Behavioral Ecology
doi:10.1093/beheco/arj016
Advance Access publication 7 December 2005
Provisioning in wild golden lion tamarins
(Leontopithecus rosalia): benefits to
omnivorous young
Lisa G. Rapaport
Department of Anthropology, University of New Mexico, Albuquerque, NM 87131, USA
Provisioning may act to cushion weaned young from dietary insufficiency and errors during the period in which they are mastering
complex foraging techniques or learning to identify appropriate dietary items. That is, young mammals who receive food from
others may gain nutritional and/or informational benefits. I conducted a longitudinal study of 13 wild golden lion tamarins 11–56
weeks of age in six groups to evaluate hypotheses regarding the functions of provisioning. All members belonging to this primate
taxonomic family (the Callitrichidae) are cooperative breeders and are known to provision their young more frequently than do
other primate species, except humans. My results, together with experimental findings, suggest that juveniles receive both
nutritional and informational benefits from being provisioned. My juvenile study subjects received animal prey (invertebrates
and small vertebrates) from others more frequently than plant resources (fruits and hardened exudates). Apparently difficult-tohandle fruits were more likely to be transferred than readily processed fruits. These results support the nutritional benefits
hypothesis because the young received items, particularly lipid- and protein-rich prey, that they might not otherwise have acquired.
That juveniles fed independently on, and were provisioned with, the same fruits on the same day is counterevidence to the
nutritional benefits hypothesis, however. The informational benefits hypothesis was supported because juveniles received a large
variety of foods (including more than 20% of fruit species eaten) and received uncommon fruits that were easily acquired. Adults
emitted food-offering calls to encourage the transfer of prey to juveniles, particularly when the prey was whole and alive.
Key words: cooperative breeding, feeding development, golden lion tamarin, provisioning. [Behav Ecol 17:212–221 (2006)]
ttaining nutritional independence is one of the most critical tasks a young animal must face. Mammals typically
experience high mortality rates from birth until complete
nutritional independence (Caughley, 1966). Postweaning survivorship rates often vary with food availability, and starvation
can be a major cause of juvenile mortality (Choquenot, 1991;
Packer et al., 1988). Increased parental investment in offspring growth, either pre- or postnatally, may act to minimize
the risk of starvation. Provisioning is one form of postnatal
investment that may be particularly effective when foraging
strategies and diets are complex because weaned young are
thereby buffered from the effects of foraging inexperience
and size and strength limitations. Immatures conceivably
may gain both nutritional and informational benefits from
being provisioned. In humans, for example, provisioning of
toddlers and adolescents appears to dampen mortality during
the extended period of dependency, which in turn has permitted selection to favor a heavy reliance on learning (Lancaster
JB and Lancaster CS, 1983; Worthman, 1993). Traditionally,
the burden of provisioning weaned children has not fallen on
mothers alone. Assistance from relatives such as older siblings,
grandmothers, and fathers is common and may allow mothers
to sustain higher reproductive rates (reviewed in Blaffer-Hrdy,
1999; Mace, 2000).
That carnivores such as orcas (Orcinus orca), most felids, and
canids provision their weanling young is well documented
(Boran and Heimlich, 1999; Ewer, 1973; Kitchener, 1999).
The mother may be the exclusive provider, as in solitary felids,
or other group members may provide food. For example, in
A
Address correspondence to L.G. Rapaport. E-mail: lrapt@bellsouth.
net.
Received 21 June 2005; revised 4 November 2005; accepted 5
November 2005.
The Author 2005. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
cooperatively breeding canids, all or most adult group members regurgitate prey for pups (MacDonald and Moelhman,
1982; Moelhman and Hofer, 1997). Presumably, reliance on
large prey and complex foraging techniques favors juvenile
provisioning as a period in which strength and skills can develop gradually.
Other cooperative breeders also provision weaned young.
Viverrids such as meerkats (Suricatta suricatta: Brotherton
et al., 2001; Clutton-Brock et al., 2001), banded mongooses
(Mungos mungo: Gilchrist, 2004), and dwarf mongooses
(Heterogale parvula: Rasa, 1989; Rood, 1978) provide invertebrates and small vertebrates to mobile young. Naked mole-rats
(Heterocephalus glaber) offer weanling colony members partially
digested fecal pellets (Lacey and Sherman, 1997).
In contrast to most other nonhuman primates, in which
food transfer from adults to immatures is infrequent and usually limited to a mother’s passive tolerance of scrounging by
her juvenile offspring (Brown et al., 2004; Feistner and
McGrew, 1989; King, 1994; Nishida and Turner, 1996), young
of the cooperatively breeding Callitrichidae are regularly
provisioned (Feistner and Price, 1990, 2000; Hoage, 1982;
Price and Feistner, 2001; Rapaport and Ruiz-Miranda, in press;
Ruiz-Miranda et al., 1999; Tardif et al., 2002). All subadult
and adult group members typically contribute to this caretaking activity (Garber et al., 1984), and in several species
and all four genera (the marmosets, pygmy marmosets, tamarins, and lion tamarins), they may actively solicit food transfer to infants and juveniles with a distinctive food-offering
vocalization (Brown and Mack, 1978; Feistner and Price,
1991; Ferrari, 1987; Tardif et al., 2002). Among the primates,
only in humans do juveniles receive a comparable degree of
foraging assistance from others after weaning (Blaffer-Hrdy,
1999; Dettwyler, 1989).
Golden lion tamarins (Leontopithecus rosalia) are diminutive
(approximately 500–600 g) callitrichid monkeys that live in
Rapaport • Provisioning in golden lion tamarins
small cohesive groups, defending year-round territories from
nongroup members (Rylands, 1993). Maturation is rapid for
a primate, with weaning at 3–4 months (Hoage, 1982), reproductive maturity as early as 17 months (French et al., 1989),
and dispersal as early as 1 year of age (Baker, 1991).
Their omnivorous diet is diverse. Plant resources consist of
fruits, flowers, nectar, and exudates from perhaps more than
160 different species, consumption of which varies seasonally
(Kierulff et al., 2002; Procópio de Oliveira, 2002). Although
lion tamarins occasionally glean camouflaged prey from
branch and leaf surfaces (personal observation), they are specialists in the capture of embedded prey. Elongated hands and
fingers allow them to reach into crevices, bromeliads, dried
foliage, and holes in their search for hidden invertebrates and
small vertebrates (Dietz et al., 1997; Rosenberger, 1992;
Rylands, 1993).
While numerous hypotheses have been advanced with regard to the adaptive significance of communal care of young
to parents and helpers, less emphasis has been placed on defining the benefits to the young themselves, perhaps because
to a non–self-feeding immature individual, the benefits of
being provisioned are self-evident (reviewed in Emlen, 1991;
Jennions and MacDonald, 1994; Koenig and Mumme, 1990;
Tardif, 1997). Among callitrichids, provisioning continues
well after juveniles begin to acquire food by independent
means (Price and Feistner, 2001; Roush and Snowdon, 2001;
Ruiz-Miranda et al., 1999). Moreover, callitrichids deviate
from the typical nonprimate pattern in which provisioning
is limited to animal prey. Anecdotal observations and brief
studies have indicated that wild infants and juveniles receive
both fruits and prey via social means, although prey is received
in greater frequency (Izawa, 1978; Passos and Keuroghlian,
1999; Ruiz-Miranda et al., 1999; Yoneda, 1984).
In general, nutritional or informational benefits may accrue
to young callitrichids as a result of provisioning (hypotheses
reviewed in Brown et al., 2004; Ruiz-Miranda et al., 1999).
