Helarctos Malayanus) By

Home , Stereotypy (non-human), Sun bear

Effects of food distribution and external factors on the activity budgets of captive sun bears (Helarctos malayanus) by

Jessica Barber

A thesis submitted to Sonoma State University In partial fulfillment of the requirements for the degree

MASTER OF SCIENCE In Biology

Committee Members:

Dr. Karin Enstam Jaffe, Chair

Dr. Dan Crocker

Darren Minier

Authorization for Reproduction of Master’s Thesis

I grant permission for the print or digital reproduction of this thesis in its entirety, without further authorization from me, on the condition that the person or agency requesting reproduction absorb the cost and provide acknowledgment of authorship.

Date: 1 May 2018 Name: Jessica Barber

iii

Effects of food distribution and external factors on the activity budgets of captive sun bears (Helarctos malayanus)

Thesis by Jessica Barber

Abstract

All free-ranging bears spend a large portion of their day on foraging activities. In captivity, many bear species spend less time or energy foraging because of the highly predictable schedule and presentation of their diets. To combat this, zoos are increasingly using enrichment to encourage animals to engage with their environment. I used principles of optimal foraging theory to test whether manipulating food distribution could be used as a type of enrichment to alter behavior for three adult female sun bears at Oakland Zoo in California. I compared the effects of scattered vs. clumped food distribution on the sun bears’ activity budgets using continuous focal animal sampling. In addition, temperature and visitor presence were also measured using scan sampling to measure the effect on the sun bears behaviors. The results indicate that manipulating food distribution successfully increased the duration of feeding behavior and frequency of foraging in captive sun bears when food was clumped. Higher temperatures and increased visitor presence was correlated with increased stereotypic pacing and nighthouse use by the study subjects. This study may provide zoos with a relatively simple and cost-effective way to incorporate existing diets and enrichment devices to enhance animal welfare by focusing on the distribution of items. More broadly, these results may inform research into the behavioral ecology of sun bears, whose natural foraging behavior is little known.

MS Program: Biology Date: 1 May 2018 Sonoma State University

Table of Contents

Introduction ...... 1 Methods ...... 6 Study Site and Animals ...... 6 Food Distribution ...... 7 Sun Bear Behavior ...... 7 External Factors ...... 8 Statistical Analyses ...... 9 Results ...... 10 Effects of Food Distribution ...... 10 Feeding ...... 10 Foraging ...... 10 Pacing ...... 10 Out of Sight Nighthouse ...... 11 Effects of External Factors ...... 11 Temperature ...... 11 Discussion ...... 12 Effects of Food Distribution ...... 12 Feeding ...... 12 Foraging ...... 13 Pacing ...... 14 Out of Sight Nighthouse ...... 16 Effects of External Factors ...... 17 Temperature ...... 17 Visitor Presence ...... 18 Future Research ...... 19 Conclusion ...... 19 Literature Cited ...... 21 Tables ...... 25 Table 1: Schedule of trials and description of each set ...... 25 Table 2. Ethogram describing behaviors used in analysis ...... 25 Figures ...... 26 Figure 1: Average bout duration of behaviors by distribution in AM...... 26

Figure 2: Average duration of bouts per clump type...... 26 Figure 3: Average bout duration of behaviors by distribution in PM...... 27 Figure 4: The frequency of behaviors in the AM and PM observations...... 27

Introduction Because wild animals forage in order to maximize energy gain and minimize energy expenditure (Schoener 1971; Pyke et al. 1977; Rapaport 1998; Schneider et al. 2014), food distribution and abundance affect foraging behavior (Charnov 1976; Pyke et al. 1977).

Distribution is defined by how far apart the individual food items are separated. In general, food is considered clumped if it occurs in large patches, while scattered food occurs in smaller patches that are more dispersed throughout the environment (Pyke et al. 1977; Isbell et al. 1998; Mathy and Isbell 2001). Researchers label food as clumped when the density in the patch is higher than the surrounding areas and scattered when food is more evenly dispersed and smaller in size

(Wiens 1976; Isbell et al. 1998; Isbell 2000). Differences between these two types of food distribution can be measured by the way animals forage. According to marginal value theorem, animals feeding on clumped resources should stay at a clump as long as the capture rate exceeds that of the surrounding environment (Charnov 1976; Pyke et al. 1977). Thus animals should feed at large clumps longer because there is more food to eat as clump size increases (as long as group size does not change). Animals feeding on scattered resources spend less time at a food site

(Charnov 1976; Pyke et al. 1977; Isbell et al. 1998). In addition to distribution, food abundance also influences how animals forage in the wild (Charnov 1976; Pyke et al. 1977; Isbell et al.

