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Environmental Enrichment for Dendrobatid Frogs

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The Central Park Zoo, one of the Wildlife Conservation Society's Living Institutions in New York, recently renovated an exhibit for dart-poison frogs. Staff developed a new hollow coconut insect feeder in conjunction with this project. When the exhibit change, coconut feeder, and other enrichments were tested for effectiveness, the coconut feeder enrichment produced the greatest increase in frog activity in traditional and new exhibits. This may be due to the coconut feeder's relatively complicated nature, which randomizes the release of insects into the exhibit. The goal of this project was to help develop a best-practices approach to dendrobatid husbandry for zoological facilities to use in the future.
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Environmental Enrichment
for Dendrobatid Frogs
Kristiina Hurme, Kittzie Gonzalez, Mark Halvorsen,
Bruce Foster, and Don Moore
Wildlife Conservation Society
Brooklyn, New York
B. Diane Chepko-Sade
Department of Biology
State University of New York at Oswego
The Central Park Zoo, one of the Wildlife Conservation Society’s Living Institutions
in New York, recently renovated an exhibit for dart-poison frogs. Staff developed a
new hollow coconut insect feeder in conjunction with this project. When the exhibit
change, coconut feeder, and other enrichments were tested for effectiveness, the co-
conut feeder enrichment produced the greatest increase in frog activity in traditional
and new exhibits. This may be due to the coconut feeder’s relatively complicated na
-
ture, which randomizes the release of insects into the exhibit. The goal of this project
was to help develop a best-practices approach to dendrobatid husbandry for zoologi
-
cal facilities to use in the future.
Environmental enrichment is a nonhuman animal husbandry technique that at
-
tempts to enhance animal welfare by providing the environmental stimuli neces
-
sary for optimal psychological and physiological well-being of the animals
(Shepherdson, 1998). There are five commonly accepted ways to an enrich an
animal’s environment: managing a dynamic habitat, encouraging social interac
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tions between individuals, encouraging foraging behavior, introducing novel ob
-
jects, and training the animal.
In addition to enhanced welfare of captive animals, the value of enrichment for
zoo animals can include reduced veterinary care, facilitated animal husbandry, in
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JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 6(4), 285–299
Copyright © 2003, Lawrence Erlbaum Associates, Inc.
Requests for reprints should be sent to Don Moore, Prospect Park Zoo, Wildlife Conservation Soci
-
ety, 450 Flatbush Avenue, Brooklyn, NY 11225. Email: dmoore@wcs.org
creased reproductive behavior, and improved public education through more dy
-
namic exhibitry (Hayes, Jennings, & Mellen, 1998). Enrichment provides an
excellent opportunity to inform the public about the natural behaviors of animals
and to encourage involvement in conservation activities. Enrichment items can
also increase the animal’s activity levels, thus making the zoo-going experience
more exciting and valuable for zoo visitors.
Despite the increased popularity of environmental enrichment methods, enrich
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ment programs for amphibians are rare (Hayes et al., 1998). Our study tested environ
-
mental enrichment methods for dendrobatid frogs. Dart-poison frogs (Anura:
Dendrobatidae) are a neotropical group of toxic, diurnal terrestrial frogs. Our four
study species were Dyeing dart-poison frogs (Dendrobates tinctorius), Blue
dart-poison frogs (D. azureus), Green and Black dart-poison frogs (D. auratus) and
Yellow-banded dart-poison frogs (D. leucomelas). D. tinctorius occur in the wild in
French Guiana, Guyana, and Surinam; D. azureus in Surinam; D. auratus from south
-
ern Nicaragua to Colombia; and D. leucomelas in Venezuela (Anonymous, 1998).
LIFESTYLES
Dendrobatid Habitat
In the wild, dart-poison frogs are active throughout the day, foraging on the forest
floor or climbing trees. D. tinctorius frogs in the wild were found in pools formed in
tree holes and cracks. They were seen sitting 10 m up on tree trunks, with as many as
five frogs inhabiting a single tree. D. tinctorius individuals live in pairs, and
Heselhaus (1992) observed that no more than two males lived together on the same
tree. In the wild, D. auratus remains well hidden during the dry periods and was
found hidden only in moist rock crevices (Heselhaus, 1992).
