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Seasonal and Daily Activity of Two Zoo-Housed Grizzly Bears (Ursus Arctos Horribilis)

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Captive grizzly bears, like their wild counterparts, engage in considerable variability in their seasonal and daily activity. We documented the year-long activity of two grizzly bears located at the Woodland Park Zoo in Seattle, Washington. We found that behaviors emerged in relation to month-to-month, seasonal, and time of day (hour-to-hour) observations, and events that occurred on exhibit, such as daily feedings. Seventeen behaviors split into seven classes of behavior were observed during their on-exhibit time over a 13-month period. Inactivity was the most frequent class of responses recorded, with most inactive behaviors occurring during the winter months. Both stereotypic and non-stereotypic activity emerged during the spring and summer months, with stereotypic activity occurring most frequently in the morning and transitioning to non-stereotypic activity in the latter part of the day. Results are discussed with respect to how captive grizzly bear behaviors relate to their natural seasonal and daily activity, as well as how events, such as feeding times and enrichment deliveries, can be used to optimize overall captive bear welfare.
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Article
Seasonal and Daily Activity of Two Zoo-Housed
Grizzly Bears (Ursus Arctos Horribilis)
Eduardo J. Fernandez 1, * , Ellen Yoakum 2and Nathan Andrews 3
1School of Animal and Veterinary Sciences, University of Adelaide, Adelaide 5005, Australia
2Ahimsa Dog Training, Seattle, WA 98107, USA; ellenyoakum@gmail.com
3Happy Hollow Park & Zoo, San Jose, CA 95112, USA; andren@uw.edu
*Correspondence: edjfern@gmail.com; Tel.: +61-206-765-7350
Received: 23 July 2020; Accepted: 21 August 2020; Published: 25 August 2020


Abstract:
Captive grizzly bears, like their wild counterparts, engage in considerable variability
in their seasonal and daily activity. We documented the year-long activity of two grizzly bears
located at the Woodland Park Zoo in Seattle, Washington. We found that behaviors emerged in
relation to month-to-month, seasonal, and time of day (hour-to-hour) observations, and events
that occurred on exhibit, such as daily feedings. Seventeen behaviors split into seven classes of
behavior were observed during their on-exhibit time over a 13-month period. Inactivity was the
most frequent class of responses recorded, with most inactive behaviors occurring during the winter
months. Both stereotypic and non-stereotypic activity emerged during the spring and summer
months, with stereotypic activity occurring most frequently in the morning and transitioning to
non-stereotypic activity in the latter part of the day. Results are discussed with respect to how captive
grizzly bear behaviors relate to their natural seasonal and daily activity, as well as how events, such as
feeding times and enrichment deliveries, can be used to optimize overall captive bear welfare.
Keywords: behavior; circadian; circannual; grizzlies; stereotypies; ursids; zoos
1. Introduction
1.1. Brown Bears in the Wild
Wild brown bears (Ursus arctos) currently reside in 44 countries, inhabiting a variety of habitats,
including dry Asian steppes, arctic shrublands, and temperate rain forests [
1
]. Researchers have found
behavioral variation in subspecies and subpopulations based on geographic location, resource availability,
and human influence [
2
5
]. The past data also suggest that most brown bear subspecies, including grizzly
bears (Ursus acrtos horribilis), spend more time active around the spring and summer, less in the fall,
and the least time active during the torpor months of winter [
3
,
6
10
]. Seasonal behavioral changes are
thought to be influenced by food availability [
3
,
9
12
], breeding [
8
,
9
], age [
2
,
13
], and sex [
14
]. Most of the
evidence on this behavioral variability is through secondary sources or non-field measures, due to the
difficulty of direct observation of an elusive, long-ranging carnivore. These methods have included scat
interpretation [
15
], radio collar tracking [
3
,
16
], observations in non-natural environments (e.g., zoos), or
a combination of two or more methods [17].
With respect to their daily activity, brown bears have primarily been found to be diurnal [
6
,
18
],
with peaks of activity in the early morning and evening. Some subpopulations have also been
reported to be crepuscular or nocturnal [
11
,
19
,
20
]. A large proportion of their daily waking activity is
thought to be foraging and eating, with bouts of rest and travel [
8
,
9
,
12
,
13
]. Brown bears have shown
flexibility in their daily activity based on weather [
6
], light levels [
19
], age [
2
,
13
,
14
], and anthropogenic
J. Zool. Bot. Gard. 2020,1, 1–12; doi:10.3390/jzbg1010001 www.mdpi.com/journal/jzbg
J. Zool. Bot. Gard. 2020,12
influences [
7
,
18
,
21
,
22
]. Seasonal and local changes in diet are thought to influence both circannual and
circadian rhythms [11,23].
1.2. Brown Bears in Zoos
Brown bears, including grizzlies, are common within zoological institutions. Like their wild
counterparts, a variety of factors influence their behavioral patterns—including, but not limited
to, enclosure settings, daily and seasonal weather variation, type and amount of food delivered,
feeding and environmental enrichment schedules, visitor and keeper interactions, and individuals
housed within an enclosure [
24
28
]. Likewise, brown bear enclosures show considerable variability,
from small, artificial enclosures to large, naturalistic exhibits [
29
31
]. Some facilities have on-exhibit
and o-exhibit enclosures that allow for the bear(s) to be secured overnight and may provide the
bear(s) with a winter den. Outdoor enclosures may have pools and/or streams, either natural or replica
fall trees and logs, and vegetation.
