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Developmental changes in food transfers in cotton-top tamarins (Saguinus oedipus).

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American Journal of Primatology 69:955–965 (2007)
Developmental Changes in Food Transfers
in Cotton-Top Tamarins (Saguinus oedipus)
Department of Psychology, University of Wisconsin, Madison, Wisconsin
We investigated the development of food transfer and independent
feeding in cotton-top tamarin (Saguinus oedipus) families. We studied
the relationship between infant-directed vocalizations and food transfers
on the development of independent feeding in infants. We experimentally
tested ten infants (eight twins and two singletons) three times a week for
17 weeks from before weaning through 20 weeks. Food transfers and
vocalizations made during tests were recorded and analyzed to determine
(1) the role of vocalizations (C- and D- chirps and D-chirp series) in food
acquisition, (2) the relationship between food transfers and individual
food acquisition, and (3) whether, owing to energetic costs of nursing and
carrying twins, food is transferred to twins sooner than to singletons.
Infants were more successful in acquiring food via begging when adults
produced repeated vocalizations than when adults did not vocalize.
Adults emitted more food-related vocalizations in rapid series when in
the presence of infants, whereas during feeding in the absence of infants
only single unit vocalizations were produced. Begging occurred frequently. Changes over infant age were not significant when all infants
were included in analysis. However, when twin data were analyzed alone,
begging success changed significantly over months, with successful
begging peaking in month 3 (week 12). Begging success rate did not
differ between twins and singletons, although twins fed independently
sooner and at a higher rate than did singletons. Am. J. Primatol. 69:
955–965, 2007. c 2007 Wiley-Liss, Inc.
Key words: Saguinus oedipus; cotton-top tamarin; food transfer;
vocalizations; longitudinal study
Active food transfers (in which food is transferred from one animal to
another) are relatively uncommon among non-human primates with notable
exceptions being great apes, Callitrichid primates and a few other Neotropical
Contract grant sponsor: Hilldale Student-Faculty Research Grant; Contract grant sponsor:
The McNair Scholars Program; USPHS Grant; Contract grant number: MH29775.
Correspondence to: Charles T. Snowdon, Department of Psychology University of Wisconsin, 1202
West Johnson Street, Madison, WI 53706. E-mail:
Received 29 March 2006; revision accepted 14 September 2006
DOI 10.1002/ajp.20393
Published online 9 February 2007 in Wiley InterScience (
r 2007 Wiley-Liss, Inc.
956 / Joyce and Snowdon
species [Brown et al., 2004]. Callitrichids have been the focus of most research
since food transfers occur not only from mother to infant but more frequently
involve fathers and helpers (alloparents). Most family members, including
subadults and juveniles, carry and transfer food to infants [Feistner & Price,
1990; Roush & Snowdon, 2001]. Food transfers begin when infants are
approximately 5 weeks old, with weaning beginning about 8 weeks of age. Here
we use distinctions of types of food transfers from Brown et al. [2004]. Food offers
involve a possessor directly passing food to another or adopting a specific posture
or vocalization that permits an infant to obtain food. A beg is when an infant
adopts a specific posture or gives vocalizations while displaying interest in food
held by another. A successful beg is when an infant begs for and receives food
from another.
Brown and Mack [1978] observed that vocalizations were important in
successful adult–adult food transfers as well as adult–infant transfers in a single
captive golden lion tamarin (Leontopithicus rosalia) group that they studied for
2 weeks. Food transfers were usually unsuccessful in the absence of vocalizations.
Roush and Snowdon [2001] confirmed this result in captive cotton-top tamarins
(Saguinus oedipus), finding high rates of food associated calls (C- and D- chirps),
but also, more commonly, repeated series of D- chirps. However Ruiz-Miranda
et al. [1999] reported low rates of adult vocalizations during food transfers in wild
and reintroduced golden lion tamarins. Rapaport [2006] also reported low rates of
adult vocalizations in food transfers, but vocalizations were most frequent when
adults held large prey or were near the location of hidden prey suggesting that
adult vocalizations might serve to direct juvenile attention to foods. Here we look
specifically at the role of vocalizations accompanying food transfers and how these
relate to infant feeding success.