Activity Patterns
D. auratus is most active in the mornings and after rain showers (Leenders,
2001). Jaeger and Hailman (1981) found that wild D. auratus in Panama ac
-
tively foraged only in the early morning and late evening, times that had similar
light levels. Heselhaus (1992) found wild D. tinctorius to be active throughout
the day but observed that they left their tree only for short periods to look for
food and rarely traveled more than 5 m from their home tree.
Foraging Behavior
Dendrobatids are opportunistic foragers who feed on small invertebrates whom
they encounter. Dendrobatids rely on sight to locate their prey and often adopt a
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sit-and-wait hunting style. In the wild, dart-poison frogs encounter a wide vari
-
ety of prey items—including termites and ants—that give them their toxicity.
Field studies have shown that ants make up 50% to 73% of the diet of wild spe
-
cies of Dendrobates, whereas ants make up only 12% to 16% of the diet of the
nontoxic Colostethus frogs, supporting the theory that the dart-poison frogs ob
-
tain their toxins from alkaloids in the ants (Leenders, 2001). Captive
dendrobatids are not toxic, however, presumably due to a routine diet of non
-
toxic small crickets and springtails.
Predators
Despite the toxins in their skin, wild dart-poison frogs do not have the luxury of
being free from predators and still have to endure a daily battle for survival.
Many predators are not deterred by the toxins of the dart-poison frogs, espe
-
cially due to the variation in levels of toxicity among the species (Heselhaus,
1992).
Parental Care
As a group, dart-poison frogs exhibit a diversity of parental care strategies.
Members of the D. tinctorius species group exhibit male parental care (Summers
& Earn, 1999). The female deposits small (2 to 8 eggs) clutches in the leaf litter
that are attended by the male; he later carries the mature (10 to 14 days) tadpoles
to small pools of water in tree holes. The male may place additional tadpoles in
the same pool who often are cannibalized by larger tadpoles (Summers & Earn,
1999). It also has been observed that males most often do not place more than
one tadpole in a pool, but may do so when they are limited by time and avail
-
ability of pools (Summers & Earn, 1999).
In species with male parental care in which only the male decides where to de
-
posit the eggs, cannibalism among tadpoles is costly for the mother because she
has no control over the placement of her tadpoles and the resulting tadpole interac
-
tions. Therefore, the female’s only opportunity to reduce tadpole conflict in which
other females’ tadpoles may be out competing hers is to prevent her mate from
mating with other females. In fact, mate guarding has been observed in the field for
D. auratus and D. leucomelas (Summers & Earn, 1999).
Dart-poison frogs from the tinctorius group who have male parental care de
-
posit tadpoles in pools and puddles and do not feed the tadpoles. Dart-poison frogs
with female parental care, such as D. pumilio, deposit tadpoles in bromeliads and
feed tadpoles with unfertilized eggs (Summers & Earn, 1999). Consequently, D.
pumilio males are territorial over bromeliads, which are limited breeding resources
(Donnelly, 1989).
DENDROBATID ENRICHMENT 287
Aggressive Behavior
In the wild, dendrobatids may defend all-purpose territories that include feeding
sites, shelter, and oviposition sites (Wells, 1977). D. auratus males are territorial,
and males will wrestle with each other to attain dominance. During the day, males
call from established sites such as trunks, logs, or rocks to attract females and keep
males out of their territory (Leenders, 2001). Aggressive behavior is not limited to
the males; female D. azureus and D. auratus individuals have been observed wres
-
tling togain access to calling males (Wells, 1977). In addition, dendrobatids may ex
-
hibit a sex-role reversal in which females initiate courtship (Wells, 1977).
Habitat Change at the Zoo
Central Park Zoo, managed by the Wildlife Conservation Society in New York,
has a large collection of dendrobatids, including genetically important reproduc-
tive groups of endangered species and “exhibit-only” groups of more common
species. When exhibit changes were made, a large habitat was created to allow
exhibition of a relatively dense population of exhibit-only dendrobatids to en-
hance the visitor experience and to observe the behavior of frogs in the larger
group versus the frogs in “traditional” aquarium exhibit terraria.