Welfare Assessment and Stereotypies
Zoos use a variety of methods to promote the proper care and welfare of their bears. One standard
measure of behavioral welfare is the comparison of wild and captive activity budgets [
32
34
]. Captive bears
may display stereotypies not typical of their wild counterparts. Stereotypies have been defined as repetitive,
largely invariant behavior patterns that serve no obvious goal or function [
34
]. Stereotypies are attributed to
numerous factors, including sub-optimal environments, lack of environmental control, and species-typical
appetitive behavior [
35
40
]. Stereotypies have been discussed as a possible indicator of poor welfare,
with the display of stereotypies in bears and other animals used as evidence of an enclosure failing to
meet the biological and/or behavioral needs of that animal [
41
44
]. Other studies have found that visitors
perceived stereotypies to indicate a lower level of care and/or are negatively correlated with interest in
financially supporting zoological institutions [
45
47
]. Thus, zoos place considerable effort in minimizing
the display of stereotypies and increasing naturalistic behaviors in bears, typically through the use of
environmental enrichment—including, but not limited, to changes in how and when food is presented
and the use of foraging devices [4852].
1.3. Study Purpose
The following study examined the seasonal and daily activity of two zoo-housed grizzly
bears. Seventeen behaviors were split into seven classes of behavior and examined in terms of
(1) month-to-month, (2) seasonal, and (3) hour-to-hour changes. The focus of the study was to (a) examine
observed behavior change patterns as they correlated with changes in the bear’s environmental and
husbandry practices, and (b) compare and contrast these patterns with those observed in their wild
counterparts. Additionally, we hoped to better understand the function of the observed behaviors
in terms of their species-typical and event-based occurrences, and thus, be better suited to provide
evidence-based suggestions for optimizing the welfare of these and other captive bears.
2. Materials and Methods
2.1. Subjects and Setting
Two captive-born grizzly bears were the subjects of the study: Keema, and Denali, ~395 kg male
bear and ~405 kg male bear, respectively. Both bears were 15-years-old at the study’s onset and were
reproductively intact. They were a brother pair that came from Washington State University’s Bear Center in
Pullman, Washington, and resided at the Woodland Park Zoo (Seattle, WA, USA) since November of 1994.
The bears resided in an exhibit in the Northern Trail zone of the zoo, and that contained three
areas: An on-view outdoor area, ~1120 m2, an o-view outdoor exercise yard, ~410 m2, and a indoor
space, ~250 m
2
. Both outdoor areas consisted of natural trees, deadfall, grass, and rocks. The on-view
J. Zool. Bot. Gard. 2020,13
area also contained an artificial river that led to a viewing window pool that held ~95 kL of water
(see Figures 1and 2).
Figure 1.
On-view outdoor area of the exhibit, with Denali (left) and Keema (right) engaged in Lying
Down (Inactive). Photo credit: Scott Richardson.
Figure 2.
On-view outdoor area of the exhibit with artificial river and pool visible. Denali is engaged
in Standing (Active). Photo credit: Scott Richardson.
Feeding enrichment was routinely provided in the form of scatter feeds and through devices,
such as boomer balls in both outdoor areas. The indoor space consisted of individual dens for each
of the bears. The indoor dens provided the bears with the opportunity to hibernate in the winter,
J. Zool. Bot. Gard. 2020,14
although their regular feeding schedule made this unnecessary (see below). The bears were typically
moved from the o-view area to the on-view area by 09:00 h, and then limited to the on-view area of the
exhibit between 09:00 and 16:00 h (Fall/Winter; October–March) or 09:00 and 18:00 h (Spring/Summer;
April–September), with some variability depending on weather conditions.
Diets for the bears varied based both on the individual and time of year, with 4.5–7 kg consumed
per bear per day. The bear diet consisted of Mazuri
®
omnivore diet, whole chickens, trout, rabbits, yams,
carrots, apples, honeydew melon, papaya, pears, cantaloupe, blueberries, romaine lettuce, celery, kale,
and grass hay. Salmon, ground turkey, oranges, and alfalfa were also occasionally added to their diet,
depending on availability. Treat items used for enrichment and/or training sessions included Marion
TM
leaf eater biscuits, Purina Omolene
®
, Iams
TM
dog food, and peanut butter. Diets were provided to the
bears either twice a day (07:30 and 15:00 h) or three times a day (07:30, 11:00, and 15:00 h), dependent
on their seasonal activity. The majority of their diet (at least half their daily diet) was provided at the
15:00 h feeding.
2.2. Materials
Materials included Palm
®
handhelds used to record behavioral data and an Event-PC program
that was run on the Palm
®
handhelds and designed specifically for this experiment by James C. Ha at
the University of Washington. Other materials included a notebook used to record potential errors and
additional observations/field notes that occurred during a session.
2.3. Data Collection and Procedure
Prior to its implementation, the study was approved through Woodland Park Zoo’s Research
Committee, as well as the University of Washington’s Institutional Animal Care and Use Committee
(IACUC #2858-06). An ethogram modified from a prior zoo bear study [
37
] and consisting of
17 behaviors split into seven classes of behaviors was also developed prior to the implementation of
the study (see Table 1).
Table 1. Behaviors, classes of behavior, and definitions for each response in the ethogram.
Behavioral Class and Behaviors
(Abbreviations) Definition
Active
Standing (St) Standing with no movement, 3 or 4 paws on the ground.
Rearing (Re) Standing up on back legs with stomach exposed.
Locomotion (Lo) Directed non-repetitive movement.
Manipulating object (Ma) Contact with a non-edible object, with any part of the body
manipulating its position.
Forage
Eating (Ea) Mouth contact with anything edible, including water.
Enriched Feeding (EF) Manipulating an enrichment device with food in it.
Social
Interacting w/another bear (IOB) Any gesture to another bear without vocalization.