Nutritional supplementation may act to favor early weaning
and permit accelerated juvenile growth rates by cushioning
the young from nutrition-associated mortality (Garber and
Leigh, 1997). Items that are high in nutrients important for
growth (such as high-protein and -lipid items like prey) and
nutrient-rich foods that are not readily obtainable by potential
recipients due to capture or processing difficulty will be provided more frequently under this hypothesis (Feistner and
Chamove, 1986; Price and Feistner, 1993). Findings that
would provide support for the nutritional supplementation
hypothesis include: (1) young receive primarily animal prey,
(2) the proportion of prey in the provisioned diet increases
with age (because immatures generally should be able to locate and process vegetation resources at an earlier age than
prey), (3) young receive proportionally more difficult-tohandle fruits than readily processed fruits, and (4) young of
a given age do not self-feed on the same plant species with
which they are being provisioned.
Alternatively, the informational benefits hypothesis posits
that immatures learn food preferences through exposure to
food items obtained from older group members (Brown and
Mack, 1978; Feistner and McGrew, 1989). Juveniles are expected to receive a wide variety of foods if provisioning does
act to inform naive young about appropriate foods. Food
items present only rarely in the diet are expected to be transferred to young group members with a higher probability
when encountered than common items in the diet, especially
when first encountered by the young. Individuals should prefer food items with which they have been previously provisioned over those that they have acquired only independently.
Predictions 1 and 2 of the nutritional supplementation hypothesis hinge on the contrasting nutritional and search and
213
handling properties of animal prey versus plant resources.
The other two predictions speculate that among fruits, provisioning will vary according to handling difficulty. The informational benefits hypothesis, in contrast, relies on variability
in food type and familiarity for its predictions. The two hypotheses are not mutually exclusive. For items that present search
or handling challenges, the young may simultaneously receive
nutritional benefits as well as information regarding search
and handling techniques. Thus, the weight of evidence, rather
than any one of the predictions alone, will allow the relative
adaptive significance of the two hypotheses to be evaluated.
The nutritional benefits hypothesis predicts that animal
prey will be provisioned more frequently than vegetation resources. Should such differential food-transfer rates occur, an
additional question would be addressed: to whom might these
differences be attributed? If juveniles drive the hypothesized
variation, begging rates will be higher for prey, whereas if
adults drive the variation, adult resistance to transfers will be
lower and offering calls more frequent for interactions involving prey.
My purpose was to investigate the influence of food type
on provisioning behavior in the golden lion tamarin and to
empirically test the functions of provisioning.
METHODS
Study site and subjects
I conducted observations on six groups of wild golden lion
tamarins living in the União Biological Reserve, Brazil: a
3126-ha mosaic of primary and late-stage secondary Brazilian
Atlantic coastal rain forest, Eucalyptus plantations, small and
scattered feral banana groves, and narrow strips of grassland.
The reserve is one of the largest tracts of mature lowland
Atlantic rain forest in the state of Rio de Janeiro (IBAMA,
2004) and prime habitat for the endangered golden lion
tamarin (Rylands, 1996). Nonetheless, a survey conducted in
1990–1992 revealed no tamarins within the area encompassed
by the reserve. In 1994–1997, six wild golden lion tamarin
family groups that had been surviving in different isolated
forest remnants were translocated into this newly protected
area (Kierulff and Rylands, 2003). During the period of study
(January 2000–February 2003), the population in the União
Reserve increased from at least 12 to 23 groups (Procópio de
Oliveira, 2002; Procópio de Oliveira and Kierulff, personal
communication).
Each group was studied longitudinally, spanning the period
when focal immatures were approximately 11–56 weeks of age
(Table 1). Provisioning in captive lion tamarins peaks at approximately 12 weeks of age (Tardif et al., 2002), and infant
golden lion tamarins may still receive 90% of their solid food
from others at 16 weeks of age (Hoage, 1982). Thus, observations were planned so as to include the period of maximum
provisioning.
All focal individuals had been weaned when formal observations on them began. Immature study subjects are considered to be juveniles, and individuals 57–112 weeks of age are
considered to be subadults, although the subadult period has
been considered to begin as early as 41 weeks of age (Dietz
et al., 1994; Hoage, 1982). Three singleton juveniles were
studied in one group (BA); one pair of twins was studied in
each of the other groups (Table 1). Groups were captured
about twice per year, at which time group members were
marked with hair dye for individual identification, and at
least one individual per group was fitted with a radio transmitter collar. Food supplementation by humans (i.e., bananas)
was provided only at trapping platforms during trapping
attempts.
Behavioral Ecology
214
Table 1
Study-group summary: composition, study period, total hours that focal juveniles were observed, identity of translocated individuals, and year
individual was translocated
Group
name
Period of study
Group composition
Hours observed and age span
studied (juveniles)
BA
December 2000–September 2001
BA
August 2002–March 2003
FU
January 2000–November 2000
GE
January 2001–November 2001
LB
January 2000–November 2000
MA
February 2001–November 2001
RE
December 2001–November 2002
1 AF, 1 AM, 0–3 NA, 0–1 NJF,
1–2 singletons
1 AF, 1 AM, 0–2 NA,
1 singleton
1 AF, 1 AM, 3 NA, twins
(1 JF, 1 JM)
1 AF, 1 AM, 1 NA, 0–1 IJ, twins
(1 JF, 1 JM)
1 AF, 1AM, 1 NA, twins
(1 JF, 1 JM)
1 AF, 1 AM, 1–2 NA, twins
(1 JF, 1 JM)
1 AF, 1–2 AM, twins (2 JM)
JF1: 65.83 h, 11–50 weeks;
JF2: 31.00 h, 17–30 weeks
JM: 67.13 h, 20–50 weeks
JF: 123.13 h; JM: 122.00 h,
13–56 weeks
JF: 124.63 h; JM: 125.67 h,
11–56 weeks
JF: 112.33 h; JM: 112.33 h,
14–56 weeks
JF: 86.40 h; JM: 88.37 h,
12–48 weeks
JM1: 133.57 h; JM2: 135.73 h,
16–56 weeks
Translocation history
AF in 1997, AM in 1997
Same as above
AF in 1995
AM in 1995
AF in 1994, AM in 1997
Group compositions changed as a result of births, deaths, emigration, and immigration. The two singleton juveniles in the BA group became
(subadult) NAs by the second year in which the group was studied. In three groups (BA, GE, and LB), the focal juveniles’ mother died when
the juveniles were 35 weeks of age. In each case, the breeding female was replaced within days by an immigrant female who was born at the
study site. AF ¼ breeding female, AM ¼ nonnatal adult male, NA ¼ natal subadult/adult, JF/M ¼ natal juvenile female/male, NJF ¼ nonfocal
but natal juvenile female, and IJ ¼ immigrant juvenile (who was not studied).
Data collection
Observers normally accompanied each group 11 days per
month. On a given observation day, data collection was focused on either subadults and adults (hereafter adults) or
juveniles. Data collection sessions lasted 20 min, and focal
individuals were alternated between sessions according to a
preset, rotating order throughout the day. Observations typically were carried out 0630 to 1430 h, with number of sessions
ranging from 1 to 20 per day. I used either focal instantaneous
sampling with a 120-s interval or continuous sampling in conjunction with sequence sampling (Martin and Bateson, 1993).
The continuous sampling method was discontinued 3 months
into the first year of the study (thus having been used on only
the LB and FU groups). Data were collected in teams of two,
using a combination of written notations (for sequential data)
and a palmtop computer (for continuous or instantaneous
data). Observers other than the author were trained for a minimum of 2 months prior to independent data collection.
