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Zoo Biology 17:231244 (1998)

Optimal Foraging Theory Predicts Effects


of Environmental Enrichment in a Group
of Adult Golden Lion Tamarins
Lisa G. Rapaport*
Department of Anthropology, University of New Mexico, Albuquerque, New Mexico

The success of environmental enrichment programs in effecting specific changes


in the behavior of captive animals has not always been uniform. Separate studies
demonstrated both an increase in food competition and a decrease in food competition among captive group-living primates upon introduction of foraging devices. The objectives of this study were to measure the effects of variation in
resource distribution and availability on food competition in a group of captive
adult golden lion tamarins (Leontopithecus rosalia). The resource variables chosen were suggested from optimal foraging theory. The energy invested to obtain
an item influenced food transfer and aggressive behaviors while food abundance
did not. All individuals obtained an equivalent number of items over the course
of the experiment from the foraging device, even though some tamarins obtained
most of their food rewards directly from the device while others received their
food rewards primarily through food transfer from other group members. Because the monkeys appeared highly motivated to obtain food from the test apparatus and did not habituate to it, the foraging device used in this experiment
could be used as regular environmental enrichment for golden lion tamarins.
One way to circumvent potentially unacceptable rates of aggression, with this or
any feeding protocol that increases foraging task complexity and search time,
may be to provide more than one foraging device per group. Zoo Biol 17:231
244, 1998. 1998 Wiley-Liss, Inc.
Key words: food abundance; food sharing; environmental enrichment; puzzle box; optimal foraging

INTRODUCTION

Environmental enrichment programs seek to improve the quality of life for


captive animals, increase breeding success, and enhance the aesthetic and educational value of exhibits. Studies designed to assess the efficacy of such programs use
behavioral and/or hormonal measures to gauge changes in psychological well-being.
Received for publication August 25, 1997; revision received April 1998.
*Correspondence to: Lisa Rapaport, Dept. of Anthropology, University of New Mexico, Albuquerque,
NM 87131. E-mail: LGRap@aol.com

1998 Wiley-Liss, Inc.

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The goal of environmental enrichment may be to elicit specific changes in recipient


behavior, such as an increase in general activity level [Chamove et al., 1982;
Reinhardt, 1993], a decrease in stereotypies or other aberrant behaviors [Akers and
Schildkraut, 1985; Bloomsmith et al., 1988; Bayne et al., 1991; Shepherdson et al.,
1993], a more even distribution of food intake among cagemates [Bloomsmith et al.,
1988], a decrease in aggression [Bloomsmith et al., 1988], and changes in behaviors
or time budgets to more closely approximate those of wild counterparts [McGrew et
al., 1986; Maki et al., 1989; Visalberghi and Vitale, 1990; Brent and Eichberg, 1991;
Shepherdson et al., 1993]. Many enrichment programs for primates rely heavily on
feeding techniques that increase the time required to search for, prepare, and eat the
daily ration. Puzzle feeders and other foraging devices have become popular and
successful agents of environmental enrichment for primates [e.g., Bloomstrand et
al., 1986; Molzen and French, 1989; Bayne et al., 1991; Reinhardt, 1993].
However, implementation of foraging enrichment programs does not always
produce the desired effect. For example, in groups of captive chimpanzees, Maki et
al. [1989] reported an increase in aggression upon introduction of a puzzle feeder. In
contrast, Bloomsmith et al. [1988] found that puzzle feeders did not increase rates of
aggression. Significantly, Maki et al. [1989] used a single puzzle feeder, whereas
Bloomsmith et al. [1988] used multiple puzzle feeders per chimpanzee group. In
general, food competition and rates of aggression tend to decrease as food becomes
more dispersed, and thus less defensible [Chamove et al., 1982; Boccia et al., 1984].
Do other patterns of food resource availability, predictability, and distribution
predict the intensity of intraspecific food competition? Individuals are expected to be
sensitive to variation in food value and foraging costs, adjusting both social behavior
and foraging strategies in response to environmental change [Brown, 1964; Crook
and Gartlan, 1966; Fretwell, 1972; Jarman, 1974; Pulliam, 1976; Clutton-Brock and
Harvey, 1977]. In general, according to basic optimal foraging theory, three key determinants of a food items value are the caloric value (i.e., the expected net energy
gain from an item), the energy invested to obtain a food item (i.e., search and
handling times), and food abundance (i.e., the encounter rate) [Pulliam, 1974;
Charnov, 1976; Stephens and Krebs, 1986]. Both within- and between-group competition for resources have been found to vary with food value. For example,
food abundance influences degree of competition over food patches in wild mixed
species groups of saddle-back (Saguinus fuscicollis avilapiresi) and moustached
tamarins (Saguinus mystax pileatus). Individuals of both species usually feed together within large food patches. In small, clumped patches, however, the saddleback tamarins are often excluded by the larger bodied and socially dominant
moustached tamarins [Peres, 1996].
My purpose was to determine whether food value influences within-group food
competition among subadult and adult golden lion tamarins (Leontopithecus rosalia).
I experimentally varied both food abundance and the energy invested to obtain a
food item while controlling for caloric value. I hypothesized that variation in specific resource attributes that affect the cost of a given food item will influence food
competition and agonistic behaviors. The number of food items present at the beginning of a test and the number of items an individual had eaten were used to represent
food abundance, whereas difficulty of foraging task and search time were used to
represent energy invested to obtain a food item.
Marmosets and tamarins (the Callitrichidae) live in highly cohesive social units