Brown et al. [2004] hypothesized that food transfer behavior must be a
dynamic process that changes as infants acquire information and skill in
obtaining food. Food transfers are ineffective if infants are too young to process
or digest solid food and adults should decrease food transfers over time to
encourage infants to feed independently. Therefore, we expect to see a higher rate
of food transfer in the form of offering and begging when the infants are younger
and still learning from where to acquire solid food. As the infants learn to eat solid
food, adults should reduce their tolerance of begs and infants should acquire food
independently at increasingly higher rates.
Roush and Snowdon [2001] demonstrated how group members vocalized during
successful food transfers but their study was cross-sectional and not longitudinal.
Feistner and Price [2000] and Price and Feistner [2001] did longitudinal studies of
food transfers in black lion tamarins (Leontopithecus chrysopygus) and pied barefaced tamarins (Saguinus b. bicolor) but no studies have examined both food
transfer behavior and adult vocalizations developmentally, which is what we set
out to do.
Hypotheses for the functions of food transfers have been reviewed by Brown
et al. [2004]. One of these, the nutritional hypothesis, argues that foods are
transferred to help infants mature more rapidly and to increase survival at
weaning. Captive cotton-top tamarin males lose up to 10% of body weight in the
first weeks after infant births [Achenbach & Snowdon, 2002; Sanchez et al.,
1999]. At the time when infant carrying ends, family members begin transferring
food to infants adding further to energetic costs. We expect that twins will be
more energetically costly than singletons. Individual singletons weigh more at the
end of 5 months than do individual twins [Washabaugh et al., 2002] and in golden
lion tamarins, singletons are provisioned more than twins [Hoage, 1982]. We
Am. J. Primatol. DOI 10.1002/ajp
Developmental Changes in Food Transfers / 957
expect that twins should be involved in food transfers at an earlier age and would
feed independently sooner than would singletons owing to the greater costs to
non-infant group members of carrying and food transfer with twins.
We tested the following predictions: (1) When adults transfer food to infants,
they will make more D-chirp series calls (strings of five or more chirps) when
infants are present and will not make D-chirp series when infants are absent. (2)
The rate of begging success by infants should increase at first and then decrease
as the infant gets older and adults become less likely to provision them. The
rate of independent food acquisition should increase monotonically with infant
age. (3) The energetic costs of nursing and carrying twins should lead family
members to transfer food to twins at an earlier age than with singletons.
Furthermore, twins should cease begging and feed independently at an earlier age
than singletons.
We tested our hypotheses in two experiments. The first experiment was a
longitudinal study that looked at cotton-top tamarin infants thrice weekly for
17 weeks. The second experiment looked at pair-bonded adult tamarins in the
absence of infants. We gathered data on food transfers and vocalizations in both
Subjects and housing
We conducted the research at the Callitrichid Laboratory in the Psychology
Department at the UW-Madison. We studied five families with one family tested
with two litters. A total of eight twin infants and two singleton infants were
studied. Of the five families, four (PN, AS, VJ and SL) included experienced
parents with other offspring living with them (Table I). The father of family PN
died before the infants included in this study were born. The remaining pair (NW)
TABLE I. Composition of Groups
Adult male, adult female,
two female juveniles,
male infant, female infant
Adult male, adult female,
female infant
Adult female,
two male juveniles, one female
two male infants
Adult male, adult female,
two male juveniles, one female juvenile,
male infant, female infant
Two adult males, two adult females,
juvenile male, juvenile female,
female infant
Adult male, adult female,
two juvenile males, two juvenile females,
two male infants
Am. J. Primatol. DOI 10.1002/ajp
958 / Joyce and Snowdon
consisted of an experienced father and a new mother. No other offspring were
present in this family.
We housed the tamarins in cages designed to provide a full range of normal
behaviors (2.9 2.3 1.9 m, L H W for large families; 1.6 2.4 1.9 m and
1.6 2.4 0.9 m for smaller families and pairs, respectively). The cages have
layered wood shavings on the floor. Branches, ropes and other platforms are
placed in the cage at a variety of heights to simulate an arboreal environment.
