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Creative Control

Permanent Link: http://ncf.sobek.ufl.edu/NCFE004223/00001

Material Information

Title: Creative Control An Explanation of Species-Specific Enrichment in Mongoose Lemurs (Eulemur Mongoz) and Bottlenose Dolphins (Tursiops Truncatus)
Physical Description: Book
Language: English
Creator: Brown, Hannah
Publisher: New College of Florida
Place of Publication: Sarasota, Fla.
Creation Date: 2010
Publication Date: 2010

Subjects

Subjects / Keywords: Mongoose Lemur
Bottlenose Dolphin
Environmental Enrichment
Captivity
Human-Animal Interaction
Genre: bibliography   ( marcgt )
theses   ( marcgt )
government publication (state, provincial, terriorial, dependent)   ( marcgt )
born-digital   ( sobekcm )
Electronic Thesis or Dissertation

Notes

Abstract: Creative enrichment designed for a species, or even for a specific individual, can provide an animal with environmental stimulation that may lead to a whole array of benefits for the animal. Exposure to speciesspecific enrichment, or enrichment that is designed for the adaptations of a particular species, encourages naturalistic behaviors by providing cues that are more biologically salient than a more generalized enrichment item. This study explores the relationship between species-specific stimuli and the production of naturalistic behaviors. An acoustic enrichment device was presented to two captive mammalian groups: mongoose lemurs (Eulemur mongoz) and bottlenose dolphins (Tursiops truncatus). Both species are highly social and communicate via vocalizations, but are they diverse in their cognitive and physiological adaptations as well as their evolutionary history. Naturalistic vocalizations from each species and a control (silence) made up three acoustic conditions that alternated during two 26-min sessions for each group. A 26-min baseline period was recorded for each group prior to object introduction. Behaviors and vocalizations were analyzed from video and audio recordings. Lemurs spent very little time interacting with the object, but they displayed more locomotion and less resting behavior during experimental sessions than the baseline session. Lemurs vocalized more when the object was present than during baseline; soft grunts were the most common vocalizations produced during any condition. Dolphins displayed more interaction/orientation behaviors overall when the experimental object was present than during the baseline condition, and they spent more time overall with the device when it was producing lemur vocalizations than when it was producing dolphin vocalizations. Dolphins spent more time vocalizing when the experimental object was present than during the baseline condition; clicks were the most common vocalizations produced by dolphins overall. These data suggest that an acoustic enrichment device will elicit an increase in a variety of behaviors, including vocalizations, in vocal species.
Statement of Responsibility: by Hannah Brown
Thesis: Thesis (B.A.) -- New College of Florida, 2010
Electronic Access: RESTRICTED TO NCF STUDENTS, STAFF, FACULTY, AND ON-CAMPUS USE
Bibliography: Includes bibliographical references.
Source of Description: This bibliographic record is available under the Creative Commons CC0 public domain dedication. The New College of Florida, as creator of this bibliographic record, has waived all rights to it worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law.
Local: Faculty Sponsor: Harley, Heidi

Record Information

Source Institution: New College of Florida
Holding Location: New College of Florida
Rights Management: Applicable rights reserved.
Classification: local - S.T. 2010 B87
System ID: NCFE004223:00001

Permanent Link: http://ncf.sobek.ufl.edu/NCFE004223/00001

Material Information

Title: Creative Control An Explanation of Species-Specific Enrichment in Mongoose Lemurs (Eulemur Mongoz) and Bottlenose Dolphins (Tursiops Truncatus)
Physical Description: Book
Language: English
Creator: Brown, Hannah
Publisher: New College of Florida
Place of Publication: Sarasota, Fla.
Creation Date: 2010
Publication Date: 2010

Subjects

Subjects / Keywords: Mongoose Lemur
Bottlenose Dolphin
Environmental Enrichment
Captivity
Human-Animal Interaction
Genre: bibliography   ( marcgt )
theses   ( marcgt )
government publication (state, provincial, terriorial, dependent)   ( marcgt )
born-digital   ( sobekcm )
Electronic Thesis or Dissertation

Notes

Abstract: Creative enrichment designed for a species, or even for a specific individual, can provide an animal with environmental stimulation that may lead to a whole array of benefits for the animal. Exposure to speciesspecific enrichment, or enrichment that is designed for the adaptations of a particular species, encourages naturalistic behaviors by providing cues that are more biologically salient than a more generalized enrichment item. This study explores the relationship between species-specific stimuli and the production of naturalistic behaviors. An acoustic enrichment device was presented to two captive mammalian groups: mongoose lemurs (Eulemur mongoz) and bottlenose dolphins (Tursiops truncatus). Both species are highly social and communicate via vocalizations, but are they diverse in their cognitive and physiological adaptations as well as their evolutionary history. Naturalistic vocalizations from each species and a control (silence) made up three acoustic conditions that alternated during two 26-min sessions for each group. A 26-min baseline period was recorded for each group prior to object introduction. Behaviors and vocalizations were analyzed from video and audio recordings. Lemurs spent very little time interacting with the object, but they displayed more locomotion and less resting behavior during experimental sessions than the baseline session. Lemurs vocalized more when the object was present than during baseline; soft grunts were the most common vocalizations produced during any condition. Dolphins displayed more interaction/orientation behaviors overall when the experimental object was present than during the baseline condition, and they spent more time overall with the device when it was producing lemur vocalizations than when it was producing dolphin vocalizations. Dolphins spent more time vocalizing when the experimental object was present than during the baseline condition; clicks were the most common vocalizations produced by dolphins overall. These data suggest that an acoustic enrichment device will elicit an increase in a variety of behaviors, including vocalizations, in vocal species.
Statement of Responsibility: by Hannah Brown
Thesis: Thesis (B.A.) -- New College of Florida, 2010
Electronic Access: RESTRICTED TO NCF STUDENTS, STAFF, FACULTY, AND ON-CAMPUS USE
Bibliography: Includes bibliographical references.
Source of Description: This bibliographic record is available under the Creative Commons CC0 public domain dedication. The New College of Florida, as creator of this bibliographic record, has waived all rights to it worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law.
Local: Faculty Sponsor: Harley, Heidi

Record Information

Source Institution: New College of Florida
Holding Location: New College of Florida
Rights Management: Applicable rights reserved.
Classification: local - S.T. 2010 B87
System ID: NCFE004223:00001


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Running Head: SPECIES SPECIFIC ENRICHMENT AND NATURAL BEHAVIOR S CREATIVE CONTROL: AN EXPLORATION OF SPECIES SPECIFIC ENRICHMENT IN MONGOOSE LEMURS ( EULEMUR MONGOZ ) AND BOTTLENOSE DOLPHINS ( TURSIOPS TRUNCATUS ) BY HANNAH BROWN A Thesis Submitted to the Division of Social Sciences New College of Florida in partial fulfillment for the requirements for the degree Bachelor of Arts Under the Sponsorship of Dr. Heidi Harley Sarasota, Florida May, 2010

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!! Acknowledgements I am in great debt to my thesis sponsor, Dr. Heidi Harley, for her continuous involvement and counsel. Thank you to Dr. Gordon Bauer and Dr. Maria Vesperi for their guidance with this project and throughout my New College educatio n. Wendi Fellner, Mo nica Mogilewsky Jenna Clark and Leandra Lyniuk contributed significantly to the process before, during and after data collection. The Lemur Conservation Foundation provided genuine encouragement and exhibited particular tolerance durin g the last minute changes of the research process. This is LCF publication # 16. T he trainers at a facility in Orlando deserve equal acknowledgement, with special respect to George for his skillful craftsmanship Marty MacPhee, Mikel Delgado and Pattie Wals h provided unique insights into this project and into the field of animal caretaking. My family is an endless source of support and ideas for me. My friends are just as cheris hed. Thank you, Isaac Brown and Anastasia Sallen for your engineering expertise. And thank you, Ida, for paving the way.

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!!! Table of Contents I. Acknowledgements. i i II. List of Figur es/Graphs iv III. Abstract v IV. Introduction.1 V. Literature Review 3 VI. Study 1 36 VII. Study 2 43 VIII. General Discussion .48 IX. References ... 53 X. Appendix A 64 XI. Appendix B 65 XII. Appendix C .82

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!# List of Figures/ Graphs 1. Figure 1. Spectrograms of Selected Vocalizations in E. mongoz .28 2. Figure 2. Spectrograms of Selected Vocalizations in T. tursio ps .. 33 3. Figure 3. Enrichment Device During Testing Session with E. mongoz 39 4. Figure 4 (a) Timeline of auditory sequence during session 1 (b) Timeline of auditory sequence during session 2 .... 41 5. Table 1. Vocalizations Emitted and Behavioral Context in E. mongoz ... 42 6. Table 2. Operation Definitions fo r Behavioral Repertoire in E. mongoz ... 43 7. Figure 5. Enrichment Device During Testing Session with T.tursiops 47 8. Table 3 Vocalizations Emitted and Behavioral Context in T. tursiops 49 9. Figure 6 Type of Vocalizations Produced by Session in E. mongoz and T. tursiops 58 10. Figure 7 Vocalizations by Condition in E. mongoz ... 59 11. Figure 8 Comparison of Behavioral Means in E. mongoz ....60 12. Figure 9 Behaviors Produced by Auditory Condition in E. mongoz ..... 61 13. Figure 10 Interaction with Objects by Auditory Condition in T. tursiop s 62 14. Figure 11 Vocalizations by Session and Type in T. tursiops 63

