The Use of Positive Reinforcement in Training Zebra Sharks (Stegostoma fasciatum)

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1 This article was downloaded by: [Dr Kenneth Shapiro] On: 09 June 2015, At: 11:00 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: Registered office: Mortimer House, Mortimer Street, London W1T 3JH, UK Journal of Applied Animal Welfare Science Publication details, including instructions for authors and subscription information: The Use of Positive Reinforcement in Training Zebra Sharks (Stegostoma fasciatum) Ashley Marranzino a b a Downtown Aquarium, Denver, Colorado b Department of Biology, Regis University Published online: 24 Jun To cite this article: Ashley Marranzino (2013) The Use of Positive Reinforcement in Training Zebra Sharks (Stegostoma fasciatum), Journal of Applied Animal Welfare Science, 16:3, , DOI: / To link to this article: PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the Content ) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.

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3 JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 16: , 2013 Copyright Taylor & Francis Group, LLC ISSN: print/ online DOI: / The Use of Positive Reinforcement in Training Zebra Sharks (Stegostoma fasciatum) Ashley Marranzino 1;2 1 Downtown Aquarium, Denver, Colorado 2 Department of Biology, Regis University Positive reinforcement training (PRT) was used on 4 adult zebra sharks, Stegostoma fasciatum, housed at the Downtown Aquarium, Denver, to determine the ability of zebra sharks to become desensitized to various stimuli associated with veterinary procedures. One male and 3 female sharks were trained for 12 weeks. As a result of PRT, all 4 zebra sharks were desensitized to staying within a closed holding tank off of the main exhibit, the presence of multiple trainers in the closed holding tank, and tactile stimulation. One of the 4 zebra sharks was also successfully desensitized to the presence of a stretcher being brought into the holding tank. All of these procedures are common in veterinary examinations, and it is hoped that desensitization to these stimuli will reduce the stress associated with examinations. The training accomplished has allowed for easier maintenance of the zebra sharks by the aquarium staff and an improvement in the care of the sharks. Keywords: aquarium husbandry, desensitization, operant conditioning Operant conditioning is widely used in behavioral studies. By causing an association between a behavior and a consequential stimulus, operant conditioning is used to alter the frequencies of behaviors (Reynolds, 1968). Two main types of conditioning are employed to alter behaviors: negative reinforcement, where an unfavorable stimulus is delivered to decrease the occurrence of a behavior, and positive reinforcement, where a reward such as food is delivered when desired behaviors are performed, thereby increasing the frequency with which Ashley Marranzino is now at the University of Rhode Island. Correspondence should be sent to Ashley Marranzino, Department of Biological Sciences, University of Rhode Island, 120 Flagg Road, Kingston, RI ashley.marranzino@gmail.com 239