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233

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

The study subjects were members of an established group of golden lion


tamarins living in a large (approximately 117 m2 with a 4.3 m high ceiling),
naturalistic indoor enclosure at the National Zoological Park. The group consisted of two males and two females: a male-female pair and two adult offspring
of the dominant male and the dominant females sister (who no longer resided in
the group). The two offspring were considered to be subordinate in the sense that
natal offspring in tamarin groups subordinate their reproduction to parents and/
or non-natal adults [Garber et al., 1984; Terborgh and Goldizen, 1985; Dietz and
Baker, 1993]; dominance hierarchies were not assessed. Several neotropical mammal species lived in the exhibit with the tamarins, including a pair of pygmy
marmosets (Cebuella pygmaea) with whom the tamarins interacted frequently
[W. Xanten, pers. comm.]. The tamarins regular diet consisted of a mixture of
fruits and a canned marmoset diet provided to them on feeding platforms two
times per day. Mealworms were given once per day.

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Experimental Design

Variation in resource distribution and availability was effected by means of an


opaque Plexiglas foraging device from which the monkeys could extract food (Fig.
1). The foraging device had 15 holes, each hole positioned behind a sliding door. A
food reward (a maximum of one grape per hole) could be found at the end of a short
tube attached to each hole.
Two resource attributes were experimentally manipulated: food quantity and
difficulty of foraging task. The caloric gain from individual food items was held
approximately constant by standardizing the size of the food reward; that is, each
grape was approximately 2 cm in diameter. There were three quantity levels, categorized according to the total number of grapes present in the foraging device at the
beginning of each test (4, 8, or 12 grapes). The foraging task variable had two levels
that differed according to how difficult it was for the tamarins to determine whether
a grape was present behind any given door. Task level 1 required that a door be
opened and that the tamarin then reach into the tube to retrieve the grape, if a grape
was present. Task level 2 required that the door be opened, the tamarin rummage

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

In callitrichids, food transfer behavior by the food possessor may range


from active sharing, passive sharing, food eaten out of the hand, to food stolen
[see Table 1] [Hoage, 1982; Feistner and Price, 1990]. For this study, passive
sharing and resistance were the behaviors chosen to represent a willingness or
lack of willingness to surrender a food item to another individual. The other
measures of food transfer were exhibited, but too infrequently for independent
comparison. Food was transferred among all tamarins and from the tamarins to
the two pygmy marmosets.
Food quantity did not affect either the rates of food transfer behavior or aggressive episodes (Friedman two-way ANOVA: N = 4; Beg: 2 = 0.00, ns; Resist: 2