1998). Food is considered abundant if it is not limited and there is an excess of food available for a population. Food is considered scarce if there is a limited amount of food available in the environment (Isbell et al. 1998; Isbell 2000). Abundant food resources allow animals to become specialists, while scarce food resources force animals to become generalists and to travel father.

(Charnov 1976; Pyke et al. 1977; Rapaport 1998).

The fact that food distribution and abundance affect the foraging behavior of wild animals suggests that this knowledge can be used to enhance the wellness of captive animals.

For animals in captivity, food abundance is determined by the amount of food needed to meet the animals’ nutritional needs and can be manipulated within the nutritional bounds. Although the amount of food and home range size is fixed for captive animals, food distribution can be manipulated in order to stimulate animals to spend more of their daily activity on investigative and feeding behaviors (Ganslosser and Brunner 1997; Schneider et al. 2014). In this way, altering food distribution can be viewed as a form of environmental enrichment, which has been defined as any improvement to the biological functioning of captive animals as a result of changing their environment (Newberry 1995). The goal of enrichment is to increase the behavioral choices offered to animals by encouraging them to use their species appropriate behaviors (Shephardson 2003).

Multiple studies have been conducted on the effects of foraging-based enrichment as a way to increase animal activity levels (e.g., plains zebra and Asiatic wild asses (Equus burchelli and E. hemionus kulan), Ganslosser and Dellert, 1997; tree-runner lizards (Plica plica),

Januszczak et al., 2016; red fox (Vulpes vulpes), Kistler et al., 2009; parrot spp., Rodríguez-

López, 2016). In captive giraffes, Fernandez et al. (2008) examined how, in the wild, giraffes normally spend a majority of their time foraging by using their tongues, but in captivity observed an increase in oral stereotypies, or repetitive behavior, possibly due to less use of the tongue to obtain food. They concluded that providing enrichment specifically to promote more use of their tongue was effective at decreasing oral stereotypies and increasing time spent foraging. Another study on two captive Australian fur seals (Ephalus pusillus doriferus) examined how using three different types of enrichment could encourage three distinct foraging behaviors aimed at mimicking natural foraging behavior (Hocking et al. 2015). This study found that using foraging- based enrichment increased the time the seals spent interacting with the devices and encouraged

them to perform different foraging tactics depending on the type of enrichment offered (Hocking et al. 2015). Lastly, Schneider et al (2014), took into account previous research on captive bear enrichment studies and used more dynamic methods for stimulating sun bears (Helarctos malayanus) by incorporating unpredictability in their enrichment regime. This study concluded that using a combination of different types of enrichment was most effective at increasing the foraging activity of the sun bears in the long-term.

Several studies have shown that bears, (including sun bears), in captivity tend to spend only about 30-60% of their day active and of that time only about 6-20% is spent on exploratory behaviors (Carlstead et al. 1991; Vickery and Mason 2004; Schneider et al. 2014). In addition, several studies have shown that captive bears spend up to 50% of their time engaged in stereotypical behaviors (Carlstead et al. 1991; Vickery and Mason 2004; Montaudouin and Le

Pape 2005; Schneider et al. 2014). While free-ranging bears spend a large portion of their day on foraging activities (Carlstead et al. 1991; Forthman and Bakeman 1992; Grandia et al. 2001; Te

Wong et al. 2002; Vickery and Mason 2004; Kitchener 2010), captive bears do not because their lives tend to be highly predictable, both temporally and spatially (Carlstead et al. 1991; Rapaport

1998; Watters et al. 2011; Schneider et al. 2014). Altering how food is distributed should reduce the predictability of the captive environment, resulting in increased time spent searching for food

(see Watters et al. 2011). If zoos can engage bears in more foraging and other exploratory behaviors by implementing novel enrichment, the frequency or duration of stereotypical behaviors may be reduced (Carlstead et al. 1991; Swaisgood and Shepherdson 2005; Shyne

2006a; Watters et al. 2011; Young 2013).

External factors such as temperature and visitor presence can also affect the behavior of captive animals (Mason 2006; Rajagopal et al. 2011; Quadros et al. 2014; Kelly et al. 2015). For

example, animals at zoos that are exposed to consistent human presence may experience heightened stress and develop stereotypies that reduce time devoted to foraging (Mason 2006;

Mason et al. 2007; Kelly et al. 2015). Additionally, extreme temperatures can affect how captive animals behave (Terrien et al. 2011; Wark et al. 2014). Depending on the enclosure, if there is not enough cover or places for an animal to escape from harsh conditions, this might also lead to aberrant behaviors and reduce time foraging (Mason 2006; Terrien et al. 2011). External factors must be considered when observing captive animals and implementing enrichment to properly understand the effects of the enrichment and other variables on the animals’ behavior.