Vocalization (Vo) Vocalization; must occur while oriented to another bear.
Groom
Licking body/Paws (LB) Tongue contact with any part of the body, including paws.
Scratching Body (SB) Using paws, mouth or non-mobile object to rub/scratch.
Inactive
Sitting (Si) Posterior and back legs on the ground in an upright position.
Lying down (LD) Most of the bear on the ground.
J. Zool. Bot. Gard. 2020,15
Table 1. Cont.
Behavioral Class and Behaviors
(Abbreviations) Definition
Stereotypy
Pacing (Pa)
Moving in a repetitive pattern, with completion from point A to
B and back to point A, (must include at least one full A-B-A
movement) or circling.
Rocking (Ro) Moving back and forth without locomotion. Must include at
least one full back-and-forth motion.
Other
Urinating or Defecating (UD) Urination or defecation.
Out of sight (OS) Not visible to the observer.
Other (Ot) Engaged in a behavior not listed above.
The behaviors observed were mutually exclusive, and the inclusion of the “Other” observation
category made the ethogram exhaustive. A modified scan sampling procedure [
53
] was used to record
behaviors for both bears during all observation sessions. The number of bears on exhibit was recorded
for behavior every 30 s for 30 min of observation for each session. These observations were then
averaged for each session based on the total number of bears engaging in each behavior, and by a
class of behavior. All observations were conducted in the on-view outdoor portion of the exhibit
between 09:30–18:00 h, seven days a week, between 12th January 2010 and 26th January 2011 (902 total
observations (1–8 observations per day) for 451 total hours of observations). Observers were typically
registered for independent research credit through the Psychology Department at the University of
Washington (PSY 499) and received observation training by live training sessions at the beginning of
each semester and weekly lab meetings throughout the study. Observations were examined weekly by
the first author for consistency across all observers, and drift was accounted for during these weekly
checks, as well as through weekly lab meetings. All observations were scheduled on a semester basis,
with observers filling times available during the week to account for as many observational times as
possible. A total of 38 observers collected behavioral data for the entire study.
2.4. Statistical Analyses
SigmaStat, version 11.0 (Systat Software Inc., San Jose, CA, USA) was used to run all the
statistical analyses. Only the classes of behavior that occurred more than 5% (Active, Forage, Inactive,
and Stereotypy) were examined for month-to-month, seasonal, and hour-to-hour activity, as well as
statistically analyzed. Because Shapiro-Wilk tests for normality failed, the dierences for the four
classes of behavior were tested for seasonal dierences (Winter: December–February, n=232 sessions;
Spring: March–May, n=325; Summer: June–August, n=136; Fall: September–November, n=209)
using Kruskal–Wallis analysis of variance (ANOVA) on ranks tests. When significant dierences
(
p<0.05
) for the ANOVAs were found, post-hoc pairwise comparisons (using Dunn’s Method) were
implemented. Dierences between the two combined January months (2010 (n=38 sessions) and
2011 (n=47 sessions); n=85 total January sessions) and July (2010; n=55 sessions) were tested
using Mann-Whitney Utests. The two January months were combined after finding no significant
dierences between each class of behaviors (also Mann-Whitney Utests). January and July were
directly compared because they were representative months for further examinations of the seasonal
dierences between the traditional winter (January) hibernation and summer (July) activity periods.
J. Zool. Bot. Gard. 2020,16
3. Results
Overall, Inactive was the most frequently occurring class of behavior (M=57.8%, SE =1.2%),
followed by Active (M=22.9%, SE =0.8%), Forage (M=7.8%, SE =0.5%), Stereotypy (M=5.9%,
SE =0.4%
), Other (M=4.1%, SE =0.4%), Social (M=1.2%, SE =0.2%), and Groom (M=0.4%,
SE =0.1%). Figure 3shows the month-to-month activity for the 13 months of observation.
Figure 3.
The average percentage of occurrence (with the standard error of the mean) for the four most
occurring classes of behavior for each month of observation during the study (x-axis).
During January through March, Inactivity was the most frequent class of behavior, occurring on
average above 75% of all behaviors recorded. All other classes of behaviors during these months
occurred ~10% or less. Starting in April, Active rose to 18% (SE =1.5) of all behaviors recorded,
until Active peaked in August at almost half of all behaviors observed (M=46%, SE =5.1).
The Stereotypy class of behaviors occurred ~3% or less of behaviors recorded during all observations,
except for May through July: 19.9% (May; SE =1.8), 18.4% (June; SE =2.7), and 17% (July; SE =2.6).
The Forage class of behaviors remained relatively stable, ranging from 5–10% of all behaviors recorded.
Figure 4shows the comparison between the four seasons:
Figure 4.
The average percentage of occurrence (with the standard error of the mean) for the four most
occurring classes of behavior (x-axis) across the four seasons. Dierent letters represent significant
dierences (p<0.05) between the seasons, while the same letters represent no significant dierence.
