Tool use, problem-solving, and the display of stereotypic behaviors in the brown bear (Ursus arctos)

Journal of Veterinary Behavior 17 (2017) 62e68

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Small Mammal/Wildlife Research

Tool use, problem-solving, and the display of stereotypic behaviors in the brown bear (Ursus arctos) Alexander J. Waroff a, Leticia Fanucchi b, Charles T. Robbins c, O. Lynne Nelson b, * a

College of Veterinary Medicine, Washington State University, Pullman, Washington College of Veterinary Medicine and Department of Veterinary Clinical Sciences, Washington State University, Pullman, Washington c School of the Environment and School of Biological Sciences, Washington State University, Pullman, Washington b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 29 March 2016 Received in revised form 2 November 2016 Accepted 9 November 2016 Available online 17 November 2016

Recent studies suggest that bears have relatively high cognitive capabilities. However, cognitive processes and problem-solving abilities remain relatively unexplored in bear species. We studied the capacity for 8 captive brown bears (Ursus arctos) to move and use inanimate objects to obtain a food reward. We recorded their behaviors during the problem-solving process using a behavioral ethogram. Three items, a large log, a small log, and a box, were placed in an outdoor enclosure. As the bears progressed through 3 stages of trials, they would need to manipulate the objects and displace them into the proper location and orientation to climb atop to reach a suspended food reward. Completion of the third and final stage was deemed to be evidence of tool use. Six of the 8 bears were capable of tool use. Most bears (>90% of trials) were successful in completing the final stage in <100 seconds. Bears exhibited behaviors such as head flips, pacing, and jumping as the trial length progressed and failure rate increased. Individual bears exhibited different tool preferences and techniques. The bears were capable of applying previously learned skills to novel items. The 2 bears that did not succeed at tool use were both free range before their relocation to the Washington State University Bear Research and Education Center; their prior history may have contributed to their inability to use tools. Ó 2016 Elsevier Inc. All rights reserved.

Keywords: cognition impatience

Introduction The ability to use tools is often used as an indicator of advanced cognition in animals. Extensive studies of the intelligence of social animals such as great apes (Schaik and Burkart, 2011) and nonprimate social animals such as corvids (Cheke et al., 2011), canids (Overall, 2011), and elephants (Foerder et al., 2011) continue to reveal an association between social living and problem-solving behaviors, including tool use. Studies suggest that social carnivores outperform nonsocial animals when presented with a problem requiring innovation (Borrego and Gaines, 2016). Brown bears (Ursus arctos) are raised for the first 2 to 3 years in a social environment and then lead minimally social lives communicating with one another primarily through physical and scent marking of their

* Address for reprint requests and correspondence: Dr. O. Lynne Nelson, Department of Veterinary Clinical Sciences, Washington State University, Pullman, WA 99164, USA. Tel: 509 335 0789; Fax: 509 335 0880. E-mail address: [email protected] (O.L. Nelson). http://dx.doi.org/10.1016/j.jveb.2016.11.003 1558-7878/Ó 2016 Elsevier Inc. All rights reserved.

environment as adults (Clapham, et al., 2013; Clapham et al., 2014; Sato et al., 2014). Interestingly, even polar bears (Ursus maritimus), which live almost entirely solitary lives as adults, still exhibit long distance social communication through scent marking (Owen et al., 2014). This makes the classification of bears as social or nonsocial difficult. American black bears (Ursus americanus) and brown bears are highly adaptable in seeking food (Lesmerises et al., 2015). Both black and brown bears learn their foraging strategies primarily through social interactions with their mothers during the first years of their life (Mazur and Seher, 2008; Gardner et al., 2014). In areas near human settlements, black bear cubs are tutored by their mothers to seek human-associated foods. They show great variability in specific strategies used depending on the individual litter and environmental factors (Mazur and Seher, 2008). This pattern of living in proximity to humans suggests plasticity in both learning and behavior when encountering a situation requiring problemsolving. Likewise, brown bears range widely across North America, Europe, and Asia and, therefore, are highly adaptable in exploiting a variety of habitats and foods (Haroldson et al., 2005;