The monkeys were fed three times a day. They receive a yogurt/applesauce
mixture in the morning around 0900 h; Purina New World Monkey Chow,
Zupreem Marmoset Diet, and a mixture of fruits, vegetables and starches between
1200 and 1300 h; and a high protein snack between 1430 and 1730 h. We
recognized the older monkeys on the basis of natural markings. We marked one
infant in each set of twins with hair dye on the cotton top for reliable
Each of the ten infants entered the study at 4 weeks of age to include any
incidents of food transfer (which typically begin at week 5 or later). We
terminated sampling at week 20, or the end of infancy as in previous studies from
our laboratory [Cleveland & Snowdon, 1984; Castro & Snowdon, 2000]. Initially,
we had been interested in testing the information hypothesis, so we divided the
five breeding pairs into two groups (pairs PN and VJ in Group A; pairs AS, SL and
NW in Group B). After we collected and analyzed our data, however, we realized
that our design did not permit us to test properly the information hypothesis. Two
equally preferred foods, banana and green grapes, were used. Group A received
three pieces of banana per individual in a food bowl as a snack in lieu of the
regular snack once a week throughout the infant’s development. Group A did not
receive grapes until the infant became involved in food transfer so that grapes
would be an initially novel food for infants. Subsequently, the families received
three pieces of grape per individual in a food bowl as a snack once a week. They
continued to receive banana in the same proportion once a week. The older
animals had experienced grapes in the past, so grapes were novel only to the
infants. Group B received snacks in the same manner, except that grapes were
given regularly throughout the infant’s development whereas banana was the
novel food. However, in retrospect we realized that by the second presentation a
novel food is no longer novel. An ideal longitudinal test of the information
hypothesis would have required identifying 17 foods of equal preference and
presenting a different one each week. In preliminary analyses we found no
differences in response to ‘‘familiar’’ versus ‘‘novel’’ foods and, therefore,
combined data from both (see Results). Roush and Snowdon [1994] found that
young tamarins often vocalized to a paper clip (used as a small manipulable
control for food pieces). Therefore, once a week, a control food bowl filled with
plastic-covered paper clips was given in lieu of the afternoon feed to both groups
to test whether or not the tamarins emitted food calls to and/or transferred nonfood objects. We removed the regular food bowls before placing either the food or
control bowls in the cage.
We tape-recorded the monkeys for 2 min to gather baseline data on C- and
D-chirp rate and begging behavior. After 2 min, we placed the test bowl in the
cage and continued data collection. Both grapes and banana were consumed
Am. J. Primatol. DOI 10.1002/ajp
Developmental Changes in Food Transfers / 959
within 5 min. The tamarins ignored paper clips that had fallen to the floor. Once
all paper clips were dropped to the floor, we stopped data collection. Trials lasted a
maximum of 5 min. After food was eaten, we recorded vocalizations for two
additional minutes of post-test data. Throughout the 9-min testing period,
we recorded all incidents of offering, begging, individual food acquisition and
‘‘C’’ and ‘‘D-’’chirp vocalizations and D-chirp series vocalizations [Cleveland &
Snowdon, 1982].
We used focal infant sampling to record what food was presented and in what
quantity, who transferred with whom, manner of transfer (begging versus
offering), and whether the infant was successful in acquiring food from an adult
or from the food bowl. We recorded vocalizations with a Marantz PMD 221
portable tape-recorder (Marantz Co., Chatsworth, CA). We analyzed vocalizations
by infants when begging and by adults when offering food, using SIGNAL-RTS,
(Engineering Design, Belmont, MA) a real-time acoustic analysis program.