Because there is a lack of complete understanding about how sun bears forage in the wild, they are an ideal study organism for testing different foraging strategies in captivity. In the wild, sun bears have large home ranges and are predominately solitary (Te Wong et al. 2004;

IUCN red list 2008). The behavioral studies that have been conducted on wild sun bears, while limited, support the morphological assessment of their diet, indicating that sun bears are active during the day and eat a variety of foods including termites, bee larvae, honey, and a variety of fruits (Te Wong et al. 2004; IUCN red list 2008). These food items are mostly distributed in patches where sun bears appear to spend time foraging using their well-developed olfactory sense (Wong 2002). They commonly search for fruits by climbing trees, digging up termite mounds and finding other insects by looking in log piles (Te Wong et al. 2002; Wong 2002;

Steinmetz et al. 2013). Sun bears are opportunistic omnivores that forage mostly by climbing trees to find fruit (Steinmetz et al. 2011, 2013). However, when fruit is more of a limiting resource, sun bears tend to eat more insects and stay lower to the ground (Steinmetz et al. 2013;

Wong et al. 2013).

Sun bears are the least studied of the eight bear species in the wild due to their remote habitat in South East Asia (Te Wong et al. 2004; Wong et al. 2013). As wild sun bear populations continue to decline due to habitat loss, deforestation, and poaching, conservation strategies are in place and more research on their status in the wild is being done to understand this threatened species (Wong 2002; Wong et al. 2004; IUCN red list 2008; Ngoprasert et al.

2011). Since sun bears are labeled as vulnerable according to the IUCN red list, zoos play an important role in their survival.

Since bears in the wild spend most of their energy and time searching for and eating food, it is important for institutions like zoos to not only provide a nutritionally balanced diet, but also one that stimulates animals to spend a large amount of their daily activity on foraging and feeding. Appropriate management practices need to be in place for each species to thrive while in captivity, because animals retain a strong instinctual drive to explore and learn about their environment (Carlstead et al. 1991; Fernandez et al. 2009; McGowan et al. 2009; Keulartz 2015).

Understanding how food distribution, temperature, and visitor presence affect behavior can provide insights into how environmental enrichment can be used to improve captive animal health (Fernandez et al. 2008; Watters et al. 2011; Schneider et al. 2014; Hocking et al. 2015).

For this study I am using behavioral ecological principles of animal foraging to assess the influence of food distribution as a form of enrichment for three adult female sun bears at

Conservation Society of California, Oakland Zoo in Oakland, California, while simultaneously accounting for the effects of changes in temperature and zoo visitor presence. I compare the effects of randomly scattering food vs. placing food in three clumps on the sun bears’ activity budgets. I hypothesize that the scattered distribution will result in increased time spent foraging while decreased time spent on feeding and stereotypical behaviors compared to the clumped

distribution, as the bears will be more engaged with their environment. Clump placement might also affect how the sun bears forage. Since previous research (Te Wong et al. 2002; Wong 2002;

Steinmetz et al. 2011, 2013) suggests sun bears are most commonly found climbing trees or searching in logs piles for food, I predict that the bears will spend an equal amount of time feeding and foraging for food on the climbing structures and logs but less time feeding and foraging when food is placed on the ground near bushes. In addition, I predict that larger numbers of visitors and higher temperatures will decrease time spent foraging and increase stereotypic behaviors and/or use of nighthouse. My results may provide zoos with a relatively simple and cost-effective way to incorporate existing diets and enrichment devices to enhance animal welfare by focusing on the distribution of items. More broadly, my results may inform research into the behavioral ecology of sun bears, whose natural foraging behavior is little known.

Methods Study Site and Animals This research was conducted at Conservation Society of California at Oakland Zoo, located within Knowland Park in Oakland, California. Oakland Zoo is accredited by the

Association of Zoos and Aquariums, and houses over 700 animals in its 100-acre campus.

Currently, Oakland Zoo has three adult female sun bears (Helarctos malayanus) in residence.

Two of the bears were born at the San Diego Zoo by the same parents but are from different litters and are 9 and 11 years old at the time of the study. The third bear is the oldest (27 years old) and was born in the wild but was orphaned as a cub and brought to the San Diego Zoo. All three bears have been on exhibit together at Oakland Zoo since 2011. The sun bear enclosure includes an enclosed night house with four entry doors that the bears had continual access to for the duration of the study. The outdoor enclosure is 1,300-sqm in size and includes three climbing

structures, 25-m tall dead eucalyptus tree, log piles, dense bushes, shade trees and palms, and a pool feature with waterfall.