J. Zool. Bot. Gard. 2020,17
All four classes of behaviors tested for dierences across the four seasons showed a statistically
significant eect: Active (x
23
=123.230, p<0.001), Forage (x
23
=14.949, p=0.002), Inactive (
x23=115.395
,
p<0.001), and Stereotypy (x
23
=133.534, p<0.001). For Active, post-hoc tests showed a significant
dierence when comparing the winter to all other seasons and also the spring to both the summer
and fall (p<0.05 for all). Active increased from 11.2% (SE =0.9) in the winter to 19.5% (SE =1.1)
in the spring, increased to 32.5% (SE =2.3) in the summer, and increased to 35.2% (SE =1.8) in the
spring. For Forage, post-hoc tests showed a significant dierence when comparing the spring to both
the winter and fall (p<0.05 for both). Forage increased from 6.5% (SE =0.9) in the winter to 9.0%
(
SE =0.9
) in the spring, decreased to 7.6% (SE =1.3) in the summer, and decreased to 7.3% (SE =1.0)
in the spring. For Inactive, post-hoc tests showed a significant dierence when comparing the winter
to all other seasons and the spring to the summer (p<0.05 for all). Inactive decreased from 77.4%
(
SE =1.7
) in the winter to 56.8% (SE =1.9) in the spring, decreased to 41.2% (SE =3.1) in the summer,
and increased to 48.2% (SE =2.3) in the spring. For Stereotypy, post-hoc tests showed a significant
dierence when comparing the winter to all other seasons and also the summer to both the spring and
fall (p<0.05 for all). Stereotypy increased from 0.3% (SE =0.1) in the winter to 9.0% (SE =0.9) in the
spring, increased to 13.8% (SE =1.5) in the summer, and decreased to 2.0% (SE =0.3) in the spring.
To further examine the behavioral dierences that occurred seasonally, we compared two months
(January and July), which in the wild would be representative of winter hibernation and summer
activity periods, respectively. Figure 5shows the comparison between the two combined January
months and July:
Figure 5.
The average percentage of occurrence (with the standard error of the mean) for the four most
occurring classes of behavior (x-axis) for January (2010 +2011) compared to July (2010). Solid bars with
* represent significant dierences (p<0.001).
Three of the four classes of behaviors tested for dierences between January and July showed
a statistically significant eect: Active (U
138
=1265, p<0.001), Inactive (U
138
=1145, p<0.001),
and Stereotypy (U
138
=783.5, p<0.001). Between January and July, Active increased from 9.9%
(
SE =1.5
) to 29.5% (SE =3.4), Inactive decreased from 77.2% (SE =3.1) to 41.5% (SE =5.0), and Stereotypy
increased from 0.2% (SE =0.2) to 17% (SE =2.6).
Figure 6shows the hour-to-hour activity for the two combined January months and July.
J. Zool. Bot. Gard. 2020,18
Figure 6.
The average percentage of occurrence for the four most occurring classes of behavior for
each hour of observation (x-axis) during January (
top graph
) and July (
bottom graph
). The month of
January included observations from 09:00–16:00 h, while the month of July included observations from
09:00–18:00 h, due to the extended facility hours.
In the January months (both 2010 and 2011), when the bears were observed in the on-view area
of the exhibit from 09:00–16:00 h, Inactive occurred from the morning until 13:00 for >90% of all
observations. As Inactive decreased to ~30% by the 15:00–16:00 h period of observation, both Active and
Forage increased from 11.6% (Active) and 5.4% (Forage) to 22.3% and 22.4%, respectively. During July,
Inactive remained below 20% except for during the 10:00–11:00 h (35.3%) and 11:00–12:00 h (28.3%)
periods, and then later increased, beginning at 15:00–16:00 h from 49.5% to 91.1% and 100% during the
16:00–17:00 and 17:00–18:00 h periods, respectively. Active, Forage, and Stereotypy showed two peaks
in activity, with Active beginning high (39.2%) from 09:00–10:00 h, decreasing, and then peaking to their
highest occurrence from 14:00–15:00 h at 67.5%. Forage occurred in its highest frequency during the
11:00–12:00 h (22.3%) and the 15:00–16:00 h periods (9.8%). Stereotypy occurred in highest frequency
from 10:00–11:00 h (48.4%), decreased, and then peaked again to 28.6% during the 13:00–14:00 h period
of observation.
J. Zool. Bot. Gard. 2020,19
4. Discussion
4.1. Seasonal Activity
The zoo-housed bears in this study showed considerable variability in their behaviors throughout
the year, with the majority of their winter spent being inactive (hibernation period), and active behaviors
increasing toward the summer/fall starting in April. As mentioned earlier, this is similar to their wild
counterparts, depending on a variety of factors, including food availability, weather, and amount of
daylight. Both circannual and circadian rhythms are known to be entrainable to a variety of stimuli,
including food [
54
]. Although Ware et al. [
20
] have documented that the circannual rhythm of brown
bears appears to be entrained by photoperiod zeitgebers, they and others have also noted that both
the daily and seasonal activity of brown bears is likely most sensitive to food availability, as opposed
to daylength or temperature [
18
]. In one study, a wild population of grizzly bears in Slovenia were
supplemented with large quantities of corn during denning months and found that they denned
for significantly shorter periods and abandoned dens more frequently than bears living at the same
latitude without the corn subsidies [55].
Stereotypies only emerged for the bears in this study for three months: May–July. During these
months, stereotypic activity, primarily in the form of pacing, occurred for ~17–20% of their monthly
activity, as opposed to ~3% or less of their monthly activity outside of these months. Stereotypies in
captive bears, and more generally, in carnivores have been argued to have an appetitive function,
related to their natural foraging behavior [
36
,
37
]. Captive bears are known to exhibit some of the
highest levels of stereotypies, which have been directly correlated with home-range size, and with
zoo-housed polar bears having some of the highest frequency of stereotypies and largest home-range
sizes for any zoo-housed carnivore [
56
]. It is likely that the low level of stereotypic activity for the
bears in this study was related to being fed multiple times a day (2 or 3 times) and an environmental
enrichment program directed at reducing this suite of behaviors, which have both been associated
with lower levels of stereotypies in bears [24,26].