Sequential sampling was concentrated on food-transfer and
social-foraging behaviors. All occurrences and sequences of
the following behaviors involving a focal animal were recorded (see also Rapaport and Ruiz-Miranda, 2002, in press):
approach (focal individual comes to within 1 m of another
tamarin who has food in hand and/or mouth), beg (individual closely inspects or reaches toward a food item with mouth
stretched wide and partially open in a begging grimace and/
or emits a ‘‘rasp’’ vocalization [Ruiz-Miranda et al., 1999] on
approaching an individual who has food), transfer (part or all
of a food item changes possession), resist (the food possessor
actively attempts to discourage a transfer by turning or moving
away, pushing, swatting, or lunging at or otherwise being aggressive to the individual without food), and food-offering call
(a staccato vocalization, also termed food-transfer call, given
by the food possessor that acts to facilitate food transfer
[Brown and Mack, 1978; Ruiz-Miranda et al., 1999]). Preliminary observations had indicated that at 1-m distance a tamarin
apparently could assess whether a group mate had food without necessarily provoking a measurable response. Observers
identified the type of food involved in provisioning interactions, and items were classified as to size. Fruits were defined
as small (1.5 cm average diam), medium (1.5 . 3.0 cm), or
large (3.0 cm) and prey items as small (,1.0 cm in body
length), medium (1.0 6.0 cm), or large (.6.0 cm).
Data analysis
A total of 1330.32 focal contact hours was collected for the
13 juveniles of the study, an average of 102.33 h per juvenile
(Table 1). These data were used exclusively to calculate rates.
Additionally, 516.55 focal contact hours were collected on
adults (average per adult, 17.81 h). These data were combined
with the juveniles’ focal samples to calculate proportional
measures (e.g., proportion of begs that resulted in transfer).
Adults attempted to receive and received food from others
infrequently; only interactions in which focal juveniles were
potential recipients are considered here.
I calculated provisioning interaction rates (i.e., approaches,
begs, food transfer, and resists) by estimating the time spent
visible from the simultaneously collected focal instantaneous
and continuous samples. Thus, rates represent the frequency
of a given behavior divided by the estimated number of hours
spent visible, for a given period. Food-offering call rates were
not calculated because observers could not consistently document these low-amplitude adult vocalizations while focused on
juveniles in the often thick vegetation and from the several
meter distances over which provisioning activities occurred.
I used either number of opportunities for transfer or number
of begs during a given period as the denominator for proportional measures. Opportunities for transfer were occasions in
which a juvenile was within 1 m of another individual who had
food in the hand or mouth. Most opportunities were preceded
by an approach by the juvenile to the food possessor (mean,
94.75%; range per juvenile, 82.56–99.14%). Otherwise, the
juvenile was already within 1 m when a food item was captured,
when a juvenile had been closely following a foraging individual, and, infrequently, when an adult with prey or fruit approached and handed the item to the juvenile. If a juvenile
repeatedly moved in and out of 1-m proximity to a food possessor holding a single item, each approach was scored as a separate
opportunity. A total of 2660 opportunities for transfer (1722
involving vegetation resources, 938 of prey) was recorded.
Rapaport • Provisioning in golden lion tamarins
Number of approaches per prey item was assessed. Multiple
approaches to vegetation resources were not assessed because
many fruits grew in clusters (e.g., Miconia latecrenata, Pourouma
guianensis) and/or were quite large relative to a tamarin (e.g.,
Cecropia hololeuca, Musa sp.). Thus, unlike most prey, fruit resources commonly could provide the opportunity for multiple
transfers from an individual source or cluster.
All tests are two tailed, and significance level was set at
either p .05 or p .0167 for Bonferroni-corrected multiple
comparison tests. Means are presented as 6SE. Data were
normalized using square root (rates) and square root arcsine
(proportions) transformations (Sokal and Rohlf, 1995). Transformations failed to normalize the data regarding identity and
size of provisioned items, so I analyzed these data using nonparametric tests.
Analyses use individual means. To investigate the effects of
age on rates of provisioning interactions and the proportion
of prey in the provisioned diet, I pooled data for each focal
individual into three age classes: 11–24 weeks, 25–40 weeks, and
41–56 weeks. I then used paired t tests or repeated-measures
ANOVAs with Bonferroni-adjusted multiple comparison tests
to assess differences between the age groups. One juvenile
(BA-JF2, see Table 1) was lost to observation after 30 weeks
of age; data from this individual are limited to analyses of
size of provisioned foods and proportion of provisioned food
that was prey.
In order to assess whether young simultaneously self-feed
on the same vegetation species with which they were being
provisioned, I examined instantaneous and continuous data
for evidence of independent feeding on provisioned fruits.
Therefore, I deleted from consideration instances of coforaging (juvenile forages after another individual has begun foraging on the same site or within 15 s after the first individual
has left: see Rapaport and Ruiz-Miranda, 2002) and when
another group member was known or suspected to have bitten
into a fruit’s outer covering prior to consumption by juveniles.
RESULTS
Variety of provisioned foods
The juveniles received a wide variety of items. Provisioned prey
included various lizard and frog species, arachnids, orthopterans, phasmids, mantids, blattaria, isopterans, lepidopterans,
and the larvae of several unidentified insect species, mostly
small but one of which was .6 cm in length. On three occasions, juveniles begged unsuccessfully for frog egg masses.
Provisioned vegetation resources consisted of fruits (including multiple fruits such as Ficus gomelleira and simple fruits
such as berries, fleshy drupes, capsules, and legumes: Appendix) as well as hardened exudates (i.e., plant resins or sap).
The tamarins plucked flowers to obtain nectar, ate bromeliad
flowers and at least one species of an arboreal fungus, but
none of these types of vegetation was transferred. Fruits of
species that had been eaten on previous observation days as
well as fruits of species that were observed to be eaten for the
first time were transferred to juveniles (Table 2). Of those
fruiting taxa eaten by the tamarins that I was able to identify
(23.54 6 1.74 taxa per group), juveniles received a mean of
21.63 6 2.28% (4.77 6 0.38 taxa per juvenile; range: 3–8).
Food-offering calls and approaches to prey
The vast majority of provisioning interactions involving prey
consisted of a rapid approach by the juvenile and immediate
transfer. However, 8.71% of approaches to prey involved multiple approaches by a juvenile to a single item, representing
61 prey items, and of which 43.86% were large. The maximum
215
Table 2
Number of provisioned fruit species, according to whether
a provisioning incident occurred the first day a given species was
observed to be consumed by a given group (first day observed) or
a day subsequent to the first time observed (after first day)
First day observed
After first day
Group name
Small
Medium
Large
Small
Medium
Large
BA (year 2)
BA (year 3)
FU
GE
LB
MA
RE
Total
0
0
0
1
0
1
1
3
1
1
3
1
4
0
2
12
2
0
1
2
3
2
2
12
0
1
0
0
0
0
0
1
1
0
1
1
1
1
2
7
4
1
1
2
2
3
2
15
Fruits are categorized as small (1.5-cm average diam), medium
(1.5 . 3.0 cm), or large (3.0 cm). When a given species of fruit was
provisioned on both the first day in which a given group was observed
to eat it as well as having been provisioned in the same group on
a subsequent day, it appears in both columns. Those fruit species were
Eugenia robustovenosa, Rollinia dolabripetala, Pourouma guianensis, and
Inga sp. The proportion of provisioned large fruits to small fruits is
statistically equivalent whether transferred on the ‘‘first day observed’’
or ‘‘after first day’’ (Fisher’s Exact test: p ¼ .3326).
number of recorded approaches to a single item was by juvenile BA-JF2 to her mother, who had captured a large (.6 cm)
vertebrate. The juvenile rasped repeatedly and approached
10 times (including five approaches after the focal period).
The mother repeatedly emitted food-offering calls. She gave
several of these calls before killing and beginning to eat the
item, but it was never transferred.
Adults emitted food-offering calls prior to 11.30 6 2.36%
(range 0–30.77% per juvenile) of food transfers involving
prey. This is likely to be an underestimate due to the caveats
discussed above. Food-offering calls were never heard during
vegetation-resource transfer.
Aggression over food
Only 18 incidents of contact aggression over food were observed. All were mild, that is, they were brief and resulted in
no visible injuries. Adults were aggressive to juveniles in six of
these incidents. In 10 cases, juveniles attacked juveniles, for
instance, to chase away a twin as the twin approached a feeding
adult whom the attacking juvenile had been following. Fourteen of the 18 incidents involved vegetation resources.