We calculated the frequency of successful attempts of begging (when an
infant approaches an adult with food and obtains food from the adult), successful
attempts at transfer (when an adult or alloparent initiated food transfer) and
incidents of self-feeding for infants for each week for both groups for each item:
banana, grape and paper clips. We compared rates of different modes of food
transfers (failed and successful) to infant age. These data were then averaged over
4-week blocks (months). We also analyzed on a week-by-week basis and found
similar results. For simplicity of presentation we present the data here by
Washabaugh et al. [2002] found that behavior of twins within a litter was
independent of each other, so we treated twins individually in data analysis. Data
were not normally distributed and we used Mann–Whitney U-tests to compare
differences between groups (twins versus singletons) and Wilcoxon-matched
pairs-signed ranks tests to compare responses with paper clips versus foods, and
w2 tests to evaluate begging success as a function of vocalization by donors. We set
a significance level of P 5 0.05. We used the Friedman non-parametric repeated
measures analysis of variance to compare behavior across months. We tested
significance between months using Wilcoxon-matched pairs-signed ranks tests.
Because the same data were used in up to three tests, significance for these tests
was set at Po.05/3 or .0167.
We quantified vocalizations of family members and matched them to
behavior. Each occurrence of single C- and D- chirps, as well as D-chirp series,
was noted along with the concurrent action. A series consists of five or more
D chirps in succession (Fig. 1).
We found no differences in behavior as a function of food type or food
‘‘novelty,’’ and subsequently we combined both foods for analysis. Paper clips
were used as a non-food, manipulable control. Two families failed to interact with
the paper clips at all. The number of calls and number of call series given were
significantly lower for paper clips than for food (Wilcoxon-matched pairs-signed
test for both number of calls and number of bouts: T 5 0, N 5 6, Po0.05).
Individuals (parents and siblings) offering food to infants repeatedly
produced food chirps in series. Older siblings also gave C- and D- chirps during
paper clip trials; only two parents did. Infant begging was more likely to be
Am. J. Primatol. DOI 10.1002/ajp
960 / Joyce and Snowdon
Fig. 1. Spectrograms of single food chirps (top) and D-chirp series (bottom).
successful when parents and siblings vocalized than when they did not vocalize
[successful food transfers with adult vocalizations 5 108, successful food transfers
without adult vocalization 5 8, unsuccessful food transfers with vocalizations 5 65,
unsuccessful food transfers without vocalizations 5 45; (X2(1) 5 36.38, Po0.001)].
Offers occurred rarely (only 4.58% of trials), so the focus of our results will be
on the relationships between begging, vocalizations and begging success. Begging
occurred in 39.12% of trials and successful begging did not change significantly
over time when all infants were included in the analysis (Friedman w2 5 2.79, NS).
However, when we analyzed twin data alone there was a significant change
with months (Friedman w2 5 12.09, Po0.01, successful begging peaked in month
3 (also week 12); Wilcoxon tests T 5 0, N 5 8, Po0.01, month 3 versus month 4
and month 5). There was no significant difference between months 2 and 3
(Fig. 2).
We found an increase in the average number of independent feeds with
increasing infant age (Friedman w2 5 18.21 Po.001, all animals, w2 5 61.67,
Po.001 for twins only). Independent feeds in months 3, 4 and 5 were greater than
in month 2 (T o2, N 5 10, P o0.01). Independent feeds in month 5 were greater
than month 3 (T 5 2, N 5 10, Po0.01) and marginally greater than in month 4
(T 5 3.5, Po0.02; Fig. 3).
Twins had their first successful beg marginally earlier than singletons (twins
median 7 weeks, range 5–9 weeks; singletons median 10.5 weeks range 8–11
weeks, N1 5 8, N2 5 2, U 5 2, P 5 0.089). Twins first fed independently at an
Am. J. Primatol. DOI 10.1002/ajp
Developmental Changes in Food Transfers / 961
Median number of successful begs
Infant age (in months)
Median number of successful independent feeds
Fig. 2. Median number of successful begs by infants to family members over time. Month 3 greater
than months 4 and 5 (P’so0.01).