In redesigning the exhibit, we considered the needs to address habitat changes
for the frogs, activity patterns of the frogs in captivity versus in nature, foraging
challenges in captivity, and behavioral interactions of species and individuals. The
goal of this project was to help develop a best-practices approach to dendrobatid
husbandry for zoological facilities to use in the future.
METHOD
This research was conducted from July to September 2001 at the Central Park
Zoo, Wildlife Conservation Society, New York. Behavioral observations were
recorded on two exhibits of captive dart-poison frogs (Dendrobates sp.). All
frogs were captive born. The new large, “nontraditional” exhibit consisted of 23
individuals of four species (6 D. tinctorius, 8 D. azureus, 4 D. leucomelas, and 5
D. auratus), and the small, traditional exhibit contained 4 D. tinctorius and 4 D.
azureus individuals. The large exhibit is a 1.07 m × 1.07 m × 1.52 m high ex
-
hibit with glass windows for viewing by the public on two adjacent sides. It is
planted with various ground plants, mosses, and bromeliads, and there are tree
branches and vines for climbing. There are overhead misting spouts on a ran
-
domly timed timer that spray a fine water mist over the exhibit for random
amounts of time during the day. The small exhibit is a 20-gallon aquarium (0.66
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HURME ET AL.
m × 0.51 m × 0.64 m) tank with one glass window for public viewing. It also
contains plants, mosses, a bromeliad, and one small branch for climbing. There
also is a misting spout that sprays at random times throughout the day.
Before the experiment, the daily husbandry routine for the dendrobatids in
-
cluded a feeding every other day of pinhead or 10-day crickets (Gryllus
domesticus), fruit flies (Drosophila melanogaster), flour beetle larvae (Tribolium
sp.), or springtails (Collembola sp.), depending on availability.
Enrichment Experiments
The frogs were presented daily with one of three experimental states—control,
coconut, and other. The experimental enrichment schedule alternated between
the three experimental states in a random order. No state was presented on any 2
consecutive days; each day was different from the previous day. On days when
the observers were not present, the frogs were fed in an open petri dish placed in
the front of the exhibit. Data were collected for 11 weeks, with 4 to 5 days of
observation per week and approximately 5 hr of observation per day. Each en-
richment state was presented at least once per week.
For the control state, the frogs were not fed. To continue the every other day
feeding schedule, two control states were not performed on consecutive days.
Within each exhibit, the only experimental variable was the feeding method.
The coconut enrichment state consisted of a dried hollow coconut shell, split in
half, with three small holes drilled in the top and a piece of artificial vine holding
the two halves together so that the insects could only escape out of the drilled
holes. The coconut was filled with pinhead and 10-day old crickets, whereas
sponge pieces plugged the holes; then the coconut was moved to the exhibit. The
pieces of sponge were then pulled out of the holes, which allowed the small insects
to escape slowly through the holes. The coconut enrichment was placed in the
front of the exhibit, in plain view of the visitors.
The other enrichment state included either the placement of flower stems cov
-
ered in aphids (Aphis sp.) in the front of the exhibit or a broadcast feed of various
insect prey items (fruit flies, flour beetle larvae, springtails), which were scattered
in the front of the exhibit.
Behavioral Observations
All D. azureus and D. tinctorius individuals were identified and named based on
dorsal color patterns. An identification chart was produced so that each observer
could accurately identify the frogs for scan sampling. Behavioral data on indi
-
vidual frogs were collected using point scan samples (Altmann, 1974). Observa
-
DENDROBATID ENRICHMENT 289
tions were timed with a digital watch and recorded on data sheets. Each
individual frog was observed for approximately 27 to 48 hr per enrichment state
(Table 1).
Throughout the 11 weeks of the study, point scan samples were recorded on the
D. tinctorius and D. azureus individuals, categorizing behaviors according to our
ethogram (Table 2). For the small exhibit, we used a 1-min scan for both D.
tinctorius and D. azureus. For the large exhibit, a 2-min scan was used, alternating
each minute between D. tinctorius and D. azureus so that the data could be col
-
lected simultaneously on all 14 study animals in the large exhibit.