4 240 MARRANZINO these behaviors occur (Reynolds, 1968). Since it became popularized by B. F. Skinner (Skinner, 1938), operant conditioning has become a very important tool in behavioral training, especially in nonhuman animals. Positive reinforcement training (PRT) is commonly used for treatment of animals in captivity to allow for better animal care (Laule, Bloomsmith, & Schapiro, 2003). In recent years, PRT has found its home in many laboratories and zoos in efforts to teach captive animals to voluntarily participate in their research or husbandry behaviors (Fernstrom, Fredlund, Spangberg, & Westlund, 2009). For nearly 80 years, training has been used on marine mammals to facilitate husbandry practices and help with the care of these animals (Brando, 2010). Beginning in the 1940s, Marian and Keller Breland worked with the use of PRT techniques for commercial use, training animals to cooperate in behaviors for public shows and for naval operations (Bailey & Gillaspy, 2005). Through training marine animals to do tricks for public pleasure, it was soon realized that the training procedures could also be used for improving animal welfare by gaining voluntary cooperation to participate in husbandry procedures (Laule et al., 2003). Today, marine mammal training is a common practice, and animals have been trained to move on and off exhibit, enter transportation chambers, and voluntarily undergo a variety of veterinary procedures including blood draws, urine and stool collection, semen collection, and in vitro fertilization (Brando, 2010). PRT allows a positive association to be made with desired behaviors and generates an animal s voluntary cooperation with the training (Laule et al., 2003). This has been shown to reduce the amount of stress on the animal (Brando, 2010; Fernstrom et al., 2009; Laule et al., 2003; Weiss & Wilson, 2003) while making husbandry practices less time-consuming and easier on the staff caring for the animals (Weiss & Wilson, 2003). A very useful PRT tool is desensitization. By pairing an uncomfortable or frightening stimulus with a positive reward, the negative reaction to the stimuli is gradually reduced. This can result in desensitization to the uncomfortable stimulus and potentially reduce the stress the animal associates with the stimulus (Laule et al., 2003; Weiss & Wilson, 2003). PRT has been widely used among nonhuman primates and marine mammals for several decades; however, training programs are just now finding a home in public aquariums (Snowden, 2007). Recently, studies involving fish cognition and learning abilities have been undertaken and it has been found that processes of learning in fishes are similar to those of land vertebrates (Guttridge, Myrberg, Porcher, Sims, & Krause, 2009) and that fishes are capable of social learning (Brown & Laland, 2003) and behaviors similar to those seen in primates (Bshary, Wickler, & Fricke, 2002). Due to the interest in fish farming, studies on fish learning have been relatively focused on commercially important teleosts and freshwater fishes who are easily bred and kept in captivity (Guttridge et al., 2009). Due to their large size and the fact that they are difficult to care for in captivity, shark cognition has not been as widely studied. Learning experiments

5 POSITIVE REINFORCEMENT IN TRAINING ZEBRA SHARKS 241 were first conducted on sharks in the 1950s by Eugenie Clark s team using operant conditioning (Guttridge et al., 2009). Because they have less complex brain structures compared with bony fishes and mammals, elasmobranchs were believed to have reduced learning abilities (Aronson, Aronson, & Clark, 1967). However, sharks have been trained to hit targets on command through the use of operant conditioning regimens (Aronson et al., 1967; Guttridge et al., 2009), and evidence has been found that sharks are able to learn to discriminate as rapidly as mice and teleost species when given comparable tasks (Aronson et al., 1967). Aquariums such as the Pittsburgh Zoo & PPG Aquarium have begun to implement training regimens, further demonstrating the ability of sharks to learn desired behaviors through operant conditioning (Snowden, 2007). The current study assesses the ability of four zebra sharks, Stegostoma fasciatum, held at the Downtown Aquarium, Denver, to learn various behaviors associated with veterinary procedures. Native to the Indo-Pacific, zebra sharks are demersal fish who feed upon mollusks, small bony fish, crustaceans, and other invertebrates (Dudgeon, Broderick, & Ovenden, 2009; Rasmussen & Reum, 2005). These sharks are often found in public aquariums (Dudgeon et al., 2009; Snowden, 2007) and have an approximate life span of 25 years in captivity (Martin, 2003). The Downtown Aquarium, Denver, is home to four adult zebra sharks. The sharks are housed in an exhibit with other elasmobranchs, including sandbars (Carcharhinus plumbeus), sand tigers (Carcharias taurus), sawfish (Pristis zijsron), and mixed teleosts. When they were added to the tank, the zebra sharks, who are normally benthic feeding fish, were trained to come to the surface and feed after touching a target (a piece of PVC sheet) to make feeding and diet maintenance easier for aquarists. Original training was performed to allow the sand tiger and sandbar sharks on exhibit to feed separately from the zebra sharks, aiding in diet maintenance for all three shark species in the exhibit. The new zebra shark training regimen described in this article was undertaken to assess the ability of the zebra sharks to be trained to move on and off exhibit on command and become desensitized to various stimuli including being within a closed holding tank, the presence of trainers in the holding tank, tactile stimulation, and the presence of a stretcher, with the hope of alleviating stress to the sharks during veterinary examinations. MATERIALS AND METHODS The training took place in an 18-foot-deep tank (approximately 32 feet wide by 56 feet long) with an attached holding tank approximately 10 feet wide by 12 feet long by 4.5 feet deep (Figure 1).

