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INTRODUCTION
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and foraging activities are tightly synchronized among group members [Menzel and
Juno, 1985; Soini, 1987]. Not only does feeding occur in close proximity to other
group members, but the family Callitrichidae is exceptional in the extent and frequency with which food items are directly passed from one individual to another.
Unlike the case in most primates [Feistner and McGrew, 1989], food transfer between callitrichid adult and subadult group members in captivity is a routine occurrence [Brown and Mack, 1978; Cebul and Epple, 1984; Feistner and Price, 1990].
The value of a food item may affect the tendency of a callitrichid adult to relinquish
a food item to other adults and subadults in the same way that food value may affect
willingness to share a food patch. Therefore, I considered the rate of food transfer
among the subadult and adult members of my study group to be an effective measure
of food competition intensity. I specifically predicted that the rate of food transfer
will increase and aggression will decrease as food abundance increases. In contrast,
as more energy is invested to obtain an item, the rate of food transfer will decrease
while that of aggression will increase.
Golden lion tamarins, with their exceptionally long fingers and claw-like nails,
are specialized extractive foragers. Invertebrate and small vertebrate prey usually are
found by manipulation of rotten wood, bromeliads, and palm crowns [Kleiman et al.,
1986; Garber, 1992]. I designed a foraging apparatus that would simulate the search
for hidden and embedded prey. Although captive golden lion tamarins typically have
little opportunity to practice this type of foraging task, they almost universally exhibit micromanipulation given an appropriate substrate [Beck et al., in press].
Thus, given the sometimes uneven success of foraging devices to enrich
the environments of captive primates, a more general theory of the effects of
enrichment on food competition is needed. Using measures obtained from basic
optimal foraging theory, this case study seeks to test predictions regarding how
variation in two measures of food value influences food competition behavior in
a captive New World primate. This study presents a conceptual approach to provide insight into factors that drive the behavioral changes resulting from environmental enrichment programs.
METHODS
Study Group and Site
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Experimental Design
Fig. 1. Schematic of puzzle box. The puzzle box was an extractive foraging device consisting of two
interlocking, opaque Plexiglas pieces. The device was designed to be suspended from eye bolts in the
top. See text for further details.
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through corn cob bedding filling the tube, and pull or rip away a paper barrier to find
the potential grape.
The tamarins were first trained to use the foraging device; 7 days of training
time were required before all individuals had retrieved at least two grapes from the
puzzle box during the task level 2 (i.e., more complicated) condition. Once all members had demonstrated competence, they were tested once per day for 3 consecutive
days per treatment. The order of treatments within the experiment and the doors
behind which grapes were placed were determined using a random number generator. Test days in which food remained in the puzzle box for more than 5 minutes
since any tamarin had investigated a hole were deleted, and the tamarins were retested for that treatment day at the end of the experiment. Three days required retesting due to food remaining or equipment failure. All tests were conducted before the
normal afternoon feedings. The tamarins were given a 2- or 3-day break between
treatments.
Observation Procedures
Two observers recorded data simultaneously. One observer focused on activities at the puzzle box, recording on videotape the identities and search times of all
individuals at the puzzle box. The other observer (the author) recorded on audiotape
the frequencies of all food transfer behaviors and aggression and the identities of
those involved in social interactions (see Table 1 for definitions). Each test lasted
until all grapes were consumed. The doors were clearly numbered and all tamarins
were individually identifiable.
Data Analysis
I scored the behaviors from videotapes and audiotapes twice, 1 week apart,
to increase accuracy and intra-observer reliability. I used a digitizer to determine
TABLE 1. Ethogram (Definitions follow closely those of Hoage [1982] and Feistner and
Price [1990])
Behavior
Definition
Begging
One individual approaches another who has a food item to within an arms length,
often while making a rasping vocalization. The begging individual closely examines
or reaches for the food item.
The food possessor turns, moves away, pushes at, or otherwise attempts to dissuade
the begging individual.
The food possessor does not visibly invite or resist attempts by a begging individual to
take its food and the item changes hands.
The category consists of four behaviors: passive share (above), active share (the food
possessor solicits anothers approach and actively hands the food over to that
individual), eaten out of the hand, and stolen (food is quickly passed without begging
or offering or in spite of a resist).
The aggressor bites, bites at, swats, and/or lunges at another individual. The
interaction is not considered to be aggression if it occurs during a resist. Each
interaction, rather than each behavioral component, is scored as an aggressive episode.
The subject is within an arms reach of the puzzle box and is facing and/or touching
the front of the box with one or both hands and is not engaged in another behavior. If
engaged in another behavior, such as eating, the subject must be actively
manipulating the box or cocking the head while facing the box to be considered
searching.
Resistance
Passive Share
Transfer
Aggression
Search
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search durations from video tape. Recorded search durations rarely differed, and
never by more than 2 sec. When disagreement occurred, the videotape was reexamined and the time chosen was the time that agreed with one of the two
previous determinations.