Food Distribution Food distribution trials alternated weekly between a ‘clump’ trial and a ‘scatter’ trial

(Table 1). ‘Clump’ trial consisted of the morning diet distributed into three even clumps. The three clumps were placed in the enclosure in three different locations (log piles, climbing structures, and on the ground near bushes) that changed after each trial (Table 1). This ensured that all three clumps were placed in the same type of environment to reduce intra-trial variation while allowing for the examination of the effect of clump placement between trials. Each

‘clump’ trial was followed by a ‘scatter’ trial (Table 1) in which the zookeepers took the same diet that was used in the clumped trial and scattered the food items individually around the enclosure randomly. Both trials consisted of the same amount of food with only the distribution changing.

Because the ‘clump’ trials consisted of three different locations and were separated by

‘scatter’ trials, it took six weeks to complete one set of trials. A total of 18 weeks of trials (a complete set of trials repeated three times) were observed to account for rotating through each bear equally. Each week the bears were observed during one weekday and one weekend day.

One complete round of observations for one day included rotating through each bear three times for AM and PM data collection. AM observations were made from 9:30AM to noon when food was present and PM observations were made from noon to 2PM, when food was not present.

Sun Bear Behavior One-hundred-and-fourteen hours of observational data were collected over four months

(June-October 2017) using focal animal and scan sampling. The focal animal’s behavior (Table

2) was recorded during ten-minute focal samples using continuous recording. Each bear was

observed for 38 hours total and all behaviors in Table 2 were recorded. The order of observation of the study subjects was consistent within each trial set, but each set of trials started with a different bear so that each bear had an equal number of observations throughout the day (Table

1). For example, during the first set of trials, each observation day started with a 10-minute focal sample of bear one, followed by a scan sample of all three bears. Then the second bear was observed followed by another scan sample and then the third bear and third scan. The protocol for the second set of trials followed that outlined for the first set, except each observation day started with a focal sample of bear two, followed by bear three, and then bear one. The third set of trials started with a focal sample of bear three, followed by bear one and then bear two.

Ten-minute focal samples were conducted during the morning feedings (10-11:30AM) and between feedings in the afternoon (12-1:30pm) to record any behavioral changes associated with changes in food distribution. If the animal went out of sight during the focal, the observation continued for the duration of the ten minutes and the focal animals was recorded as

‘out of sight’. If the next focal animal was out of sight at the start of a focal, the observer waited up to five minutes to see if the animal came into view. If the animal came into view within five minutes then the focal began. If the animal did not come into view during this time then the observed moved onto the next animal in the rotation and then went back to the animal that was skipped. If the animal was still out of sight for the second attempt, the observed started the focal with the animal as out of sight. All observational data were collected using HanDBase software

(DDH Software, Inc.), a database app, on an IPad (Apple Inc.).

External Factors Scan sampling was used before and after each focal to examine the effects of visitor presence and seasonality on the sun bears’ behavior. Scans of the outdoor exhibit were

conducted from left to right for 30 seconds and the following was recorded: 1) the identity, 2) behavior (Table 2) and 3) location of each bear, 4) number of visitors present at the viewing deck of the exhibit, and 5) temperature using the weather app for iPhone. Any bear not visible during the 30-second scan was marked as out of sight. Number of visitors was recorded in a Likert scale of 5: 0 (none present), 1-5, 6-10, 11-15, etc. Since the number of visitors and temperature varied during this study, data were analyzed using the average number of visitors present for each range. Temperature data were collected in five-degree increments (e.g. 55-59, 60-64, 65-69, etc.)

Temperature data were then analyzed using the average temperatures of each range to see if there was an overall trend of the effect of temperature on behavior.

Statistical Analyses Only the behaviors shown in Table 2 were used in statistical analyses due to insufficient amounts of data on other behaviors. JMP Pro 13 (SAS Institute Inc., Cary, NC, USA) and SAS

9.4 were used to perform all statistical analyses. I performed a Linear Mixed Model to examine the effects of food distribution the average bout duration of behavior (Table 2). Only AM data were used in analyses related to food distribution since observations were not conducted during the PM feeding. All other analyses included both AM and PM data. The effect of food distribution was evaluated using the interaction of behavioral category with food distribution in a model that contained bear ID as a random effect. Temperature and number of visitors were also included as covariates. Evidence for a significant interaction of food distribution and behavioral type on the duration of a behavior was followed by post-hoc students t-tests. Additionally, a

General Linear Model was used to evaluate the effects of food distribution on the duration of stereotypic behavior. Model residuals were visually assessed for approximate normality and residuals plots were assessed for homoscedascity. A Generalized Linear Mixed Model was used to examine the effects of clump type on behavior (SAS 9.4, Raleigh, NC). This model included

bear ID as a random effect and number of visitors and temperature as covariates. Behavior was modeled using a multinomial response distribution with a cumulative logit linking function. If significant effects on behavior were evident these models were followed by post-hoc tests on behaviors reorganized as binomial responses (e.g. feeding vs. not-feeding). Odds ratios (OR) were calculated for nominal explanatory factors. Statistical significance was assessed using α

=0.05.

