1 Picture Recognition of Food by Sloth Bears (Melursus ursinus) 2 Tabellario, S., Babitz, M.A., Bauer, E.B., Brown-Palsgrove, M. 3 4 Abstract 5 Pictures are often used in cognitive research to represent objects and many species have demonstrated the ability to 6 recognize two-dimensional pictures as representations of their three-dimensional counterparts. However, for ursids 7 picture recognition has been reported in only one study of a single 11-year-old female American black bear 8 (Johnson-Ulrich et al. 2016). We tested the picture recognition abilities of an additional species, the sloth bear. 9 After a food preference test by which the bears’ food options were ranked and categorized as high-, mid-, and low- 10 preference items, we tested a sub-adult male and an adult female sloth bear by presenting two pictures of food in 11 each testing trial – a high-preference food and a low-preference food. Both bears met criterion by choosing the 12 pictures of their preferred foods in at least 80% of the trials in three consecutive testing sessions. We then presented 13 never before used pictures of high-preference versus low-preference food items and they again met our criterion. 14 15 Keywords 16 Picture recognition, sloth bear, Melursus ursinus, choice, control 17 18 Introduction 19 In 2017, Amici pointed out that “studies of animal cognition are not equally distributed across taxa”. Scientists focused 20 mainly on non-human primates or birds. However in investigations of how animals see the world and process 21 information, research has demonstrated that several other species have the ability to recognize two-dimensional (2D) 22 pictures as representations of their three-dimensional (3D) counterparts, including a number of sheep, fish, and lizards, 23 as reviewed by Bovet and Vauclair (2000), horses (Hanggi 2001), and tortoises (Wilkinson et al. 2013). However only 24 one bear, an American black bear (Johnson-Ulrich et al. 2016) is noted in the literature to have displayed this ability. 25 Recognizing 2D pictures can be a starting point for many cognitive tests – discrimination tasks, categorization, and 26 memory tests. It is not a given that all animals understand the correspondence between 2D pictures and the real life 27 objects that they represent. Even some adult humans who have not previously been exposed to photographs are not 28 able to identify objects in photographs (Miller 1973) and on some occasions chimpanzees have been unable to 29 recognize 2D photographs (Winner and Ettlinger 1979). 30 People generally perceive bears as intelligent (Nakajima et al. 2002). In fact, animal trainers and zookeepers regard 31 bears as the most intelligent carnivore, with intelligence levels comparable to primates (Breiter 2008). However, the 32 cognitive abilities of bears are understudied (Perdue 2016; Vonk 2016; Vonk and Jett 2018) and there is little scientific 33 research to back up these claims. Even less is known about sloth bears in particular. Finding evidence that sloth bears 34 can recognize 2D pictures as representations of their real life counterparts will add to our knowledge base about sloth 35 bear cognition (Amici et al. 2017; Hartmann et al. 2017). Once we know this cognitive task is possible, other avenues 36 of investigation open up, allowing the development of a deeper understanding of how the cognitive ability of bear 37 species compare to one another, and to other carnivores. 38 If we can learn more about the cognitive abilities of bears, then we will be able to take better care of them in captivity, 39 managing their mental and emotional well-being in addition to their physical health (McGuire et al. 2017; Perdue 40 2016; Vonk 2016). 41 One main source of abnormal stereotypic behavior in captive animals is an animal’s lack of control over their 42 environment (Leotti et al. 2010). Bears in particular are a species that are prone to stereotypies in captivity (Shih et al. 43 2016; Vickery and Mason 2004). Giving an animal an opportunity to make choices gives them the perception of 44 control (Leotti et al. 2010). Control and the choices that are so closely associated with feeling in control in captivity 45 are critical elements of good animal welfare (Mellor 2014; Reiss 2006). Giving captive animals a way to communicate 46 their preferences and increasing their opportunities to make choices could help reduce stereotypic behaviors and 47 improve their well-being, consequently increasing their overall welfare (Buchanan-Smith 2011; Ross 2006). 48 This project emerged as a novel approach to give Smithsonian National Zoological Park’s (NZP) sloth bears an 49 opportunity to make choices and communicate their preferences to their keepers about their daily management. 50 51 Methods 52 Subjects 53 Two captive born sloth bears participated in the study – one 3-year-old, mother-reared male (Niko) and one 5-year- 54 old, hand-reared female (Remi). They both reside at NZP. Although they regularly participate in operant 55 conditioning tasks for husbandry behaviors, they were both experimentally naive. Neither bear had any history with 56 pictures of food prior to these experiments. Each bear was tested in his or her regular night house while temporarily 57 separated from his or her conspecific. Each testing session was voluntary, and the subject could choose to participate 58 or not. 59 60 Materials 61 The testing board was approximately 25 ½” x 9” x 3” (65cm x 23cm x 8cm). During the food preference test, the 62 surface was flat, and items were placed approximately 16” (40cm) apart in plastic plates on opposite ends of the flat 63 board (Figure 1). During the picture recognition tests, a card stand was added to the board so that the picture cards 64 would stand at a 45 angle facing the bear. Dividers kept the centers of the cards 12” (30cm) apart (Figure 2). 