6 242 MARRANZINO FIGURE 1 Diagram of the tank zebra sharks were trained in. Solid lines indicate the boundaries of the main exhibit and dashed lines indicate the holding tank. Numbers show feeding locations: 1 indicates the initial zebra shark target feeding location and 2 indicates the new target feeding location used for the new training regimen. Subjects Four adult zebra sharks held in the tank were subjects of the training regimen: 3 females (F1, F2, and F3) and 1 male (M1). F1 and M1 were caught in the wild and brought to the aquarium in 1999 as adults from Cannes, Australia. F2 was obtained from a private broker in Nevada in 2000 as an adult. F3 was the only captive-bred zebra shark housed at the Downtown Aquarium, Denver, and was the youngest of the 4 sharks. She was born at the Shedd Aquarium in Chicago, Illinois, and brought to the Downtown Aquarium, Denver, in Exact ages of the 3 live-caught sharks are unknown, but F3 was brought to the Downtown Aquarium, Denver, only a few months after her birth in Prior Training All 4 sharks were initially trained to surface feed, feeding at the surface of the water from an aquarist outside of the tank, after touching a target with their rostrum. This targeting, defined by the shark touching his or her rostrum to a PVC sheet target for at least one second before food was presented, originally took place on the side of the exhibit opposite the holding tank. The feeding area was moved to the other side of the tank, adjacent to the holding area, to facilitate training the sharks to move on and off exhibit (Figure 1). In an attempt to separate 1 shark from the other 3, each individual zebra shark received his or her own target (Figure 2). In the initial phases of this training regimen, F1 and F2 were the most responsive to the new targets and were the first to come

7 POSITIVE REINFORCEMENT IN TRAINING ZEBRA SHARKS 243 FIGURE 2 online). Targets for F1, M1, F2, and F3 in order from left to right (color figure available to the targets for feedings. All 4 sharks began coming over to the new feeding location and targeting within 2 weeks. New Training Regimen The zebra sharks were fed three times a week during the public feeding of the sandbar sharks and sand tiger sharks. This allowed the other sharks to be fed without distraction from the zebra sharks and for specific records of each zebra shark s diet to be kept. Twice a week when there was no public shark feed taking place, more individualized training sessions were held with whichever zebra sharks were willing to participate. All training sessions were completed using PRT. Successful Targeting Each zebra shark was presented with his or her individual target. In order to receive a food reward, the zebra shark was required to successfully target. This was distinguished by the individual breaking his or her swimming pattern and

