibling
Received December 17,1985; revision accepted April 17,1986.
Address reprint requests to Dr. Suzette D. Tardif, Marmoset Research Center, Oak Ridge Associated
Universities, Oak Ridge, TN 37831-0117.
0 1986 Alan R. Liss, Inc.
104 I Tardif, Carson, and Gangaware
TABLE I. Comparison of Group Composition: C. jacchus and S. oedipus
Older litters
No. of
Group ID
Species
2
32
Cj
so
2
2
1M:lF
1M:lF
11.1
10.6
31
C.i
1
7-2
so
2
1M:lF
1F
1M:lF
2F
16.5
9.4
14.9
7.9
6
Cj
1
1M:lF
10.4
39
19
7-1
so
Cj
1
2
2
2F
1M:lF
1M:lF
12.5
7.0
7.1
so
infants
Sex
Age (mo)
involvement in infant care and the development of infant independence were compared in these two species.
METHODS
Subjects and Procedure
The subjects for this study were the parents, older siblings, and infants in four
groups of cotton-top tamarins (S. oedipus) and four groups of common marmosets (C.
jacchus). The composition of each group is indicated in Table I. All of the parents in
both species had successfully reared offspring previously.
Each group was housed in a cage measuring 152 x 183 x 183 cm. All groups
were visually isolated from other conspecific groups. Further details of the housing,
diet, and management of these animals are described in Clapp and Tardif [1985]
and Richter 119841.
Each group was observed for two to four 20-min sessions per week during the
infants‘ first 8 weeks of life. Observations were conducted between 0800 and 1700
hr from behind a blind. Each group was observed at least once in the morning and
once in the afternoon each week so that any potential effects of time of day would
not be confounded with the variables of interest.
Observations were recorded, using either a cassette recorder and stopwatch or a
Hewlett-Packard 71-B hand-held computer programmed to function as a n event
recorder. During each 20-min session, the time that each individual spent carrying
a n infant was compiled by noting who was carrying the infant as the period began,
and then noting each transfer of a n infant, either from one carrier to another or on
or off a single carrier. A carry was defined as any position in which time infant was
clinging with at least two limbs. In groups with two infants, each infant was a focal
animal for half of the observation period, and all carrying of the focal infant was
recorded. A carry of either one or two infants was recorded as one carry.
A transfer of a n infant was defined as movement from a first carrier to a second
carrier or movement on or off a single carrier. For each transfer of a n infant, the
following information was recorded:
1. identity of the first carrier (Cl)-could
be either a n animal identity or “off”
(infant not being carried);
2. identity of the second carrier (C2)-could
be either a n animal identity on
‘<off’;
3. rejection of infant by C1-consisted of biting or grabbing the infant or rubbing
the infant on a perch or cage side during the minute prior to the transfer;
Infant Care in Marmosets and Tamarins I 105
4.retrieval of infant by C2-consisted of touching the infant and directing its
movement or pulling it away from the first carrier.
Any movement of a n infant between two carriers that involved the infant being
off a carrier for a n interim period was recorded as two transfer events (i.e. C1 to
“off,” then “off’ to C2).
Observations on each group were conducted by each of three observers. Observers were tested for inter-observer reliability by comparing simultaneous observations by each combination of two observers, for a total of 13 observation periods.
Levels of agreement were 100% on identity of carrier, 100% on carrying time (within
60 sec), 90%on occurrence of rejection, and 90% on occurrence of active retrieval ton
a total of 19 transfers).
Analyses
The percent of the total observation time in which a n infant was carried by each
group member was computed for two time periods, weeks 1-4 and weeks 5-8.