65 The picture cards were color photos of familiar foods displayed in the same form as the foods were presented to the 66 bears throughout the food preference test (for example, a 1” (2.5cm) piece of apple, 3 almonds, 1 prune, etc.). The 67 pictures were printed life sized, in color with a matte finish and white background on 5”x7” (13cm x 18cm) 68 cardstock. There was a single image of each food, but the picture cards were randomly rotated 180 degrees 69 throughout the tests. 70 71 Procedure 72 No pre-training took place before the food preference test or before either phase of the picture recognition tests. No 73 novel food items were included in any of the tests. The testing took place in the afternoons when the bears would 74 normally have a training session – after a snack, but before their large PM diet. The coder was blind to the “right” 75 answer. 76 77 Food Preference Test 78 Twenty-five foods were presented in all possible combinations, two at a time using a paired stimulus preference 79 assessment (Hopper et al. 2019). Foods were counter balanced for left/right placement and trial order was 80 randomized as determined by an online generator. 81 Foods were presented simultaneously side by side on the testing board approximately 16” (40cm) from the mesh. 82 Then the board was immediately pushed up to the mesh bear enclosure (see Figure 1) so the bear could make a 83 choice. Each bear was tested in a total of 42 sessions. Each of the first 41 sessions contained 14 trials. The last 84 session contained 26 trials to reach the 600 trials needed to make all possible combinations of food counterbalanced 85 for left/right placement. During the first trial of the first session of the food preference test the bear was given free 86 choice to choose how to indicate their choice (by blowing, pawing, or nosing towards the food they wanted). Both 87 bears chose to indicate by blowing in the direction of one item or the other. The bear was given the food they chose, 88 which they were free to eat or discard. The food the bear did not choose was taken away. If the bear did not select 89 either food after five seconds, the testing board was momentarily withdrawn and the trial was immediately repeated. 90 Foods were scored based on how many times the bear selected each food and whether or not a chosen food was 91 eaten or discarded (1 point for choosing and eating, 0.5 points for choosing and discarding, 0 points if not chosen). 92 Out of all of the foods in the preference test, 12 were selected by the experimenters to use in the picture recognition 93 phase– these foods included six of the most preferred foods (mealworms, almonds, leafeater biscuits, raisins, prunes, 94 and grapes for Niko and raisins, prunes, mealworms, pecans, brazil nuts, and cheerios for Remi) and six of the least 95 preferred foods (butternut squash, turnip, banana, omnivore kibble, orange, and mango for Niko and honeydew, 96 orange, omnivore kibble, broccoli, celery, and zucchini for Remi), omitting foods in the mid-value preference range 97 to clearly delineate high-value versus low-value preferences. Niko’s preferences remained consistant over time. 98 Remi’s preferences changed during hyperphagia, when bears typically eat more. At this time, Remi would eat even 99 her least preferred foods, causing the experimenters to take a break from testing until her appetite returned to 100 normal. Remi was tested on 42 days over an 8 month period. Niko was tested on 42 days over a 2 month period. 101 Roughly the same volume of each type of food was used so that quantity would not likely influence the bears’ 102 choices. 103 104 Picture Recognition - Phase 1 105 Using the testing board from the food preference test with the addition of a card stand (see Figure 2), the bear was 106 presented with two picture cards. Again we presented the stimuli – this time the pictures of food – simultaneously 107 while the testing board was approximately 16” (40cm) away from the mesh. Then the board was immediately 108 pushed up to the mesh for the bear to make a choice. We used three of each bear's most preferred foods and three of 109 each bear's least preferred foods from the food preference test (the other three most preferred and three least 110 preferred food items were reserved for use in Phase 2). When each bear indicated one of the pictures by blowing at 111 it, the keeper gave them the food they chose. The picture of the unselected food was taken off the testing board and 112 the picture of selected food remained on the board while the bear ate or discarded the food. Across all phases of the 113 experiment, roughly the same volume was used for each type of food so that the bear would not likely learn to 114 associate larger or smaller quantities to the pictures. 115 116 Photos were paired by matching every most preferred food with every least preferred food and counterbalancing 117 those pairings for left/right placement. Each session consisted of 15 randomized individual trials. When each bear 118 selected their preferred foods in 80% of the trials over three consecutive testing sessions, we concluded that that bear 119 recognized the pictures and moved to Phase 2. Note that this is a more stringent criteria than that used in other 120 similar studies, which required reaching 80% in 2 consecutive trials (Spetch and Friedman 2006; Truppa et al. 2009; 121 Wein et al. 2015). Remi was tested on 7 days over a 9 day period. Niko was tested on 3 days over a 7 day period. 122 123 Picture Recognition Transfer - Phase 2 124 In Phase 2, we tested whether the picture recognition transferred to novel stimuli (i.e., pictures that the bear had 125 never seen before). For the transfer, we used pictures of the three most preferred foods and three least preferred 126 foods that were not used in Phase 1 of the experiment. The experiment followed the same procedure as in Phase 1. 