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The Use of PositiveReinforcement in TrainingZebra Sharks (Stegostomafasciatum)Ashley Marranzino a ba Downtown Aquarium , Denver , Coloradob Department of Biology , Regis UniversityPublished online: 24 Jun 2013.

To cite this article: Ashley Marranzino (2013) The Use of Positive Reinforcement inTraining Zebra Sharks (Stegostoma fasciatum), Journal of Applied Animal WelfareScience, 16:3, 239-253, DOI: 10.1080/10888705.2013.798555

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JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 16:239–253, 2013

Copyright © Taylor & Francis Group, LLC

ISSN: 1088-8705 print/1532-7604 online

DOI: 10.1080/10888705.2013.798555

The Use of Positive Reinforcement inTraining Zebra Sharks(Stegostoma fasciatum)

Ashley Marranzino1;2

1Downtown Aquarium, Denver, Colorado2Department 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 asso-

ciation 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, Uni-

versity of Rhode Island, 120 Flagg Road, Kingston, RI 02881. Email: ashley.marranzino@gmail.com

239

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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 train-

ing 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 desensiti-

zation 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

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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 fas-

ciatum, held at the Downtown Aquarium, Denver, to learn various behaviors as-

sociated 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 zijs-

ron), 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 desen-

sitized 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).

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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 2007. 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 2007.

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

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POSITIVE REINFORCEMENT IN TRAINING ZEBRA SHARKS 243

FIGURE 2 Targets for F1, M1, F2, and F3 in order from left to right (color figure available

online).

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

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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

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POSITIVE REINFORCEMENT IN TRAINING ZEBRA SHARKS 245

FIGURE 3 M2 responding to a target moved away from wall (color figure available

online).

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,

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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

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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).

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Once the sharks were determined to be desensitized to the presence of mul-

tiple 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 pre-

sented 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).

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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

M1 8 7 7 6 Not achieved Not achievedF1 Not achieved 8 10 10 Not achieved Not achieved

F2 4 3 7 7 Not achieved Not achievedF3 4 2 4 4 7 8

Note. Significant steps in the training regimen are noted with the number of weeks after the beginningof the training regimen to achieve each step. Not all training goals were achieved for all zebra sharks.

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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.

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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 vari-

ations 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 back-

grounds. 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

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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 move-

ment 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.

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