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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
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
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:
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
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).
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
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.
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,
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).
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.
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
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
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
Total Observation Time per Individual
Total Time Observed
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
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).
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.
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
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.
Proportion of Time Spent Active for Each Enrichment State
Large Exhibit Small Exhibit
D. azureus D. tinctorius D. azureus D. tinctorius
Active N
Active N
Active N
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.
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).
Statistically Significant Wilcoxon Matched-Pairs Signed Rank Tests for Dart-Poison Frogs
Under Different Enrichment Strategies and Switched Between Small and Large Exhibits
Wilcoxon Matched-Pairs
Signed Tank Test
One- or
H1: >
D. azureus Large: coconut vs.
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
Two 8 3 < .05
Coconut: Original vs.
One Experimental 7 2 .025
D. tinctorius Large: Coconut vs.
One Coconut 10 1 < .005
Small: Coconut vs.
One Coconut 8 1 < .01
Large: Coconut vs. other Two 10 4 < .02
Small: Coconut vs. other Two 8 2 .02
Coconut: Original vs.
One Experimental 8 0 .005
H1: > proportion active indicates that state was predicted to have a higher proportion active for a
one-tailed test.
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
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.
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
Active N
Active N
Active N
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.
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
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.
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
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
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.
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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... There are five main ways in which environmental enrichment may be provided: by (1) creating and managing a dynamic habitat, (2) encouraging social interactions between individuals, (3) encouraging foraging, (4) introducing novel objects and (5) training [21]. These methods aim to increase behavioural diversity, reduce abnormal behaviours, increase the range of natural behaviours demonstrated, increase the positive use of the environment, and increase the animal's ability to cope with challenges in a more natural way [22]. ...
... It is also important for the wellbeing of long-term captive individuals. Finally, effective enrichment can have positively influence on visitor perception, which may in turn promote in situ projects [21]. In sum, it is essential that further enrichment studies implement robust, well-balanced protocols that monitor and evaluate the impact of a range of randomly presented enrichment items over time. ...
Full-text available
Environmental enrichment has been shown to enhance the behavioural repertoire and reduce the occurrence of abnormal behaviours, particularly in zoo-housed mammals. However, evidence of its effectiveness in reptiles is lacking. Previously, it was believed that reptiles lacked the cognitive sophistication to benefit from enrichment provision, but studies have demonstrated instances of improved longevity, physical condition and problem-solving behaviour as a result of enhancing husbandry routines. In this study, we evaluate the effectiveness of food- and scent-based enrichment for three varanid species (Komodo dragon, emerald tree monitor lizard and crocodile monitor). Scent piles, scent trails and hanging feeders resulted in a significant increase in exploratory behaviour, with engagement diminishing 330 min post provision. The provision of food- versus scent-based enrichment did not result in differences in enrichment engagement across the three species, suggesting that scent is just as effective in increasing natural behaviours. Enhancing the environment in which zoo animals reside is important for their health and wellbeing and also provides visitors with the opportunity to observe naturalistic behaviours. For little known and understudied species such as varanids, evidence of successful (and even unsuccessful) husbandry and management practice is vital for advancing best practice in the zoo industry.
... Such attachments have been found in other reptiles as well (Bowers and Burghardt, 1992) Precocial courtship in some turtles and squamate reptiles has characteristics similar to play fighting in rodents (Kramer and Burghardt, 1998). There is less evidence for amphibians, but tadpoles of the Vietnamese mossy frog Theloderma coricale (Hylidae) repeatedly allow themselves to be swept up in airstreams and 'harmless fighting' in adult dart poison frogs suggests that some amphibians also play fight (Burghardt, 2005;Hurme et al., 2003). The conclusion is that environmental features and social partners may be useful components of 'enrichment' in reptiles and amphibians. ...
... In other words, for many amphibians successful breeding and maintenance require attention to specific microclimate and structural details that are often less necessary for feeding and breeding most mammals. However, there is scope for study here, as shown in work on developing behaviorally appropriate settings for bullfrogs (Bang and Mack, 1998) and dendrobatid dart poison frogs (Hurme et al., 2003;McRobert, 2003). Since frogs have been used in much physiological and biomedical research, it is important that such research is not compromised due to keeping the animals in crowded inappropriate housing and until the time they are needed for often terminal experiments. ...