8 244 MARRANZINO pressing his or her rostrum to the target for at least 1 s. When the desired behavior was performed, a food reward was immediately held to the zebra shark s mouth to reinforce the behavior. Once the shark consistently and successfully targeted, the shark was required to remain in contact with the target for increasing periods of time. Successful targeting was measured by the ability to follow one target and respond by targeting to it at various positions, not just at its position next to the wall. Targets were moved through the water while the zebra shark kept his or her rostrum in contact with the target. If the target could be moved to the side or even behind the zebra shark and the individual still responded and moved to successfully target on multiple occasions, the shark was considered successfully target trained (Figure 3). Bringing Zebra Sharks Into Holding Two times a week, when the public shark feed was not taking place, the zebra sharks were given more individualized attention. In order to do this, they were brought into the holding tank to isolate them from other distractions caused by other animals on exhibit interfering with the training sessions. Metal feeding tongs were hit on the side of the wall in the method normally used to call the zebra sharks to their feeding area during shark feeds. When a zebra shark approached, it was moved through the holding tank entrance and given a reward for coming into the holding tank. Movement into the holding tank was progressively trained. First, the sharks were baited into the holding tank by having the shark follow a presented piece of food through the holding tank doors. Second, the target was presented and, while the shark targeted, moved directly to the holding door opening before the food reward was presented to bait the shark in the remaining distance. As a final training step, the target was presented from within the holding tank, visible to the sharks through the open doors, and the sharks were required to swim into the holding tank and target before a reward was presented. Acclimation to the holding tank also took place in stages. Initially, sharks were brought into the holding tank and targets were presented for rewards while the holding doors remained open so the shark could leave the holding tank at will. After several training sessions with the doors open, the zebra sharks were brought into the holding tank and the doors were closed to keep the sharks from leaving before the training session was over and to keep other animals from entering and distracting the sharks. While in the holding tank, the target was presented and rewards were given for targeting (Figure 4). If the zebra shark appeared stressed (distinguished by changed swimming patterns) due to being in the holding tank with closed doors, food rewards were given without requiring targeting to create a positive association with the holding tank. When individuals showed no apparent changes

9 POSITIVE REINFORCEMENT IN TRAINING ZEBRA SHARKS 245 FIGURE 3 online). M2 responding to a target moved away from wall (color figure available in swimming pattern while in the closed holding tank, they were only rewarded for targeting. Because the individuals were less distracted by other animals on exhibit, it was easier to move the target around and allow them to follow it than during training sessions during shark feeds. Training sessions lasted until the zebra sharks had received their allotted rewards for the training session or when the sharks appeared to be losing interest in the target and began swimming around the holding tank rather than approaching the target. In the latter case,

10 246 MARRANZINO FIGURE 4 F1 receiving reward after targeting to a trainer out of the water while in the closed holding tank (color figure available online). one more reward was presented to end the training session on a positive note before the holding doors were opened. Desensitization to Veterinary Procedures After the individual sharks consistently came into holding and were determined to be desensitized to targeting within the holding tank (distinguished by their ability to target in the closed holding tank as they normally would while on exhibit), acclimation to a person being in the water with the sharks began. The zebra sharks were called into the holding tank as previously mentioned and the target was presented. After targeting once successfully, the trainer would enter

11 POSITIVE REINFORCEMENT IN TRAINING ZEBRA SHARKS 247 the holding tank with the shark. At first the trainer would stand in the tank near the target (which was being held by a second trainer out of the water) out of arm s reach of the zebra shark. When the shark behaved as normally observed within holding, the trainer in the water would gradually move closer and closer to the target, prompting the zebra shark to be in close proximity to the trainer in order to receive a reward. Eventually, the in-water trainer would take the target from the trainer outside of the water and the sharks would be required to target to the trainer in the water to receive a reward (Figure 5). When the shark behaved normally while one trainer was in the water, a second trainer was brought into the water to desensitize the zebra shark to the presence of multiple people in the confined space as would be common of most veterinary procedures. FIGURE 5 F3 targeting to an in-water trainer within the closed holding tank (color figure available online).

12 248 MARRANZINO Once the sharks were determined to be desensitized to the presence of multiple trainers in the tank, designated by consistent targeting, tactile conditioning began. Tactile conditioning began with the presence of only one trainer in the water with the sharks. Whenever the zebra shark targeted, the trainer would stroke the zebra shark laterally while the individual received a reward. Once the individual showed observably normal behavior while being presented with tactile stimulation from the trainer, the stretcher was brought into the holding tank to desensitize the zebra shark to the presence of a stretcher that would be used in veterinary procedures (Figure 6). The trainer would get into the holding tank as mentioned earlier and, while the zebra shark was targeting, the stretcher was gradually opened to allow the shark to get used to its presence. The stretcher was gradually brought nearer to the target prompting the zebra shark to swim closer to the stretcher for a food reward. If the shark swam to the stretcher and came in contact with it, food rewards were given to try to desensitize the sharks to touching the stretcher. Gradually the target was placed in the opening of the stretcher, so the zebra sharks were called to place their rostrum in the stretcher entrance to receive a reward. The target was then moved farther within the stretcher opening. If the zebra sharks voluntarily swam entirely into the stretcher after targeting within the stretcher entrance, rewards were given to the FIGURE 6 Stretcher used for desensitization procedures being unfolded during a training session by in-water trainer (color figure available online).