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McCarthy et al., 2009; Ware et al., 2012; Fortin et al., 2013). The high level of resource adaptability by a relatively nonsocial species may require cognitive abilities most often associated with more social species (Finn et al., 2009). Bears are most closely related to canids, mustelids, and procyonids (Choi et al., 2010), which are known for their relatively highlevel cognitive abilities (Hall and Schaller, 1964; Michener, 2004; Overall, 2011). Similarly, bears have unusually large brains relative to their body size, even when compared to close phylogenetic relatives (Gittleman, 1999; Rushton and Ankey, 2000; Ware et al., 2013). Empirical research supports some relationship between a carnivore’s relative brain size and problem-solving ability (BensonAmram et al., 2016). Black bears have been recently shown to perform at a similar level to primates with respect to quantification, estimation, and counting (Vonk et al., 2012). These data raise the question of whether selective pressures beyond social living play a role in developing highly functioning cognitive capabilities. The great adaptability seen in black bears prompts additional questions about the cognitive capacity and capabilities of bears, which remain relatively unexplored. The most widely accepted definition of tool use is the revision of Alcock’s definition (1972) by Beck (2011) that states the following: “tool use is the external employment of an unattached environmental object to alter more efficiently the form, position, or condition of another object, another organism, or the user itself when the user holds or carries the tool during or just prior to use and is responsible for the proper and effective orientation of the tool.” According to this definition, tool use has been demonstrated in many species including corvids which manufactured tools out of wires to retrieve food (Bird and Emery, 2009; Cheke et al., 2011), elephants which positioned a box as a stepping stool to reach suspended food (Foerder et al., 2011), beavers which use sticks for communication (Thomsen et al., 2007), and bottlenose dolphins (Tursiops sp.) which manipulated sponges to create foraging opportunities (’Krützen et al., 2014). Many other mammals shown to use tools include mustelids (Hall and Schaller, 1964; Michener 2004) and primates (Gruber et al., 2010; Boose et al., 2013). Some species which rarely use tools in the wild readily use tools in a captive environment with ability that rivals that of chimpanzees’ (Pan troglodytes) (Emery and Clayton, 2009). Köhler (1925) described several stages of tool use and manufacture in chimpanzees and suspected problem-solving behavior when approaching novel problems. Suspected tool use has been documented in a free-ranging brown bear; however, the purpose and objective remain uncertain (Deecke, 2012). This study assessed whether captive brown bears have the ability to solve a problem by manipulating freely moveable objects to reach a food reward. Our observations in captive bears reveal that bears very often use physical force when approaching new problems which will lead to trial and error problem-solving. This type of learning is often observed when testing bear-resistant products (http://igbconline.org/bear-resistant-products/; http:// www.grizzlydiscoveryctr.org/research/product-testing/). When force does not work, bears often appear to demonstrate insightlike behavior, with individual variability. We hypothesized that brown bears have the ability to manipulate objects in their captive environment using them as tools to achieve a goal. We predicted that (1) bears would position large objects (logs and boxes) to obtain a food reward; (2) bears would initially go through trial and error until the concept was learned and, if successful, transfer this skill to different conditions and tools; (3) bears would show behaviors consistent with impatience and eventually abandon the experiment if unsuccessful at obtaining the food reward. We discuss evidence of tool usage in captive brown bears from a proximate perspective, with respect to the immediate environmental factors that may influence the behaviors.