Full-text available
Reptiles and amphibians have been neglected in research on cognition, emotions, sociality, need for enriched and stimulating environments, and other topics that have been greatly emphasized in work on mammals and birds. This is also evident in the historic lack of enriching captive environments to reduce boredom and encourage natural behavior and psychological well-being. This paper provides those responsible for the care of reptiles and amphibians a brief overview of concepts, methods, and sample findings on behavioral complexity and the role of controlled deprivation in captive herpetological collections. Most work has been done on reptiles, however, and so they are emphasized. Amphibians and reptiles, though not admitting of easy anthropomorphism, do show many traits common in birds and mammals including sophisticated communication, problem solving, parental care, play, and complex sociality. Zoos and aquariums are important resources to study many aspects of these often exotic, rare, and fascinating animals, and rich research opportunities await those willing to study them and apply the wide range of methods and technology now available. (c) 2013 Elsevier B.V. All rights reserved.
... Model studies: Hurme et al. 2003. ...
... • Enabling optimal mate choice to maximise fitness of offspring (Felton et al 2006;Heatwole and Sullivan 1995). • Elucidating interesting and unique behaviours, thus increasing publicity and educational potential (Hurme et al. 2003). • Methodology, Martin andBateson 2007, Lehner 1996;Wells 2007, Heatwole 1995, Duellman and Trueb 1994. ...
... Model studies: Hurme et al. 2003. ...
... • Enabling optimal mate choice to maximise fitness of offspring (Felton et al 2006;Heatwole and Sullivan 1995). • Elucidating interesting and unique behaviours, thus increasing publicity and educational potential (Hurme et al. 2003). • Methodology, Martin andBateson 2007, Lehner 1996;Wells 2007, Heatwole 1995, Duellman and Trueb 1994. ...
Full-text available
The Amphibian Conservation Research Guide (ACRG) is an international initiative to build a framework for research that supports amphibian conservation breeding programs. To support amphibian conservation there is a need for increased research across a wide range of overlapping disciplines. The guide offers projects unique to the management of amphibians in conservation breeding programs, and also projects that deal with more fundamental aspects of biology. We have considered zoos as focal institutions for research as they provide facilities, a means to focus the public’s attention on amphibian conservation, and have a strong tradition of supporting conservation breeding programs. Research is emphasized that; 1) directly contributes to both ex situ and in situ components of amphibian conservation, 2) extends research programs widely throughout scientific fields, 3) involves the global community, 4) targets conservation breeding programs, 5) encourages collaborations, 6) directly benefits participating institutions and more broadly humanity, 7) supports young conservation scientists, and 8) develops benign research techniques. There are many direct benefits to zoos and other institutions through engaging in amphibian research. Perhaps the most significant of these is that amphibians offer many of the best species and habitat projects for biodiversity conservation. An increasing number of conservation breeding populations are supporting species rehabitation. Amphibian research is low cost, and offers opportunities for education, display, and publicity and outreach. Amphibians in general collections and in conservation breeding programs are equally amenable to a range of research possibilities. Zoo research can involve amphibian collections in studies that improve their welfare and management, and their health and reproduction. Amphibian conservation research can also extend to all segments of the scientific and conservation network. Zoos and other institutions can also use their populations of amphibians to provide otherwise difficult to obtain amphibians, or with biological samples including genetic or other molecular samples. In response, universities and other research institutions can engage elaborate large scale studies including physiology, behavior, reproduction, genetics, host-pathogen interactions, and pathology. The ACRG provides projects with clearly demonstrated benefits to zoos including improved husbandry, veterinary service, reproduction rates, reduced morbidity and mortality, and improvement in genetic management. However, there are also wider benefits of amphibian conservation research including providing information to improve management, and direct benefits to humanity including the development of novel pharmaceuticals and support for ecosystem services. Perhaps the greatest benefit amphibian conservation research can offer is the provision of research opportunities to young scientists and conservationists. In particular these programs provide a portal for young biologists to engage in research that directly provides for amphibian conservation and could lead to careers in conservation, biotechnology, and many other fields. The ACRG investigates the current state of research and management in amphibian conservation breeding programs, discusses research potentials and how multi-disciplinary and multi-institutional projects can provide an increased resource base and greater innovation. The ACRG then provides the background to a series of research categories, their research potentials, model studies, and references and other resources.
... Reptiles [75], fish [76], and invertebrates [77] are all under 3% of the work. No amphibian studies were found, though enrichment studies before 2010 included them [78]. This variety of species is strongly impacted by the study context, as primates and rodents are common in lab studies while ungulates are common in agriculture studies. ...
Full-text available
Environmental enrichment is adding complexity to an environment that has a positive impact on a captive animal as a necessity of care. Computing technology is being rapidly weaved throughout the space in both enrichment devices as well as evaluating enrichment outcomes. In this article, we present a scoping review of 102 captive animal enrichment studies and propose a contextual lens for exploring current practices. We discuss the importance of directed growth in species inclusion, transitioning beyond anthro-centric designs, and utilizing shared methodologies.