To compare the effects of the exhibits and a change in environment and social
surroundings, we switched D. tinctorius and D. azureus individuals between the
small and large exhibits after 7 weeks of observation. The frogs then were ob
-
served for 4 more weeks to determine if there were any activity level changes in the
experimentally switched individuals. Four D. tinctorius individuals and four D.
azureus individuals were moved from the large exhibit to the small exhibit, and
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HURME ET AL.
TABLE 1
Total Observation Time per Individual
Total Time Observed
a
Species Individual Control Coconut Other
D. azureus A 27:05:00 35:43:00 41:51:00
B 29:44:00 37:04:00 41:19:00
C 29:44:00 37:04:00 41:19:00
D 29:44:00 37:04:00 41:19:00
E 27:05:00 35:43:00 41:51:00
F 27:05:00 35:43:00 41:51:00
G 29:44:00 37:04:00 41:19:00
H 19:50:00 23:38:00 27:40:00
I 29:14:00 27:26:00 36:35:00
J 29:14:00 27:26:00 36:35:00
K 29:14:00 27:26:00 36:35:00
L 29:14:00 27:26:00 36:35:00
D. tinctorius A 32:01:00 46:50:00 37:29:00
B 34:38:00 48:11:00 37:02:00
C 32:01:00 46:50:00 37:29:00
D 34:38:00 48:11:00 37:02:00
E 32:01:00 46:50:00 37:29:00
F 32:01:00 46:50:00 37:29:00
G 29:12:00 32:11:00 36:40:00
H 29:12:00 32:11:00 36:40:00
I 29:12:00 32:11:00 36:40:00
J 29:12:00 32:11:00 36:40:00
a
Time is in hours:minutes:seconds.
four D. tinctorius individuals and four D. azureus individuals were moved from
the small exhibit to the large exhibit, thus keeping the total number of frogs and
frogs per species in each exhibit constant.
Our null hypothesis was that there would be no change in activity between exhib
-
its or between experimental states. We predicted that in both the large and small ex-
hibits, there would be a significantly higher level of activity for the enrichment states
compared with the control state. We could not predict if the coconut or other enrich-
ment states would have a higher activity level, so we tested them against each other.
We predicted that there would be a difference in activity levels for the control state in
both exhibits, but we did not predict which would have higher activity levels.
For the experimental exhibit switch, we expected activity levels to increase
from the original exhibit to the new experimental exhibit for all experimental/en-
richment states (including the control state). We also expected activity levels to in-
crease for individuals moved from the small exhibit to the large exhibit. We did not
predict whether activity levels would increase or decrease for individuals moved
from the large exhibit to the small exhibit. The Wilcoxon matched-pairs signed
rank test was used to test these predictions (Siegel, 1956).
RESULTS
Activity Levels
To determine the change in activity levels across enrichments, the behaviors
were grouped into active, inactive, and out of sight (Table 3). Data collected be
-
fore an enrichment item was presented on an enrichment day were not included
in the data analysis. For both D. azureus and D. tinctorius in both exhibits, the
coconut enrichment state increased activity levels from the control state but
failed to produce a statistically significant change (Figure 1; Table 4). The other
enrichment state had a varied effect on the frogs, either increasing activity from
the control state or remaining near control state activity levels.
DENDROBATID ENRICHMENT 291
TABLE 2
Ethogram
Behavior Included Behaviors
Moving Moving, vertical climbing, jumping
Hunting Hunting, walking towards prey
Agonistic Wrestling, chasing, being chased
Resting Sitting still
Breeding In plant, laying eggs, rubbing body on leaf, courtship behavior
Out of sight Not visible to observer
TABLE 3
Revised Ethogram—Active Versus Inactive
State Included Behaviors
Active Moving, hunting, agonistic behavior, breeding
Inactive Resting
Out of sight Out of sight
FIGURE 1 Proportion of time spent active for each enrichment state with 95% confidence in
-
tervals. Values for each species are the mean activity levels of all the individuals, including indi
-
viduals included in the experimental exhibit switch.