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Methods Subjects Eight brown bears (N ¼ 8) were included in this study: 5 adult females, LU, KI, PE, CO, and OA (11-15 years of age) and 3 subadult males, RO, PA, and TA (3 years of age). Three of the adult females (LU, KI, and PE) were born in captivity and 2 (CO and OA) were relocated from free-ranging locations 3 years before this study. The subadult males were born in captivity. Three of the adult captiveborn females (LU, KI, and PE) had previous experience with positive reinforcement training for husbandry purposes. The remaining 5 bears did not. All animals were housed at the Washington State University Bear Research, Education, and Conservation Center and maintained in compliance with American Society of Mammologists guidelines (Sikes and Gannon, 2011) and the Bear Care and Colony Health Standard Operating Procedures approved by the Washington State University Institutional Animal Care and Use Committee (IACUC) (ASAF #3054). Enclosure and materials The bears were tested in 1 section of a large outdoor grassy 0.56-ha enclosure. A corner of the enclosure was used to construct four 7.6 m  7.6 m zones and one 15.2 m  1.8 m zone which were used to identify animal location and movement (Figure 1). The zones were marked on the shorn grass with white commercial paint (High Performance Enamel, Rust-Oleum Corporation, Vernon Hills, IL). An adjustable rope was suspended across the corner of the yard so that a food reward could be suspended above the center of zone 1 at heights ranging from 2 to 3 m. The height of the suspended food reward was adjusted to be 0.5 m beyond the reach of each individual bear when it was standing on the ground bipedally. Zone 1 contained the tools necessary to complete each trial including: a 0.57 m  0.57 m  0.57 m plastic enrichment box, a 0.33 m tall  0.64 m diameter large log round and a 0.4 m tall  0.5 m diameter small log round. A surveillance camera (Pan/tilt/zoom Esprit HD camera, Pelco, Surrey, BC, Canada) above the fence at zone 2 filmed the testing area. The behaviors were recorded using video that recorded the bears’ activity while in or near the 5 zones. The large log round was placed in the enclosure 1 week before beginning trials to habituate the bears to the new stimulus. The large log was the only item used for stages 1 and 2. The small log and box were added in stage 3 to determine if bears would apply previously learned knowledge to new or novel items. Procedures The trials began when the bear entered the enclosure in zone 5 and were terminated when the bear was no longer interested in the task and left the test area for >10 minutes, an arbitrary determination but appeared a rational cutoff as when (primarily the 2 previously free ranging) bears gave up on the test area, they did not return to interact for that trial set up. Trial success rate for stages 2 and 3 was based on intentional objective movement to retrieve reward. Intentional movement of the object was defined as the bear looking at the reward and object in succession followed by deliberate manual displacement and positioning of the object in the appropriate direction and location that would allow successful retrieval of the reward. If the bear did not obtain the reward through intentionally manipulating the object, the trial was considered a failure. The experimental design was divided into 3 stages.

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A.J. Waroff et al. / Journal of Veterinary Behavior 17 (2017) 62e68

Figure 1. Map of trial area layout and tools available. The top and left corners of the enclosure were bordered by a chain link fence. The bears entered through the gate at the top left corner. The reward and tools were located in the center of zone 1.

Stage 1 A large log round was placed beneath the suspended food reward (2 glazed doughnuts obtained from a local store). The bear was given the opportunity to climb onto the log and stand on its hind legs to obtain the reward for a total of 4 repetitions before advancing to stage 2 (Supplementary Figure 1). Stage 2 The log was balanced on its round side <2 m away from the suspended reward so that the bear had to displace the log onto its flat face before climbing atop and reaching the doughnuts as in stage 1 (Supplementary Figure 2). Initially, the displacement could be by trial and error, but in order for the bear to have a successful trail and advance to stage 3, it would have to demonstrate intentional and purposeful manipulation of the log into place for 3 trials. If the bear accidentally knocked the log into place trying to obtain the reward, the action was not considered to be intentional and the trial was not deemed as successful for understanding the concept of object manipulation. Stage 3dcriteria for tool use The bears were introduced to potentially useable novel items in addition to the large log. A plastic enrichment box and a smaller log round were introduced into the testing area. Additional nonusable items were added to the testing area including long logs ranging from 1 to 3 m in length and 10.16 cm  10.16 cm  1 m wooden posts. These additional items were used as discriminatory items to see if bears would manipulate these items as readily as the items that were potentially useful for problem-solving. The bears did occasionally touch the items, and doing so was recorded in the ethogram, but because this was a low frequency behavior, it was excluded from the statistical analysis. Stage 3 was designed to eliminate the possibility of accidental food retrieval (without object manipulation) to test our hypothesis that captive brown bears have the capacity to solve a problem by manipulating freely moveable objects to reach a food reward (tool use); stage 3 also tested the prediction that bears could transfer knowledge of the skill to novel items. The large log, small log, and enrichment box were placed at horizontal distances of >2 m from the suspended doughnuts. At

this distance, the bears would have to manipulate the objects in a specific manner requiring intentional positioning of an object under the doughnuts to retrieve the reward. This stage eliminated the possibility of accidental retrieval of the reward by unintentional log movement. Stage 3 also determined if the bears would use unassociated and novel items as tools in addition to the habituated large log round. Intentional manipulation of the objects to retrieve the reward was necessary to complete stage 3 (Supplementary Figures 3 and 4). The bear was deemed to definitively use a tool if stage 3 was successfully completed (Figure 2). Video recordings of all trials were reviewed by 2 independent observers. An ethogram was developed to record individual behaviors (Table 1) observed from video recordings. Behaviors were measured via scan sampling every 2 seconds as marked with * or an absolute count of a particular behavior was recorded as marked with # in Table 1. Percent agreement between the 2 observers was 90.1%.