Infant age (in months)
Fig. 3. Median number of successful independent feeds by infants over time. For twins only, months
3, 4 and 5 greater than month 2 (P’so0.01, month 5 is greater than month 3, Po0.01).
earlier age than singletons (twins median 7.5 weeks, range 7–10 weeks, singletons
median 12 weeks, range 10–14 weeks, N1 5 8, N2 5 2, U 5 0.5, P 5 0.033). Infants
first fed independently within 0–2 weeks of their first successful beg and age of
first successful beg was highly correlated with age of first independent feed
(r 5 0.956, Po0.01).
There was no significant difference in begging rate between twins and
singletons. However, twins fed independently at a higher rate than did singletons
Am. J. Primatol. DOI 10.1002/ajp
962 / Joyce and Snowdon
(Mann–Whitney U-test, N1 5 8, N2 5 2, U 5 0, Po.05). Months 3 and 4 differed
significantly with twins feeding independently at a higher rate than singletons
(month 3, Mann–Whitney U-test: N1 5 8, N2 5 2, U 5 0, Po0.05, Month 4,
N1 5 8, N 2 5 2, U 5 0, Po0.05).
The second experiment determined whether adults vocalized differently
toward food in the presence of infants than in their absence. Roush and Snowdon
[2001] reported that family members emitted D-chirp series when offering food to
infants, suggesting that adults modified vocalizations for use with infants, but
they provided no data on adults without infants. Brown and Mack [1978] found a
high rate of feeding vocalizations both with successful adult–adult and with
adult–infant food transfers.
We hypothesized that D-chirp series were used specifically for food transfers
with infants. Therefore, we predicted that the average number of D-chirp series
given per individual should be higher for adults in families with infants present
than for adults in male–female pairs without infants present. We predicted that
both the average number of calls per bout per individual and the average number
of calls per session per individual should be higher for the adults with infants
than for adults without infants.
We studied a total of four-adult non-breeding male–female pairs (DF, CO, KJ
and FW). One member of each pair had been sterilized for management purposes.
Six of these animals were previously members of the families tested (father,
brother or sister of tested infants). No offspring were present with these pairs.
Design and procedure
We tested each pair for a total of 2 weeks, three times each week: once with
banana, once with grape and once with paper clips as a control. Since we were not
expecting developmental change in adults, a 2-week test was thought adequate to
gather data. Each pair received three pieces of food per individual in a food bowl
as a snack in lieu of the regular snack. We followed the same procedure as with
We analyzed the food chirps given by the animals. We counted both types of
chirp (C or D) as well as whether the chirps were given in series. Rates of series
and the total number of food chirps made by adults in four family groups with
infants (SL, NW, AS and VJ) were compared with the pairs without infants using
Mann–Whitney tests.
No incidents of food transfer occurred in adult pairs. The number of D-chirp
series given and total number of calls given by adults in the non-family condition
were significantly lower than for those adults in the family condition (series with
infants present: median 5 1.15, range is 0.1–1.66; series without infants present:
median 5 0, range is 0–0.75; Mann–Whitney U test of series with and without
infants present, N1 5 10, N2 5 8, U 5 4, Po.002; calls with infants present:
Am. J. Primatol. DOI 10.1002/ajp
Developmental Changes in Food Transfers / 963
median 5 8, range is 1.3–23.4; calls without infants present: median 5 3.5, range
is 0.75– 9.75; Mann–Whitney U-test of calls with and without infants present,
N1 5 10, N2 5 8, U 5 13, P 5 .02). Thus, adult cotton-top tamarin food-related
vocalizations differed significantly both in terms of absolute numbers of calls and
the presence of D-chirp series depending on the presence or absence of infants.
The food-transfer behavior of both cotton-top tamarin infants and other
family members changed over time. Adult food-related calls appeared important
in infant success at food acquisition during transfers. Specifically, D-chirp series
were produced almost exclusively during infant food transfers and rarely
appeared when infants were absent. As infants became older, adults produced
these calls less often and successful food transfers decreased.
Successful food transfers to infants appeared as a result of specialized
vocalizations (bouts of food calls). Non-infant tamarins altered their food calls to
D-chirp series in the presence of infants. Adults without infants produced fewer
D-chirp series and fewer calls in a feeding session. Furthermore, infants were
likely to acquire food through transfers only when the family member in
possession of the food produced D-chirp series. We observed that some animals
called to the paper clips with single food vocalizations, but not with D-chirp series.