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# CREA TIVE CONTROL: AN EXPLORA TION OF SPECIES SPECIFIC ENRICH M E NT IN MONGOOSE LEMURS ( EULEMUR MONGOZ ) AND BOTTLENOSE DOLPHINS ( TURSIOPS TRUNCATUS ) Hannah Brown New College of Florida, 2010 ABSTRACT Creative enrichment designed for a species, or even for a specific individual, can provide an animal with environmental stimulation that may lead to a whole array of benefits for the animal. Exposure to species specific enrichment, or enrichment that is designed for the adaptations of a particular species, encourages naturalistic behaviors by providing cues that are more biologically salient than a more generalized enr ichment item. This study explores the relationship between species specific stimuli and the production of naturalistic behaviors. An acoustic enrichment device was presented to two captive mammalian groups : mongoose lemurs ( Eulemur mongoz ) and bottlenose d olphins ( Tur s i ops truncatus ). Both species are highly social and communicate via vocalizations, but are they diverse in their cognitive and physiological adaptations as well as their evolutionary history Naturalistic vocalizations from each species and a contr ol (silence) mad e up three acoustic conditions that alternated during two 26 min sessions for each group. A 26 min baseline period was recorded for each group prior to object introduction. B ehaviors and vocalizations were analyzed from video and audio reco rdings Lemurs spent very little time interacting with the object, but they dis played more locomotion and less resting behavior during experimental sessions than the baseline session Lemurs vocalized more when the object was present than during baseline; soft grunts were the most common vocalizations produced during any condition. D olphins displayed more

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#! interaction/orientation behaviors overall when the experimental object wa s present than during the baseline condition and they spent more time overall wit h the device when it was producing lemur vocalizations than when it was produc ing dolphin vocalizations. Dolphins spent more time vocalizing when the experimental object was present than during the baseline condition; clicks were the most common vocalizati ons produced by dolphins overall. These data suggest that an acoustic enrichment device will elicit an increase in a variety of behaviors, including vocalizations, in vocal species. Dr. Heidi Harley Divis i on of Social Sciences

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 0 ) ) Creative control: An exploration of species specific enrichment in mongoose lemurs ( Eulemur mongoz ) and bottlenose dolphins ( Turisops truncatus ) As an apprentice at the Chimpanzee and Human Communication Institute (CHCI) at the University of Central Washi ngton in Ellensburg I was trained to serve the three famous chimpanzees that were housed in the facility. The chimpanzees at the facility were raised in the wake of Washoe, the subject of a series of landmark studies on interspecies communication. Tatu, D ar and Loulis underwent the same treatment as Washoe they were raised as if they were human children ( wearing diapers and eating peanut butter from a spoon) And like Washoe, t hey were immersed in an environment where humans communicated with them using Am erican Sign Language (ASL). Consequently, they began using ASL with each other as well. Thirty years after this initial wave of research, the se chimps still us e ASL O bservational research is continually conducted with them in order to investigate the uniq ueness that their situation presents. "Welcome to the Ellensburg pris on," said Dr. Mary Lee Jensvold to a group of fresh faced apprentices on the first day of orientation. The reality she explained, was that the three remaining chimpanzees were trapped. T hey had been raised as if they were human children, but they had to be isolated from the freedom that accompanies humanity when they grew up. We had come from all over the country to work with them W e would return to our res pective homes after 10 weeks ha d ended, but the chimps weren't going anywhere and they hadn't been anywhere new for decades. The situation was portrayed as bitterly tragic But CHCI acknowledged the tragedy and worked to counteract it by providing as much stimulation and variation as po ssible in

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 1 ) ) the chimps' environment. Environmental enrichment was a part of the everyday routine. A plethora of items would be presented daily including clothes, toys, magazine s laminated photos, cups, mirrors, blankets, food forages, etc. Special enrichmen t activities were offered upon re quest (through ASL) such as painting or using makeup. A garden was planted around the outdoor cage; chimps would sign BERRY or ONION to get a freshly picked treat. Human caregivers maintained an ongoing dialogue with the ca ptive chimps, asking them what they would like to eat for dinner and if they wanted to play chase games or participate in grooming activities. While these accommodations do not negate the constrained position that these chimps o ccupy, enrichment has served to keep the ir situation interesting and engaging despite the unbending cert ainty of a captive environment. Opinions on the purpose of enrichment in captivity vary by facility (see Appendix B for interviews on enrichment). C reative enrichment designed for a species or even for a specific individual can provide an animal with environment al stimulation that may lead to a whole array of benefits for the animal A more complex and engaging environment is beneficial for animals in that it reduces the number o f their sedentary behaviors (Maloney & Meiers, 2006), increases brain mass (Uphouse, 1980) and is correlated with successful reproduction (Carlstead & Sheperdson, 1994). Enrichment can also re duce stereotypic ( abnormal) behaviors ( Pizzutto, Nichi, Corra, Ades, Alcindo & Guimar‹es, 2007; Swaisgood, White, Zhoi, Zhang, Zhang, Wei, Hare, Tepper & Lindburg, 2001 ; Tarou, Bloomsmith & Maple 2005 ), increase exploratory behavior ( Carlstead, Brown &

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 2 ) ) Seldensticker, 1993; Cummings, Brown, Rodden & Songsasen, 200 7) and encourage intraspecies social interaction ( Baker, 2004 ; Maloney & Meiers, 2006). While there has been a substantial body of research conducted to determine the effectiveness of differing enrichment techniques there has been little focus on d iscer ning whether device s that incorporate biological cues that are related to a specific species will elicit a larger number of healthy behaviors than a more generalized enrichment device Biological signals in enrichment devices may lead animals to produce m ore species t ypical behaviors. This study will investigate the effect of naturalistic vocalization s emitted through an enrichment device on the production of natural behaviors in captive populations of two species : mongoose lemurs ( Eulemur mongoz ) and bot tlenose dolphins ( Tursiops truncatus ). Vocal recordings and behavioral analyses will help to answer the question of whether the research population s are influenced by natural cues (species specific vocalizations) and if there is a correlation between these cues and the performance of more natural behaviors (behaviors seen in free ranging circumstances) Food as Enrichment for Captive Animals Carlstead and Sheperdson (1994) have defined environmental enrichment as "environmental manipulations that provide g reater physical and temporal complexity, excluding ma nipulations of social groupings (p. 448). In Second Nature Sheper d son (1998) elaborates on the definition with the following description: "environmental enrichment is an animal husbandry principle that seeks to enhance the quality of animal

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 3 ) ) care by identifying and providing the environmental stimuli necessary for optimal psychologic al and physiological well being (p.1). Evaluating captive animals for their psychological health based on the behavior of their wild conspecifics is an idea that implies the occurre nce of natural behaviors within a species. Model behavioral repertoires are often created from field studies of wild animals; wild behaviors are considered the "best fit" for a species (Seidenstick er & Forthman, 1998). However, b asing psychological health solely on wild behavioral repertoires is not always the most beneficial for individual animals, because the behavioral needs of captive animals may differ from their wild counterparts (Sheperdson, 1998). The food preferences of the chimps housed at CHCI exemplify this disconnect. CHCI used a concrete block with holes in it to mimic a termite mound as enrichment for the chimpanzees. However, the holes of the mound were filled with honey and ketchup not termites. Because they had never consumed termites in captivity, a termite filled mound would not be enriching for them. Acquisition of food is a quick way to induce naturalistic behaviors for animals that are not residing in wild settings. The tenden cy for animals to revert to untrained naturalistic behaviors during a instrumental conditioning paradigm sustained by food rewards was recognized long ago with the concept of "instinctive drift" (Breland & Breland, 1961). While attempting to train simple b ehaviors through the use of operant conditioning, the Brelands recognized a peculiar habit that occurred consistently across various species of animals. This behavior can be exemplified in the description of a pig

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 4 ) ) ( Sus scrufa ) that was trained to deposit l arge wooden coins in a "piggy" bank. The following account was presented: "At first the pig would eagerly pick up one dollar, carry it to the bank, run back, get another, carry it rapidly and neatly, and so on, until the ratio was complete. Thereafter, ov er a period of weeks the behavior would become slower and slower. He might run over eagerly for each dollar, but on the way back, instead of carrying the dollar and depositing it simply and cleanly, he would repeatedly drop it, root it, drop it again, root it along the way, pick it up, toss it up in the air, drop it, root it some more, and so on"(p. 683). This same behavior was observed in several pigs who were trained in a similar fashion. Behaviors of comparable origins were recognized in several other s pecies including raccoons, chickens and hamsters. After some deliberation, Breland and Breland (1961) hypothesized that these aberrant behaviors represented the emergence of instinctive responses to the stimuli that the animals eventually received namely a food reward. Rooting behavior is often observed when pigs are in a feeding context. Aberrant behaviors that were observed in other species, such as the rubbing of coins by raccoons, were also observed entangled within behaviors that were rewarded with fo od providing a clue that food handling instincts were influencing these trained behaviors. The Brelands coined the term "instinctive drift" to describe the occurrence of these instinctive behaviors despite the delay in perceiving a food reinforcement for t he production of the behaviors. The feeding behaviors exhibited represented an intrusio n of classical conditioning within an instrumental framework. Apparently, the behaviors were reinforcing in themselves causing the animals to disregard training procedu res and

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 5 ) ) indulge in naturalistic tendencies. Breland & Breland (1961) described the emergence of these behaviors as an involuntarily response: "It seems obvious that these animals are trapped by strong instinctive behaviors, and clearly we have here a demon stration of the prepotency of such behavior patterns over those which have been conditioned" (p. 684). Food enrichment has been correlated with a reduction in unhealthy behaviors for animals in captive settings. Large felids (n=9) produced more feeding b ehavior and less stereotypic behaviors in an off exhibit enclosure when given whole calf carcasses (McPhee, 2002). Carcasses were supplied to captive felids in off exhibit and on exhibit enclosures. Behaviors were measured beginning immediately as the calf carcasses were presented and continuing for two hours following. Behaviors were analyzed and compared to a baseline period in which animals were fed traditional processed diets. Overall, cats displayed a significant increase in feeding behavior (52% at hi ghest) when compared to baseline levels (5%), however these results varied per cat as some displayed no significant changes. For all cats pooled, a significant increase was seen in natural behaviors off exhibit (92% at highest level), although n o signific ant decrease in stereotypic behavior was observed in the on exhibit condition. The presence of food enrichment also increased appetitive behaviors and activity level (exercise) in k enneled dogs ( Canis familiaris ) (Schipper, Vinke, Schilder, & Spruijt, 2 008). Seventeen healthy laboratory dogs of various breeds were divided into two groups: an experimental group (n=8) and a control group (n=9). Dogs were housed individually, except for 4 females in the control group, and were housed in barren cages