127 Each session consisted of 15 individual trials. When the bear selected their preferred food in 80% of the trials on 128 three consecutive testing sessions, we concluded that the bear recognized the pictures. For Phase 2, Remi was tested 129 on 5 days over a 5 day period and Niko was tested on 3 days over an 8 day period. 130 131 Results 132 Phase 1: With no prior exposure to pictures of food, Niko showed evidence of spontaneous picture recognition, 133 scoring at or above the 80% correct criteria in the first three sessions. Remi also showed evidence of picture 134 recognition; however, it took her seven sessions to reach the 80% correct criteria in three consecutive sessions 135 (Table 1). Although, Remi scored 93% and 100% on her first and second sessions, her performance dropped off 136 before she was successful. 137 Phase 2: In the picture recognition transfer phase, Niko met the criteria immediately, scoring above 80% correct on 138 the first three trials. It took Remi five trials to meet the criteria in this phase (Table 2). 139 140 Discussion 141 This task showed that sloth bears have the ability to recognize 2D pictures as equivalents of their real, 3D 142 counterparts. Both bears responded to the pictures of food just as they did the pieces of food during the preference 143 test phase, by using a characteristic sloth bear behavior of blowing (Laurie and Seidensticker 2009) to select the one 144 they wanted. While both bears recognized the pictures relatively quickly, Niko recognized the pictures 145 spontaneously, without any training, in both phases of the experiment. Remi acquired the skill through learning 146 (Bovet and Vauclair 2000) after a few sessions. We suspect it took Remi longer to acquire this skill because her 147 testing was impacted by factors of natural bear biology – hyperphagia, breeding season, and a pseudo-pregnancy – 148 which affected her food preferences, hunger, and motivation. Hyperphagia and breeding season did not affect Niko’s 149 performance since he was immediately successful and therefore went through the tests so quickly that he did not 150 encounter hyperphagia and breeding season during his tests. These physiological changes should be considered 151 when doing cognitive tests with any bear species. In order to properly assess food preferences in a species with such 152 seasonal variation, a wide variety of choices should be tested to create the clearest possible delineation between high 153 and low value foods. Alternatively, preferences could be tested at various times throughout the year, addressing each 154 physiological change. 155 Notably, Niko was able to demonstrate a spontaneous preference for photos that represented his preferred foods. 156 However, it is unclear what this truly means about a sloth bear’s cognition. Some hypothesize that animals that 157 recognize pictures spontaneously are simply confusing the pictures with the real objects (Bovet and Vauclair 2000). 158 It is unlikely that an animal with such a strong olfactory sense would make that mistake. Interestingly, when humans 159 are capable of picture recognition from a very early age (2-3 months old), those same researchers hypothesize that 160 the ability is simply innate (Bovet and Vauclair 2000). More research is needed to reveal the cognitive implications 161 of Niko recognizing all of the pictures spontaneously. 162 When animal caretakers are more familiar with the cognitive abilities of the animals in their care, they are better 163 able to provide the best possible care to their animals, addressing both their physical and mental needs. Utilizing 164 methods similar to those used in this study (choice between picture cards) could provide an opportunity for sloth 165 bears to communicate other preferences to their keepers (for example, preferences for specific enrichment items, 166 yard or enclosure access, or social partners). Adding this type of choice and control into their daily management can 167 positively enhance the welfare of bears under human care (Mellor 2014; Reiss 2006). 168 In conclusion, this study provides evidence that sloth bears can recognize 2D pictures of food as representations of 169 their 3D counterparts. Their ability to recognize 2D pictures of other items is likely. However, further research on 170 the cognitive abilities of sloth bears is recommended. Since little is known about the cognitive abilities of bears in 171 general, comparative studies with other bear species are also warranted. Future studies could include increasing the 172 sample size and comparing inter-individual differences for this methodology, comparing 2D picture recognition 173 ability in sloth bears to other bear species, as well as exploring whether this ability transfers to more abstract picture 174 representations such as black and white pictures, illustrations, or line drawings. 175 176 Acknowledgments 177 Thank you to Dr. Betsy Herrelko for her guidance and support as well as the entire NZP Asia Trail team who made 178 this work possible. 179 180 Compliance with ethical standards 181 All applicable international, national and/or institutional guidelines for the care and use of animals were followed. 182 All procedures performed in studies involving animals were in accordance with the ethical standards of the 183 institution or practice at which the studies were conducted. 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Table 2: Phase 2 Results Session 1 2 3 4 5 13/15 13/15 14/15 NIKO (87%) (87%) (93%) 9/15 10/15 12/15 12/15 12/15 REMI (60%) (67%) (80%) (80%) (80%) 243 244 Caption for Table 2: Number of correct trials out of 15 trials per session for Picture Recognition Transfer – Phase 245 2. 246