TABLE 4
Proportion of Time Spent Active for Each Enrichment State
Large Exhibit Small Exhibit
D. azureus D. tinctorius D. azureus D. tinctorius
Enrichment
State
Proportion
Active N
Proportion
Active N
Proportion
Active N
Proportion
Active N
Control 0.38 12 0.45 10 0.48 8 0.48 8
Coconut 0.50 12 0.63 10 0.60 7 0.64 8
Other 0.40 12 0.51 10 0.62 8 0.50 8
Note. Values for each species are the mean activity levels of all the individuals, including
individuals included in the experimental exhibit switch.
292
Wilcoxon Matched-Pairs Signed Rank Test
Although the effects of the enrichments on activity levels were not statistically sig
-
nificant when tested across species and exhibits, some enrichment states produced
significant results when tested within a species (Table 5). For D. azureus, proportion
of time spent active was significantly greater for the coconut enrichment versus the
control state in the large exhibit (N = 11, T =9,p < .025), the other enrichment versus
the control state in the small exhibit (N =7,T = 1.5, p < .025), and the other enrich
-
ment versus the control state in the large exhibit (N = 12, T = 9.5, p < .025). For D.
tinctorius, proportion of time spent active was significantly greater for the coconut
enrichment versus the control state in the large exhibit (N = 10, T =1,p < .005), the
coconut enrichment versus the control state in the small exhibit (N =8,T =1,p < .01),
the coconut enrichment versus the other enrichment in the large exhibit (N = 10, T =
4, p < .02), and the coconut enrichment versus the other enrichment in the small ex
-
hibit (N =8,T =2,p = .02).
DENDROBATID ENRICHMENT 293
TABLE 5
Statistically Significant Wilcoxon Matched-Pairs Signed Rank Tests for Dart-Poison Frogs
Under Different Enrichment Strategies and Switched Between Small and Large Exhibits
Species
Wilcoxon Matched-Pairs
Signed Tank Test
One- or
Two-Tailed?
H1: >
Proportion
Active
a
NT
p
Value
D. azureus Large: coconut vs.
control
One Coconut 11 9 < .025
Small: Other vs. control One Other 7 1.5 < .025
Large: Coconut vs. other Two 12 9.5 < .025
Other: Large vs. small
b
Two 8 3 < .05
Coconut: Original vs.
experimental
b
One Experimental 7 2 .025
D. tinctorius Large: Coconut vs.
control
One Coconut 10 1 < .005
Small: Coconut vs.
control
One Coconut 8 1 < .01
Large: Coconut vs. other Two 10 4 < .02
Small: Coconut vs. other Two 8 2 .02
Coconut: Original vs.
experimental
b
One Experimental 8 0 .005
a
H1: > proportion active indicates that state was predicted to have a higher proportion active for a
one-tailed test.
b
Note that these tests were performed only on individuals that were experimentally
switched between exhibits.
Experimental Exhibit Switch—Original Versus
Experimental Exhibit
Activity levels increased for each enrichment state when individuals were
moved from their original exhibit to the experimental exhibit—regardless of
which the exhibit to which they were switched (Figure 2; Table 6). These in
-
creases in activity were not statistically significant for the species as a whole but
produced some significant trends when we looked at the activity of the individu
-
als within a species. As predicted, the proportion of time spent active was signif
-
icantly greater for the coconut enrichment in the experimental exhibit when
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HURME ET AL.
FIGURE 2 Experimental exhibit switch: Original versus experimental exhibit—proportion of
time spent active in original versus exhibit for each enrichment state with 95% confidence intervals.
TABLE 6
Experimental Exhibit Switch: Original Versus Experimental Exhibit—Proportion of Time
Spent Active for Original Versus Experimental Exhibit for Each Enrichment State
Original Exhibit Experimental Exhibit
D. azureus D. tinctorius D. azureus D. tinctorius
Enrichment
State
Proportion
Active N
Proportion
Active N
Proportion
Active N
Proportion
Active N
Control 0.41 8 0.40 8 0.46 8 0.49 8
Coconut 0.48 8 0.50 8 0.68 7 0.75 8
Other 0.45 8 0.41 8 0.57 8 0.56 8
compared with the coconut enrichment in the original exhibit for both D.
azureus (N =7,T =2,p = .025) and D. tinctorius (N =8,T =0,p = .005). We
also predicted that activity levels would be higher in the experimental exhibit
compared with the original exhibit for the control and other enrichment states,
but they failed to show a statistically significant trend within each species.