Statistical analysis All analyses in this study were performed using IBM SPSS 23.0 (IBM Corporation, Armonk, NY). Descriptive statistics were calculated across success versus fail, total time, log manipulations, attempts at doughnuts, head flips, jumps, and line crosses. Jumps, line crosses, and head flips were all relatively uncommon behaviors. Many trials lacked these behaviors altogether resulting in a 0 value for the trial.

Figure 2. Flow chart of the 3-stage experimental design.

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Table 1 Ethogram of all behaviors recorded from video review of each trial Category

Behavior

Mutually exclusive states a Orientation Oriented toward gate a Orientation Oriented toward log/box a Orientation Oriented toward reward a Orientation Oriented elsewhere a Location Near gate a Location Near log and reward a Location In zone 2 a Location In zone 3 a Location In zone 4 Tool used Big log Tool used Small log Tool used Box Total time (s) N/A Nonmutually exclusive events a Behavior Partially on log a Behavior Fully on log b Behavior Manipulating log b Behavior Attempts at doughnut b Behavior Head flips a Exploration Behavior b Behavior Jump b Behavior Line crosses a b

Description Head position, body movements aligned toward entrance gate, includes sitting, standing, or running Head position, body movements aligned toward log/box in zone 1, visual, oral or attempts Head position, body position, visual or olfaction aligned toward suspended doughnut in zone 1 Head position, body movements not aligned with gate, log, or reward Time spent in zone 5 near entrance gate Time spent in zone 1 containing object log and reward doughnut Time spent in zone 2, closest zone to camera Time spent in zone 3, zone uphill from zone 1 and farthest from camera Time spent in zone 4, zone diagonal from zone 1 and uphill from zone 2 Big log used to reach doughnut Small log used to reach doughnut Box used to reach doughnut Length of trial from entrance of yard to success or fail One to three feet supported by log Full weight of bear supported by log Each time the bear touches and physically moves the log Reaching with snout or paws towards doughnut. Does not include distant olfaction Aggressively fast rotation of the head Examining the yard excluding gate, log, and reward. Includes olfaction, visual, oral while mobile or stationary Bear leaves contact with log and ground Number of times that bear moves across zone boundaries marked as lines in grass

Scan sampling recorded every 2 seconds. Total number recorded.

Spearman rank-order correlations were run to assess the relationship between successes versus fail and the behaviors during nonmutually exclusive events. Before the analyses, an examination of the scatterplot was conducted to observe monotonic relationships across the variables. This examination yielded evidence of monotonic, nonlinear relationships across the following variables: log manipulations, attempts at doughnuts, head flips, jumps, line crosses, successes, and total time. No transformations were performed. The data are presented as percentages and means. All analyses were conducted at a ¼ 0.05. Results Six of the 8 bears were capable of using tools to reach a specific goal. Four of these 6 bears used novel tools in stage 3 of the

experiment including an enrichment box and a small log. These tools had not been previously introduced to the bears (Figure 3). All bears were able to complete stage 1 and move to stage 2 at a success rate averaging 97% for all stage 1 trials across all bears. At stage 2, all bears had an overall success rate of 32% for all stage 2 trials, including 2 bears that did not complete the stage. All bears that were deemed successful at stage 2 were immediately successful at stage 3. The success rate for completing stage 3 was 100% for all bears and trials. In stage 2, the accidental retrieval of the reward consisted of unintentionally displacing the log or balancing and jumping from the log positioned on its round edge (without intentional manipulation). Sometimes, accidental retrieval was due to inadequate assessment of the reward height by the researchers. There were 19 trials ending as accidental reward retrievals compared to 25 trials ending as

Figure 3. Overview of trial successes and failures along with respective tool used in stage 3. *Letter “A” in stage 2 trials indicates the trials that bears achieved the reward by accident which included jumping from the log, unintentional displacement of the log, or inadequate assessment of reward height placement.^Lettering in stage 3 trials indicates the tool which was used to obtain the reward. Large log (LL), small log (SL), or box (B) were available during stage 3. CO trials 19 and 20 were excluded from statistical analysis since she never successfully completed stage 2.