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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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Shopland [1987], in a study of feeding interference in young wild baboons,


also found that processing time was the resource variable most likely to influence willingness to forgo feeding. The baboons in Shoplands [1987] study were
less disposed to terminate a feeding bout in response to the approach or aggression from another individual when feeding on difficult-to-process foods. However, in contrast to the results of the present study, aggression did not increase as
food yield rate declined.
The agonistic interactions observed among the golden lion tamarins during the
experiment were noninjurious and infrequent, even when the foraging task was difficult and aggression was at its highest rate (an average of nine events per hour). That
rates of aggression would increase with the introduction of a new and interesting
food dispenser was not entirely unexpected. The single foraging device was a defensible resource. It might be prudent to furnish more than one foraging device to a
group if the device were to be used for regular environmental enrichment, particularly if increased foraging time is a desirable goal, to circumvent potentially unacceptable rates of aggression [see also Bloomstrand et al., 1986].
The phenomenon of variability of response to the test situation as a function of
social status could only be hinted at in this case study. Consistent with other reports
of extractive foraging devices for captive golden lion tamarins [Kleiman et al., 1986;
Molzen and French, 1989], the dominant individuals in this study acquired less food
from the foraging device than did subordinate group members. Further studies on
multiple groups of tamarins are needed to elucidate the interplay between social status and resource qualities in regard to food transfer and aggression.
The tamarins quickly learned even the more difficult foraging task and then
enthusiastically searched for food rewards in the foraging device on all test days
throughout the 40-day duration of the experiment. The puzzle box had two characteristics that may have contributed to the lack of habituation evinced by the
tamarins to the device: (1) it allowed the tamarins to acquire food by means of
directed, natural foraging behaviors and (2) the tamarins could not predict which
tubes would contain grapes. Shepherdson et al. [1993] have suggested that two
theoretical models of behavioral motivation may explain why environmental enrichment protocols that both allow natural foraging behavior and increase uncertainty of food location produce the most beneficial and long-lasting effects on
captive animals. The first model [Hughes and Duncan, 1988] proposes that animals need to engage in functional, goal-directed behavior. According to this view,
foraging enrichment protocols typically are successful because they provide the
opportunity to link an appetitive behavior (foraging) with its functional consequence (eating). The second model suggests that information gathering is a
very basic behavioral motivator for animals [Inglis and Fergusson, 1986]. Thus,
a well-fed individual is highly motivated to seek out information in a changing
environment.
This study also proposes that a theoretical framework may allow us to anticipate which features of environmental enrichment protocols have the potential
to most strongly influence behavior. The theory, that of optimal foraging, provided the measures of resource quality and successfully predicted that the energy
invested to obtain a food item would influence food competition, even in a highly
cooperative social forager. This type of study demonstrates the potential to pre-

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dict design features in captive environments that will optimize natural behaviors
and minimize conflict.
CONCLUSIONS

1. Two measures of resource distribution and availability, suggested by optimal


foraging theory, were used to predict food competition in a group of captive adult
golden lion tamarins.
2. Consistent with predictions, food competition increased as the energy invested to obtain an item increased, but contrary to predictions, food competition did
not vary according to food abundance.
3. Optimal foraging is a promising theoretical framework for predicting which
features of foraging enrichment protocols have the greatest potential to influence
behavior.
4. The tamarins appeared highly motivated to obtain grapes from the extractive foraging device used throughout the 40-day duration of the experiment.
Given the lack of habituation, the apparatus designed for this study could be
used for regular captive golden lion tamarin environmental enrichment. However, because devices that increase foraging time also tend to increase rates of
aggression, a prudent approach would be to furnish more than one extractive
foraging device per group.
ACKNOWLEDGMENTS

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.
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