Previous observations of cotton-top tamarins [Cleveland and Snowdon, 19841, as well
as our own preliminary observations, indicated that consistent decreases in the
amount of time infants were carried as well as a general decrease in attraction to
infants begins when the infants are about 5 weeks old. For this reason, these two
time periods were chosen. The percent of time that mothers and fathers of each
species carried infants for each time period was compared, using paired t-tests, after
arcsin square-root transformation of the data [Gill, 19781. The percent of time that
infants of each species were off carriers for each time period was also computed
using paired t-tests.Comparison of carrying by siblings in each species was hindered
by the wide range in ages in each group (7.0-16.5 mo) and the small sample for any
given age. Therefore, the data for each individual are presented and examined for
suggestion of species differences.
Infant transfers were classified into five categories relative to the action of the
first and second carriers and the infants as follows, with C1 referring to a carrier
losing a n infant and C2 referring to a carrier receiving a n infant:
1. rejection-the infant is rejected by C1 and crawls onto C2 or a perch or side of
cage;
2. rejection + retrieval-the infant is rejected by C1 and actively retrieved by
c2;
3. retrieval-the infant is not rejected by C1 but is actively retrieved by C2;
4. infant to C2-the infant moves independently onto C2. Infant may initially
be on C1 or on a perch or cage side;
5. infant off-the infant moves independently off C1 onto perch or side of cage.
In virtually all transfers, crawling by infants was involved. Therefore, infants
essentially played a n active role in all transfers. Transfer types 4 and 5 refer to
those transfers in which action of the infant, alone, was responsible for the transfer.
The sample was pooled across groups for analysis. When a significant result
was found, the data from each group were compared to determine whether the result
represented a consistent effect across groups.
Chi-square analyses were used to determine whether the frequency of different
transfer types was related to species or age of infant within species.
RESULTS
Time Spent Carrying Infants
Table I1 indicates the percent of observation time that mothers and fathers in
each species spent carrying infants. Paired comparisons revealed no significant
difference between the species in the percent of time that mothers carried infants
106 I Tardif, Carson, and Gangaware
TABLE 11. Comparison of Percent of Observation Time That Mothers
and Fathers Carried Infants*
Parent
Infant age
(weeks)
Pair
compared
Mother
1-4
2/32
3117-2
6/39
1917-1
5-8
2132
3117-2
6/39
1917-1
Species
C. jucchus S. oedipus
21.9
35.1
33.4
-
28.5
X=
29.7
2.0
16.0
0.0
24.0
10.5
25.4
31.8
22.7
62.9
35.7
6.6
27.5
0.0
4.5
9.6
-
X=
Father
1-4
2132
3117-2
6/39
1917-1
-
X=
5-8
3/32
3117-2
6/39
1917-1
-
X=
*% carrying time = carrying timekotal time x
86.5
15.6
52.3
14.8
42.3
37.2
16.2
0.0
6.0
14.8
13.5
43.3
22.0
84.4
40.8
42.7
36.5
5.4
27.7
28.1
~
~
~
100.
TABLE 111. Percent of Time Each Sibling Spent Carrying Infants
During Weeks 1-4 and 5-8
Carrying time
(weeks)
1-4
5-8
%
Species
Sex
Age (mo)
C. jacchus
M
S. oedipus
M
C. jucchus
F
16.5
11.1
10.4
7.0
14.9
10.6
7.1
16.5
11.1
S. oedipus
F
10.4
9.4
7.0
14.9
12.5
12.5
10.6
7.9
7.9
7.1
33.1
35.1
40.2
1.5
7.7
0.0
0.0
0.0
17.5
0.0
0.3
0.0
25.8
25.6
0.0
0.0
0.0
0.0
0.0
7.6
1.2
0.1
0.0
1.5
0.0
15.1
5.9
3.6
0.0
0.0
0.0
20.4
37.4
0.0
0.0
0.5
0.5
10.9
Infant Care in Marmosets and Tamarins I 107
TABLE IV. Percent of Time Infants Spent Off
Carriers During Weeks 5-8
Pair
comoared
2/32
3117-2
6/39
19117-1
Total (XI
Species
C. iacchus
s. oedipus
86.7
43.0
94.2
70.5
73.6
11.7
12.2
57.2
36.0
29.3
during either age interval. There was no signfkant difference between the species
in the percent of time that fathers carried infants during weeks 1-4; however, S.
oedipus fathers carried infants significantly more often than did C. jacchus fathers
during weeks 5-8 (t = 3.71, p < .05).