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successful intentional object manipulation reward retrievals in stage 2. Failed trials (including accidental reward retrievals in stage 2) lasted twice as long (mean ¼ 72.5 seconds) as successful trials (mean ¼ 36.1 seconds). Two bears did not complete stage 2 and were not deemed successful for using a tool. One bear, CO, had a high rate of accidental retrieval of the food reward during stage 2 compared to the other bears, so it was difficult to ascertain if she truly had the ability to problem solve or if she was persistent in exploring the area, eventually creating a circumstance where the reward could be retrieved. To test this hypothesis, we allowed this bear to have 2 attempts at stage 3 to determine if she could manipulate the objects for a goal. The bear failed in both trial attempts. These 2 attempts at stage 3 were not included in statistical analyses. There was a significant negative correlation between the number of log manipulations and log contacts and between the numbers of reaching attempts for the reward with successful trials. Thus, the most successful bears made fewer individual attempts at the doughnuts and had fewer log manipulations (Table 2). Total time spent per trial had a significant negative correlation with success as trial length increased the bears became less likely to succeed (rs ¼.0.82, P < 0.008, n ¼ 114). Frequency of line crosses between zones (pacing) was nearly significantly (negatively) correlated with successful trials (P ¼ 0.054). Bears with a high number of attempts at the reward (and lower number of successes) demonstrated a significantly increased frequency of head flips, jumping, and line crossing from 1 zone to another. Likewise, head flips with line crosses and jumping with line crosses were significantly positively correlated. Bears that demonstrated behaviors associated with a lower trial success rate tended to try a number of differing positions and strategies. Out of 114 total trials, 73 (64%) were deemed as successful trials where the bear obtained the reward by proper utilization of the objects. Out of these 73 successful trials, only 7 (10%) lasted over 100 seconds. Most bears (>90% of trials) that succeeded did so in <100 seconds per trial. Total trial time was significantly positively correlated with head flips. Bears were more likely to demonstrate the head flipping behavior as trial time increased. The behavior is first apparent at <1 minute of trial time and becomes more frequent after 1-2 minutes of trial time. Head flips were observed in most (78%) trials running >4 minutes. Discussion Captive brown bears have the capacity to solve problems by manipulating freely movable objects, using them as tools, to obtain a food reward. Serial stages set the conditions that bears needed to acquire the concept of the problem. The completion of stage 3 was the criterion we used to establish that bears used tools. All bears Table 2 Correlations (Spearman correlation) of behaviors and events to one another and to trial successes (SPSS test) Log manipul Reward attempts Head flip Jump Line crosses Success

rs

0.01

n rs n rs n rs n rs n

77 0.08 77 0.12 77 0.04 77 0.28* 77

rs, Correlation coefficient. *P < 0.05; **P < 0.01.

Attempts

Head flip

Jump

Line crosses

0.22 114 0.19* 114 0.47* 114 0.22* 114

0.34** 114 0.5** 114 0.16 114

0.22* 114 0.17 114

0.18 114

that successfully completed stage 2 (which required an intentional log manipulation component) also successfully completed stage 3 in serial trials without failure. In stage 2, none of the bears intentionally manipulated the object to obtain the reward on the first trial. Most bears required several attempts at this stage, often creating random motions that accidentally displaced the object. Once the concept of object displacement was learned, bears were successful in completing this stage in succession. This suggested that the bears may first solve problems by trial and error, before cognitively adapting their behavior to solve the problem. The efficiency with which bears completed stage 3 suggests that a planned action led to success versus trial and error during this stage. We also found that brown bears were capable of using previously learned skills with novel items. As predicted, 4 of the 6 bears chose to manipulate novel objects in stage 3 that were not present for the first 2 stages of the study, supporting a problem-solving concept versus rote memory of performance. These bears also showed a variety in techniques and preferences in methodology. Each individual bear demonstrated alternative techniques for displacing the log, moving the tools, and reaching for the food reward. An example of these individual variances can be seen in Figure 3. In stage 3, bear KI opted to use the box for 2 of her 3 successful stage 3 trials. She not only had the capacity to use learned skills on novel tools, but this behavior suggests that she preferred to use the box for 2 of 3 trials, compared to bear PE, who opted to use only the large log. This capacity to use different tools for the same purpose is suggestive of an elaborated cognitive understanding of the environment. The individual difference in tool preference indicates that each bear, although presented with nearly identical stimuli, had alternative “high-level” or “offline” processing of the signal before producing the response to the stimuli, which could help explain the differences in tool preference (Toates, 2004). Two of the 8 bears did not progress successfully past stage 2 because they were not able to demonstrate purposeful movement of the log. Interestingly, the 2 bears that did not succeed were born in the wild and were later relocated to a captive environment. All 6 of the successful bears were born in captivity. There are many possible explanations for this finding. Three of the captive born bears had prior experience with training for husbandry procedures and may be more accepting or inquisitive regarding new experiences or routines. It is also possible that the captive born bears, in general, were accustomed and desensitized to numerous stimuli and variable situations that occur in captivity. The captive bears might have outperformed the wild bears due to a “captive bias” effect, where the captive environment is predictable and provisioning, and not necessarily due to a difference in cognitive ability between bear populations (Haslam, 2013). This experiment may have revealed information about the general attention span of captive brown bears. When presented with a problem, over 90% of all successful trials occurred in a relatively short time of <100 seconds. Beyond this time range, behaviors including head flipping, pacing, and abandoning the experimental setup were noted. Although little research has offered evidence of other specific behaviors which may indicate emotional states in bears, head swinging or head flipping has been associated with states of stress (Cremers and Geutes, 2012). We examined head swinging/head flipping in the context of problem-solving and found that head flips were more commonly demonstrated during longer trials where the bear did not succeed at obtaining the reward. It is possible that head swinging/head flipping, pacing, and abandoning the trail were exacerbated by delayed expected food reward, as observed in pigs (Haskell et al., 2000) and primates (Lyons et al., 2000). Another possibility is that the observed behaviors in our bears were not truly stereotypy but similar to perseveration behaviors observed in extinction trials (Vickery and Mason, 2005).