DISCUSSION
Activity Levels
For D. azureus and D. tinctorius individuals in both exhibits, the coconut enrich
-
ment state increased activity levels from the control state. The D. azureus indi
-
viduals in the small exhibit experienced higher activity levels with the Other en
-
richment than with the Coconut enrichment. The D. azureus individuals in the
large exhibit and the D. tinctorius individuals in the small and large exhibits re-
mained at activity levels near control state levels for the other enrichment state.
These increases in activity between enrichment states for each species showed
interesting trends but probably were not statistically significant because of large
confidence intervals resulting from the large amount of individual variation
within each species. Although across species the changes in activity levels were
not significant, some enrichment states produced statistically significant results
within each species.
Within both species in the large exhibit, the coconut enrichment state resulted
in a significantly greater proportion of time spent active than in the other and con-
trol states. Within the D. tinctorius individuals in the small exhibit, the coconut
state again significantly increased activity levels over the other and control states.
Within the D. azureus individuals in the small exhibit, the other enrichment state
significantly increased activity levels when compared with the control state.
Experimental Exhibit Switch
To compare the effects of the exhibits and a change in environment and social
surroundings, 16 D. azureus and D. tinctorius individuals were switched be
-
tween the large and small exhibits. As predicted, activity levels increased from
the original exhibit to the new exhibit regardless of the exhibit to which the
frogs were moved. One might expect that individuals moved from the large ex
-
hibit to the small exhibit might exhibit a suppressed activity level due to space
constraints and lack of social interactions. Although this may affect the frogs’
behavior, they also are exposed to many new stimuli that could increase activity
levels. The small exhibit provides the switched individuals with opportunities
DENDROBATID ENRICHMENT 295
for new spatial learning due to the novel physical environment. It also provides
them with an altered social composition due to the new dominance hierarchy
created by separating a small part of the group.
Control State
The control state provided the baseline behavioral data with which we could an
-
alyze the effects of the enrichment states. We assumed that there was no residual
effect of the enrichments and treated each control day equally, regardless of the
enrichment state that came before it.
Coconut Enrichment State
As predicted, the coconut enrichment state produced the greatest increase in ac
-
tivity. This may be due to the coconut feeder’s complicated nature, which ran
-
domizes the release of insects into the exhibit. Similar to ants leaving a nest in
the wild, the frogs have to wait until the prey “decides” to exit the feeder, unlike
open-dish feeders in which the prey are vulnerable at all times. Because the prey
are released at random times, each emerging insect reinforces the frogs’ waiting
behavior. Like gamblers “working” a one-armed bandit slot machine and other
variable interval reinforcement schedules, the frogs cannot “predict” when an in-
sect will emerge for consumption. We observed that they continued to wait until
the interval between insect emergences had been sufficiently long to allow them
to lose interest. Some individuals took much longer to lose interest and would
hunt around the coconut as long as it was in the exhibit. Note that the rate of in-
sect emergence can increase or decrease the size of the holes in the coconut.
Other Enrichment State
The other enrichment state increased activity levels when compared with the
Control state but was a less “effective” enrichment than the coconut feeder,
given our goal of increased activity levels. The broadcast feed was extremely ef
-
fective at initially increasing activity. Because the prey had no protection, how
-
ever, they were consumed very quickly, and activity levels returned to control
levels. The aphid enrichment and petri dish feeding method had the same draw
-
back of an initial burst of activity as the prey quickly were consumed.
Coconut Enrichment Versus Other Enrichment
The coconut enrichment provided a sustained increase in activity and foraging
behavior because of the random distribution of prey, whereas the other enrich
-
ment provided an initial burst of activity as the unprotected prey are consumed.
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Both enrichments provide the daily diet allotment, but the coconut enrichment
provides enrichment over a greater period.