The emergence of stereotypies from May–July for zoo-housed bears may be less clear, however;
it coincides with the breeding season for grizzly bears when, typically, wild grizzlies would be foraging
less [
57
]. Other researchers have shown a similar occurrence in a solitary zoo-housed American black
bear (Ursus americanus) [
58
]. In their study, stereotypies increased in prevalence during the months
of May through July, the pacing/circling response observed changed in form and location to areas
closer to a female brown bear exhibit, and feeding enrichment was less eective at deterring the
stereotypic activity. Carlstead and Seidensticker [
58
] were able to eectively intervene on the black
bear’s stereotypies by introducing bear odors as a form of environmental enrichment.
4.2. Daily Activity
As observed by comparing the months of January and July, the daily activity of the bears in this
study showed considerable variability that corresponded with the season. In January, the bears were
primarily inactive, increasing in activity and eventual foraging behaviors toward the largest 15:00 h
daily feed. In July, when stereotypies accounted for 17% of their monthly activity, stereotypic activity
showed two spikes: One leading to the 11:00 h feeding time, and the other increasing to the 15:00 h
feeding time. Although, as noted above, mate-seeking behavior may be causally related to the May
through July occurrence of stereotypies, the times at which these stereotypies occurred still appeared
entrained to the feeding schedules. Past research has shown similar patterns for stereotypic pacing in
zoo bears, with pacing occurring in anticipation of food events and reduced as a result of providing
multiple feeding opportunities [26,37,5961].
While the relationship between stereotypies, general activity, and feeding schedules for zoo-housed
animals is less clear, it appears that many aspects of feeding schedules and feeding enrichment directly
entrain the circadian rhythms of those captive animals. Aside from the use of multiple feedings and
environmental enrichment previously discussed, simply changing the predictability/variability of
J. Zool. Bot. Gard. 2020,110
feeding events is eective at increasing general activity and reducing abnormal behaviors, such as
stereotypies [
60
,
61
]. In addition, grizzlies will choose to engage in foraging-related activity over freely
distributed feeding opportunities (i.e., contrafreeloading) [
62
]. By attending to when events occur
both seasonally and daily, we are better suited to understand the relationship between environmental
events, species-typical behaviors, and the behavior of zoo-housed brown bears.
4.3. Captive Grizzly Bear Activity Concluded
The behavioral patterns of zoo-housed bears are related to both the ways in which those bears
are exhibited and the natural behaviors of their wild counterparts. Studying both the seasonal and
daily activity of captive bears allows us to better understand how to manage zoo-housed bears,
which includes how circannual and circadian rhythms are entrained by environmental events. Equally
so, academicians, conservationists, and researchers should look to the behavior of captive bears and
other zoo-housed animals as a means to better understand the causal factors responsible for the
behaviors they observe in the wild. Zoos provide a unique environment for the study of bears, since
direct observation or experimentation of variables related to bear behavior is otherwise dicult in the
wild. While most zoological facilities are limited by the number of individuals for any one species
housed, and care should be taken in generalizing results beyond the settings or subjects studied, such
research can be critical for fostering any animal research endeavors. Done successfully, behavioral
research conducted in zoos can produce information that directly benefits our understanding of bear
behavior, as well as how to manage those zoo-housed bears [
63
]. Mutual collaborations between
scientists and practitioners should foster new research ideas, new management techniques, and new
ways to benefit the welfare and conservation of all bears.
Author Contributions:
Conceptualization, E.J.F.; methodology, E.J.F.; software, E.J.F.; formal analysis, E.J.F.;
investigation, E.J.F.; resources, E.J.F., E.Y., and N.A.; data curation, E.J.F.; writing—original draft preparation, E.J.F.,
E.Y., and N.A.; writing—review and editing, E.J.F., E.Y., and N.A.; project administration, E.J.F. All authors have
read and agreed to the published version of the manuscript.
Funding:
This study was completed while the first author was funded by a National Science Foundation
Postdoctoral Fellowship in the Psychology Department at the University of Washington.
Acknowledgments:
The authors would like to thank all the Behavioral Enrichment Animal Research (BEAR)
group’s Research Assistants for help in collecting the data. The authors would also like to thank the Woodland
Park Zoo stafor making this research possible and assisting in its implementation.
Conflicts of Interest:
The authors declare no conflict of interest. The funders had no role in the design of the
study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to
the results.
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2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
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(CC BY) license (http://creativecommons.org/licenses/by/4.0/).
... It has been noted that blue lights used in reverse cycle light systems may negatively impact activity and health [72]. Seasonality is evident in many captive species including African elephants (Loxodonta africana) [74], grizzly bears (Ursus arctos horribilis) [75], Rothschild's giraffes (Giraffa camelopardalis rothschildi) [76], and ring-tailed lemurs (Lemur catta) [77], and this needs to be factored in when using behavioral measures as indicators of welfare. For example, in some species, inactivity may be observed more frequently during winter due to innate hibernation behaviors [75] while other species may become more active [78]. ...
... Seasonality is evident in many captive species including African elephants (Loxodonta africana) [74], grizzly bears (Ursus arctos horribilis) [75], Rothschild's giraffes (Giraffa camelopardalis rothschildi) [76], and ring-tailed lemurs (Lemur catta) [77], and this needs to be factored in when using behavioral measures as indicators of welfare. For example, in some species, inactivity may be observed more frequently during winter due to innate hibernation behaviors [75] while other species may become more active [78]. Some animals might spend less time feeding and more time lying down during the warmer months [74]. ...