13 POSITIVE REINFORCEMENT IN TRAINING ZEBRA SHARKS 249 sharks continuously for the duration the sharks remained in the stretcher before swimming out. RESULTS Training occurred over a 12-week time period in which all 4 zebra sharks achieved three distinct training goals: desensitization to being in a closed holding tank, desensitization to the presence of trainers within the holding tank, and desensitization to tactile stimulation. Three of the 4 zebra sharks achieved a fourth training goal (reliably following a target away from the wall) and 1 achieved a fifth training goal (desensitization to the presence of a stretcher). Each shark responded differently to training procedures, and different lengths of time were required to finish each training goal for the individual sharks (Table 1). On average, it took 5.3 weeks for each shark to be trained to follow a target away from a wall and respond to a target being placed in various positions around the shark s body. An average of 5 weeks was required to desensitize the sharks to being in a holding tank with closed doors. The zebra sharks became desensitized to the presence of trainers in the holding tank with them within an average of 7 weeks from the beginning of training, and within 6.75 weeks of training on average, the sharks had become desensitized to tactile stimulation. F3 was the most responsive to new training steps. F2 also responded very quickly to new stimuli, whereas M1 and F1were much slower to respond and required smaller steps to become acclimated to different procedures. F2 and F3 both were considered able to successfully target within 4 weeks of the start of the training sessions. By this point, they both would obviously break their swimming pattern, touch their rostrums to the target for at least 1 s, and when the target was moved on the sides of their heads and away from the wall, they would move in response and target. TABLE 1 Training Landmarks Achieved by Each Zebra Shark Shark Follow Target Away From Wall Desensitized to Being in Closed Holding Tank Desensitized to Trainer in Holding Tank Desensitized to Tactile Stimulation Desensitized to Stretcher Presence Began Desensitization to Swimming Into Stretcher M Not achieved Not achieved F1 Not achieved Not achieved Not achieved F Not achieved Not achieved F Note. Significant steps in the training regimen are noted with the number of weeks after the beginning of the training regimen to achieve each step. Not all training goals were achieved for all zebra sharks.

14 250 MARRANZINO It took M1 around 6 weeks to noticeably target. It took longer for M1 and F1 to respond to being called to the feeding area and neither would generally stay for more than 30 s, whereas F2 and F3 would frequently stay at the training site for 5 min or longer. Because F1 and M1 were less responsive, smaller steps were taken in their training. First F1 and M1 were rewarded just for coming to the feeding area, then they were baited toward their targets, and finally they were not given rewards unless they targeted on their own. Even as F1 became more responsive to targeting, she did not distinctively target: instead of actively breaking her swimming pattern to approach the target and touch the target with her rostrum, she would generally run into the target while continuing with her swimming pattern. She frequently would brush against her target without hitting it with her rostrum and then swim away, but she was only rewarded when her rostrum touched the target for at least 1 s. As with the targeting, each shark progressed at different rates for training procedures within the holding tank. Participation in the more individualized training sessions was entirely dependent upon the sharks coming to the feeding area when called. Because each shark responded differently to being called to the feeding area, times required to progress in the training varied greatly among individuals. F2 and F3 were both determined to be acclimated to being in the holding tank within one training session (3 weeks and 2 weeks after the onset of training, respectively). After four training sessions, desensitization to the presence of a person in the water was started. F2 proceeded to target as usual and no visible differences in behavior were observed. Because F2 behaved as normal while exposed to the new stimuli of the presence of the trainer in the water, tactile conditioning was attempted in the same session. No visible changes in behavior or swimming pattern were seen when the trainer approached or when the trainer touched her and even stroked her down the entire lateral side of her body, and she was considered desensitized to tactile stimulation 7 weeks after the beginning of training. Upon beginning stretcher acclimation, F2 showed initial interest to the stretcher breaking her swimming pattern to approach the stretcher but not coming in contact with it. However, after the first introduction to the stretcher, F2 seemed to be less interested in targeting near the stretcher and would swim away from the stretcher after coming in contact with it. F3 did not come into the holding tank as frequently, yet she moved forward with the training steps more readily. Within three training sessions (2 weeks after the beginning of training) of targeting with the holding doors closed, she was considered desensitized to being in the holding tank and desensitized to both the presence of a trainer in the holding tank and tactile stimulation 4 weeks after the start of training. Within six sessions (7 weeks after the beginning of training) F3 was considered ready to begin acclimation to the stretcher. When the stretcher was completely unfolded, F3 showed no negative response and even swam into it partially when the target was presented on top of the stretcher.