The main differences in the two exhibits are the size and number of frogs in each
exhibit. The large exhibit has a complex physical layout withmanyhiding places and
is able to support many individuals. The large exhibit also includes a large amount of
vertical space and stratification, which provides more spatial area for use and allows
different species to coexist peacefully. Smaller species such as D. leucomelas spent
more time climbing the branches and the walls, whereas larger species such as D.
tinctorius spent more time on the ground and in the lower vegetation.
An additional difference between the two exhibits concerns the reliability of
observed activity levels. For data analysis, the behaviors were grouped into active,
resting, and out of sight. In the small exhibit because there were few places for the
frogs to hide completely from the observer, most of the activity of the frogs was re
-
corded accurately. In the large exhibit, however, approximately half the ground
area of the exhibit was hidden from view by the observer. Therefore, it was not al
-
ways possible to find the individuals, resulting in a relatively higher out of sight
proportion than in the small exhibit. Because it is not possible to determine how
much time the frogs were active while out of sight, the active proportion for the
large exhibit may be less accurate than for the small exhibit.
The large exhibit provided increased interspecific and intraspecific contact by
housing a larger number of individuals in the same exhibit. The increased social
contact resulted in some breeding behavior and agonistic behavior such as wres-
tling and chasing but no visible dominance hierarchy. There was no visible compe-
tition for food; when a foraging enrichment item was presented, the frogs simply
climbed on top of one another to access the prey. This multispecies setup, how-
ever, is not recommended for breeding populations because all eggs laid by D.
auratus and D. tinctorius were consumed by D. leucomelas.
Foraging enrichments often are the most effective type of enrichment. Prey di
-
versity and presentation were increased during the experimental enrichment pe
-
riod. Hayes et al. (1998) stated that prey who are difficult to catch can be enriching,
and both the coconut feeder and the aphid enrichment made the prey items more
difficult to obtain. The aphid enrichment increased difficulty in foraging because
the aphids did not move and dart-poison frogs normally hunt by searching for
movement. Even though the aphids did not move, the frogs discovered them al
-
most immediately the first time the aphid enrichment was presented to them. Per
-
haps the aphids fit the frogs’ instinctive prey search image, which would explain
how they would know to hunt the aphids.
The coconut enrichment item was presented to the frogs between 10 a.m. and 2
p.m., and this randomized presentation schedule was meant to imitate the random
availability of prey in nature and encourage opportunistic foraging. However, be
-
cause the coconut enrichment randomizes the frequency of insect emergences, op
-
portunistic foraging would be encouraged even if the enrichment was presented at
DENDROBATID ENRICHMENT 297
the same time every day. More important than variation in feeding time might be
variation in feeding location, preventing individuals from aggregating at the
learned feeding site. The individuals in the large exhibit spent a large amount of
time resting and foraging at the feeding site in the front of the exhibit, even when
no foraging item was present, indicating that they associated feeding with that one
site. Changing the feeding location and the uncertainty it introduces for the frogs
can be an enrichment in itself; one drawback is that certain feeding locations may
minimize visibility for the public.
Imitating tropical rain showers, misting occurred at random times and for ran
-
dom lengths throughout all experimental states in both exhibits. Dart-poison frogs
are most active after a rain shower in the wild (Leenders, 2001) and in captivity.
Dendrobatids need sufficient humidity to obtain water from the environment.
They spend a lot of time hiding in moist crevices between rocks and plants to avoid
desiccation, and the frogs’ activity was directly proportional to the amount of
moisture in the exhibit. Misting increased activity and visibility of frogs to observ
-
ers in each state and can be used as a habitat enrichment item. Similar to a foraging
enrichment that has unpredictable food availability, a randomly timed water mister
provides unpredictable water availability.
The enrichments succeeded in increasing activity levels in the frogs’ diurnal
time budgets and in enhancing the frogs’ physical and mental activities. The large
exhibit provided a large amount of physical surroundings to explore, which in-
creases the frogs’ physical well-being, as behaviors such as climbing are encour-
aged. Dendrobatids have good spatial memory; the males return to specific pools
of water to deposit tadpoles. The frogs may adjust to a large amount of stimuli pro-
vided by new physical surroundings. In addition, the frogs must learn the feeding
site, which encourages mental activity and presumably an increase in well-being.