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 6 ) ) that we re situated along two aisles. Visual contact with conspecifics was not possible for individually housed animals. The experimental group underwent three trials: pre toy, toy interaction and post toy. A three day habituation period was conducted prior to the first condition, the presence of video cameras and a researcher were introduced during this time. Neither group received any feeding enrichment during the pre toy trial. In the toy interaction trial, the experimental group received a toy filled with peanu t butter paste, dog biscuits and some bread which were distributed to the dogs twice a day. Dogs in the control condition received the same treatment (i.e., t he researcher walking around and standing in front of kennels) but did not receive food enrichment In the third phase, no groups received food enrichment. Behavior was recorded on video during trials in 20 min sessions per dog per day. Dogs interacted with the food enrichment 8.26% of the time observed. Animals in the experimental group displayed a si gnificantly lower level of inactive behavior than the animals in control group, but only during the toy interaction trial. Animals in the experimental group spent more time moving and standing and less time sitting and lying during the second trial than th ose in the control group. Barking was higher in the control group for trials 1 and 2, whereas the reverse was found in trial 3. Animals in the experimental group barked more in the post toy condition than those in the control group. Another study found a similar correlation between the introduction of foraging enrichment and the occurrence of exploratory behavior. Maned wolves ( Chrysocyon brachyurus ) showed an increase in exploratory behaviors after environmental enri chment was introduced. Peak levels of fecal corticoids a hormonal measure of stress were

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 7 ) ) higher during foraging enrichment than "boomer balls" treatment condition periods (Cummings, Brown, Rodden & Songsasen, 2007). Four adult males and 2 females were housed alone in 10 x 30 m enclosures with access to a heated building. The study was divided into four 2 week periods. No enrichment was given during the first period (baseline). The second period con sisted of a food forage: dead mice were hidden around the enclosure. During the third period, fora ging enrichment was taken away and no new enrichment was presented. "Boomer balls" (approximately 5 heavy duty plastic balls of various sizes) were presented during the fourth 2 week period. Behavioral data were collected during 30 min observation session s after feeding. Activity levels were recorded by noting the behavioral state every 30 sec. Exploratory behavior was recorded by documenting behaviors such as sniffing, digging and scent marking. Fecal samples were collected daily to test concentrations of glucocorticoid. Exploration and activity levels significantly increased in all but one animal when enrichment was provided. Exploratory rates were significantly higher in the foraging condition that when the boom er balls were introduced. Only male wolve s showed a significant difference in behavior with boomer balls; scent marking significantly increased in one male in the boomer ball condition. Enrichment significantly affected peak and baseline levels of fecal corticoids in males, but not in females. Th ese results suggest that a food forage was more stimulating than boomer balls. Higher levels of activity and stress during the food forage ind icate that food stimuli produce an increased behavioral and physiological response in maned wolves.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 8 ) ) Effects of C aptive Environments on Behavior Stereotypic behaviors can occur as the result of organism environment mismatches (Carlstead, 1998). Stereotypie s are commonly referred to as unvarying, repetitive behaviors that h ave no obvious goal or function (Carlstead, 1 998; Tarou et al., 2005 ). The actual function of stereotypic behaviors for animals that produce them is widely debated. Stereotypic behavior has rarely been observed in wild animals, indicating its correlation to factors associated with captive environment s. One hypothesis claims that the performance of stereotypic behavior physiologically or psychologically ameliorates a less optimal environment (Carlstead, 1998). This hypothesis is supported by the correlation of stereotypies with environments that are i n s ome way aversive or stressful. The nature of captive habitats may require animals to develop specific adaptations (Mellen & MacPhee, 2001); however, environmental enrichment can reduce stereotypies. With the introduction of an environmental enrichment p rogram, giant pandas ( Ailuropoda melanoleuca ) spent significantly more time active and produced significantly fewer stereotypic behaviors (Swaisgood, White, Zhoi, Zhang, Zhang, Wei, Hare, Tepper & Lindburg, 2001). Fourteen giant pandas were housed semi so cially, with room to interact between enclosure bars. Five enrichment treatments were presented over a 2.5 month period. All objects were novel to the study population before treatment began. Behavioral observations were conducted for 45 min after each enr ichment item was in troduced. Baseline measures with no enrichment were also conducted approximately 24 48 h prior to enrichment presentation s Each enrichment trial was paired with its own no enrichment control. Stereotypic behavior, feeding anticipation, object directed behavior,

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 09 ) ) object investigation and activity level were recorded at 1 min intervals during observation. Pandas spent significantly more time active and showed greater behavioral diversity during enrichment tr ials than during control trials. Stereotypic behaviors (i.e. head toss, pirouette, cage climb, tongue flick) were reduced under the same conditions. Feeding anticipation occurred significantly less frequently in the presence of enrichment. Even when pandas were not specifically focused o n an enrichment item, both the rate and percentage of time spent in stereotypic behavior were significantly reduced. The introduction of an enriched environment also produced positive behav ioral effects in crossbred pigs (Weerd, Docking, Day, Breuer & Ed wards, 2005). Three hundred and sixty pigs were exposed to multiple enrichment conditions. Pigs were originally housed in pens with solid concrete floors. Enrichment consisted of a straw dispenser in which pigs could root and pull straw through the chain m ail, a rootable feed dispenser through which flavored feed was released into a dish after activating the machine with rooting behavior and a chewable liquid dispenser tha t released flavored water. E ffects of these objects were compared to the effects of a commerc ially available object a red plastic cone with four protruding plastic sticks and a fully bedded straw pen. Video recorded behavior s from the first day of week 1, the first day of week 3 and the first day of week 7 were analyzed. Tail biting defi ned as each occasion in which fresh blood resulted on the tail of at least one pig in a group, was specifically recorded. Stereotypic p en manipulation occurred more often in the straw pen condition as compared to the straw rack and feed dispenser treatment s Pig manipulation, defined as "all pig dire cted chewing or biting behavior" ( p. 240 ) w as lowest in the straw pen in

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 00 ) ) comparison to other treatments Inactivity levels were lowest in the straw pen and straw rack conditions E nriched housing conditions affect rats ( Rattus norvegicus ) (Harst, Fermont, Bilstra & Spruijt, 2003). Rats were exposed to a cueing stimulus and then exposed to one of multiple co nditions. R ats were trained to expect to go to an enriched cage, to receive sexual contact, to return to a standard unenriched cage or to go no where after the presentation of the cueing stimulus The enriched cage was a standard cage with several extension s: a rim, three objects and gnawing sticks. Enriched cages were also bigger than standard cages Forty eight male rats were used; they were between 10 11 weeks old. Thirty six sexually receptive female rats were used for the sexual contact condition. Rats were housed separately by gender in no n experimental conditions. Subjects were randomly divided into four experimental groups (N = 12 animals each). Animals were trained once a day for 4 days and then tested every fifth day for 5 consecutive weeks. The ant icipatory behavior displayed in the interval between the cueing stimulus and the experience of the group condition was compared between groups. Rats conditioned to receive enriched housing or sexual contact showed significantly more arousal behaviors and a generally higher level of activity than rats that stayed in the home cage or rats that were transferred to a standard cage. Rats that received enriched housing showed the same level of activity as rats that received sexual contact. According to the diff erential maturation hypothesis enriched animals reach developmental stages more quickly than t hose in impoverished conditions (Uphouse, 1980). D ifferences in the rapidity of development were smaller between conditions when

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 01 ) ) t reatment began on older animals Rats also developed heavier cerebral cortices and differential dendritic branching when placed in a more stimulating environment. Uphouse's data suggest that animals experience maximum benefits when they are placed in enriching environments from an early age. A large literature exists on t he effect of an enriched environment on phy siological changes in the brain suggesting that i t is unlikely that any single variable involved in enrichment presented to the rats could account for all physiological differences Leopard cats ( Felis bengalensis ) also benefit from enriched conditions. Four cats displayed more explorat ory behavior under enriched conditions than baseline measures (Carlstead, Brown & Seldensticker, 1993). Two female and two male captive born leopard cats were subjected to a series of experimental changes in their environments. Cats were first translocate d to novel, barren cages. Video recordings were made of each cat for 24 hr periods over a period of 7 days. Urine was collected every morning (when available) from the aluminum cage floor. Cats were then transferred to a second novel cage, where 24 hr vide o recordings were made 3 times weekly for 8 weeks. Urine was also collected. After 10 weeks, cats were transferred to a third cage. Here they remained for the remainder of the experimentation process. Urine was collected each morning and 24 hr video survei llance occurred approximately 3 times a week through the first 8 weeks. Urine samples were analyzed for their concentrations of cortisol a hormonal indicator of stress and video recordings were coded for behaviors including stereotypic pacing, exploration, eating, grooming, lying down, etc. Urinary cortisol concentrations were significantly elevat ed from baseline levels during the first week of being moved to