15 POSITIVE REINFORCEMENT IN TRAINING ZEBRA SHARKS 251 F1 and M1 showed behavioral changes in the holding tank with doors closed and would swim in circles around the holding tank and continually brush against the closed doors. It took 7 and 8 weeks for M1 and F1 to become desensitized to being in the closed holding tank, respectively. Although M1 appeared agitated and did not display usual swimming patterns, he would break his swimming pattern to eat food rewards when presented, suggesting he was not overstressed. M1 also was introduced to tactile stimulation when he swam near enough to be touched. No visible behavioral change or apparent negative response was seen when this occurred, and it was determined that M1 had become desensitized to tactile stimulation after 6 weeks. M1 was not responsive to the target while in the holding tank and would not target unless baited toward his target. F1 became desensitized to the presence of trainers in the holding tank and tactile stimulation 10 weeks after the start of the training regimen and, like the other 3 sharks, showed no behavioral changes when introduced to tactile conditioning. F1 did not respond to the target within the holding tank either. However, because both F1 and M1 were the least responsive to the targets outside of the holding tank, targeting within holding was not considered a necessity for moving forward in the training process, and it was determined that tactile conditioning could begin without consistent targeting. DISCUSSION Each shark took different lengths of time to reach training milestones. The variations in training times were partly caused by different levels of responsiveness among each shark. Because training sessions could not begin without a shark s appearance at the feeding area when called, each shark received a different amount of training. F3 was the most responsive to approaching the feeding area when called and therefore participated in training sessions more frequently. Conversely, F1 and M1 were not as responsive to approaching the feeding area when called and received less training. The responsiveness of each shark could be caused by their various backgrounds. F3 was the most responsive zebra shark. This could be an artifact of her breeding in captivity. Because she has spent her entire life in captivity, becoming desensitized to the stimuli presented might not have been as difficult as it was for the 3 wild-caught sharks. Sharks who have become desensitized to life in captivity may be more responsive to behavioral training regimens compared with mature, wild-caught individuals. Age might have also be a factor in the slower responses of F1 and M1. Similar to the decrease in learning ability reported in rats as they grow older (Liu, 1982), the learning capacity of the zebra sharks may decrease with age. Although they had different rearing backgrounds, F2 and F3, the 2 youngest sharks, progressed with training in fewer sessions than