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Zoos are increasingly implementing formalized animal welfare assessment programs to allow monitoring of welfare over time, as well as to aid in resource prioritization. These programs tend to rely on assessment tools that incorporate resource-based and observational animal-focused measures. A narrative review of the literature was conducted to bring together recent studies examining welfare assessment methods in zoo animals. A summary of these methods is provided, with advantages and limitations of the approaches presented. We then highlight practical considerations with respect to implementation of these tools into practice, for example scoring schemes, weighting of criteria, and innate animal factors for consideration. It is concluded that there would be value in standardizing guidelines for development of welfare assessment tools since zoo accreditation bodies rarely prescribe these. There is also a need to develop taxon or species-specific assessment tools to complement more generic processes and more directly inform welfare management.
... Significant variations in behavior of zoo animals based on season and time of day are documented in the literature. This seasonality is evident in captive species including African elephants (Loxodonta africana) [73], Grizzly bears (Ursus Arctos Horribilis) [74], Rothschild's giraffes (Giraffa camelopardalis rothschildi) [75] and ring-tailed lemurs (Lemur catta) [76], highlighting the need for caution when using behavioral measures as indicators of welfare. For example, in some species, inactivity may be observed more frequently during winter to reflect innate hibernation behaviors [74] where other species may become more active [77]. ...
... This seasonality is evident in captive species including African elephants (Loxodonta africana) [73], Grizzly bears (Ursus Arctos Horribilis) [74], Rothschild's giraffes (Giraffa camelopardalis rothschildi) [75] and ring-tailed lemurs (Lemur catta) [76], highlighting the need for caution when using behavioral measures as indicators of welfare. For example, in some species, inactivity may be observed more frequently during winter to reflect innate hibernation behaviors [74] where other species may become more active [77]. Some animals might spend less time feeding and more time lying down during the warmer months [73]. ...
Preprint
Zoos are increasingly putting in place formalized animal welfare assessment programs to allow monitoring of welfare over time, as well as to aid in resource prioritization. These programs tend to rely on assessment tools that incorporate resource-based and observational animal- focused measures since it is rarely feasible to obtain measures of physiology in zoo-housed animals. A range of assessment tools are available which commonly have a basis in the Five Domains framework. A comprehensive review of the literature was conducted to bring together recent studies examining welfare assessment methods in zoo animals. A summary of these methods is provided with advantages and limitations of the approach es presented. We then highlight practical considerations with respect to implementation of these tools into practice, for example scoring schemes, weighting of criteria, and innate animal factors for consideration. It is concluded that would be value in standardizing guidelines for development of welfare assessment tools since zoo accreditation bodies rarely prescribe these. There is also a need to develop taxon or species- specific assessment tools to inform welfare management.
... For example, a sloth bear housed at a zoo in India was observed to be more active in the winter (December-February) than the spring (March-May; Prajapati & Koli, 2020). Grizzly bears at Woodland Park Zoo in Seattle demonstrated higher pacing rates in the spring/summer (May-July) and higher activity levels in summer/fall (June-November; Fernandez et al., 2020). A black bear paced in different locations in the exhibit at different times of year, possibly in response to differing motivations between the seasons, such as mate-seeking behavior in spring/summer (May-July) and foraging in late summer/fall (August-November) (Carlstead & Seidensticker, 1991). ...
... On warmer winter days, tropical bears were given access to their outdoor habitats, and on those days, their foraging rates were likely similar to other times of year. Other studies of bears in zoos have found variation in rates of foraging and stereotypy by season and visitor presence (Fernandez et al., 2020;Liu et al., 2017;Soriano et al., 2013), but we found that rates of foraging, stereotypy and social behaviors did not vary by season, crowd size, or daily attendance. ...
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In natural environments, bear behavior follows seasonal patterns but the zoo environment differs from the natural environment in several ways, including the presence of zoo visitors. Although typically difficult to disentangle, we were able to tease apart the effects of seasonal changes and visitor density on the visibility and behavior of 10 bears representing five species housed at Cleveland Metroparks Zoo due to the disruption caused by COVID-19. We conducted a longitudinal bear behavior monitoring project from June, 2017-November, 2020. Bears were more visible in the spring and in the presence of visitors, locomoted more and were less inactive when large crowds were present, foraged and locomoted more when it was earlier in the day, and locomoted more at higher temperatures. There were limited differences in bear visibility to observers between 2020 (when the zoo was temporarily closed to visitors) and the previous three years. There were no differences in rates of stereotypy or social behavior across seasons, crowds, or daily attendance categories. Based on these limited differences, neither season nor visitor density seemed to have an apparent effect on bear behavior or welfare.
... This marks an important guideline in the species selection criteria, considering that alterations in these cycles can cause certain problems, not only in the animals but also in the plants, such as alterations in the immune system or changes in their morphology [36,37]. In the care and management of certain animal species where seasonal cycles are very important, being able to emulate these cycles would be essential for their well-being and behavioral development [38]. ...
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The detailed evaluation of environmental parameters can be a great tool for the optimal selection and location of vegetable species, not only in vegetable production facilities and greenhouses but also in zoological and botanical gardens, which frequently maintain delicate and exotic plant species with strict environmental requirements in immersive exhibits where conditions can vary remarkably. This study, developed at an indoor zoological garden (Biodomo—Parque de las Ciencias de Granada, Spain), evaluates a sampling protocol for the determination of seven environmental parameters: daily light integral (DLI) was determined at nine different locations of the facility using a portable Light Quantum SQ-500 sensor; air temperature, atmospheric pressure, and air relative humidity were measured using a fixed ATMOS14 sensor; and soil temperature, soil water content, and soil conductivity were determined using a fixed TEROS12 sensor. Values recorded for DLI showed statistically significant variations across the nine different sampling locations, as well as between the different months in all sampling spots. Significant variations were also detected across the 12 months of study for the rest of environmental parameters evaluated, and correlations were found between the studied parameters, with the correlation between soil and air temperature the strongest (rs = 0.758) and soil temperature significantly superior to air temperature. The methodology described in this study can be easily reproduced in similar indoor zoological and botanical facilities, increasing the knowledge of the environmental conditions, and allowing corrections that could improve species selection, location, and management.