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 02 ) ) the second and third novel cage Cortisol concentration remained elevated throughout the 8 week per iod. Stereotypic pacing increased for the first week only after the cats were moved to the second cage. Exploratory behavior significantly decreased in the 2 8 week period after having b een relocated to the third cage. Cats remained in the third cage for the second experiment, however animals were removed from their cages for one day so that the cages could be enriched with the following objects: 3 or 4 tree branches, 5 m of synthetic rope, 3 wooden shelves, a cluster of bamboo leaf, 2 cardboard boxes, 3 litter pans filled with mulch, sand or dirt and 2 hollow stumps or logs. Urine was collected each morning (when available) for 6 months. Behavioral observations were made via 24 hr video recording over the first 3 months. The elevated urinary cortisol con centrations observed during the last 4 weeks in the third cage significantly decr eased under enriched conditions. Stereotypic pacing occurred significantly less often and exploration also occurred significantly more often in the enriched environment. Aco ustic Enrichment Utilizing all sensory modalities can be beneficial when designing new forms of enrichment for an animal. Research on the effects of auditory enrichment has demonstrated results similar to physical changes in an animal's environment. For e xample, n ewborn rats exposed to music developed an enhanced learning ability in an auditory signal detection task and in a sound duration discrimination task (Xu, Yu, Cai, Zhang & Sun, 2009). Male rats were divided into two conditions: a music condition in which subjects were exposed to a piano sonata by Mozart beginning 14 days after birth,

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 03 ) ) and a control condition in which no sound was presented. Rats in the music condition were placed in a sound attenuating room with music playing at a comfortable ampli tude The same parameters were used in the normal condition, except no music was played. Auditory behavior testing began 56 days after birth for rats in the behavioral testing condition. Subjects were deprived of water for 48 h, while having free access t o dry food pellets. After deprivation, subjects were placed in a box with a waterspout, monitor and speaker. Water was available through the spout when a sound (white noise) was played. The auditory task consisted of a signal detection task and a sound d uration discrimination task. In the signal detection task, rats obtained water by licking the spout when the sound stimulus was played. The stimulus was repeated 5 times for a period of 500 ms with an interval of 5 ms between repetitions. The task was repe ated every 30 s throughout a test session of 1 hr/day. Responses were coded as either: lick, miss (no response), or false positive (licking prior to and sustained after the stimulus was presented). The sound duration discrimination task was similar to the initial task except that two sounds of different time lengths were presented, and only one of the sounds was rewarded with water. The reward and non reward stimuli were randomly presented. Tests of sound discrimination were conducted on rats after 7 and 10 days of training. During training for the signal detection task, correct licking rate increased gradually in both groups. The rate increased more rapidly in the music group (79% by day 4) than in the control group (61% by day 4), but the rate reached 82 84% for both groups by day 6. The number of false positives decreased over time for both groups, providing evidence for learning. In the sound duration discrimination task, the rats in the music

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 04 ) ) group acquired the behavior much faster for the first task. I n the second task, performance immediately dropped for both groups and then recovered at a significantly faster rate for rats in the music group than those in the control group. These data support the hypothesis that early auditory enrichment with music e nhances auditory discrimination learning. Acoustic enrichment has been explored as a method for presenting naturalistic cues as well. Markowitz, Aday and Gavazzi (1995) studied the effect of an acoustic enrichment item on the locomotion of a 16 year old f emale African Leopard ( Panthera pardus ). A system of four speakers was arranged in a 4.3 m x 6.4 m x 3.8 m cage in which the animal had been residing for the majority of its life. The speakers were arranged in a formation that was intended to simulate the flight of a bird. Once the leopard activated the first motion sensor, bird noises would be emitted from each speaker in a successive order. The leopard was given 60 sec to go from the first motion sensor to the second motion sensor (located at the fourth s peaker) to activate the release of a food reward into the cage. The apparatus was controlled by a computer system that automatically recorded the number of cycles that the apparatus was activated, as well as the number of food rewards dispensed. The devic e was turned on at 10 a.m. and continued to operate all day until all food items were delivered or the device was turned off at 4 p.m. The locomotive behaviors of the leopard were analyzed before and after the implementation of the acoustic apparatus. Bas eline measures were recorded four months prior to the installation of the speakers. These measurements were compared to the five month period post introduction of the acoustic device. Observations were conducted for

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 05 ) ) 2 h periods in the morning and afternoo n. Locomotive behaviors were analyzed and recorded in 30 sec intervals. Once the leopard became familiarized with the device through traini ng, she used the device Stereotypic behaviors occurred less often after installation when compared to baseline leve ls. Her usage depended upon the food reward that was offered; she foraged more frequently when dead chicks were offered than horsemeat or frankfurters. Overall, she showed a significant increase in activity level after the apparatus was installed. Signific antly more walking occurred during both the morning and afternoon with the apparatus, and significantly more jumping, pouncing and rolling were observed during the morning session. A decrease in abnormal behaviors was also observed; pacing occurred signifi cantly less in the morning and the afternoon after installation. The leopard also spent significantly less time during the day in her night quarters. There was no indication by her behavior that the device became less appealing over time. On the contrary, she consistently showed more species typical behaviors when the device was on or had been on earlier that day. The nature of this particular enrichment device is unique in its alternative approach. Marko witz et al. (1995) advocates for acoustic enrichment claiming it is an effective and accomplishable means of providing meaningful stimulation. Compared to the cost of live prey, mechanical "prey" such as the apparatus described in the study above are less expensive and more sustainable (Markowitz et al., 1 995). T his enrichment device allowed the animal to have an effect on the stimuli through its own behaviors. Additionally, th e leopard did not habituate to the enrichment device Repeated

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 06 ) ) presentations of the same stimuli often lead to habituation and thus, a decreased interest and interaction with the stimulus (Tarou & Bashaw, 2007) Habituation occurs much more quickly (within a single exposure) to enrichment that is extrinsically motivated. Providing a variety of reinforcers often prolongs interest, which may have contributed to sustained interest in the enrichment device by the leopard. When an animal cannot control aspects of its life, it may experience learned helplessness. Proposed by Maier and Seligman (1976), learned helplessness explains the respon ses of dogs that experienced inescapable electric shocks. This study had three groups of dogs: a group that experienced inescapable shocks, a group that was able to escape shocks and a group that experienced no averse stimuli. After an initial phase of co nditioning individual animals based on group variables, all animals had a period of escape training. Animals that initially experienced inescapable shocks showed significantly less ability to escape shocks (28%) when they were given the opportunity to do s o. In contrast, the groups that were given no shock (78%) or escapable shocks (74%) were able to learn to avoid shocks in most circumstances. Maier and Seligman (1976) suggested that animals that experienced inescapable shocks developed emotional, cognitiv e and motivational deficits including their incapacity to escape shocks even after having been trained that escape from the shocks was possible. This study has important implications for enrichment geared towards captive animals because it suggests that wh en an animal is denied agency in its own environment, the animal may learn that its actions are irrelevant to what it experiences. Establishing the lack of a contingency between

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 07 ) ) behavior and experience may lead animals to be less motivated to attempt to ma nipulate their environments at all. Poole (1998) outlines "achievement" as one of the four fundamental principles necessary to consider when designing enrichment for animals in captivity. According to Poole (1998), a n environment should reinforce motivati on to achieve objectives. The animal should be given "control" in that it can rely on its environment to reinforce its decisions. Providing opportunities to make decisions and achieve objectives should be held as a priority over creating a seemingly natura listic setting, as environments that appear to be reminiscent of wild settings often lack realistic sources of motivating interest for captive animals. Human Interaction as Enrichment Human presence in zoos and aquariums is an inevitable reality. Humans can provide meaning ful stimulation through training and social interaction, but captive animals do not always receive their presence favorably For example, t hree species of primates, cotton top tamarins ( Saquinus oedipus ), Diana monkeys ( Cercopithecus di ana ) and ring tailed lemurs ( Lemur catta ), disp layed more aggressive behaviors and a decrease in other behaviors when visitors were present ( Chamove, Hosey & Schaetzel, 1988). All animals were housed in captive indoor enclosures that were separated from th e visitor viewing area with thick glass. Animals were observed in two conditions: when at least 6 visitors were present and when no visitors were present. Each animal was observed for two 10 min periods separated by two weeks; observation sessions occurred at the same time of day for each group. Four behavioral categories were recorded: agonistic

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 08 ) ) (aggressive) behavior grooming behavior affiliation (positive social) and inactivity. Agonistic behavior significantly increas ed by a factor over 5 while a sign ificant decrease occurred in grooming (80%), inactivity (55%) and affiliative (50%) contexts. Visitors were then instructed to display a low crouched posture when present at the exhibit. The exhibition of a crouched posture by visitors was correlated with a reduction in behaviors induced by stress (Chamove, et al., 1988). Eight groups of volunteers were instructed to alter their physical posture when viewing the animal exhibits. Volunteers were told to either stand as tall as possible n ext to the viewing w indow of an exhibit or to crouch low to the ground so that only their head s were above the base of the window. Individual animals were observed for 1 min each, with the previously outline d behavioral contexts recorded at 5 sec intervals. Significantly less inactivity, less grooming and more agonistic behavior occurred when visitors were fully visible than when only their heads were visible. In a similar trend, s ignificantly more births occurred on weekends and during nocturnal hours in pregnant chimpanzees than during periods when human presence was more prevalent (Alford, Nash, Fritz & Bowen, 1992). Three chimpanzee colonies were studied; pregnant individuals were housed in their social group s or singly in cages close to their group s Animals in the colon y participated in primarily non manipulative behavioral research. Research procedures and preventative medical surveillance routines that required restraint and anesthes ia ordinarily occurred on Tuesdays and Wednesdays. The timing of 153 live, full term ch impanzee births was recorded. Data on stillbirt hs and premature deliveries were omitted from the final analysis. Ninety percent of births were