More diverse prey availability also should enhance the frogs’ mental wellness as
they encounter items that fit their instinctive prey search images. Increased social
interactions due to the larger number of individuals in one exhibit contributed to
physical well-being, as certain individuals engaged in harmless agonistic behav
-
iors such as short bouts of wrestling. The species we housed together are from dif
-
ferent areas of Latin America, and it is highly unlikely that they would encounter
the same mix of species in nature. When planning multispecies exhibits, it is im
-
portant to obtain adequate information about the behavior of each species to pre
-
vent potential harmful conflicts between species.
Although “lower” taxa are commonly forgotten when designing environmental
enrichment programs, enrichment can be very beneficial for amphibians. Enrich
-
ment can encourage innate foraging behaviors and enhance animal activity and
visibility for the public. In redesigning the Central Park Zoo’s dart-poison frog ex
-
hibit, we considered the needs to address habitat changes for the frogs, activity pat
-
terns of the frogs in captivity versus in nature, foraging challenges in captivity, and
behavioral interactions of species and individuals. The goal of this project was to
298
HURME ET AL.
help develop a best-practices approach to amphibian husbandry for zoological fa
-
cilities to use in the future. However, this study focused on a small species group of
charismatic frogs, and the results may not apply to all amphibians. In addition, we
focused on only a single frog life stage by testing nonbreeding adults in the enrich
-
ment scenarios we designed. Additional research with other innovative enrich
-
ment devices that are consistent with each species’ natural history needs should be
tested to increase the welfare of the wide variety of other amphibians living in zoos
and aquariums.
ACKNOWLEDGMENTS
This research project was made possible because of the Wildlife Conservation
Society Animal Enrichment Program Fund. We thank the Wildlife Conservation
Society Herpetology Department for helpful review of this project and the re
-
sults. We extend a special thanks to Amaury Quinoñes and Jeremy Tuschak for
exhibit construction, maintenance, and husbandry.
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... Model studies: Hurme et al. 2003. ...
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During the past decade, increased concern for the psychological as well as the physical well-being of animals has allowed environmental enrichment to mature as a focal concept in their captive management (Shepherdson 1989, 1991a,b, 1992). As the concept has developed, its scope has expanged to include almost any variable linked to the perceptual universe, or umwelt (von UcxkiillI909), of the captive animal (Shepherdson 1992). Despite this rapid conceptual growth, environmental enrichment remains an approach applied largely to mammals (Warwick 1990a; Shepherdson 1992; King 1993); other groups, such as amphibians and reptiles, are rarely addressed. For example, a recent extensive catalogue of enrichment ideas (Copenhagen Zoo 1990) devoted only a single page to these taxa. In other reviews, amphibians and reptiles either are not mentioned (duBois 1991; Griede 1992; Shepherdson 1991a; Tudge 1991) or appear only briefly in passing discussion (Markowitz 1982). Nascent efforts have been made to address the psychophysiological problems of reptiles in captivity (Bels 1989; Warwick 1990a,b; Burghardt and Layne 1995), but these are the salient exceptions. The purpose here is to provide a foundation for designing environmental enrichment programs for amphibians and reptiles. Because amphibians and reptiles are species-rich groups (more than 4,000 species of amphibians and 6,000 species of reptiles are currently recognized; Zug 1993) and the literature on their behavior is vast, this review is not intended to be comprehensive. Rather, we address selected topics that provide a basis for exploring enrichment opportunities. In particular, we review the requirements of captive amphibians and reptiles in three areas: (1) contact with conspecifics, (2) interaction with other species, and (3) physical characteristics of the captive environment. Further, we interpret experimental and observational data that address these areas in an enriclunent context and identify opportunities to improve the well-being of captive amphibians and reptiles. Finally, because the maturation and socialization of captive-reared amphibians and reptiles may require some form of emichrnent (see Miller et aI., Chapter 7, this volume), we emphasize the pivotal role of enrichment in captive-breeding programs that have repatriation as a goal (i.e., repopulation of extirpated wild populations as per Reinert 1991; see also Nielsen 1988).
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