... Resting is seen as a state of regeneration in which the organism can gain new strength for the coming challenges of activity. Life is therefore a circadian sequence of rest and activity, oscillating daily (around 24 h), seasonally or circannually [1,7,8]. To better understand the biology and natural needs of a species, these restactivity cycles have recently been increasingly studied in various mammals (for example, by [9][10][11][12]). ...
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Mammals are constantly exposed to exogenous and endogenous influences that affect their behaviour and daily activity. Light and temperature, as well as anthropogenic factors such as husbandry routines, visitors, and feeding schedules are potential influences on animals in zoological gardens. In order to investigate the effects of some of these factors on animal behaviour, observational studies based on the analyses of activity budgets can be used. In this study, the daily and nightly activity budgets of six lions (Panthera leo) and five cheetahs (Acinonyx jubatus) from four EAZA institutions were investigated. Focused on the influencing factor light and feeding, we analysed these activity budgets descriptively. Behaviour was recorded and analysed during the winter months over an observation period of 14 days and 14 nights using infrared-sensitive cameras. Our results show that lions and cheetahs exhibit activity peaks at crepuscular and feeding times, regardless of husbandry. Thus, lions in captivity shift nocturnal behaviour familiar from the wild to crepuscular and diurnal times. In cheetahs, in contrast, captive and wild individuals show similar 24hr behavioural rhythms. The resting behaviour of both species is more pronounced at night, with cheetahs having a shorter overall sleep duration than lions. This study describes the results of the examined animals and is not predictive. Nevertheless, the results of this study make an important contribution to gaining knowledge about possible factors influencing the behaviour of lions and cheetahs in zoos and offer implications that could be useful for improving husbandry and management.
... The degree of exhibit naturalism might also differ across the sites. Seasonal changes in behavior have been documented in other studies of zoo bears [41,42], and seasonal changes in behaviors are well-documented in a number of bear species in the wild (see [7,13] for summaries). ...
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Long-term evaluations of whether modern zoological exhibits help to maintain variation in the behavior of zoo animals are lacking despite the hope that animals avoid falling into monotonous patterns of behavior or boredom. This study evaluated changes in behavior and habitat use over multi-year periods in nine individuals of five bear species at two zoological facilities. Behavioral data gathered over months to years were analyzed graphically for trends in the direction of change. The habitat use dynamics were assessed graphically by looking for trends in the entropy values over time. We found that the activity budgets remained diverse and were dynamic over time, more so in younger compared to older bears. Changes in behavior suggesting positive welfare were observed, while changes that may reflect declining welfare seemed more likely to be due to age or seasonality. The observed behavioral changes suggest that the bears did not become bored with their habitats; there was likely one to several hours of daily variation in behavior, and stereotypy was rare. The diversity in the habitat use decreased over time as the animals settled into patterns of use reflecting preferences for certain areas of their habitats.
... Bears experiencing torpor are easily disturbed, and studies in the wild show that disturbances during torpor or 'hibernation' may result in metabolic derangements and activity for several days [43]. For zoo bears experiencing daily disturbances due to husbandry routines and visitor activity, achieving torpor may not be possible, even when bears demonstrate significant behavioural inactivity (e.g., [71]). Allowing bears to hibernate requires the provision of appropriate environmental provisions and a secluded and undisturbed environment [72]. ...
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Animal welfare assessments are essential for the identification of welfare hazards and benchmarking of welfare improvements, though welfare assessments for zoo species are lacking. Bears are commonly housed in zoos but currently no composite welfare assessment tool exists for captive bears. This study describes the development of such a tool for use across hibernating bear species. A draft tool was developed using indicators derived from the literature and a modified Delphi analysis with an international group of bear keepers. A total of 18 bear keepers from 12 zoos were recruited to trial the tool on 24 brown bears and American black bears. The participating keepers assessed their bears three times across a period of nine days. Intraclass correlation coefficients analysis was used to analyse inter-, intra-rater and item reliability. The inter- and intra-rater reliability showed good to excellent levels of agreement (>0.7, p < 0.05). Item reliability was also assessed and showed good to excellent levels of agreement (>0.75, p < 0.05). The resulting bear welfare assessment is an important step in identifying and understanding challenges to bear welfare in captivity.
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Repetitive pacing behavior is exhibited by many species in zoos and is particularly prevalent in carnivores with large home ranges, such as bears. Pacing can be a behavioral indicator of poor welfare, however, understanding this behavior can be challenging. As many bears that pace are singly housed, efforts to systematically examine and ameliorate pacing may be strengthened by multi-institutional studies. However, there is currently no standardized method to quantify pacing, which makes cross-institutional analyses of causal factors and intervening measures challenging. The purpose of this study was to compare multiple sampling methods and definitions for quantifying pacing in bears to understand how they affect outcome measures. We analyzed video recordings of two grizzly and two black bears pacing, using three sampling methods (continuous, instantaneous 30-s interval, instantaneous 1-min interval), and three definitions of pacing (AB—two repetitions of the path, ABA—three repetitions, ABAB—four repetitions). A generalized linear mixed model revealed that continuous and instantaneous 30-s interval methods captured more pacing than instantaneous 1-min methods, and definitions captured a decreasing amount of pacing from AB to ABA to ABAB. AB also captured the highest number of pacing bouts. The importance of comparability across institutions is growing, and a standard methodology and definition for recording pacing would be useful. We suggest that the combination of instantaneous sampling and the ABA definition presents a good balance between capturing the right data and being flexible enough for a variety of institutions to implement. Research Highlights • We found that different sampling methods and definitions used to observe pacing in bears do affect the amount of pacing behavior recorded. • We recommend using instantaneous sampling and the ABA definition of pacing for bear behavior studies.