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 19 ) ) unobserved because they happened nocturnally (84%) or during times when caregivers were not present. Significantl y fewer births occurred on Wednesday and Thurs day. S ignificantly more births occurred on Sunday and Mon day Results from this study suggest that pregnant chimpanzees differentially gave birth during periods of t ime when there were likely to have fewer inte ractions with hu man caregivers. This finding is likely influenced by the presence of anesthesia and occasional restraint, which occurred during some interactions with human caregivers. Affiliative interactions with familiar human caregivers have also been correlated with positive behavioral effects in captive animals. During periods of increased interaction with familiar human caregivers, chimpanzees ( Pan troglodytes ) displayed more grooming behaviors and lower levels of abnormal behaviors and inactivity th an baseline levels (Baker, 2004). Seven female and 5 male adult chimpanzees with Huma n Immunodeficiency Virus (HIV) were observed during two conditional phases of human interaction with familiar caretakers. Baseline data w ere derived from periods of time i n which routine twice daily caretaking took place. Total care staff presence in the facility averaged 2.25 h per day. A second condition consisted of routine caretaking as well as an additional 10 mins of interaction for each chimpanzee. During this condit ion, care staff presence in the facility averaged 4.25 h per day. Human chimpanzee interactions consisted of unstructured play, grooming, treat feeding and talking. A total of 97 h were recorded, approximately 5 h per subject during baseline conditions and 3 h during testing. Both regurgitation/reingestion and other abnormal beh aviors with oral components were significantly reduced during the period of additional human interaction. Less time was

PAGE 27

!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 10 ) ) spent in an inactive context during test conditions and consp ecific grooming behavior nearly doubled from baseline levels. Similarly, a decrease in stereotypic behavior and an increase in self grooming behaviors r esulted from human interaction and/or treat provisioning with 8 rhesus monkeys ( Macaca mulatta ) (Bayne, Dexter & Strange, 1993). Monkeys were singly housed in stainless steel 4.3 or 8.6 sq.ft. cages (depending on the animal's weight). Monkey chow was provided twice a day, and water was available ad libitum. No enrichment devices were present during the cou rse of this study. An A B A experimental paradigm was used to test the impact of food provisioning by humans. The baseline, experimental and post experimental phases were each a duration of 10 weeks. Animals were videotaped between 9 a.m. and 12:30 p.m. on ce a week for a total of 5 hours per condition. Dur ing the experimental condition a handful of monkey treats (approximately 10 treats) were provided to the monkeys three times a week. Behavioral technicians attempted to use species specific submissive cues (i.e., eyes cast downward, making lip smacking sounds, kneeling for animals in lower cages) when presenting food treats. Cage directed behaviors to manipulate, pick at, rub, or bite any part of a cage in a repetitive manner were significantly reduced duri ng the ex perimental condition and remained at a reduced level during the post experimental period. Self grooming activity levels were significantly higher in the experimental condition than in the b aseline condition and continued to increase during the pos t experimental phase. Additionally, the total number of stereotypic behaviors w as significantly reduced from the baseline to t he experimental period and decline d even further in the post experimental phase.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 11 ) ) One on one training can provide an engaging mea ns of stimulation, especially in the absence of other types of stimulation such as conspecific social interaction. Enrichment that is varied, goal based, based on intrinsic reinforcement and presented on a variable ratio schedule has been suggested to be m ost effective in supporting psychological well being in captive animals (Tarou & Bashaw, 2007). Human interaction with captive animals through training provides an opportunity to utilize these strategies. Virgulino, a singly housed captive male adult gori lla ( Gorilla gorilla gorilla ) displayed less abnormal behaviors when exposed to increased social interaction and training with a human caregiver (Pizzutto et al., 2007). Data were collected over a period of 5.5 years. This net time was divided into 2 peri ods, a baseline period of six months where no contact was established between the animal and the researcher and a second period of training and human gorilla interaction Behaviors were recorded by sampling every 30 sec during one hour daily sessions thre e times a week. After each hour long session, the researcher approached Virgulino in a submissive attitude and gave him a piece of dehydrated fruit the aim of this maneuver was to gain the animal's trust. After six months of observations, unnoticed observa tions were no longer possible as Virgulino began to look consistently for the researcher and would position himself facing the researcher until the end of the recording. During the second phase of the study, t hirty min operant conditioning sessions took pl ace twice a week over 5 years. Positive reinforcement was given for the correct response to short verbal commands including sit, mouth (open), hand (present), feet (present), stand, lie down commands were always vocalized in this order. A time out was appl ied for any kind of aggressive behavior; the

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 12 ) ) session would be interrupted for one minute and the trainer would turn her back to the animal and stand in silence. After each training session, a 10 min interval occurred where Virgulino was left alone. Follow ing isolation, a researcher spent 20 min socializing with him. During this time, the researcher offered the animal various foods (the same foods offered in his regular diet), played music and handled objects (toys and dolls). Observations in the off exhib it area of abnormal behaviors [ regurgitation/reingestion (2.3%), coprophagy (.49%), self mutilatio n (4.2%) and intimidation (10%)] were recorded during the baseline period. A reduction of the same behaviors occurred after the first year that social interac tion was instated: regurgitation/reingestion (.42% of observation time ), coprophagy (.05%), self mutilation (.01%) and intimidation (.03%). These levels of behaviors were maintained for the next four years. Similar results were seen in the indoor exhibit a rea as well. Browsing increased beyond baseline levels (6.5%) after the third year of testing (8.02% ). Inactivity showed a similar pattern; an increase beyond baselines levels (56.9%) occurred after the first year (77.9%) for inactive behaviors. These res ults indicate an increase in more naturalistic behavior and less abnormal behaviors during periods of human interaction. Human interaction has proved beneficial for captive animals, particularly in situations where the animal would otherwise be without so cial interaction of any kind (Pizzuto et al., 2007). However, in some circumstances captive animals display avoidance behavior (Alford et al., 1992) and increased aggression (Chamove et al., 1988) when humans are present. Affiliative interaction can be beneficial (Baker, 2004), suggesting that the human animal relationship is dependent upon the human's attitude during the

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 13 ) ) interaction. Although human interaction has proved to be beneficial in some captive circumstances, intraspecies interaction is likely to be an even more effective form of enrichment. T he current study attempts to mimic some aspects of intraspecies interaction by presenting a species specific enrichment device to captive animals. Two differently adapted mammalian species mongoose lemurs ( Eulemur mongoz ) and bottlenose dolphins ( Tursiops truncatus ) were test ed to investigate whether the device is generalizable among multiple species in captivity. Mongoose lemurs and bottlenose dolphins are undoubtedly diverse in their adaptations and ecolo gical niche, however, they share an emphasis on intraspecies vocal communication. Mongoose Lemur Ecology and Enrichment Strategies Indigenous to the Northwest forests of Madagascar and the Comores Islands, Mongoose Lemurs ( Eulemur mongoz ) are 1 of 99 r ecognized species and subspecies of lemurs ( Mittermeier & Nash, 2006 ). The climate of Northwest Madagascar is clearly demarcated by wet (Dec Apr) and dry (May Nov) seasons, w hich may contribute to the unique variations in social structure and activity cyc le s of E.mongoz (Curtis & Zaramody, 1999). Curtis and Zaramody (1999) documented foraging strategies i n a 10 month observation al study of two wild populations of E. mongoz Instances of isolation were observed during foraging, with the isolated individu al staying connected to the group through vocalizations and scent marking. A commonly seen foraging group consist s of a small family composed of an adult male, an adult female and the bonded pair's offspring. Cohe sion between pair mates is f airly consisten t, although it is not known whether pairs

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 14 ) ) generally stay monogamous throughout their lives. In some cases several smaller family groups form a large group Group size varies extensively; larger groups have been found to contain up to 8 individuals Scent ma r king was observed in two forms: anogenital marking and head rubbing. Head rubbing occurred only in males, while anogenital marking occurred in both sexes and appeared to represent two separate functions. Anogenital marking appeared to serve a territor ial function; individuals show ed an increase in marking on fruit trees (prized food) and during territorial conflicts. Anogenital marking also appeared to reinforce the pair bond between tw o mating adults. Paired mates w ere observed participating in mutual scent marking, which is described as one adult mar king over another adult's scent mark. Mates have been observed rubbing their genitals together in what is considered to serve a similar purpose of providing cues to surrounding conspecifics of the linked r elationship between the two individuals. An activity budget calculated during this study indicated that the majority of a lemur's time was spent resting (69%), followed by alert behaviors (11%), traveling (6%), feeding (4%) and other activities (1%). Pos tural and locomotive behaviors were also measured Animals were recorded sitting approximately 57% of the time, which was followed by standing (29%), curled up (6%), clinging (2%), lying (2%) and other (4%). Quadrapedal locomotion was by far the most commo n mode (78%) of tran sit Leaping (19%), climbing (3%) and other (1%) modes also occurred. V ocal communication between mongoose lemurs was also documented Two different categories of vocalizations were recognized: pulse trains (i.e., screech, grunt, sneeze snort, creak,

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 15 ) ) warble) and tonal vocalizations (i.e., hmm, rap, cak) S ee Figure 1 for vi sual representations of creak, grunt, and sneeze The combination of grunt sneeze was observed frequently in the subject population See Table 1 in Methods for the vo cal repertoire Enrichment is effective when it encourages the natural behaviors of the species. Scent marking is a regularly practice behavior among many prosimians, including E. mongoz. One example of effective enrichment which focused on the productio n of scent marking was described in an interview with the research manager of a facility that houses and breeds endangered prosimians (Unpublished data ) (see Appendix B). At this facility, scent marking was induced by placing a raw sheet of wood in an ani mal's enclosure. The animal, or group of animals, would scent mark the piece of wood after which the wood would be taken out of the enclosure and placed in the cage of another animal that engages in scent marking behavior. The second group of animals would scent mark over the marks of the first animals. Scent marking is a territorial behavior use d to communicate information from group to group and from individual to individual (Curtis & Zaramody, 1999). By providing an opportunity to engage in scent marking with other individuals the captive environment becomes more reminiscent of the wild in that naturalistic behaviors are used. S et s of observations like these give researchers and animal keepers an idea of the behaviors naturally seen in wild circumstances and at what frequency these behaviors occur. B ehavioral repertoires of wild animals provide insight when compare d to those of captive animals Behaviors that occur in captivity, such as stereotypic behavior,