Results Effects of Food Distribution Feeding

Food distribution had an effect on the duration (F6,1819=6.67,p<0.0001) and frequency

(F1,1038=27.65, p<0.0001) of sun bear behavior. The average feeding bout was longer when the food was clumped compared to scattered (Figure 1). The sun bears were more likely to exhibit feeding behavior when food was scattered than clumped (OR=3.308). Clump type also had an effect on sun bear behavior (F 2,496.9=4.86, p=0.0081). The average feeding bout was longer for clumps that were placed in the climbing towers and bushes compared to logs (Figure 2).

Foraging There was no difference in the duration of foraging for clumped compared to scattered food distribution (Figure 1). Frequency of foraging differed depending on distribution

(F1,1038=12.31, p=0.0005). The frequency of foraging was less when food was scattered than clumped (OR=0.585). Clump placement had no effect on the average duration of foraging bouts for the bears (Figure 2).

Pacing Food distribution did not affect the average bout duration of pacing behavior during AM feedings (F1,157.9=0.840, p=0.361; Figure 1) or during PM observations (F1,1=0.055, p=0.815;

Figure 3). There was a difference in the frequency of pacing between clumped and scattered food 10

distributions (F1,2110=9.43, p=0.0022). The sun bears were less likely to exhibit pacing behavior when food was scattered than clumped (OR=0.637). There was a difference in the frequency of pacing between AM and PM (F1,2110=9.66, p=0.0019). The sun bears were more likely to exhibit pacing behavior during the PM than AM (OR=1.596; Figure 4).

Out of Sight Nighthouse The duration of time spent out of sight in the nighthouse differed depending on food distribution (Figure 1). Frequency of nighthouse use differed depending on food distribution

(F1,2110=12.13, p=0.0005). Overall, the sun bears were in the nighthouse for longer and more frequently when the food was scattered compared to clumped (OR=1.420). Frequency of nighthouse use differed depending on time of day (F1,2110=25.38, p<0.0001). The sun bears were more likely to be in the nighthouse during the PM observations compared to the AM (OR=1.681;

Figure 4).

Effects of External Factors Temperature

Frequency of feeding (F1,1038=10.42, p<0.0013) and foraging (F1,1038 =35.82, p<0.0001) differed depending on temperature. Overall the sun bears decreased their foraging and feeding as the temperature increased (β=-0.073, -0.050). Temperature had no effect on the frequency of pacing (F1,2110=0.02, p=0.889). Frequency of nighthouse use differed depending on temperature

(F1,2110=34.23, p<0.0001). The sun bears were significantly more likely to be in the nighthouse when the temperature was warmer (β= 0.04).

Visitor Presence

Frequency of foraging (F1,1038=16.16, p<0.0001) and frequency of feeding (F1,1038=12.06, p=0.0005) differed depending on number of visitors present. As the number of visitors increased the sun bears were less likely to be foraging or feeding (β=-0.05, -0.075). Visitor presence had

an effect on the frequency of pacing (F1,2110=8.03, p=0.0046). The sun bears are significantly more likely to exhibit pacing behavior when the number of visitors present increased

(FE=0.027). Visitor presence also had an effect on the frequency of nighthouse use (F7,2096=2.99, p<0.0039). The sun bears were more likely to be in the nighthouse when more visitors were present (β=0.016).

Discussion Effects of Food Distribution Feeding I used principles of optimal foraging theory to test whether manipulating food distribution could be effectively used as a type of enrichment to alter feeding behavior in captive sun bears. Optimal foraging theory suggests that animals should forage efficiently by finding resources and using them in the most profitable way in order to maximize their energy gain

(Schoener 1971; Pyke et al. 1977; Rapaport 1998; Schneider et al. 2014). According to the marginal value theorem, when the capture rate of finding food in a patch drops to equal the average capture rate for the entire habitat, the animal should leave the current clump they are at and find another (Charnov 1976; Pyke et al. 1977). In other words, animals are expected to remain at larger clumps (if group size remains constant) for longer because larger patches of food take longer to deplete (Isbell et al. 1998). Although the sun bears at Oakland Zoo are not under the same constraints faced by their free-ranging counter-parts, when food was placed in clumps in the enclosure, they spent more time feeding at a clump compared to when the food was scattered around the enclosure, as predicted by the theory. As the sun bears sat at a clump and ate food, the rate of food intake decreased over time until it was optimal to leave the current clump of food and attempt to find another clump (Charnov 1976).