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Zoos are increasingly putting in place formalized animal welfare assessment programs to allow monitoring of welfare over time, as well as to aid in resource prioritization. These programs tend to rely on assessment tools that incorporate resource-based and observational animal- focused measures since it is rarely feasible to obtain measures of physiology in zoo-housed animals. A range of assessment tools are available which commonly have a basis in the Five Domains framework. A comprehensive review of the literature was conducted to bring together recent studies examining welfare assessment methods in zoo animals. A summary of these methods is provided with advantages and limitations of the approach es presented. We then highlight practical considerations with respect to implementation of these tools into practice, for example scoring schemes, weighting of criteria, and innate animal factors for consideration. It is concluded that would be value in standardizing guidelines for development of welfare assessment tools since zoo accreditation bodies rarely prescribe these. There is also a need to develop taxon or species- specific assessment tools to inform welfare management.
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Modern zoos strive to educate visitors about zoo animals and their wild counterparts' conservation needs while fostering appreciation for wildlife in general. This research review examines how zoos influence those who visit them. Much of the research to-date examines zoo visitors' behaviors and perceptions in relation to specific exhibits, animals, and/or programs. In general, visitors have more positive perceptions and behaviors about zoos, their animals, and conservation initiatives the more they interact with animals, naturalistic exhibits, and zoo programming/staff. Furthermore, zoo visitors are receptive to conservation messaging and initiatives at zoos and are more likely to participate in on-site conservation opportunities as opposed to after their visits. The research also suggests that repeat visitors are even more inclined to seek out conservation efforts compared to those visiting zoos for the first time. While current research suggests that repeat visitors are more likely to engage in conservation efforts, little is known about causal factors related to such findings, and almost no research exists to-date comparing the conservation efforts of visitors vs. non-visitors. This latter comparison will likely play a greater role in future zoo visitor research, since it poses one of the most important metrics for evaluating the specific effects visiting a zoo can have on people engaging in conservation efforts in general.
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Large quantities of food subsidies provided by humans to animal communities have the potential to change a variety of animal life traits, including denning behaviour of facultative hibernators like bears. Brown bears Ursus arctos regularly use anthropogenic food, but it has remained unclear if human food subsidies affect their hibernation and denning behaviour, despite the consequences this could have for bear interactions with humans and other species. We studied denning behaviour of European brown bears in Slovenia, where intensive supplemental feeding with corn is practiced throughout the year, including winter. We used GPS telemetry data to locate den sites and to monitor bear denning chronology. We conducted a meta-analysis to compare our results with other bear populations across Europe, Asia and North America. A consistent relationship between latitude and time spent denning was observed for male and female brown bears across the species’ range (for each degree of latitude northwards, denning period increased for 3.1 days), and males on average denned 10.3 days longer than females throughout the latitudinal gradient. However, our study area deviated strongly from regions where supplemental feeding was not practiced. In Slovenia, denning period averaged 82 days for females and 57 days for males, which was 45 and 56% shorter compared to the time predicted for this latitude, respectively. We also observed regular den abandonments (61% of bears abandoned dens, on average 1.9 times per winter). During the winter period bears increased use of supplemental feeding sites for 61% compared to the non-denning period. We conclude that the availability of anthropogenic food is an important driver of denning behaviour in brown bears. Reduction in the denning period increases the potential for bear interactions with other species, including humans, and we highlight possible management and ecological implications of this human-caused perturbation to denning behaviour of wild ursids.
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Hibernation has been a key area of research for several decades, essentially in small mammals in the laboratory, yet we know very little about what triggers or ends it in the wild. Do climatic factors, an internal biological clock, or physiological processes dominate? Using state-of-the-art tracking and monitoring technology on fourteen free-ranging brown bears over three winters, we recorded movement, heart rate (HR), heart rate variability (HRV), body temperature (T b ), physical activity, ambient temperature (T A ), and snow depth to identify the drivers of the start and end of hibernation. We used behavioral change point analyses to estimate the start and end of hibernation and convergent cross mapping to identify the causal interactions between the ecological and physiological variables over time. To our knowledge, we have built the first chronology of both ecological and physiological events from before the start to the end of hibernation in the field. Activity, HR, and T b started to drop slowly several weeks before den entry. Bears entered the den when snow arrived and when ambient temperature reached 0 °C. HRV, taken as a proxy of sympathetic nervous system activity, dropped dramatically once the bear entered the den. This indirectly suggests that denning is tightly coupled to metabolic suppression. During arousal, the unexpected early rise in T b (two months before den exit) was driven by T A , but was independent of HRV. The difference between T b and T A decreased gradually suggesting that bears were not thermoconforming. HRV increased only three weeks before exit, indicating that late activation of the sympathetic nervous system likely finalized restoration of euthermic metabolism. Interestingly, it was not until T A reached the presumed lower critical temperature, likely indicating that the bears were seeking thermoneutrality, that they exited the den. We conclude that brown bear hibernation was initiated primarily by environmental cues, but terminated by physiological cues.
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Building Ethical Arks.- Defining Animal Welfare.- Welfare Metrics Applied.- Wellness as Welfare.- Psychology & Animal Welfare.- Environmental Enrichment.- Behavior Analysis & Training.- Designing for Animal Welfare.- Launching Ethical Ark.- References.
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