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 16 ) ) communicate information about the differences that are experienced by an animal in captivity vs. a free ranging setting. Of course, the limited number of studies specifically focused on mongoose lemurs may constrain our knowledge of their full repertoire. A recent survey in vestigated the presence of stereotypic behavior in captive prosimians (Tarou, Bloomsmith & Maple, 2005). Surveys were sent to 96 American Zoological Association (AZA) institutions that were known to house prosimians. Each facility was instructed to have the person with the most fa miliarity with the history, behavior and daily routine of prosimians to answer the questions. Forty eight of the 96 facilities responded with data from their collections. Approximately 13% of the animals reportedly produced stereotypic behaviors, a signif icant increase when compared to the Bollen and Novak (2000) report of a 7% prevalence rate in captive prosimians (Tarou et al., 2005). Gender correlations as well as trends in specific patterns within species occurred. Stereotypic behavior was more preval ent in males than in females. Animals of the genus Varecia were most commonly found to exhibit stereotypic behaviors (21%, n= 161) when compared with all other prosimians. Stereotypic behaviors included pacing, somersaulting, overgrooming and self injuriou s behavior. Eulemur also exhibited stereotypic behavior, (17%, n=53). Eulemur and Varecia may have been more susceptible to displaying abnormal behavior because they are mostly arboreal, while animals within

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 17 ) ) Figure 1. Spectrograms of Selected Vocal izations in E. mongoz (a) (b) (c) (a) Creak, (b) grunt and (c) sneeze were recorded from the subject population in Study 1. Time is on the x axis of the figure and frequency is on the y axis. the genus Lemur which are much more terrestrially orient ed produced considerably fewer stereotypies. Forty eight percent of the institutions reported trying to eliminate stereotypic behavior, but only 58% reported success. The most common approaches used to address stereotypic behavior were environmental enrich ment and training.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 18 ) ) Many enrichment studies on lemur genera have used food based enrichment to test the effects of various enrichment designs on behavior. Complex foraging enrichme nt increased play, grooming and object manipulation and decr eased resting be havior in b lack lemurs ( Eulemur macaco ) and r ing tailed lemurs ( Lemur catta ) (Maloney & Meiers, 2006). Three types of enrichment were individually presented to lemurs in captivity Nine adult subjects were studied in all: 6 black lemurs (3 m, 3 f) and 3 ri ng tailed lemurs (3 m). Lemurs were housed in three separate enclosures, 2 with male female pairs and 1 mixed enclosure. Five behaviors were observed and recorded during this study: resting, playing, grooming, feeding, foraging and interacting with enrich ment. The occurrence of stereotypic behavior was undocumented in the study Observations were made Monday Friday from 11 a.m to 4 p.m. for 12 weeks. Three hundred hours were documented in all. One of three types of feeding enrichment was presented each w eek. Enrichment item 1 was a large feeding bowl filled with mealworms and covered in sawdust. Item 2 consisted of a paper towel roll stuffed with cereal and closed off with pieces of bread. Item 3 was a wire box with whole grapes and hal f slices of apple p laced inside; t he box was suspended and had openings big enough for a lemur hand but too small for a lemur head. A week of no item presentation was used as a control condition. No significant differences occurred based on sex. Item 3 the wire fruit box, e licited significantly higher rates of play, grooming and enrichment interaction and a significantly lower rate of resting as compared to the other items and the control. No differe nces were found between the cardboard roll and feeding bowl Some evidence o f habit u ation was shown to a single item within a week's time.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 29 ) ) The higher rates of play and grooming behaviors with the wire fruit box s uggest s that the introduction of some kinds of enrichment may cause an increase in the amount of time spent in social i nteraction The complexity of the enrichment device was a significant factor in this study, with the more complex apparatus eliciting more naturalistic behaviors. However, d ifferences in food reinforcement could account for the variations in significance b etween items as some food items may be more desirable than others leading to a motivation difference between enrichment items. Variations in the structure of the physical environment provided for lemurs have also been explored in a study with a captive p opulation of ring tailed lemurs. Increasing the spatial complexity of food presentation and adding browse to make obtaining food more difficult raised activity levels and decreased unwanted stealing behaviors for conspecifics in ring tailed lemurs (Dishman Thomson & Karnovsky, 2009). This study examined simple and straightforward approaches to feeding enrichment and analyzed its behavioral effect on the captive subjects. The subjects consisted of 8 ring tailed lemurs ( 7 m and 1 f). Subjects were housed in an open air aviary directly adjacent to a porcupine and rock hyrax habitat. Two factors were studied: the visibility of food and the arrangement of food. Visibility was varied by the addition of browse compared to a no browse condition in which food was presented in plain sight. Variations in the arrangement of food were achieved by utilizing boxes. Food was placed inside the boxes, which were either "aggregated" or "scattered" within the habitat. All four combinations of factors were replicated three ti mes (in the same sequence) and were applied for a week at a time.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 20 ) ) Observations were collected two days a week for 2 h a day. Observations were recorded individually and behaviors we re classified as either "active : moving (walking, running, climbing, o r jumping), social grooming, and feeding on lemur diet or on pirated food (chewing on, holding between bites, or picking out food from treatment boxes, lemur biscuits or h yrax or porcupine diets); or "resting : lying down, sleepin g, standing, sitting, and pausing in other activiti es where animals were in motion for at least 5 s. The 2 h observation period was divided into the first 70 min and the latter 50 min for statistical analysis. The presence of browse during feeding had no effect on the level of acti vity in the first 70 min, but significantly increased activit y levels in the 50 min period that follow ed When compared to baseline levels, addition of browse doubled the number of 10 min periods when at least one animal was active. Present ing food boxes i n a more spaced out configuration decreased the amount of food pirating significantly. Th e data suggest that simple approaches to enrichment are often effective ways of decreasing undesirable behaviors. Bottlenose Dolphin Ecology and Enrichment Strategies Unlike lemurs, b ottlenose dolphins have a wide global distribution; they occupy temperate and tropical waters with surface temperatures between 10 and 32 degrees Celsius (Reynolds Wells, & Eide, 2000) They range in size from 2 m to 4 m long with a st reamlined body structure that is suppor ted by an elaborate musculature. An interesting and unique adaptation of the species is its ability to echolocate. Echolocation clicks are produced in the blowhole and focused thr ough the melon. Echoes are received th rough the bottom jaw and provide information about the make up of objects within the dolphin's

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 21 ) ) environment Burst pulses are broadband cover ing a wide frequency range sounds similar to clicks but burst pulses are more compressed. Dolphins also produce nar row band isolated in a narrow frequency range sounds called whistles Whistles and clicks can be produced simultaneously. S ee Figure 2 for visual representations of clicks, burst pulse s and a whistle Bottlenose dolphins generally have a diurnal activity pattern. Resting beh aviors of 16 captive dolphins were observed, showing that dolphins' resting cycles change when social conditions change (Sekiguchi & Kohshima, 2003). Observations were conducted between March 1997 and March 2001. Visitors were present during the day as the animals were housed in three different aquariums. Training and performance shows also occurred regularly. Diurnal activity rhythm was analyzed with two activity indexes: the Swimming Speed Index (SSI) and breath frequency. Sound anal ysis was also conducted. Activity indic es tended to increase during the day and decrease at night. Vocal production, clicks (broadband) and whistles (narrowband), were significantly less frequent during periods of low activity than during high speed swim ming. One female showed a decrease (72.2% to 57.9%) in nighttime resting behavior after childbirth. Resting behaviors resurfaced 12 weeks after childbirth. A similar pattern was observed in a female when novel tank partners were added to her tank. Total r esting time decreased from 84.3% to 43.1%. Her original resting rate recovered after 2 weeks of irregularities. These results show the adaptive potentialities of the species in a captive setting.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 22 ) ) Figure 2. Spectrograms of Selected Vocalizations in T. tursiops (a) (b) (c) (a) Whistles, (b) burst pulse s and (c) clicks are represented via spectrogram s. Time is represented on the x axis and frequency is represented on the y axis. ):;;)&<=+>&) ?#,#),#$<,>#> )(,<.)&=@A#$/)"<"=;B/%<+)%+) !/=>C)1D ) Efforts t o provide enriching stimuli for the species while in captivity have been sparsely documented. Captive dolphins experience training and human interaction in the

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 23 ) ) majority of aquariums. A Dolphin Interaction Program with trainer supervision was shown to elici t increased levels in p lay behaviors, and no indication of averse effects on th e dolphin subjects (Trone Kuczaj, & Solangi, 2005). The study took place at Marine Life Oceanarium in Gulfport, Mississippi. Three dolphins were studied: 2 adolescent males and 1 35 year old female. A trainer was present during the Dolphin Interaction Programs, as well as three paying guests. Unsupervised interaction also took place on occasion. All unsupervised (without the presence of a trainer) interaction was voluntarily in itiated by the dolphins and included guests who were behind a fence that surround ed the dolphin pool. All in teraction occurred through toys; no conta ct occurred with dolphins when a trainer was not present. Throughout a month long period, a baseline measur e was taken on days when no Dolphin Interaction Program occurred Observations of the Dolphin Interaction Program consisted of two 90 min observation sessions: one occurred before the program and the other occurred afterward. There were 12 days of observat ion every month, for four months. A final set of observations was obtained after the Dolphin Interaction Program had terminated. Each dolphin was observed for social behaviors (solitary, dolphin dolphin or dolphin human) and "behavioral event" (play, swimm ing, motor movements, orienting, sexual, aggressive, resting and misc ellaneous) categories. A focal animal sampling technique was employed, with 19 sub observation periods (lasting 5 min) occurring within every 90 min period. Each subject was observed for 10s in rotation throughout each sub observation period. P lay behavior s occurred more frequently

