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; email@example.com
3Happy Hollow Park & Zoo, San Jose, CA 95112, USA; firstname.lastname@example.org
*Correspondence: email@example.com; Tel.: +61-206-765-7350
Received: 23 July 2020; Accepted: 21 August 2020; Published: 25 August 2020
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
1.1. 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 [
]. Researchers have found
behavioral variation in subspecies and subpopulations based on geographic location, resource availability,
and human influence [
]. 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 [
]. Seasonal behavioral changes are
thought to be influenced by food availability [
], breeding [
], age [
], and sex [
]. 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
], radio collar tracking [
], observations in non-natural environments (e.g., zoos), or
a combination of two or more methods .
With respect to their daily activity, brown bears have primarily been found to be diurnal [
with peaks of activity in the early morning and evening. Some subpopulations have also been
reported to be crepuscular or nocturnal [
]. A large proportion of their daily waking activity is
thought to be foraging and eating, with bouts of rest and travel [
]. Brown bears have shown
ﬂexibility in their daily activity based on weather [
], light levels [
], age [
], 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
]. 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 [
]. Likewise, brown bear enclosures show considerable variability,
from small, artiﬁcial enclosures to large, naturalistic exhibits [
]. Some facilities have on-exhibit
and oﬀ-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 [
]. 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 [
]. Stereotypies are attributed to
numerous factors, including sub-optimal environments, lack of environmental control, and species-typical
appetitive behavior [
]. 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 [
]. 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 [
]. 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 [48–52].
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 oﬀ-view outdoor exercise yard, ~410 m2, and a indoor
space, ~250 m
. 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).
On-view outdoor area of the exhibit, with Denali (left) and Keema (right) engaged in Lying
Down (Inactive). Photo credit: Scott Richardson.
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 oﬀ-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
leaf eater biscuits, Purina Omolene
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.
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 [
] 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
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.
Eating (Ea) Mouth contact with anything edible, including water.
Enriched Feeding (EF) Manipulating an enrichment device with food in it.
Interacting w/another bear (IOB) Any gesture to another bear without vocalization.
Vocalization (Vo) Vocalization; must occur while oriented to another bear.
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.
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
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.
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 [
] 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 diﬀerences for the four
classes of behavior were tested for seasonal diﬀerences (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 diﬀerences
) for the ANOVAs were found, post-hoc pairwise comparisons (using Dunn’s Method) were
implemented. Diﬀerences 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
diﬀerences 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
diﬀerences between the traditional winter (January) hibernation and summer (July) activity periods.
J. Zool. Bot. Gard. 2020,16
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%,
), 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.
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:
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. Diﬀerent letters represent signiﬁcant
diﬀerences (p<0.05) between the seasons, while the same letters represent no signiﬁcant diﬀerence.
J. Zool. Bot. Gard. 2020,17
All four classes of behaviors tested for diﬀerences across the four seasons showed a statistically
signiﬁcant eﬀect: Active (x
=123.230, p<0.001), Forage (x
=14.949, p=0.002), Inactive (
p<0.001), and Stereotypy (x
=133.534, p<0.001). For Active, post-hoc tests showed a signiﬁcant
diﬀerence 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 diﬀerence 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%
) 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 diﬀerence when comparing the winter
to all other seasons and the spring to the summer (p<0.05 for all). Inactive decreased from 77.4%
) 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
diﬀerence 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 diﬀerences 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:
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 diﬀerences (p<0.001).
Three of the four classes of behaviors tested for diﬀerences between January and July showed
a statistically signiﬁcant eﬀect: Active (U
=1265, p<0.001), Inactive (U
and Stereotypy (U
=783.5, p<0.001). Between January and July, Active increased from 9.9%
) 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
The average percentage of occurrence for the four most occurring classes of behavior for
each hour of observation (x-axis) during January (
) and July (
). 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
J. Zool. Bot. Gard. 2020,19
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 [
]. Although Ware et al. [
] 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 [
]. 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 .
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 [
]. 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 [
]. 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
]. Other researchers have shown a similar occurrence in a solitary zoo-housed American black
bear (Ursus americanus) [
]. 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 eﬀective at deterring the
stereotypic activity. Carlstead and Seidensticker [
] were able to eﬀectively 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 [26,37,59–61].
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 eﬀective at increasing general activity and reducing abnormal behaviors, such as
]. In addition, grizzlies will choose to engage in foraging-related activity over freely
distributed feeding opportunities (i.e., contrafreeloading) [
]. 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 diﬃcult 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 [
]. 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.
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.
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.
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 staﬀfor 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
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