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Head flipping was significantly correlated with attempts at retrieving the doughnuts, jumps, and line crosses (or pacing). We found correlations between all stereotypic behaviors including pacing, head flips with prolonged trial length, and behaviors related to failures such as increased attempts at reward retrieval and jumps. After about 1-2 minutes of failing to succeed, head flips increased in frequency and a tendency to try new behaviors developed such as jumping toward the reward, suggesting that in these particular bears, attention span or patience is rather short when faced with a new or difficult problem. A proximate approach on problem-solving and tool use in bears encompasses Thorndike’s (1933) theory of connectionism and the aftereffects of a connection. The theory suggests that if a stimulus results in a favorable reward then the 2 become intimately connected and function more like a unit. If a bear is rewarded for learning, then it is more likely to offer behaviors that result in learning. This is a classic example of instrumental conditioning. The response(s) to these stimuli included attempts at reward, manipulation of tools during the trial, and trying new strategies such as alternate tool choice when previous strategies had failed. This may explain the relatively low success rate of 36% of all trails during stage 2 (versus stage 3 with a success rate of 100% after reinforcement of learned strategies even when presented with novel items). Generally stated, as bears are rewarded for learning, they become better, faster, and more efficient learners, a characteristic commonly noted for species that are highly cognitive. Problem-solving and tool use in bears can also be supported through an ultimate view. Bears are omnivores and can feed on a wide variety of food types, each filling different components of bears’ nutritional needs. An omnivorous diet and varying metabolic demands throughout the season requires diverse foraging strategies which initially are learned from social interactions with the mother (Mazur and Seher, 2008; Gardner et al., 2014). An adaptable and dynamic capacity for learning multiple foraging strategies can be advantageous to surviving selective pressures when annual food availability changes over a bear’s long life span. Research on the cognitive capacity of brown bears has potential applications to wildlife conservation, human and animal safety, management of free-ranging bears, and the welfare of captive animals. For example, assessing bear problem-solving skills may help to recognize how bears adapt to selective pressures such as climate change, fluctuating food resources, and human encroachment. Understanding how captive bears interact with their environment may help to improve their management and welfare by enhancing keeperebear interactions. Creating behavioral and environmental enrichment for each species is critical for the prevention of stereotypic behaviors that may indicate stress or distress. Although stereotypic behaviors may develop for a variety of reasons, they are commonly exhibited by captive animals that lack sufficient behavioral and environmental stimulation (Shepherdson et al., 2013). Conclusions Captive brown bears have the capacity to solve problems by manipulating freely moveable objects as tools to obtain a food reward. We found that brown bears were capable of applying previously learned skills on novel, newly introduced items. When unable to obtain a reward, specific classes of stereotypic behaviors became common. Acknowledgments Funding was provided by the College of Veterinary Medicine (CVM) Veterinary Research Fellowship Program and the Bear