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 24 ) ) during the second observation session (the session that occurred immediately after the Dolphin Interaction Program) versus the first Although human interactio n provides beneficial stimulation, s timuli that are reminiscent of cues from conspecifics are uniquely salient to captive animals. Cardiac responses to playback stimuli (conspecific vocalizations) were measured in a captive dolphin (Miksis, Grund, Nowacek, Solow, Connor & Tyack, 2001). Heart rate recordings were collected from a 22 year old wild born female. Recordings were conducted in a pool that contained another bottlenose dolphin for a portion of the study and 3 female beluga whales that were section e d off from the dolphin area. Heart rate was measured acoustically using a broadband microphone. Playback stimuli were composed of vocalizations from familiar pool mates. A second playback condition was composed of tank noise with no vocals present. One pla yback session occurred per week; one session was composed of four playback trials over a period of 10 to 20 min. The dolphin was isolated and stationed 3 m below the surface for approximately 90 to 120 s during playback trials. An initial acceleration of h eart rate followed the playback stimulus. A significant difference in acceleration was recorded for jawclap stimuli when compared to baseline measures. Heart rates continued to increase after 10 beats in the vocalization playback condition, while they retu rned to baseline levels in the tank noise condition. The results of this study suggest that vocalizations of conspecifics as playback stimuli invoke a physiological response in captive dolphins Finding ways to utilize acoustic stimuli to provide increased stimulation for captive dolphins may benefit them.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 25 ) ) The Current Study Enrichment benefit s animals in captivity by re ducing stereotypic, abnormal behaviors ( Pizzutto, et al. 2007; Swaisgood, et al. 2001 ; Tarou et al. 2005 ), increasing exploratory behav ior (Carlstead, et al. 1993; Cummings, et al. 2007) and encouraging intraspecies social interaction (Baker, 2004 ; Maloney & Meiers, 2006). Enrichment through presentation of food (McPhee, 2002; Schipper et al., 2008; Cummings et al., 2007 ), environmental manipul ations (Carlstead et al., 1993; Harst et al., 2003; Swaisgood et al., 2001; Weerd et al., 2005) and human interaction (Baker, 2004; Bayne et al., 1993; Pizzutto et al., 2007) have produced desirous results in modifying maladaptive behavior displaye d in captive settings. The naturalistic behavioral tendencies of a species have been considered in some very successful designs (Markowitz et al., 1995), however many more topics could be investigated as potentially enriching stimuli for captive animals. More research is needed to pinpoint spec ific ally what makes an enrichment item effective. Approaching behavioral issues with creative solutions that consider the specific biological needs of the animal may encourage greater engagement with the animal's en vironment and higher production of naturalistic behaviors. The following study aims to utilize a biologically relevan t stimulus to influence the production of naturalistic behaviors (i.e., vocalizations) in captive mammals A v ocalization emitting enrichme nt item was presented to two populations of vocally productive animals: mongoose lemurs ( Eulemur mongoz ) and bottlenose dolphins ( Tursiops truncatus ). Both species are highly social and co mmunicate via vocalizations. However, both species are very in diff erent in their cognitive and physiological adaptations Therefore, by testing both species with the same

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 26 ) ) device we can learn whether some stimuli are generalizable between species despite vast differences. Behavioral effects including vocal responses, fro m the presentation of each stimulus were compared to baseline measures of activity. The effect of a species specific enrichment item on the production of naturalistic behaviors was investigated. This study explores how effective the experimental device is at providing salient stimuli to supplement the limited variance that accompanies a captive environment. Methods were nearly identical between the two species, providing a way to generalize about the effect of this specific enrichment device for a variety o f vocal species. Study 1: Effect of Species specific Enrichment on the Production of Naturalistic Behavior s in Mongoose L emurs ( E. mongoz ) Method Subjects M ongoose lemurs ( Eulemur mongoz ) were tested in the first study. The subject population was compo sed of a family group: 1 adult male (approximately 4 years old) 1 adult female (approximately 4 years old) and 2 adolescent twin males (approximately 2 years old) All subjects were born and raised in a captive setting. T he adults ha d resided at this lemu r research and conservation facility in Southwest Florida for the majority of their lives. The male twins we re born in the facility and had lived w ith their parents since birth. The subject group had access to indoor and o utdoor enclosures (the indoor cag e was approximately 1.5 m x 2.1 m x 2.4 m and the outdoor cage was approximately 2.1 m x 2.1 m x 3.1 m ). Data were collected in the outside cage only. Approximately 30 individuals from 8 distinct species were housed in caged and semi free ranging habita ts

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 27 ) ) of the facility. Subjects were habituated to the presence of humans in daily interaction s such as feeding, medical and other routine husbandry procedures. The majority of individuals in the facility had engaged in cognitive research and training at some po int; the adults in this group had previous research and training experience. Materials All subjects were exposed to the same environmental enrichment device. The device consisted of a waterproof speaker encased in a hard pla stic ball (30.5 cm x 30.5 cm x 30.5 cm ). The speaker was an Audio Unlimited PoolPod made of plastic with a rubber cushion around the body. It was secured inside the ball with Styrofoam padding and duct tape. It communicated with a wireless transmitter ( 11.4 cm x 8.9 cm x 2.5 cm ) up to a range of 150 ft. The speaker itself could be submerged for up to a period of 30 min without c ausing functional complications, although the speaker was not submerged in this study. A Sennheiser microphone and Marantz recording system captured vocalization s produced during research sessions. Video footage was recorded with a Sony digital camera. Audio and visual footage was later coded for inter rater reliability to ensure consistency. Procedure Three auditory conditions were presented during t esting. The lemur condition (LC) consisted of 2 m in segments of lemur vocalizations capture d under naturalistic conditions, i.e., the vocalizations were selected from an audio track that included active segments of vocalization strings which were selected in their en tirety V ocalizations were

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 28 ) ) Figure 3. Enrichment Device During Testing S ession with E. mongoz The enrichment device was placed in the cage. It emitted three auditory conditions. All lemurs were tested simultaneously. previously recor ded from the testing population; all individuals (n=4) were represented in the track. The dolphin condition (D C ) was organized in a similar manner to L C ; it was composed of 2 min segments of vocal emissions from the population of bottlenose dolphins ( Tursiops trunctatus ) test ed in Study 2. A third control condition (S L ) contained no sound. A 26 m in auditory loop was presented via a speaker inside the enrichment device. The loop consisted of alternating 2 m in segments from all three conditions (see Figure 3 and 4 for a visual representation of auditory conditions by session ). A period of habituation (~5 m) to the researcher occurred prior to every session. Lemurs did not have

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 39 ) ) a prior r elationship with the researcher; the researcher was present and visible to the subject group during all session s All sessions took place between 12:30 p.m. and 4 p.m. between March 31 and April 5, 2010. All subjects had previous experience with balls, but no subjects were exposed to the specific enrichment device prior to testing. Auditory condi tions in sessions 1 and 2 ( 1560 sec each or 26 min ) were counterbalanced for order effects. A baseline session ( 1560 sec or 26 min ) was recorded prior to animal exposure to the enrichment device. Behavioral responses a nd vocal production were recorded duri ng all sessions, h owever, because the lemurs entered the indoor enclosure and were out of recording range during a section of session 2, their behaviors and vocalizations were only analyzed for 960 sec. Cumulative measures of v ocalizations and behavior wer e analyzed during a 1560 sec period for both session 1 and the baseline session. Coding Lemur vocalizations were counted and categorized based on the previously outline d vocalization repertoire of E. mongoz presented in Table 1 (Curtis & Zaramody, 1999). V ocalizations were coded in a digital acoustic analysis program, Avisoft Pro (version 2.1 ). Originally, interactions with the object were going to be the primary assessment of motor behavior, but responses to the object made a more finely tuned behavioral a nalysis more useful. Therefore, behavioral categories from Maloney and Meiers (2006) were coded. Be havior was analyzed and was recorded every minute for each individual animal. Individual differences were not analyzed, instead group rates were compared bet ween sessions. Behaviors were listed as occurring within each minute

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 30 ) ) Figure 4 (a) Timeline of a uditory sequence during session 1 Figure 4 (b) Timeline of au ditory sequence during session 2 Lemur and dolphin conditions were taken from prerecorded sessions of vocalizations of subjects from Study 1 and Study 2. Session 2 differs from session 1 in the order that auditory conditions were presented. The order of presentation was changed to counterbalance for order effects. The select ed area represents the period that was excluded from analysis because the lemurs were out of recording range. segment. Coded behaviors are listed in Table 2. All video observations were coded from video footage after testing was completed. A second researc her coded 10% of the session time in order to ensure reliability. Eighty one percent agreement was calculated between the two coders.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 31 ) ) Table 1. Vocalizations E mitted and Behavioral Context in E.mongoz Vocalization Behavioral Context Screech (SC) t erritoria l; antipredator Soft grunt (SG) group cohesion Agitated grunt (AG) territorial; antipredator Sneeze (SN) territorial Creak (CR) territorial Hmm (HM) group cohesion Vocalizations listed represent a partial selection from a previously proposed E.mongoz vocal repertoire (Curtis & Zaramody, 1999). All vocalizations are common. Results Lemurs vocalized more often during both experimental sessions (670 /1560 sec 42.95%) in session 1 ( 117 /960 sec 12.19%)in session 2 than durin g baseline session (40 /1560 sec 2.56 % ) when n o object was present. See Figure 5 for vocal production by session More soft grunts (over 540 sec in duration) were produced during session 1 than any other vocalization in any condition. Lemurs very rarel y interacted with the object ( 90/1560 sec, 5.77%). However, they produced more locomotive behaviors during the first experimental session ( 885/1560 sec, 56.73%) than during baseline ( 165/1560 sec, 10.58%), and lemurs rested less during session 1 ( 495/1560 sec, 31.73 %) than during baseline ( 975/1560 sec, 62.5%). However, resting behavior was high in session 2 (750/960 sec, 78.13 %).