Placement of clumps within the enclosure also had an effect on the length of feeding bouts for the sun bears. I predicted that the sun bears would spend more time feeding in the climbing structures and on the logs because previous research has suggested that these are preferred feeding sites for wild sun bears (Te Wong et al. 2002; Wong 2002; Steinmetz et al.

2011, 2013). However, my results only partially confirm my prediction. The sun bears spent more time feeding when clumps were placed in the climbing structures and bushes than when they were placed on the logs (Figure 2). This could be due to the level of difficulty of finding food at these different locations, since the logs have gaps and holes for food pieces to fall through. Thus, the log piles made it more challenging for the sun bears to feed for longer periods if they were only finding individual pieces of food at a clump site instead of the food all placed in one pile. This finding is also consistent with the marginal value theorem, which implies that the sun bears should give up on a clump site that was too difficult to find food items and continue foraging for food at another clump site (Charnov 1976).

As predicted, the frequency of feeding increased when food was scattered compared to clumped. When food was scattered, the sun bears had more frequent but shorter feeding bouts compared to the clumped distribution because scattered food is essentially smaller clumps that are more spread out in the environment. When patch size was smaller, it took less time for the sun bears to consume the food items and therefore they moved onto another patch faster in order to meet their energy requirements (Charnov 1976; Pyke et al. 1977; Rapaport 1998).

Foraging Changing the distribution of food did not affect time spent foraging in the ways that I predicted. I expected the bears to forage longer when the food was scattered due to increased time spent searching for individual food items. Rather, the sun bears’ average duration of foraging when food was scattered or clumped did not differ statistically (Figure 1). Within clump

distribution, clump placement also did not affect foraging bout times (Figure 2). Because I conducted the food distribution experiments twice a week and alternated distribution patterns weekly (see Table 2), it is possible that the bears were not provided with sufficient time to learn where and how food was distributed each week, requiring about the same search/foraging time regardless of distribution (Carlstead et al. 1991).

Foraging frequencies increased when food was clumped compared to scattered, which was also not expected. Little evidence of competition was observed during this study and could contribute to this finding. Rather than competing with conspecifics, the sun bears might have chosen to continue searching for another clump if one clump was already monopolized by a conspecific (Isbell 1991; Mathy and Isbell 2001). If the bears chose to continue searching for a clump that was not already occupied, more frequent foraging would occur when food was clumped.

Pacing Since pacing is the most common stereotypic behavior observed in all three sun bears at the Oakland Zoo (V. Salonga, pers. comm.), pacing behavior was also analyzed in regard to food distribution. The exact causes of pacing behavior in bears as well as most other stereotypic behaviors in captive animals is still widely unknown, however many hypotheses exist (Vickery and Mason 2004; Mason 2006; Shyne 2006b; Mason and Rushen 2008; Rees 2009). These behaviors are often believed to be indicators of suboptimal living conditions, stress from living in captivity, or a lack of stimulation (Mason 1991; Shyne 2006b; Mason et al. 2007), and are therefore of concern for zoos. Some examples of stereotypic behaviors include rhythmic head movements and swaying in elephants (Rees 2009), oral fixations in ungulates, sham-chewing by sows and tongue-rolling by cattle and giraffes (Mason 2006), excessive self-grooming in non-

human primates (Mason 2006), somersaulting in European starlings (Feenders and Bateson

2012) and pacing and swimming in polar bears (Wechsler 1991).

Contrary to what I predicted, the sun bears did not differ in the average duration of pacing bouts for AM or PM observations (Figure 3). Mason (2006) explains that once a stereotypic behavior is established in an individual it can be very challenging to reduce or eliminate the stereotypy. Regardless of presence of food, once the bears began pacing, the average bout length was the same possibly because the pacing has been repeated so many times it is now a habit for the sun bears (Mason 2006). Mason (2006) also explains that once a stereotypic behavior begins, animals may have to complete the behavior over a certain length of time, possibly as a way to cope with their surroundings or because it has become a habit. In light of this, if pacing is an established behavior in the sun bears, it is not surprising that duration of pacing was not affected by changes in food distribution.

Although duration of pacing did not change during my study, the frequency of pacing was affected by the way food was distributed. The bears were more likely to pace when their food was clumped compared to scattered. When captive animals are frustrated, performing a stereotypic behavior has been hypothesized to help cope with stress in the environment (Mason

1991, 2006). If an individual bear was able to monopolize a clump and deny another bear access to the clump, then this could attribute to pacing in the other bear if it became frustrated (Mason

2006; Mason et al. 2007; Burgener et al. 2008). If the bears are using stereotypic pacing to deal with the frustration of being denied access to a clumped food source, this could explain the low frequency of competitive behaviors observed during the course of the study, which precluded statistical analyses.