Provisioning rates and age effects
In total, 141 transfers to juveniles of vegetation resources and
480 transfers of vertebrate and invertebrate prey were recorded. Juveniles approached group members who were eating
vegetation resources at higher rates than group members who
were eating prey (paired t test, fruit versus prey: df ¼ 11, t ¼
4.969, p ¼ .0004). Conversely, they begged for (paired t test,
fruit versus prey: df ¼ 11, t ¼ 4.589, p ¼ .0008) and received
(df ¼ 11, t ¼ 6.691, p , .0001) prey more frequently than
nonprey. Rates of resistance to provisioning did not vary according to item type (df ¼ 11, t ¼ 1.704, ns; Figure 1).
Provisioning interaction rates per hour involving both prey
and vegetation resources varied with age of the potential recipient. While rates at which juveniles approached others who
had vegetation resources did not vary with age, the rates at
which they begged for and received these items did decline as
Behavioral Ecology
216
Table 4
Repeated-measures ANOVA results for the effect of recipient
age on approach, beg, and food-transfer rates per hour involving
animal prey
Age class 1
Figure 1
Mean rates per hour 1 SE of provisioning interactions with prey and
vegetation resources. Paired t tests show that juveniles approached
adults who were eating or handling vegetation resources more frequently than those who had prey but begged for and received prey
more frequently. Rate of adult resistance to juveniles was not influenced by the type of item that the adults were handling. *.05 p .
.01; **.01 p . .005; ***.005 p . .001; *****p .0005.
juveniles got older. Bonferroni-adjusted post hoc tests reveal
differences between the first and third age classes for begging
rates and between all age-group comparisons for vegetationresource transfer rates (Table 3). In contrast to approach rates
to vegetation resources, approach rates to prey significantly
declined with age. Begging and food-transfer rates involving
prey also significantly decreased with juvenile age. In the case
of prey, post hoc tests showed significant differences between
all age-class comparisons for approaches, begs, and transfers
(Table 4). Rates of resistance were too low for analysis as a
function of age.
Provisioning corrected for opportunity
Proportional measures have the advantage of permitting comparison of provisioning behaviors while controlling for opportunity and interest in transfer. This is important given the
large disparity in approach and begging rates between prey
and vegetation resources. I examined relative interest in food
transfer (i.e., proportion of opportunities in which the juvenile begged), relative resistance by adults to potential food-
Age class 2
Approach prey
1.100 6 0.131
0.644 6 0.050
Age class 1 3 age class 2
Age class 1 3 age class 3
Age class 2 3 age class 3
Beg for prey
0.981 6 0.123
0.591 6 0.049
Age class 1 3 age class 2
Age class 1 3 age class 3
Age class 2 3 age class 3
Receive transfer of prey
0.779 6 0.112
0.381 6 0.056
Age class 1 3 age class 2
Age class 1 3 age class 3
Age class 2 3 age class 3
Age class 3
F2,22
p value
0.311 6 0.064
29.174
,.0001
.0026
,.0001
.0006
0.184 6 0.056
50.958
,.0001
.0084
,.0001
,.0001
0.072 6 0.030
47.843
,.0001
.0027
,.0001
.0112
Significance levels are set as in Table 3.
transfer events (i.e., proportion of opportunities resisted by
adults), and relative begging success (i.e., proportion of begs
that resulted in food transfer; Figure 2). There was a higher
probability that a juvenile would beg when approaching an individual with prey as opposed to a vegetation resource (paired
t test, prey versus vegetation resources: mean percentage of
opportunities with beg, df ¼ 11, t ¼ 22.920, p , .0001). Given
that a juvenile did beg for an item, successful transfer was a
more likely outcome if the item was prey than if it was a vegetation resource (percentage of begs resulting in transfer,
df ¼ 11, t ¼ 2.582, p ¼ .0255). Even though begging success
was higher for prey, opportunities for transfer were resisted
proportionately more often when the food possessor had prey
compared to nonprey (paired t test, prey versus vegetation
resources: mean percentage of resisted approaches, df ¼ 11,
t ¼ 3.886, p ¼ .0025).
Table 3
Repeated-measures ANOVA results for the effect of recipient age on
approach, beg, and food-transfer rates per hour involving vegetation
resources
Age class 1
Age class 2
Approach vegetation resources
1.028 6 0.143 1.165 6 0.115
Beg for vegetation resources
0.410 6 0.067 0.285 6 0.065
Age class 1 3 age class 2
Age class 1 3 age class 3
Age class 2 3 age class 3
Age class 3
F2,22
p value
1.015 6 0.094
0.536
.5925
0.134 6 0.030
7.479
.0033
.1298
.0008
.0394
31.903
,.0001
,.0001
,.01
.0112
Receive transfer of vegetation resources
0.264 6 0.158 0.066 6 0.074 0.018 6 0.021
Age class 1 3 age class 2
Age class 1 3 age class 3
Age class 2 3 age class 3
ANOVAs were performed on square root–transformed data, although
untransformed rates per hour 6 SE are presented in the table.
Bonferroni-adjusted post hoc significance level is set at 0.0167, and
comparisons in bold are statistically significant.
Figure 2
Begging, transfer, and resistance, corrected for opportunity. The
percentage of opportunities for transfer in which juveniles begged
and the percentage of begs that resulted in successful transfer were
significantly higher when the contested item was prey compared to
a vegetation resource. The percentage of opportunities in which
adults resisted transfer was higher for prey than for nonprey.
Significance levels of paired t tests are indicated as in Figure 1.
Rapaport • Provisioning in golden lion tamarins
217
Figure 3
Proportion of total approaches to (a) vegetation resources and (b) prey and proportion of approaches within a size category resulting in
transfer. The scale is the same in both (a) and (b). A bar’s height represents the proportion of approaches to the given size category out of the
total approaches. The filled portions of the bars illustrate the proportion of approaches to items within a category that resulted in successful
transfer; this number is also noted above each bar. For example, 44.63 6 3.62% of all vegetation resources approached was to large-sized fruits
(the height of the bar). When within 1 m of others who were handling a large fruit, however, 15.36% of the time juveniles received the item (the
area in black). Friedman tests, with size of fruit or size of prey as treatment effects, demonstrate that probability of transfer was significantly
higher for large fruits than small fruits and for medium-sized prey than small prey. The probability of exudate transfer did not differ from that of
overall fruit transfer. Approaches to vegetation resources other than fruits were infrequent. Significance levels are indicated as in Figure 1.
The proportion of prey in the provisioned diet increased
from 70.28 6 4.60% to 79.36 6 4.52% from weeks 11–24 to
weeks 25–40, but the difference was not statistically significant
(paired t test, df ¼ 12, t ¼ 1.704, ns).
Characteristics of provisioned foods
To analyze the probability of transfer as a function of size,
I normalized encounter rates by comparing proportions of
successful transfer, given an approach, rather than transfer
rates per hour.
Ninety percent of approached fruit that was being handled
by others was characterized according to size and thickness or
toughness of skin. Approaches to large fruits resulted in a
higher probability of transfer than did approaches to small
fruits (Friedman test, v2 ¼ 10.308, df ¼ 2, p ¼ .0038; Scheffé
multiple comparison tests, large versus small, p ¼ .0301, medium versus small and large, ns; Figure 3a). Only 4.17 6
2.57% of all size-categorized fruits that juveniles received
was small, 18.16 6 4.56% was medium, and 77.68 6 5.70%
was large. Moreover, 34.70 6 7.08% of transferred fruit had
a thick and/or tough outer covering; approaches to these
fruits were more likely to result in transfer than approaches
to thin-skinned fruits (thick/tough versus thin skins: 13.38 6
3.68 versus 7.33 6 1.66%; Wilcoxon signed-rank test, n ¼ 13,
T ¼ 17, p .05). Juveniles approached other tamarins who
were handling exudates, flowers, and fungi at low frequencies
(Figure 3a). Juveniles never were provisioned with flowers and
fungi. Exudates were not frequently eaten, and thus not approached often, but when juveniles did approach adults who
were eating exudates, the probability of exudate transfer did
not differ from the overall probability of receiving a fruit that
had been approached (exudates versus fruits: 24.95 6 11.93%
versus 8.86 6 1.57%; Wilcoxon signed-rank test, n ¼ 13,
T ¼ 44, ns).