Previously, sub-adults have been found to overgeneralize food calls and thus
vocalize to non-food objects [Roush & Snowdon, 1994].
The most obvious cost of food transfer is the relinquishment of a highly
preferred food item. We tested tamarins with highly preferred, high-quality, highenergy foods, compared with the rest of their diet. Feistner and Chamove [1986]
found that cotton-top tamarins with higher food motivation were more likely to
transfer food than tamarins with a lower food motivation. Any benefit received by
the donor is not immediate. Similarly, Rapaport [2006] found that wild golden
lion tamarins transferred food high in lipids and protein.
At the time when family members reduced carrying of infants, they began
transferring food to infants, continuing their energetic costs. Fathers can lose up
to 10.8% of their body weight during infant carrying when they have no helpers.
Even with helpers present, all carriers lost some weight [Achenbach & Snowdon
2002]. Food transfers begin at the start of weaning, when the mother was already
engaged in a high-energy transfer through lactation. Furthermore, the mother is
often pregnant again. Both parents transfer food at a time when their own energy
costs have been high. But the result of food transfers may be reduced total energy
expenditure since transfers lead to more rapid independent feeding.
Twins are more energetically expensive than singletons, and we expected
twins to show independence of feeding sooner than singletons. Twins began to beg
and to receive food through transfers earlier than singletons and twins also began
to feed independently sooner and at a higher rate than did singletons. Twins
obtained almost twice as much of their food through independent feeding than did
singletons in the study.
We found an inverse relationship between successful begging and independent feeding. As the number of successful begs decreased over time, the number
of independent feeds increased. This suggests that the infants learned where food
was located and learned to eat on their own. Castro and Snowdon [2000] found
that out of five chirp vocalizations used by adult tamarins, infant tamarins
(20 weeks or younger) used only food chirps (D- chirps) correctly and with an
adult-like structure within the first 20 weeks. These data suggest that the
Am. J. Primatol. DOI 10.1002/ajp
964 / Joyce and Snowdon
behavior of the family members changes the behavior of the infant. The tendency
for adults to begin food transfer earlier with twins, coupled with the fact that
twins fed independently significantly earlier, suggests that differential behavior
by older tamarins to twins versus singletons had differential effects on the timing
of independent food acquisition. Future studies on the energetics involved in food
transfer could be done on other pair-bonded species. Of specific interest would be
to compare how food transfers change over time in pair-bonded species that give
birth to singletons (such as Callicebus sp., Callimico goeldii and Hylobates sp.).
Although our data could not evaluate the hypothesis that food transfers
provide information to infants, adult tamarins did behave differently during food
transfers with infants by using different vocalizations. Adult tamarins incurred a
cost in transferring preferred foods to infants and food transfers occurred less
often as infants increased their ability to forage independently. This suggests that
adults are adjusting transfer behavior according to the nutritional demands of
their offspring and, perhaps, themselves.
A direct test of the information hypothesis would be a logical next step.
Brown et al. [2005] found that common marmosets did not transfer novel foods
more often than familiar foods and that adults transferred both palatable and
unpalatable foods equally. A more complete study of food novelty using a larger
number of novel foods, paired with vocalization analysis, would be beneficial to
see if tamarins behave differently with foods that are novel to infants or if
tamarins are similar to marmosets. We noticed anecdotally that, when infants
were young, family members vocalized toward food both at the food bowl and on
substrates away from the food bowl. However, as the infants got older, the family
members tended to vocalize more at the food bowl than away from it. A closer look
at the process by which infants learn to acquire food independently by recording
changes in the position of the food possessor and where vocalizations occur would
be an important future study.
We thank Drs Karen B. Strier, Tatyana Humle and Rosamunde E.A. Almond
for helpful suggestions and feedback, and David S. Krall and the Callitrichid
Laboratory staff for support. We also thank two anonymous reviewers whose
comments helped to improve the manuscript.
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