... Moreover, amphibians are a diverse group with high degrees of species-level specialization [16], making it important to understand behavioral repertoires, activity budgets, and measures of welfare for individual species [17,18]. In the handful of species where these data have been collected under captive conditions, welfare impacts of basic husbandry conditions have been identified through behavioral measures [19][20][21][22][23][24], highlighting the importance of the development of such tools. Furthermore, for animals involved in ex situ conservation, welfare may have impacts on conservation success [25]. ...
Full-text available
Animal behavior and welfare science can form the basis of zoo animal management. However, even basic behavioral data are lacking for the majority of amphibian species, and species-specific research is required to inform management. Our goal was to develop the first ethogram for the critically endangered frog Xenopus longipes through observation of a captive population of 24 frogs. The ethogram was applied to produce a diurnal activity budget and to measure the behavioral impact of a routine health check where frogs were restrained. In the activity budget, frogs spent the vast majority of time swimming, resting in small amounts of time devoted to feeding, foraging, breathing, and (in males) amplexus. Using linear mixed models, we found no effect of time of day or sex on baseline behavior, other than for breathing, which had a greater duration in females. Linear mixed models indicated significant effects of the health check on duration of swimming, resting, foraging, feeding, and breathing behaviors for all frogs. This indicates a welfare trade-off associated with veterinary monitoring and highlights the importance of non-invasive monitoring where possible, as well as providing candidates for behavioral monitoring of acute stress. This investigation has provided the first behavioral data for this species which can be applied to future research regarding husbandry and management practices.
... Enrichment tends to be in feeding and tactical forms, as these methods are less time consuming, financially viable, and effective for enrichment [16]. Foraging enrichment has been explored in many forms, such as automated feeders with Fennec foxes [46], contrafreeloading feeding preferences with puzzle feeders for giraffes [37], and unique feeding methods for frogs [17]. ...
Conference Paper
Full-text available
Animal enrichment in zoos is evolving faster than ever, with more technical approaches being found across disciplines, particularly in Animal-Computer Interaction (ACI). Captive orangutans are a unique population that are commonly im-pacted by health concerns that may be alleviated through increased physical activity. In this study protocol, we aim to examine the potential for a drone delivery system to distribute food to encourage natural foraging behaviors while minimizing animal care staff burden. We discuss conducting a survey with animal care staff and the general public to look at zoo perceptions, use case feedback, and perceptions of technology in enrichment. We also outline conducting observations of a specific population of captive orangutans to establish a baseline for a future system deployment, as well as compare to their wild counterparts.
... In captivity, insectivorous lizards are typically 'broadcast' or 'scatter' fed, whereby multiple prey insects are distributed around the enclosure at one time. Altering the way in which food is presented can be used to provide behavioural enrichment for captive insectivores (Hurme et al., 2003) by increasing physical activity and exploration of space and by eliciting a larger frequency and variety of behaviours; thus reducing the risk of psychological or physical diseases (mainly obesity, which can commonly occur in captive reptiles, (Dinse, 2004;Donoghue, 2006)). ...
Staggering food availability through a delivery device is a common way of providing behavioural enrichment as it is usually thought to increase the amount of natural behaviour due to the unpredictability of the food source. Tree-runner lizards (Plica plica) are a Neotropical, scansorial, insectivorous species. We provided these lizards with an enrichment device that slowly released insect prey and tested its effect on the activity and frequency of a number of behaviours in comparison with a scatter control (where prey items were broadcast in the enclosure; standard food presentation for captive insectivorous lizards) and a non-feeding control. Both types of food increased activity and counts of several behaviours in comparison with the non-feeding control. However, we found the provision of the behavioural enrichment device led to a significantly lower frequency of almost all analysed behaviours in comparison with scatter control trials, mainly in behaviours associated with activity (unsuccessful strikes (= unsuccessful capture of prey) (p = 0.004), locomotion (p = 0.004), alertness (p = 0.004) and the number of times a boundary in the enclosure was crossed ie. activity (p = < 0.001)). The frequencies significantly increased in the enrichment trials (relative to the scatter control) were the number of successful strikes (= successful capture of prey; p = <0.001) and targeting prey (p = <0.001). There was no significant difference in latency to first strike (p = 0.24), duration of hunting activity (p = 0.83) or enclosure use (p>0.05) between scatter and enriched trials. The relative success of the scatter feed in promoting activity and increasing hunting difficulty was likely partly due to the enclosure design, where the complex physical environment contributed to the difficultly in catching the prey. However, when the feeding duration and enclosure use was analysed there was no significant difference between the scatter control and enrichment trails. The results from this study highlight the importance of evaluating enrichment strategies, and the role of complex enclosure design in creating effective enrichment for insectivores, which can contribute to their welfare in captivity.