Table rII shows the percent of observation time that each older sibling spent
carrying infants in each speices during weeks 1 4 and 5-8. Comparison of these
sibling groups for species differences is hindered by the wide range in ages in each
group (7.0-16.5 mo) and by the small sample for any given age. However, examination of the data for each individual suggests some trends. In weeks 1-4, siblings at
7.0 months of age rarely carried infants, regardless of sex or species. In the agerange of 10.0 to 16.0 months, C.jacchus males were frequent infant carriers, while
the two S. oedipus males carried infants infrequently. The carrying times of female
siblings over 10 months of age indicated wide inter-individual variation. During
weeks 5-8, carrying time decreased to less than 10%of total time for all C. jacchus,
while four S. oedipus siblings still carried infants more than 10%of the time.
The species differences seen in carrying times are reflected in the amount of
Paired comparisons revealed no
time infants were off a carrier (see Table N).
difference between species in percent of time infants were off carriers during weeks
1-4, with all groups carrying infants > 95% of the time; however, during weeks 58, C. jacchus infants were off significantly more often than were S. oedipus infants
(t = 4.34, p < -025).
Infant Transfers
Figure 1 illustrates the percent of infant transfers of each type for each species
during infant ages 1-4 weeks and 5-8 weeks. The results indicate differences in the
frequency of the various transfer types between species for weeks 5-8 (x2 = 27.6,
df = 4, p < .005). This difference is attributable to a higher percentage of transfers
involving harassment in C. jacchus, particularly of transfers in which harassed
infants were not retrieved (45.4vs 13.6%).Conversely, there was a higher percentage
of infant-initiated transfers off carriers in S. oedipus than in C. jacchus (25.0 vs
6.4%).The percentage of transfers within each group that involved rejection with no
retrieval ranged from 42.9 to 51.3% for C. jacchus and from 6.7 to 33.3% for S.
oedipus (species difference is significant when compared by a Mann-Whitney U Test,
p < .05).
DISCUSSION
The results indicated that, under the specified captive conditions, C. jacchus
infants were independent at a significantly earlier age than were S. oedipus infants.
This advanced independence in C. jacchus was primarily due t o a more frequent
108 I Tardif, Carson, and Gangaware
O R A U 8612
60 1
/H
S. oedipus
C.lacchus
20
E
E
E
-
0
1
...
......
......
....
.:
......
:
:,.,.;< '
c
I-
1. 1
Weeks 1-4
181
(0)
0
.. .....
. ..
.......
.....
......_
...
...
_....
:..::;.::;..;
_.....
Weeks 5 8
i
20
n
4
0
1
Reject
Reject +
Retrieve
Retrieve
Infant
to c2
Infant
Off
Fig. 1. Percent of transfers of each type for each species during each infant age (1-4 and 5-8 weeks). See
Methods for description of transfer types.
occurrence of rejection of carried infants in this species, rather than to increased
infant-independent activity. This result is very similar to that reported by LockeHaydon and Chalmers [1983] for C. jacchus and Buchanan-Smith [1984] for C.
argentata, who found that the growing independence of marmosets is promoted
primarily by caregivers. However, there are clear species differences in the development of infant independence within callitrichids, with rejection of infants less
important in S. oedipus than infant independent activity.