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Research and Conservation Endowment. The authors thank Joy Erlenbach, Danielle Rivet, and Tenzin T. Lama and the other dedicated researchers at WSU’s Bear Research, Education and Conservation Center for their assistance in data collection and captive bear care. They would also like to acknowledge the anonymous manuscript reviewers; their efforts have greatly improved this work. Ethics statement This research was approved by Washington State University Bear Research and Education Center to be noninvasive and ethical. The idea for the paper was conceived by O. Lynne Nelson; the experiments were designed by A.J.W., O.L.N., L.F., and C.T.R. The experiments were performed by A.J.W., O.L.N., C.T.R., Joy Erlenbach, and Nicklas Waroff. The data were analyzed by A.J.W., A. J. Delgado, Tenzin T. Lama, O.L.N., and L.F. The article was written by A.J.W. and edited by O.L.N. and L.F. Conflict of interest The authors declare no conflict of interest. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.jveb.2016.11.003. References Alcock, J., 1972. The evolution of the use of tools by feeding animals. Evolution 26, 464e473. Beck, B., 2011. Animal Tool Behavior: The Use and Manufacture of Tools. Garland STPM Press, New York, NY, p. 5. Benson-Amram, S., Dantzer, B., Stricker, G., Swanson, E., Holekamp, K., 2016. Brain size predicts problem-solving ability in mammalian carnivores. Proc. Natl. Acad. Sci. U. S. A. 113 (9), 2532e2537. Bird, C., Emery, N., 2009. Insightful problem solving and creative tool modification by captive nontool-using rooks. Proc. Natl. Acad. Sci. U. S. A. 106 (25), 10370e 10375. Boose, K., White, F., Meinelt, A., 2013. Sex differences in tool use acquisition in bonobos (Pan paniscus). Am. J. Primatol. 75 (9), 917e926. Borrego, N., Gaines, M., 2016. Social carnivores outperform asocial carnivores on an innovative problem. Anim. Behav. 114, 21e26. Cheke, L., Bird, C., Clayton, N., 2011. Tool-use and instrumental learning in the Eurasian jay (Garrulus glandarius). Anim. Cogn. 14, 441e455. Choi, E., Kim, S., Ryu, S., Jang, K., Hwang, U., 2010. Mitochondrial genome phylogeny among Asiatic black bear Ursus thibetanus subspecies and comprehensive analysis of their control regions. Mitochondrial DNA 21 (3-4), 105e114. Clapham, M., Nevin, T., Ramsey, D., Rosell, F., 2014. Scent marking in wild brown bears: time investment, motor patterns and age-related development. Anim. Behav. 94, 107e116. Clapham, M., Nevin, T., Ramsey, D., Rosell, F., 2013. The function of strategic tree selectivity in the chemical signalling of brown bears. Anim. Behav. 85 (6), 1351e 1357. Cremers, P., Geutes, S., 2012. Stereotypic behavior in a male polar bear (Ursus maritimus). In: Proceedings of Measuring Behavior. Utrecht, The Netherlands, August 28e31. Deecke, V., 2012. Tool-use in the brown bear (Ursus arctos). Anim. Cogn. 15 (4), 725e 730. Emery, N., Clayton, S., 2009. Tool use and physical cognition in birds and mammals. Curr. Opin. Neurobiol. 19, 27e33. Finn, J., Tregenza, T., Norman, M., 2009. Defensive tool use in a coconut-carrying octopus. Curr. Biol. 19 (23), R1069eR1070. Foerder, P., Galloway, M., Barthel, T., Moor, D., Reiss, D., 2011. Insightful problem solving in an Asian elephant. PLoS One 6 (8), 1e7. Fortin, J., Ware, J., Jansen, H., Schwartz, C., Robbins, C., 2013. Temporal niche switching by grizzly bears but not American black bears in Yellowstone National Park. J. Mammal. 94 (4), 833e844. Gardner, C., Pamperin, N., Benson, J., 2014. Movement patterns and space use of maternal grizzly bears influence cub survival in Interior Alaska. Ursus 25 (2), 121e138. Gittleman, J., 1999. Hanging bears from phylogenetic trees: investigating patterns of macroevolution. Ursus 11, 29e40. Gruber, T., Clay, Z., Zuberbühler, K., 2010. A comparison of bonobo and chimpanzee tool use: evidence for female bias in the Pan lineage. Anim. Behav. 80 (6), 1e11.

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