I assessed the size of 66.50% of the prey items that juveniles
approached. The proportion of approached items that was
fed to juveniles varied significantly with size (Friedman test,
v2 ¼ 10.308, df ¼ 2, p ¼ .0058): medium-sized items were
relinquished to juveniles proportionally more frequently than
small prey (Scheffé multiple comparison tests, medium versus
small, p ¼ .0033; other comparisons, ns). Overall, 6.05 6
2.04% of all size-classified prey received was small, 76.88 6
2.43% was medium, and 17.07 6 2.98% was of large size
(Figure 3b).
For 43.24% of provisioned prey items, observers noted
whether all or part was transferred to the juvenile. The entire
item was transferred in 35.08% of these cases. In contrast,
considering only those cases when the adult first either uttered a food-offering call or approached the juvenile and
offered the prey, 70.97% of time the adult ate none before
relinquishing the entire and often still-living item.
Provisioning versus independent feeding
Eleven of the 13 juveniles were recorded as having fed independently on a given type of fruit on the same day on which
they were provisioned with the said fruit. Six juveniles did so
for more than one type of fruit (maximum: 3 taxa). The remaining two juveniles (both of GE group) were each recorded
to have fed independently on two different species of fruits
within the same week in which they received those fruits via
social means (and in all four cases, the days on which the fruits
were provisioned, observers were recording adult behavior
and so would not have noted juvenile feeding behavior). Thus,
inability to acquire an item independently did not appear to
be the determining factor behind all fruit provisioning.
DISCUSSION
All juvenile study subjects received both animal prey and plant
resources from other group members. As in all wild callitrichid populations studied to date, prey was provisioned more
frequently than nonprey (Izawa, 1978; Neyman, 1980; Passos
and Keuroghlian, 1999; Ruiz-Miranda et al., 1999; Yoneda,
1984). In a nutritional analysis of dietary vegetation and animal
218
prey among the golden lion tamarins of the União Reserve,
Erbesdobler (2003) found that animal prey had consistently
higher concentrations of proteins and lipids than any of the
34 species of fruits and flowers in the sample. Thus, given its
nutrient value and because prey is in general more difficult to
acquire than vegetation resources, the findings that juveniles
were provisioned more than four times as frequently with
prey as with vegetation resources point to a nutritional function for provisioning. Also in agreement with nutritional
hypothesis predictions, the proportion of prey received
increased as juveniles matured, but the difference was not
statistically significant. Previous studies have concurred that
callitrichid young typically receive fruits from others (Izawa,
1978; Neyman, 1980; Passos and Keuroghlian, 1999; RuizMiranda et al., 1999; Yoneda, 1984), but this is the first
published report of exudate provisioning. Rates of both prey
and vegetation-resource provisioning declined gradually as
the juveniles matured.
Prey of medium size was more likely to be relinquished to
juveniles than small-sized prey. In contrast, when a fruit was
involved a juvenile who approached another individual was
more likely to receive the item if the food possessor had a
large-sized fruit than a smaller fruit. All else being equal,
larger fruits might be expected to provide more nutritional
value, if entire fruits are transferred. However, very large fruits
were never transferred whole. Caloric density, as well as other
nutritional factors such as mineral, vitamin, and enzyme contents may influence provisioning decisions, the values of
which may vary among trees, seasons, and individual fruits.
Aside nutritional considerations, large fruit size may present
handling challenges to an immature tamarin. Properties other
than size also may create variance in handling difficulty. For
instance, more than one-third of transferred fruit had thick
and/or tough skin and thus may have been difficult for juveniles to process. This is a higher percentage than that observed in another population of golden lion tamarins: RuizMiranda et al. (1999) found that 12% of the transferred fruit
in the nearby Pocxo das Antas Reserve appeared to be difficult
for juvenile golden lion tamarins to handle. In this study,
fruits with thick and/or tough outer coverings were more
likely to be provisioned than thin-skinned fruits. Experiments
have shown that captive infant lion tamarins both beg more
and experience higher begging success when food is difficult
for them to acquire independently (Price and Feistner, 1993).
On the other hand, all juvenile study subjects demonstrated
an ability to independently acquire fruits with which they had
been very recently provisioned. At least 11 out of the 13 juveniles ate both provisioned and independently acquired fruits
of the same kind on the very same day. Clearly then, difficulty
of independent access to an item is not the only factor that
drives provisioning of vegetation resources in this population.
A broad variety of prey and vegetation-resource species was
transferred to juveniles, as predicted by the informational benefits hypothesis. For example, of all identified kinds of fruits
that were eaten by the tamarins, more than 20% were transferred to juveniles. Some of these were fruits to which the
juveniles had been exposed on prior occasions, while others
they may have been experiencing for the first time. Thus, both
common and previously uncommon species of fruits were
transferred to the young. Three out of the four provisioned
species of small fruits were received by juveniles on the first
day the group was observed to eat the species. None of these
small fruits appeared to present processing difficulties to the
juveniles. Ruiz-Miranda et al. (1999), in contrast, reported
that only common fruits were transferred to young golden
lion tamarins in the nearby Poc
xo das Antas Reserve. Habitat
variation could explain these divergent findings. The tamarins
in the Pocxo das Antas Reserve (which in contrast to União
Behavioral Ecology
contains early successional stages and no primary Atlantic
coastal rain forest) are reported to consume fewer vegetationresource species than those at União: approximately 60 versus
more than 160 (Kierulff et al., 2002; Procópio de Oliveira,
2002). Therefore, the probability that a tamarin group will
encounter a rarely eaten fruit species may be higher at União.
Patterns of prey and vegetation-resource provisioning differed in important ways. Although juveniles closely approached individuals who had a vegetation resource in hand
or mouth almost twice as frequently as they did those with
prey, active interest in prey that others had captured, was
more evident than interest in nonprey. That is, juveniles both
begged for and received prey more frequently than vegetation resources, even after controlling for opportunity. Adults
encouraged the transfer of captured prey, never vegetation
resources, with food-offering calls. What is more, given the
proximity of a juvenile to an adult with food, the adult was
more likely to resist transfer if the item of interest was prey.
That adults resisted prey transfer relatively more frequently
but juveniles experienced relatively higher begging success
for these items is counterintuitive and implies that resistance
to prey transfer tends to be less effective. Perhaps, juveniles
tend to beg more intensively or approach more quickly when
the contested item is prey, thus reducing successful resistance
to transfer. Alternatively, adults may tend to employ less effective resistance behaviors, or juveniles may be more likely to
interact with individuals who are less determined in their
resistance, when prey is involved.
Most incidents of aggression over food or feeding sites involved fruits even though apparent interest in transfer was
higher for prey. Aggression was not a significant deterrent
to feeding or food transfer, however, because aggression over
food was mild and extremely infrequent. Aggression from
adults to juveniles was less frequent than that between twins:
adults aggressed on juveniles only six times, and juveniles on
juveniles 10 times, in approximately 1850 h of observation.