The sun bears were also more likely to pace during the PM observations compared to the

AM. This is most likely because the bears spent more time feeding and foraging in the AM

(Figure 4). It is possible that once the food was depleted the bears were more likely to engage in pacing, perhaps because their environment is still too predictable temporally and they revert back to pacing (see also: Mason and Rushen 2008; Watters 2009; Schneider et al. 2014). This study changed the way food was distributed in the enclosure but did not change the time of day food was presented to the bears. Therefore, once the sun bears were finished with their morning feeding, they had to wait until the next feeding in the afternoon before they had reason to resume foraging. This can become a problem if the sun bears have too much time in-between feedings where stereotypic behaviors can arise, which may have occurred during this study (Watters 2009;

Schneider et al. 2014). Although more research must be conducted to determine how predictability of feeding time affects the sun bears, if this is the case, it suggests that altering food distribution may be an effective enrichment strategy.

Out of Sight Nighthouse Another important factor that I examined during this study was how the sun bears used their nighthouse living quarters. Enclosure use has been studied in zoo animals and suggests that preference for a particular area within an enclosure can vary when animals are given the choice to utilize the space (Ross 2006b; Ross et al. 2011). Some species prefer to stay in certain areas within an enclosure such as by the entryways or inside the night quarters for a majority of the day (Ross 2006b; Ross et al. 2011). Since the sun bears have 24hr access to their indoor nighthouse, data on the nighthouse use was included for this study. This study did not observe the bears’ behaviors inside the nighthouse, but I did record duration and frequency of nighthouse use.

Analyzing time spent in the nighthouse as a behavior reveals that the sun bears spent more time in the nighthouse than in any other behavior during this study (Figures 1 and 3), contrary to what I predicted. Furthermore, the sun bears were more likely to be in the nighthouse when the food was scattered. This is an opposite finding compared to pacing behavior for the bears. Considering these findings, the sun bears could be using the nighthouse as part of their foraging routine since they are fed a very small amount of food before being let out in the morning. Since the nighthouse is open to them at all times the bears could have food items in the nighthouse or simply prefer to go through it as a way to move throughout the enclosure or remove themselves from any outside elements and/or conspecifics (Ross 2006b; Ross et al.

2011).

Effects of External Factors Temperature As the temperature increased the sun bears were less likely to be feeding and foraging.

Although previous research found that sun bears are mostly crepuscular and most active at dusk and dawn (Te Wong et al. 2002; Wong 2002; Wagman et al. 2018), in this study, this result is likely due to their routine morning feeding schedule. Due to the interaction with time of day, temperature is most likely a confounding variable: as the time since feeding passed, the temperature increased, and the bears finished most or all of their morning diet. The frequency of pacing was not affected by temperature. Again, this might be because pacing is an established behavior in the sun bears.

Additionally, the bears were more likely to be in the nighthouse as the temperature increased. This could also be due to time of feeding but could also be as a form of shelter when the temperature increased. Giving animals control of their environment is important for zoo animal welfare. Previous research suggests that when animals have more control over their

environment, they are less likely to feel stressed and exhibit stereotypic behaviors (Mason 1991,

2006; Ross 2006a; Watters 2009). Since the bears always had access to their nighthouse during this study, they were able to make the choice at any time to go inside and remove themselves from the outdoor exhibit.

Visitor Presence The bears were less likely to be feeding and foraging as the number of visitors increased.

Previous research suggests that loud noises and disturbances from large crowds can negatively affect captive animal behavior (Mason 2006). However, as with temperature, this result may be due to the time of day. The bears are fed right when the zoo opens and there are usually fewer people compared to the afternoons (V. Salonga, pers. comm.). By the time many visitors are present at the viewing deck, the bears have usually finished with their morning diets and are not feeding or foraging. However, this was not always the case, and the bears could possibly be trying to escape an adverse stimuli when many visitors are present and therefore stop their normal foraging behaviors (Mason 1991, 2006; Vickery and Mason 2004).

The number of visitors did have an effect on the frequency of pacing by the sun bears. As the number of visitors increased, the sun bears were more likely to be found pacing in the enclosure. This may be a stress-response to the loud noises that the increase in visitors brings to the enclosure. The sun bears could be coping with the stress of large crowds by pacing as a way to alleviate their frustration (Vickery and Mason 2004; Shyne 2006b; Mason and Rushen 2008).

Another explanation could also be related to the time of day. Since larger crowds often come later in the afternoon the chances of observing the sun bears pacing increases because they have already eaten and are less stimulated, so they resort to pacing. This finding could potentially be unrelated to the number of visitors present. (Mason 1991, 2006; Mason et al. 2007).