Hoage [1978] suggests that a slower maturation rate and longer infant dependence occurs in the larger callitrichid species in general. However, review of the
data available on maturation rates of various callitrichid species [Hershkovitz, 1977;
Kirkwood, 1983; Tardif, unpublished data] suggests that C. jacchus and S. oedipus
grow at comparable rates, each obtaining approximately 25-30% of adult body
weight by 2 months of age. Therefore, earlier rejection of infants in C. jacchus is
apparently not due to faster growth rate. The earlier infant independence in C.
jacchus suggests that the energy demands of rearing a given infant may be less for
C. jacchus groups than for S. oedipus groups. This difference may explain the
superior reproductive performance of C. jacchus in captivity [Tardif et al, 19841. The
difference may also be related to differing needs for transport of older infants in the
wild. Marmosets (Callithrix)are specialized gum feeders with ranges generally much
Infant Care in Marmosets and Tamarins / 109
smaller than those of tamarins (Suguinus)[Stevenson, 1978; Maier et al, 19821. It is
possible that this specialized feeding, involving more limited movement during the
day, allows the rejection of infants at an earlier age.
The suggestion that participation of males in infant care is more critical in
tamarins than in marmosets [Cleveland & Snowdon, 19841 was supported by the
present study. Fathers in S. oedipus groups carried infants significantly more often
than did C. jacchus fathers during weeks 5-8. This species difference was not
observed between mothers, with mothers of both species carrying less frequently
during weeks 5-8, but was reflected in the fact that S. oedipus infants were carried
more often than were C. jucchus infants during weeks 5-8. Examination of the
factors that precipitate infant rejection (or decline in attraction to infants) for
mothers and fathers of each species is needed. While the growth rates of the two
species are apparently similar, other aspects of behavioral or morphological maturation may differ between species, accounting for the decline in attraction to C.
jacchus infants at an earlier age. Alternatively, the species difference may reflect a
differential responsiveness of C. jucchus and S. oedipus fathers to similar infant
behavior (e.g., clinging, vocalizing).
Determination of species differences in sibling involvement in infant care was
hindered in the present study by the wide age range of older siblings and by the
small sample size at any particular age. In S. oedipus groups, age of siblings is
significantly related to extent of infant-carrying [Cleveland & Snowdon, 1984; Tardif, unpublished data]. One consistent result in the present study was that animals
at 7.0 months of age, regardless of sex or species, rarely carried infants. This result
is not surprising given the small size of a 7.0 month old juvenile. For older siblings
(in this case 10.5-16.0 months), the results suggest that C. jucchus males carried
infants regularly and more frequently than did C. jucchus females. This result
differs from those of Ingram [1977], Box [1975], and Locke-Haydon & Chalmers
[1983], who found that adolescent female C. jucchus were more interested in infants
than males were. The results also suggest that S. oedipus siblings in this age range
carry infants less often than do C. jacchus siblings. This may reflect a maturational
difference between the two species, with C. jucchus consistently carrying infants at
an earlier age. Evaluation of groups of each species containing fully adult siblings
(e.g., over 24 months of age) would be of interest to determine whether these
suggested species differences would also be present.
CONCLUSIONS
1. Infant independence began significantly earlier in C. jacchus than in S.
oedipus.
2. Earlier infant independence in C. jacchus was primarily due t o more frequent
rejection of carried infants in C. jacchus than in S. oedipus.
3. There were no significant species differences in extent of maternal involvement in infant-carrying. However, s. oedipus fathers carried infants significantly
more often during weeks 5-8 than did C. jacchus fathers.
4. The results suggest that infant-carrying by older siblings occurred consistently a t an earlier age in C. jucchus than in S. oedipus.
ACKNOWLEDGMENTS
This research was supported by NIH grant R24 RR02022-02,NCI Contract N01CP-51006, NIH grant 2 SO7 RRO5746-13, and Oak Ridge Associated Universities
Corporation. The efforts of R. Tardif, C. Lushbaugh, and N. Clapp, in reviewing
previous versions of the manuscript, are gratefully acknowledged. The submitted
manuscript has been authored by a contractor of the U S . Government under Con-
110 I Tardif, Carson, and Gangaware
tract No. DE-AC05-760R00033.Accordingly, the US.Government retains a nonexclusive, royalty-free license to publish or reproduce the published form of this
contribution, or allow others to do so for U S . Government purposes.
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