Overt aggression may be just one manifestation of sibling
competition. Manser and Avey (2000) have suggested that
meerkat pups increase the intensity of their begging calls on
capture of prey by a potential provider in order to increase the
probability that the caller, and not a sibling, will receive the
item. Like meerkats, golden lion tamarins are provisioned as
mobile young with sibling competitors. Also like meerkats, the
vocalizations of begging young often become more intense as
juveniles approach adults with food in hand (Ruiz-Miranda
et al., 1999; personal observation).
Differences in distribution patterns of prey and vegetation
resources may help to explain provisioning-behavior variability. Many of the fruits eaten by tamarins either occur in
bunches (e.g., Cecropia spp., Euterpe edulis, P. guianensis) or
multiple fruits ripen simultaneously in the same vicinity
(e.g., Myrcia fallax), thus allowing one tamarin to approach
another closely enough to see what the other is eating yet feed
on a separate item. Prey, in contrast, typically is found as single
items; feeding on social insects such as termites was relatively
uncommon. In the case of fruits, juveniles may approach feeding group members and not obtain food through direct transfer, yet may obtain food, foraging information or feeding
assistance by observing, for example, what kind of fruit or
color of fruit that an adult is eating and then cofeeding on
a nearby similar fruit or by feeding on a fruit that is still
attached to the parent tree, bush, or vine but which has been
opened by an adult. Such cofeeding is rarely possible for prey
due to its highly depletable nature. From this perspective, the
observation that approach rates by juveniles to adults who
were eating vegetation resources did not decline with age,
while approaches to adults with prey did, is not surprising.
Nonetheless, juveniles do forage at the same sites where adults
Rapaport • Provisioning in golden lion tamarins
have just found prey, even though juveniles rarely capture
prey as a result of these coforaging interactions (Rapaport
and Ruiz-Miranda, 2002).
The nutritional benefits hypothesis was generally supported by prey-provisioning results, but provisioning interactions suggest more than a simple nutritional supplementation
function. Aspects of adult behavior appear to actively facilitate the foraging effectiveness of juvenile group mates in
several ways. Food-offering calls, in particular, may function
to enhance the prey capture–learning process. It is well established that food-offering calls function to alert juveniles that
food has been obtained and is available for transfer (Brown
and Mack, 1978; Feistner and Price, 1991). My observations
generally concur with these studies of captive tamarins, although food-offering calls were not heard during vegetationresource transfer among my wild study subjects. On the very
few occasions that adults gave food-offering calls while eating
vegetation resources, the juveniles who approached then simply cofed from the same plant (Rapaport LG, unpublished
data). Beyond informing the young that food is available,
adults appear to use these vocalizations specifically to encourage the young to approach and take live prey from the caller’s
hand. The percentage of prey that was relinquished whole,
and often living, when the transfer had been preceded by
a food-offering call was twice as high as the overall percentage
of prey that was transferred whole. In addition, adults with
large prey were observed to give food-offering calls repeatedly
when juveniles approached and retreated without taking the
item. Reluctance of juveniles to take large prey may explain
why large-sized prey was no more likely to be transferred than
medium-sized prey, even though from the perspective of
potential energy gains a preference for large prey would be
predicted. If juveniles are hesitant to take live prey (perhaps
because the item could bite, sting, or escape), adults might
selectively promote transfer of more difficult-to-handle prey
over other resources such as small or dead prey or fruits. Roush
and Snowdon (2001), in a study of captive cotton-top tamarins,
also suggested that food-offering calls act as encouragement,
focusing the young on opportunities to learn about novel,
rare, and difficult-to-obtain foods. Wild black lion tamarins
(Leontopithecus chrysopygus) reportedly consume a high proportion of relatively large insect prey (Passos and Keuroghlian,
1999). Although adults of this species produce food-offering
calls at low frequencies in captivity (Feistner and Price,
2000), one might expect that wild adults transfer prey to immatures in conjunction with a high rate of food-offering calls.
Food-offering calls also enhance juvenile prey-foraging success by alerting the young to the location of hidden prey.
Adults in this population have been observed to initiate extractive foraging, stop, and then emit a food-offering call,
although no prey capture is evident. Juveniles who approach
in response to the call then begin to forage immediately and
always find prey (Rapaport and Ruiz-Miranda, 2002). Juveniles
may learn about potentially productive prey-foraging substrates from these directed interactions.
Although I documented the first time a study group was
observed to feed on a given species of fruit, I did not know
whether any or all group members had previously encountered such naturally occurring foods. Collection of this information would entail development of a complete inventory
and phenological profile of at least the primary fruit resources
within a study group’s territory and more continuous monitoring of the animals’ movements. Laboratory environments can
provide valuable complementary data with regard to the informational benefits hypothesis, even though they do not offer the
range of food and foraging options available to wild individuals, because the experimenter can have complete knowledge
regarding a subject’s food-exposure history. Experimental stud-
219
ies using experienced-model paradigms suggest that social
interactions do play a role in the development of food recognition and acceptance. Cotton-top tamarin (Saguinus oedipus)
adults produce facial signals that dissuade other group members from eating unpalatable foods (Snowdon and Boe, 2003).
Immature common marmosets (Callithrix jacchus) prefer novel
foods that they have previously received from other group
members to those that they have previously experienced alone
(Vitale and Queyras, 1997). Golden lion tamarin adults are
more likely to transfer to young foods that are familiar to adults
but novel to the young compared to foods that are familiar to
all. Novel foods received from adults are more likely to be
eaten than those that the young have acquired independently
(Rapaport, 1999).
In contrast, Price and Feistner (1993) reported that rates of
adult resistance were higher and transfer rates lower when
lion tamarins were presented with novel compared to familiar
food. Brown et al. (2005) also found that adult common marmosets were more likely to resist transfer attempts when food
was novel, as opposed to familiar, while juveniles begged more
for novel foods. The apparent lack of consistency between
studies may rest, at least in part, with the definition of novel.
Adults had prior experience with the foods used in the experiments demonstrating mechanisms for information transfer,
while only some of the adults of Price and Feistner (1993)
and none of the adults of Brown et al. (2005) had previously
sampled the novel foods before the experiments. Further indication that a food provider’s experience with a food may
influence provisioning is as follows: captive adult golden lion
tamarins immediately discarded foods that were novel to
them more frequently than known foods, thus effectively
providing less opportunity for provisioning (Rapaport, 1999).
Wild callitrichid adults probably encounter foods about
which they have no prior knowledge, at least occasionally. In
this study, four of the six study groups contained one to two
breeding adults who had been translocated from physically
distinct Atlantic coastal rain forest remnants to the União
Reserve 3–6 years prior to observations. Given the fact that
some frutiferous species reproduce only once every few years
(Morellato et al., 2000), the more recently translocated breeding adults, as well as young adults, may not have been familiar
with all of the fruit species exploited by their group. As the
experimental studies indicate, reactions of an adult to a foodsoliciting immature group mate may differ depending on the
familiarity of the food possessor to the food item in question.
In summary, my results suggest that wild juvenile golden
lion tamarins receive both nutritional and informational
benefits from being provisioned. Supporting a nutritional
benefits function were my findings that juveniles received
prey from others more frequently than vegetation resources,
that the juveniles’ interest in transfer as well as begging
success was higher for prey than for vegetation resources,
and that presumably difficult-to-process fruits were more
likely to be transferred than readily processed fruits. Conversely, informational benefits are indicated because a large
variety of foods were provisioned to the young, and juveniles
fed independently on, and were provisioned with, the same
fruits on the same day. A dual function for fruit provisioning, related to both unfamiliarity and handling difficulty, is
suggested because both previously uncommon and commonly eaten fruits were transferred to juveniles. Elevated
prey-provisioning rates were reflected in the behavior of
both participants: juveniles begged more frequently for prey
while adults exclusively emitted food-offering calls when
transferring prey as opposed to vegetation resources. In addition, my findings suggest a training role for food-offering
calls, but further study is needed to clarify the functions of
this vocalization.