To determine whether food quantity and foraging task complexity influenced
rates of food transfer behaviors and aggression, the average rates of behavior per
individual per test were calculated for each of these two independent variables. I
defined test durations as having started when the first search began and ended when
the last grape was eaten. The sum of the test durations was 85.083 min. Aggression
and food transfer behaviors were then further examined as functions of search duration. Each behavior was scored as having occurred or not occurred over a given
grape [that is, one-zero sampling: Altmann, 1974], including grapes acquired both
socially and from the foraging device. I tested whether search time prior to obtaining
a given grape influenced the occurrence of aggression after a monkey had obtained
the grape, but before the next grape was obtained. For example, a tamarin who threatened another individual after having eaten its second grape, but before having acquired its third, was considered to have exhibited aggression over the second grape.
The number of searches comprising this analysis of aggression was 205. I also examined willingness to relinquish a grape as a function of search duration. Passive
sharing and resistance were the behaviors analyzed, and both required, by definition,
that a potential recipient first beg for or attempt to steal the item in question. Therefore, for these analyses, I standardized the data by only considering those search
durations for grapes over which begging or attempted stealing occurred. The number
of searches used for these analyses was 84.
Due to the small sample size, I used non-parametric analyses of variance
(ANOVAs) for many analyses. Search duration data were analyzed with parametric
tests. Duration data first were tested for normality and homoscedasticity [Zar, 1984].
When untransformed duration data did not meet the assumptions of normal distributions and homogeneity of variances, a square root transformation corrected the problem. One-tailed values are used when the direction of the hypothesized change was
predicted a priori, and these cases are noted. This approach is justified because I was
only interested in whether behavioral changes occurred in the predicted directions
[Zar, 1984]. Nonetheless, it must be noted that a more conservative approach would
be to present two-tailed values.
RESULTS
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= 0.50, ns; Passive Share: 2 = 4.63, ns; Aggression: 2 = 3.50, ns; Fig. 2). In contrast, foraging task complexity affected both food sharing and aggression (Fig. 3). As
predicted, the average rate of passive sharing per minute was higher during task
level 1 compared to task level 2 (Friedman two-way ANOVA, 2 = 4.00, N = 4, P <
0.05), and rates of aggression were lower during task level 1 versus task level 2 (2
= 4.00, N = 4, P < 0.05). Begging (2 = 0.00, ns) and resists (2 = 1.00, ns) did not
vary with this measure of energy invested to obtain a food item. Task level 1 was the
Fig. 2. Mean rate per test of food transfer behaviors and aggression as functions of the number of
grapes present in the puzzle box at the beginning of a test. None of the behaviors examined varied with
this measure of food abundance. The error bars in all figures indicate standard errors.
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Fig. 3. Mean rate per test of food transfer behaviors and aggression as functions of foraging task
complexity. *P < 0.05 in all figures.
simpler and less time-consuming task. The monkeys took an average of 10.3 (S.E. =
+ 0.5) sec to acquire a grape from the puzzle box during task level 1 compared to an
average of 51.8 (S.E. = + 15.5) sec during task level 2.
Search time did not significantly influence an individuals tendency to relinquish a grape. Average duration of search for grapes that were not passively shared
was not significantly longer than the average search duration for grapes that were
passively shared (paired sample t-test, T = 0.367, df = 3, ns, one-tailed; Fig. 4).
Moreover, the average search duration did not vary according to whether an indi-
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vidual did or did not resist transfer of the grape (paired sample t-test, T = 0.708, df =
3, ns; one-tailed; Fig. 4).
Aggression was exhibited to conspecifics and to the sakis (Pithecia pithecia)
and pygmy marmosets who shared the exhibit with the golden lion tamarins. The
average search duration for a grape was longer when the possessor exhibited
aggression over the grape than when the possessor did not exhibit aggression
(paired sample t-test on square root transformed data, T = 2.677, df = 3, P <
0.05; one-tailed; Fig. 4). Notably, the average duration of search for grapes over
which aggression occurred was longer than the average when aggression did not
occur for all four individuals.
Aggression was not evenly distributed among group members. The dominant
male was the aggressor in 35 agonistic episodes, but the other group members rarely
exhibited aggression. The dominant female exhibited aggression only four times, all
to the sakis as one or the other saki approached the puzzle box. The subordinate
male was an aggressor five times, and the subordinate female two times, during the
course of the experiment.
Degree of satiation appeared not to influence willingness to relinquish a food
item. Neither the probability of passive sharing (Friedman two-way ANOVA, N = 3, 2 =
3.50, ns) nor the probability of resistance (Friedman two-way ANOVA, N = 3, 2 = 2.70,
ns) in response to begging varied with number of grapes previously acquired.