Lastly, the sun bears were more likely to be in the nighthouse when more visitors were present. This may be a way to escape the larger crowds due to loud noises and unfamiliar smells

(Mason 2006; Ross 2006b; Fernandez et al. 2009). Overall, there might be many confounding factors that are at play when the bears choose to go into the nighthouse or pace and the number of visitors present could play a role in the behavioral choices the bears make.

Future Research Since this was a relatively short-term study, there are a few changes and additions I would make if this study were conducted again. First, having access to the nighthouse to collect data would be ideal given how much time the bears spend there. Alternatively, placing cameras inside the nighthouse would enable collection of behavioral data without disturbance by human observers. Second, I would also implement a design to change the time of day the sun bears are fed in addition to spatially changing the diet. This would help us understand how differing levels of temporal (un)certainty affect the bears’ behavior, particularly searching/foraging behavior.

Increasing the unpredictability of the food (in both time and space), should increase investigative behaviors and help diminish the stereotypic pacing that was observed in the time between routine feedings (Watters 2009, 2014; Watters et al. 2011). This would help elucidate the effects of external factors like temperature and crowd size on the sun bears’ behaviors. Third, I would conduct this study every day of the week to see if habituation to novel enrichment plays an important role in the sun bears’ behaviors.

Conclusion 1. Manipulating food distribution successfully increased the duration of feeding

behavior and frequency of foraging in captive sun bears when food was clumped.

2. Clump location increased time spent feeding at the climbing towers and bushes but

not log piles.

3. Higher temperatures and increased visitor presence was correlated with increased

stereotypic pacing and nighthouse use in captive sun bears.

4. The sun bears were more likely to be pacing and out of sight in the nighthouse in the

afternoon than in the morning.

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Tables Table 1: Schedule of trials and description of each set Total of 18 weeks of observation. Trial Distribution & Set 1: Set 2 Set 3 Location Start date Start date Start date 6/20/17 8/1/17 9/11/17 1 Clumped Bear 1 Bear 2 Bear 3 Climbing structures Bear 2 Bear 3 Bear 1 Bear 3 Bear 1 Bear 2 2 Scattered Bear 1 Bear 2 Bear 3 Bear 2 Bear 3 Bear 1 Bear 3 Bear 1 Bear 2 3 Clumped Bear 1 Bear 2 Bear 3 Ground Bear 2 Bear 3 Bear 1 Bear 3 Bear 1 Bear 2 4 Scattered Bear 1 Bear 2 Bear 3 Bear 2 Bear 3 Bear 1 Bear 3 Bear 1 Bear 2 5 Clumped Bear 1 Bear 2 Bear 3 Log piles Bear 2 Bear 3 Bear 1 Bear 3 Bear 1 Bear 2 6 Scattered Bear 1 Bear 2 Bear 3 Bear 2 Bear 3 Bear 1 Bear 3 Bear 1 Bear 2

Table 2. Ethogram describing behaviors used in analysis Behavior Description Solitary Move Bear locomotes terrestrially on ground using all four limbs other than pace Feed Bear uses paws and/or mouth to obtain food Forage Bear searches for food by moving throughout enclosure or visually searching for food and/or smelling for food Inactive Bear lies, sits, or stands non-mobile with eyes open or closed Out of Sight Bear is not visible Out of Sight Bear is inside nighthouse and is not visible Nighthouse Stereotypic Pace Bear walking repeatedly in the same path, such as on a log or ground

Figures

300 * 250

200 *

150 * Clumped 100 Duration (s) Scatter 50

0 Feeding Foraging Move Inactive Pace OOSN OOS Solitary Behaviors

Figure 1: Average bout duration of behaviors by distribution in AM. The * denotes significant difference in the Least Squared Means (LSM) assessment using student’s t-test. LSM controlled for difference between bears.

A 140 A

120

100 B B 80 Bushes

60 Logs

Duration (s) 40 Climbing Towers

0 Feeding Foraging Behavior Figure 2: Average duration of bouts per clump type. The letters denotes significant difference in the LSM assessment using student’s t-test. LSM controlled for difference between bears.

400 350 300 250 200 Clumped 150

Duration (s) Scatter 100 50 0 Foraging Move Inactive Pace OOSN OOS Behaviors

Figure 3: Average bout duration of behaviors by distribution in PM. No behaviors were statistically significant when the LSM assessment was used for the student’s t-test. LSM controlled for difference between bears.

Frequency of Behaviors AM Frequency of Behaviors PM Feeding 11% Foraging Move 2% 4% OOS Inactive 18% 12% OOS Foraging 28% 28% * OOSN Pace 27% 15% Pace * 10% Move OOSN Inactive 2% 39% 4%

Figure 4: The frequency of behaviors in the AM and PM observations. * denotes significance using the odds ratio estimate.