Behavioral Ecology
220
APPENDIX
Identities of fruits transferred to juveniles; additional transferred
species were not identified in detail but described according to size
and skin thickness only
Scientific name
Common name
Size category
Cecropia glaziovii
Cecropia hololeuca
Cecropia pachystachya
Eugenia robustovenosa
Euterpe edulis
Ficus gomelleira
Helicostylis tomentosa
Inga edulis
Inga sp. 1
Miconia hypoleuca
Musa spp.
Passiflora sp. 1
Posoqueria sp. 1
Pourouma guianensis
Pouteria bangii
Psidium sp. 1
Rollinia dolabripetala
Rubiaceae sp. 1
Sarcaulus brasiliensis
Simarouba amara
Sp. 1
Sp. 2
Sp. 3
Sp. 4
Sp. 5
Embauba do brejo
Embauba
Embauba preta
Ameixa da mata
Palmito
Figo
Pelucinha
Ingá commun
Ingá
Pixirica amarela
Banana
Cipó maracujá
Jambo amarelo
Arixixá
Abiu, abil
Arac
xá
Biribá
Marmelo
80,000
Poque
Jamelão
Large
Large
Large
Large
Small
Medium
Medium
Large
Large
Small
Large
Medium to large*
Large
Medium
Medium
Medium* to large
Large
Medium* to large
Medium
Medium
Large
Large
Medium
Small
Small
Common names are the regional Brazilian (Portuguese) terms for the
fruits. As the table shows, three reliably identified species produced
fruits that spanned two size categories. In those cases, the size of the
individual transferred fruit is indicated with an asterisk.
I would like to thank the Translocation Team of the Golden Lion
Tamarin Association, run by Paula Procópio de Oliveira and Maria
Cécilia Kierulff, for their constant help and cooperation. They translocated the original six groups of tamarins to the União Reserve and
monitored the population. They kindly provided my project with
maps of the Reserve and fruit identifications. I would like to warmly
acknowledge IBAMA, especially Whitson José da Costa, Jr, the Golden
Lion Tamarin Association, CNPq, Carlos Ruiz-Miranda, and Jane
Lancaster for logistical assistance. National Institute of Mental Health
(grant # MH59175) and the Pittsburgh Zoo Conservation Fund provided financial support. The University of New Mexico Statistics Lab is
thanked for statistical advice. Thanks are also due three anonymous
reviewers who improved the manuscript with their helpful suggestions. E. Almeida, A.P. da Silva Amorim, G. Vieira Faria, M. Moraes,
A. Ferreira Ramos, B.M. Roberts, C.R. Ruiz-Miranda, J.J. da Silva, R.
Tabet, and B. Tressoldi contributed to data collection. This research
adhered to University of New Mexico Main Campus Animal Care and
Use Committee guidelines (Protocol #9801) and to all relevant Brazilian laws, regulations, and guidelines.
REFERENCES
Baker AJ, 1991. Evolution of the social system of the golden lion
tamarin (Leontopithecus rosalia): mating system, group dynamics,
and cooperative breeding (PhD dissertation). College Park: University of Maryland.
Blaffer-Hrdy S, 1999. Mother nature. New York: Ballantine Books.
Boran JR, Heimlich SL, 1999. Social learning in cetaceans: hunting,
hearing and hierarchies. In: Mammalian social learning: comparative and ecological perspectives (Box HO, Gibson KR, eds).
Cambridge: Cambridge University Press; 282–307.
Brotherton PNM, Clutton-Brock TH, O’Riain MJ, Gaynor D, Sharpe L,
Kansky R, McIlrath GM, 2001. Offspring food allocation by parents
and helpers in a cooperative mammal. Behav Ecol 12:590–599.
Brown GR, Almond REA, Bates NJ, 2005. Adult-infant food transfer
in common marmosets: an experimental study. Am J Primatol 65:
301–312.
Brown GR, Almond REA, van Bergen Y, 2004. Begging, stealing, and
offering: food transfer in nonhuman primates. Adv Study Behav
34:265–295.
Brown K, Mack DS, 1978. Food sharing among captive Leontopithecus
rosalia. Folia Primatol 29:268–290.
Caughley G, 1966. Mortality patterns in mammals. Ecology 47:
906–918.
Choquenot D, 1991. Density-dependent growth, body condition and
demography in feral donkeys: testing the food hypothesis. Ecology
72:805–813.
Clutton-Brock TH, Brotherton PNM, O’Riain MJ, Griffin AS, Gaynor R,
Kansky R, Sharpe L, McIlrath GM, 2001. Contributions to cooperative rearing in meerkats. Anim Behav 61:705–710.
Dettwyler KA, 1989. Styles of infant feeding: parental/caretaker control
of food consumption in young children. Am Anthropol 91:696–703.
Dietz JM, Baker AJ, Miglioretti D, 1994. Seasonal variation in reproduction, juvenile growth, and adult body mass in golden lion tamarins (Leontopithecus rosalia). Am J Primatol 34:115–132.
Dietz JM, Peres CA, Pinder L, 1997. Foraging ecology and use of space
in wild golden lion tamarins (Leontopithecus rosalia). Am J Primatol
41:289–305.
Emlen SJ, 1991. Evolution of cooperative breeding in mammals and
birds. In: Behavioural ecology: an evolutionary approach, 3rd ed
(Krebs JR, Davies NB, eds). Oxford: Blackwell Scientific; 301–337.
Erbesdobler ED’A, 2003. Ecologia nutricional do mico-leão dourado
(Leontopithecus rosalia): composic
xão quı́mico-bromatológica da dieta, aspectos do comportamento alimentar, digestibilidade e metabolismo energético (PhD dissertation). Campos dos Goytacazses:
Universidade Estadual do Norte Fluminense.
Ewer RF, 1973. The carnivores. Ithaca: Cornell University Press.
Feistner ATC, Chamove AS, 1986. High motivation toward food
increases food-sharing in cotton-top tamarins. Dev Psychobiol 19:
439–452.
Feistner ATC, McGrew WC, 1989. Food-sharing in primates: a critical
review. In: Perspectives in primate biology, vol. 3 (Seth PK, Seth S,
eds). New Delhi: Today and Tomorrow’s Printers and Publishers;
21–36.
Feistner ATC, Price EC, 1990. Food-sharing in cotton-top tamarins
(Saguinus oedipus). Folia Primatol 54:34–45.
Feistner ATC, Price EC, 1991. Food offering in New World primates:
two species added. Folia Primatol 57:165–168.
Feistner ATC, Price EC, 2000. Food sharing in black lion tamarins
(Leontopithecus chrysopygus). Am J Primatol 52:47–54.
Ferrari SF, 1987. Food transfer in a wild marmoset group. Folia
Primatol 48:203–206.
French JA, Inglett BJ, Dethlefs TM, 1989. The reproductive status of
nonbreeding group members in captive golden lion tamarin social
groups. Am J Primatol 18:73–86.
Garber PA, Leigh SR, 1997. Ontogenetic variation in small-bodied new
world primates: implications for patterns of reproduction and
infant care. Folia Primatol 68:1–22.
Garber PA, Moya L, Malaga C, 1984. A preliminary field study of the
moustached tamarin monkey (Saguinus mystax) in northeastern
Peru: questions concerned with the evolution of a communal breeding system. Folia Primatol 42:17–32.
Gilchrist JS, 2004. Pup escorting in the communal breeding banded
mongoose: behavior, benefits, and maintenance. Behav Ecol
15:952–960.
Hoage RJ, 1982. Social and physical maturation in captive lion tamarins Leontopithecus rosalia rosalia. Smithson Contrib Zool 354:1–60.
[IBAMA] Instituto Brasileiro do Meio Ambiente and Recursos Naturais Renováveis, 2004. Unidade: área de protec
xão ambiental da Bacia
do Rio São João/mico-leão-dourado/RJ. http://www.ibama.gov.br.