There is a wealth of evidence demonstrating the benefits of environmental enrichment across a range of different animal species. However, there is comparatively little such research into the effect of enrichment provision on captive reptiles. The aim of this study was therefore to ascertain if an increase in environmental complexity was beneficial to the behaviour and welfare of corn snakes (Pantherophis guttatus). The study used a combination of behavioural observations in the home enclosure, behavioural tests of anxiety, and a preference test. The snakes used the enrichment when it was available to them and enriched snakes showed changes in general behaviour reflective of improved welfare. However, the anxiety tests revealed few effects of enrichment provision on performance. In contrast, the snakes exhibited a strong preference for the enriched enclosure when given a choice. These findings suggest that the provision of environmental complexity to the enclosure was beneficial to the behaviour and welfare of captive corn snakes. We therefore recommend enrichment should be used when keeping captive snakes.
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p>Objetivou-se aqui aplicar diferentes enriquecimentos ambientais a dois indivíduos de tamanduá-mirim ( Tamandua tetradactyla ) do Aquário de São Paulo em três fases: (1) pré-enriquecimento; (2) enriquecimento; (3) pós-enriquecimento. Alterações nas frequências de alguns comportamentos interativos e associados à locomoção foram observadas para ambos os indivíduos, de forma a apontar que a aplicação dos enriquecimentos teria favorecido nos animais maior atividade, promovendo estímulos e refletindo, portanto, maior bem-estar, além de contribuir para o aumento da variabilidade e complexidade do ambiente onde estes são mantidos. Palavras chave : Comportamento Animal, Etologia, Xenarthra, Vermilingua.</p
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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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Temporal patterns of anuran reproduction fall into two broad categories: prolonged breeding and explosive breeding. The spatial and temporal distribution of females determines the form of malemale competition. Males of explosive breeders in dense aggregations engage in ‘scramble competition’, attempting amplexus with every individual and struggling among themselves for possession of females. Males of prolonged breeders usually call from stationary positions to attract females and often maintain some sort of intermale spacing. Many aspects of vocal behaviour and chorus organization can be viewed as consequences of intrasexual competition. Males of some prolonged breeders defend allpurpose territories, oviposition sites, or courtship areas against conspecific males. Males with high quality territories may enhance their attractiveness to females and obtain several mates in one season. The social organization of some species resembles the lek behaviour of other vertebrates. Males or females of some tropical species care for eggs and tadpoles, but the evolution of parental care has not yet been studied in detail.
Previous research on a variety of organisms indicates that polygyny can impose a cost on the reproductive success of females. Some authors have hypothesized that this cost may have caused the evolution of female parental care from paternal or biparental care in some lineages, particularly in poison frogs of the genusDendrobates. In this paper, we evaluate the assumptions and theoretical implications of this hypothesis and present several game-theoretic models that clarify some of the issues. We conclude that a cost of polygyny is unlikely to drive a female care strategy to fixation on its own; however, if caring males suffer a cost of lost mating opportunities then a cost of polygyny may destabilize male care and result in the evolution of uniparental female care. A cost of polygyny on its own may be able to drive a transition from male care to biparental care. We also discuss other factors that may have influenced the evolution of parental care in the poison frogs, including results from recent field and laboratory research, and we evaluate the possibility that female care evolved from biparental, as opposed to male care.
Previous laboratory studies on phototactic behavior of five species of neotropical anurans led to predictions that they would be active in natural habitats under only a limited range of ambient illuminations relative to the range available during 24-h periods. Generally, the species were found to be active within a <4 log-unit range of illuminance and to feed within an even narrower range. Evidence suggests that photic cues may aid in niche partitioning among species. Bufo marinus and Leptodactylus pentadactylus were active at night, the former in brighter, open places, the latter in the dimmer forest. Dendrobates auratus had bimodal diel activity periods in early morning and late evening. Bufo typhonius and Physalaemus pustulosus were active during the day, the former in the dimmer forest, the latter in brighter, open areas. Thus, activity rhythms, phototactic behavior, and habitat selection interact to allow an anuran to be active under a relatively narrow range of light levels during a day, theoretically the range within which its eyes are best adapted evolutionarily.