16 252 MARRANZINO F1 and M1, lending support to the conclusion that age plays a role in learning ability. This training regimen successfully desensitized the 4 zebra sharks to movement on and off exhibit, tactile stimulation, and the presence of a stretcher. The training of these sharks has made it easier for aquarists to maintain a consistent diet for the sharks. Previously, the sharks would only come to feed during shark feeds intermittently and would more frequently try to catch food being given to other fish in the exhibit. After implementation of this training regimen, the 4 zebra sharks come to their designated feeding area during almost every shark feed, making it much easier to monitor exactly what each shark is being fed and giving aquarists the ability to supplement each shark s diet with necessary vitamins. Training sessions within the holding tank have also made it much easier to examine the sharks on a regular basis. Because the sharks have become desensitized to touch, regular physical examinations of the sharks have become easier. CONCLUSION Training endeavors with these sharks are ongoing. Future training goals for the zebra sharks include desensitization to being held in the stretcher, tactile conditioning within the stretcher, and desensitization to taking blood samples. By continuing training, it is hoped that any stress experienced by sharks during veterinary checkups will be minimized, allowing for overall better health care for the sharks on exhibit in the aquarium. ACKNOWLEDGMENTS I thank the Downtown Aquarium, Denver, for supporting my research. Special thanks to Christine Light, Jen Oelschlager, and Lori Boatwright for helping during the training process and to Judy Rowe for advising me on the training progression and for helping with the procedures during training sessions. I also thank my advisor, Dr. Catherine Kleier, for all of her help and mentoring during this process. REFERENCES Aronson, L. R., Aronson, F. R., & Clark, E. (1967). Instrumental conditioning and light-dark discrimination in young nurse sharks. Bulletin of Marine Science, 17, Bailey, R. E., & Gillaspy, J. A. (2005). Operant psychology goes to the fair: Marian and Keller Breland in the popular press, The Behavior Analyst, 28,

17 POSITIVE REINFORCEMENT IN TRAINING ZEBRA SHARKS 253 Brando, S. I. C. A. (2010). Advances in husbandry training in marine mammal care programs. International Journal of Comparative Psychology, 23, Brown, C., & Laland, K. N. (2003). Social learning in fishes: A review. Fish and Fisheries, 4, Bshary, R., Wickler, W., & Fricke, H. (2002). Fish cognition: A primate s eye view. Animal Cognition, 5, Dudgeon, D. L., Broderick D., & Ovenden, J. R. (2009). IUCN classification zones concord with, but underestimate, the population genetic structure of the zebra shark Stegostoma fasciatum in the Indo-West Pacific. Molecular Ecology, 18, Fernstrom, A. L., Fredlund, H., Spangberg, M., & Westlund, K. (2009). Positive reinforcement training in rhesus macaques-training progress as a result of training frequency. American Journal of Primatology, 71, Guttridge, T. L., Myrberg, A. M., Porcher, I. F., Sims, D. W., & Krause, J. (2009). The role of learning in shark behavior. Fish and Fisheries, 10, Laule, G. E., Bloomsmith, M. A., & Schapiro, S. J. (2003). The use of positive reinforcement training techniques to enhance the care, management, and welfare of laboratory primates. Journal of Applied Animal Welfare Science, 6, Liu, S. Y. (1982). The relation of age to the learning ability of the white rat. Journal of Comparative Psychology, 8(1), Martin, R. A. (2003). Order Orectolobiformes: Carpet sharks in biology of sharks and rays. Retrieved from Rasmussen, P., & Reum, J. (2005). Stegostoma fasciatum. Retrieved from ummz.umich.edu/site/accounts/information/stegostoma_fasciatum.html Reynolds, G. S. (1968). A primer of operant conditioning. New York, NY: Scott, Foresman and Company. Skinner, B. F. (1938). The behavior of organisms: An experimental analysis. New York, NY: Appleton-Century. Snowden, R. (2007). Target training and tactile conditioning of two zebra sharks, Stegostoma fasciatum. Drum and Croaker, 39, Weiss, E., & Wilson, S. (2003). The use of classical and operant conditioning in training Aldabra tortoises (Geochelone gigantea) for venipuncture and other husbandry issues. Journal of Applied Animal Welfare Science, 6,