Izawa K, 1978. A field study of the ecology and behavior of the blackmantled tamarin (Saguinus nigricollis). Primates 19:241–274.
Jennions MD, MacDonald DW, 1994. Cooperative breeding in mammals. Trends Ecol Evol 9:89–93.
Kierulff MCM, Procópio de Oliveira P, Beck BB, Martins A, 2002.
Reintroduction and translocation as conservation tools for golden
lion tamarins. In: Lion tamarins: biology and conservation
(Kleiman DG, Rylands AB, eds). Washington: Smithsonian Institution Press; 271–282.
Rapaport • Provisioning in golden lion tamarins
Kierulff MCM, Rylands AB, 2003. Census and distribution of the
golden lion tamarin (Leontopithecus rosalia). Am J Primatol 59:29–44.
King BJ, 1994. Primate infants as skilled information gatherers.
Pre- Perinat Psychol J 8:287–307.
Kitchener AC, 1999. Watch with mother: a review of social learning
in the Felidae. In: Mammalian social learning: comparative and
ecological perspectives (Box HO, Gibson KR, eds). Cambridge:
Cambridge University Press; 236–258.
Koenig WD, Mumme RL, 1990. Levels of analysis and the functional
significance of helping behavior. In: Interpretation and explanation
in the study of animal behavior (Bekoff M, Jamieson D, eds).
Boulder: Westview Press; 269–303.
Lacey EA, Sherman PW, 1997. Cooperative breeding in naked molerats: interpretations for vertebrate and invertebrate society. In:
Cooperative breeding in mammals (Solomon NG, French JA,
eds). Cambridge: Cambridge University Press; 267–301.
Lancaster JB, Lancaster CS (eds), 1983. Parental investment: the hominid adaptation. In: How humans adapt: a biocultural odyssey.
Washington, District of Columbia: Smithsonian Institution Press;
33–65.
MacDonald DW, Moelhman PD, 1982. Cooperation, altruism, and restraint in the reproduction of carnivores. In: Perspectives in ethology, vol. 3: ontogeny (Bateson PPG, Klopfer PH, eds). New York:
Plenum Press; 433–467.
Mace R, 2000. Evolutionary ecology of human life history. Anim Behav
59:1–10.
Manser MM, Avey G, 2000. The effect of pup vocalizations on
food allocation in a cooperative mammal, the meerkat (Suricata
suricatta). Behav Ecol Sociobiol 48:429–437.
Martin P, Bateson P, 1993. Measuring behavior: an introductory guide,
2nd ed. Cambridge: Cambridge University Press.
Moelhman PD, Hofer H, 1997. Cooperative breeding, reproductive
suppression, and body mass in canids. In: Cooperative breeding in
mammals (Solomon NG, French JA, eds). Cambridge: Cambridge
University Press; 76–128.
Morellato LPC, Talora DC, Takahasi A, Bencke CSC, Romera EC,
Zipparro V, 2000. Phenology of Atlantic rain forest trees: a comparative study. Biotropica 32:811–823.
Neyman PF, 1980. Ecology and social organization of the cotton-top
tamarin (Saguinus oedipus) (PhD dissertation). Berkeley: University
of California.
Nishida T, Turner LA, 1996. Food transfer between mother and infant
chimpanzees of the Mahale Mountains National Park, Tanzania. Int
J Primatol 17:947–968.
Packer C, Herbst L, Pusey AE, Bygott JD, Hanby JP, Cairns SJ,
Borgerhoff Mulder M, 1988. Reproductive success of lions. In: Reproductive success: studies of individual variation in contrasting
breeding systems (Clutton-Brock TH, ed). Chicago: University of
Chicago Press; 363–383.
Passos FC, Keuroghlian A, 1999. Foraging behavior and microhabitats
used by black lion tamarins, Leontopithecus chrysopygus (Mikan)
(Primates: Callitrichidae). Rev Bras Zool 16(suppl. 2):219–222.
Price EC, Feistner ATC, 1993. Food sharing in lion tamarins: tests of
three hypotheses. Am J Primatol 31:211–221.
Price EC, Feistner ATC, 2001. Food sharing in pied-faced tamarins
(Saguinus bicolor bicolor): development and individual differences.
Int J Primatol 22:231–241.
221
Procópio de Oliveira P, 2002. Ecologia alimentar, dieta e área de uso
de micos-leões-dourados translocados e sua relac
xão com a distribuic
xão espacial e temporal de recursos alimentares na Reserva
Biológia União-RJ (PhD dissertation). Belo Horizonte: Universidade Federal de Minas Gerais.
Rapaport LG, 1999. Provisioning of young in golden lion tamarins
(Callitrichidae, Leontopithecus rosalia): a test of the information
hypothesis. Ethology 105:619–636.
Rapaport LG, Ruiz-Miranda CR, 2002. Tutoring in wild golden lion
tamarins. Int J Primatol 23:1063–1070.
Rapaport LG, Ruiz-Miranda CR, in press. Ontogeny of provisioning
in two populations of wild golden lion tamarins (Leontopithecus
rosalia). Behav Ecol Sociobiol.
Rasa OAE, 1989. Helping in dwarf mongoose societies: an alternative
reproductive strategy. In: The sociobiology of sexual and reproductive strategies (Rasa OAE, Vogel C, eds). Beckenham: Croom Helm;
61–73.
Rood JP, 1978. Dwarf mongooses helpers at the den. Z Tierpsychol
48:277–287.
Rosenberger A, 1992. Evolution of feeding niches in New World
monkeys. Am J Phys Anthropol 88:525–562.
Roush RS, Snowdon CT, 2001. Food transfer and development of
feeding behavior and food-associated vocalizations in cotton-top
tamarins. Ethology 107:415–429.
Ruiz-Miranda CR, Kleiman DJ, Dietz JM, Moraes E, Gravitol AD, Baker
AJ, Beck BB, 1999. Food transfers in wild and reintroduced golden
lion tamarins (Leontopithecus rosalia). Am J Primatol 48:305–320.
Rylands AB (ed), 1993. The ecology of the lion tamarins, Leontopithecus: some intrageneric differences and comparisons with other callitrichids. In: Marmosets and tamarins: systematics, behavior and
ecology. Oxford: Oxford University Press; 296–313.
Rylands AB, 1996. Habitat and the evolution of social and reproductive behavior in Callitrichidae. Am J Primatol 38:5–18.
Snowdon CT, Boe CY, 2003. Social communication about unpalatable foods in tamarins (Saguinus oedipus). J Comp Psychol 117:
142–148.
Sokal RR, Rohlf FJ, 1995. Biometry: the principles and practice of
statistics in biological research, 3rd ed. New York: WH Freeman
and Company.
Tardif SD, 1997. The bioenergetics of parental behavior and the evolution of alloparental care in marmosets and tamarins. In: Cooperative breeding in mammals (Solomon NG, French JA, eds).
Cambridge: Cambridge University Press; 11–33.
Tardif SD, Santos CV, Baker AJ, Van Elsacker L, Feistner ATC, Kleiman
DG, Ruiz-Miranda CR, Moura AC de A, Passos FC, Price EC,
Rapaport LG, De Vleeschouwer K, 2002. Infant care in lion tamarins.
In: Lion tamarins: biology and conservation (Kleiman DG, Rylands
AB, eds). Washington: Smithsonian Institution Press; 213–232.
Vitale A, Queyras A, 1997. The response to novel foods in common
marmoset (Callithrix jacchus): the effects of different social contexts.
Ethology 103:395–403.
Worthman CM, 1993. Biocultural interactions in human development. In: Juvenile primates: life history, development, and behavior
(Pereira ME, Fairbanks LA, eds). New York: Oxford University
Press; 339–358.
Yoneda M, 1984. Ecological study of the saddle-backed tamarin
(Saguinus fuscicollis) in northern Bolivia. Primates 25:1–12.