All study subjects appeared highly motivated to acquire grapes during every
test day. All grapes were found and consumed during all except two tests (test days:
12 grapes/task level 2 and 8 grapes/task level 1). In both cases, the test was approximately mid-way through the experiment and one grape was left in the foraging device. In other words, there was no apparent habituation to the test situation over the
Fig. 4. The average search duration for grapes (1) that were not passively shared versus were passively shared in response to begging (left panel), (2) over which the possessor did not or did resist
attempts by another individual to take the grape (middle panel), and (3) when the possessor did not or
did exhibit aggression after having obtained the grape but before obtaining another (right panel). NO
indicates that the behavior in question did not occur and YES indicates that it did occur, after a grape
had been acquired.
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40-day span of the experiment. The total number of grapes eaten during the experiment did not vary greatly among the study subjects. The average number of grapes
and partial grapes acquired per monkey over the course of the entire experiment was
51 (range: 4163). The monkeys nonetheless exhibited highly individualistic responses
to the test situation. For example, the dominant male received 40% of his grapes
from others and the dominant female received 77.5% of her grapes from others. In
contrast, only 9.1% of the subordinate males and 3.1% of the subordinate females
grapes were socially acquired.
The average search duration did not vary significantly according to whether
the grape was acquired from the foraging device or by social means (paired sample
t-test, T = 1.97, df = 3, ns). However, the average search duration for grapes obtained from the foraging device was more than 1.5 times that for socially acquired
grapes (18.8 + 7.0 vs. 31.8 + 7.3 sec, respectively).
DISCUSSION
A food-sharing event is a social interaction and, as such, the outcome is determined by the individuals involved. The potential recipient must decide if, when, and
from whom food will be requested while the potential donor must decide whether
to offer an item for transfer, resist transfer, or simply release a contested item
[Shopland, 1987]. I examined the influence of several measures of resource distribution and availability on food-sharing decisions. The tendency for a potential
recipient to request food (that is, beg) was not affected by any of the resource
variables examined. Of the potential donors behaviors, only passive sharing and
aggression were influenced by the distribution and availability of resources in
the test situation.
The energy invested to obtain a food item was a more important resource attribute than abundance in terms of influence on food competition. None of the behaviors measured varied as a function of food quantity or degree of satiation. The
prediction that the energy invested to obtain an item or search and handling time will
influence food sharing and agonistic behaviors was, in general, borne out by test
results of foraging task complexity and search duration. The rates of passive sharing
were lower and aggression higher when the foraging task was more complex and
time-consuming. Surprisingly, search time did not influence willingness to relinquish
a food item. On the other hand, the tendency to exhibit aggression was a positive
function of search time.
One possible explanation for why variation in food abundance was not associated with variation in food competition could be that the test measures of food abundance were inadequate. Although I varied food quantity by a factor of three, perhaps
for the individual tamarin, the average acquisition of between one and three grapes
was not a sufficiently large difference to influence the degree of food competition.
Similarly, the degree of satiation was measured by a tamarin having obtained between zero and three grapes. A golden lion tamarin adult is probably not satiated
after eating three grapes. Relevant to this point, the study subjects usually ate at least
some of their regular afternoon meal shortly after tests. On the other hand, if food
abundance were a strong predictor of food competition, some measurable change in
food transfer behavior and aggression would be expected, given the resource variation provided by the test situation.
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dict design features in captive environments that will optimize natural behaviors
and minimize conflict.
CONCLUSIONS
This research could not have been conducted without the enthusiastic cooperation and logistical support provided by the staff of the National Zoological Park.
Specifically, I would like to thank B. B. Beck, D. Davis, D. G. Kleiman, L. Newman,
A. Rosenberger, S. Skitek, and B. Xanten. Friends of the National Zoo intern P.
Moss, postdoctoral research fellow M. Hersek, and volunteer K. Dailey, all kindly
assisted with data collection. A. Rosenberger generously offered the use of his data
collection and analysis equipment. I am indebted to J. L. Beacham, B. B. Beck, J.
Froehlich, A. Kodric-Brown, J. B. Lancaster, and C. Ruiz-Miranda for insightful
discussions. The constructive comments of D. Shepherdson and three anonymous
reviewers substantially improved the manuscript. Financial support was provided by
NSF Dissertation Improvement grant #BNS-9204342 and Grants-in-Aid of Research
from Sigma Xi, The Scientific Research Society. The extractive foraging device was
designed with advice from APCO Plastics of Greenville, SC, and built to exact specifications by them.
REFERENCES
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Bayne, K.; Mainzer, H.; Dexter, S.; Campbell, G.;
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board. AMERICAN JOURNAL OF PRIMATOLOGY 23:2335, 1991.
Beck, B.B.; Kleiman, D.G.; Castro, I.; RettbergBeck, B.; Carvalho, C. Preparation of captiveborn golden lion tamarins for release into the
wild. In: A CASE STUDY IN CONSERVATION
BIOLOGY: THE GOLDEN LION TAMARIN.
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