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 33 ) ) Discussion Differences between experimental and baseline measures for behavior and vocal production suggest that the enrichment device tested had a clear effect on E. mongoz I ncreased scent marking and locomotion accompanied by substantially more vocal productions in lemurs during experimental session s suggest validity for the device as a prompter of naturalistic behaviors. However, variations in behavior or vocal production were not observed between the presentat ion of different vocalization types by the device. More naturalistic behaviors did not occur based on periods of species specific vocalizations On the other hand, the strong response during the lemur vocalization condition in session 2 suggest s that the l emur auditory condition was particularly salient for the lemur group. During session 2, t he lemur group moved from the outside enclosure, where the device was placed, to the inside enclosure immediately before the device began to emit sound. The group stay ed inside for approximately 10 min (600 sec) and were neither visible nor within range of the recording microphone during this time. However, the behaviors that followed provided valuable information about the effect of the device. The lemur group began ex hibiting high alert behaviors when they returned to the outdoor enclosure during the lemur vocalization condition. They moved to the outside enclosure as a group, exhibiting alert behaviors (i.e., rapid head movement, increased locomotion, upright tail pos ture). Their behavior appeared to be correlated directly with the acoustic condition of the enrichment item, suggesting validity for the device as a tool to engage natural istic behaviors in the species especially in the species specific auditory condition.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 34 ) ) Although this information is somewhat anecdotal, it should motivate future research on the salience of specie specific vocalizations as enrichment. Analysis of vocal production data was problematic in this study. Vocalizations produced from the subject po pulation were intermixed with vocalizations produced by the enrich ment device. In order to quantif y vocal production, vocalizations had to be intricately picked out by referring to the spectrogram of the auditory stimuli emitted from the device. Because of the jumbling of these sounds, some vocalizations produced because of the auditory stimuli were likely indecipherable. This is unfortunate because this section of data is arguably the most interesting. A second study was conducted on a separate species ( Tu rsiops truncatus ) with an array of more sensitive hydrophones (underwater microphones) in an attempt to combat this logistical issue. An familiar non vocal object was also added to the baseline condition in order to have a basis for comparing interaction w ith the experimental object. An identical method and enrichment device were used. The effect of the enrichment device on an aquatic mammal with advanced cognitive abilities was tested in Study 2. Additionally, the validity of a specie specific enrichment i tem across diverse species was investigated. Study 2 : Effect of Species specific Enrichment on the Production of Naturalistic Behaviors in b ottlenose dolphins ( T. truncatus ) Method Subjects Four male bottlenose dolphins ( Tursiops truncatus ) housed at a public facility in Fl orida were subjects in Study 2. Subjects were paired 14 and 9 years old formed

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 35 ) ) group 1 a nd 27 and 17 years old dolphins formed group 2 Group pairings were based on pairings from previous research and typical living arrangements. On e group was tested at a time Three of the 4 subjects were born in captivity and all had extensive experience with cognitive training and research. All dolphins had lived at the Florida facility since at least 2005. Dolphins had access to several tanks. The entire aquarium system in which they lived held 22 million liters in total but dolphins were tested in two small tanks: 7.6 m x 7 m by 7.6 m by 2.1 m deep and 7 m by 8.2 m by 2.1 m deep Materials The enrichment device was identical to the device used in Study 1. A permanently installed surveillance camera a system of hydrophones that allowed localization of vocalizations and Avisoft Pro (version 2.1 ) digital recording program were used for data collection. Procedure The procedure used in Study 2 wa s designed to mimic Study 1. The auditory stimuli used in sessions 1 and 2 were identical to Study 1 (see Figure 3 for timeline of auditory conditions by session). However, some alterations between procedures occurred. Subjects in Study 2 were familiar wit h the researcher present during testing. Dolphins had experience with balls similar to the ball used for the enrichment device, but they did not have experience with the enrichment device itself. The enrichment device was waterproof, durable and made of fl oatable materials; therefore, no adaptations were made between the design of the devices used in Study 1 and 2. As with the lemurs, data

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 36 ) ) collection took place between 12:30 p.m. and 4 p.m during March and April 2010 A baseline session (1560 sec) was condu cted with each group a week after A baseline session (1560 sec) was conducted with each group a week after session 1 data collection. A non experimental enrichment object (a Frisbee) was placed in the tank during the baseline session. Figure 5 Enrichment D evice D uring T esting S ession with T. tursiops The enrichment device was placed in one of two dolphin pools. It emitted three auditory conditions. Dolphins (n=4) were tested in two groups of two. Coding Behavioral coding in dolphins was based on the du ration of interaction or orientation with the enrichment object or the control object Interaction was operationally

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 37 ) ) defined as: an animal touching, nudging, or manipulating the enrichment device. Physical orientation of the animal's body towards the objec t was included in this definition. ( A more extensive behavioral repertoire was not used because the frequency with which dolphins interacted with the device was a useful measure of interest in contrast to lemur subjects). Therefore, the amount of interacti on/orientation displayed by the dolphin group provided substantial information on the interest of the device to the subject group. Vocalizations were analyzed using Avisoft Pro (version 2.1) (see Table 4 for vocalization repertoire) Vocalizations and beh avior were analyzed by group but not by individual. A second researcher coded 10% of sessions to ensure reliability. Ninety six percent agreement was calculat ed between the two coders Results Both groups of dolphins produced very few vocalizations in a ny condition (250/4680 sec, 5.34 %) except for group 2 in session 2 (196/1560 sec, 12.56 %). One vocalization was recorded during baseline (1.4/1560 sec, 09%). See Figure 8 for vocalization type by session. Clicks (192 /197 sec, 97.5%) occurred more than othe r vocalization during this session. Dolphins produced more interaction/orientation behaviors overall with the experimental object (505/3120 sec, 16.19 %) than during baseline with a Frisbee (158/1560 sec, 10.13 %) See Figure 7 for interaction by session. Dolphins spent more time overall interacting with the device in the lemur auditory condition (293/720 sec, 40.69 %) than in the dolphin auditory condition (212/720 sec, 29.44 %). See Figure 7 for interaction by auditory condition.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 38 ) ) "#$%&!) ( )\<$B;%]B/%<+& )*.%//#>)B+>)H#-BI%<,B;)Q<+/#^/)%+) >"#2?/4.%14 # ) ) \<$B;%]B/%<+ ) ) ) Q<+/#^/ ) ) ) Q;%$Z& ) ) ) ) Y&#>)(<,)#$-<;<$B/%<+ )/<)%+I#&/%NB/#)#+I%,<+.#+/ )B+> ) ) ) ) ) B&)B)&<$%B;)&%N+B; ) ) H=,&/)W=;&# ) ) )))))))))))))) !<$%B;)&%N+B; ) ) U-%&/;# ) ) )))))))))))))) !<$%B;)&%N+B; ) ) # HB&#>)<+) JB;&/ <+)B+>)_#,.B+ )K08 78 MD # !##)G%N=,#)1)(<,)&"#$/,
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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 49 ) ) sounds were clear or not is questionable considering the design of the device. The waterproof speaker that made up the device was a n Audio Unlimited PoolPod, a commercial product designed to play music in a pool. It was chosen for this project because it was wireless and affordabl e, but the quality of the sounds that were emitted from the speaker was not reliable. During session 1, the speaker was weighted with the speaker side up which meant that sound projected from the speaker and was emitted into the air instead of the water un less the device was rolled over by the dolphins to face speaker side down. Whether the dolphins perceived sound coming from the speaker is also ambiguous because of their tende ncies to lift their heads above water. This behavior was observed frequently dur ing sessions in which the device was present and sounding, however the same behavior was also observed when the device was not present and when i t was present but not sounding. Problems arose during session 2 for both dolphin groups. Equipment inconsisten cies presented a delay between some conditions The enrichment device had to be taken out of the pool and restarted in order to complete the 26 min session. Technological issues were not uncommon with the device. A more dependable device could have elicite d more reliable results and could have possibly allowed for more efficient use of time, leaving room for more experimental sessions to be conducted. The device used in this study was in essence a prototype. A device that utilized more reliable technology w ould probably produce more consistent results. Nevertheless, the dolphins did interact preferentially with the device.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 40 ) ) General Discussion This study explored the effect of a species specific enrichment device on the production of naturalistic behaviors i n two captive mammalian species. Both the lemur and dolphin groups displayed increased production of naturalistic behaviors during experimental session s than during the baseline session. Variations in behavior in response to auditory conditions were harder to interpret, but some evidence suggested (i.e. the increase in lemur vocalizations in response to the lemur auditory condition) that species specific stimuli were more effective at inducing naturalistic behaviors than stimuli that were not geared toward s the specific species W hat do these results mean in terms of potential benefits for animals in captivity? Increased activity level, vocal production and interaction with the object are all ways to describe engagement with the device Both species were re sponsive to it in some way, and this interest did not subside during the second session in some respects behavioral signs of engagement increased. A limited amount of data prevents definite conclusions; however available data suggest that continued resear ch on device s that emit species specific vocalizations would be worthwhile. Bo th species studied have extensive vocal repertoires and communicate frequently through a vocal medium. The enrichment device presented in this study could have been stimulating to these species merely by the fact that it produced sound. By taking advantage of an animal's natural proclivity to gather information through auditory signals, the device provides a cue that is already salient to the individual. However, it is not clear from this study how important it is to provide enrichment

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 41 ) ) that is specific only to one species as opposed to enrichment that considers the adaptations of the species but can still be generalized to other species with similar adaptations. Both species resp onded to the vocal stimuli, often vocally, but the role of the species matching vocalizations was not clear. The next study should isolate auditory conditions and present them for longer periods of time. This would give a more accurate picture of the behav iors produced by species specific versus generalized enrichment vocalizations or even environmentally appropriate sounds. The behavioral effects of the proposed enrichment device on the E. mongoz and T. tursiops suggests that a device inspired by this des ign could b e beneficial to captive animals Emphasis on catering to the natural behavioral proclivities of a spec ies was attempted in this study and should be a focus of future studies. As more information is gathered about various species, and as their be havioral tendencies in the wild and in captivit y are understood more clearly, researchers will have many potential areas of focus for sculpting captive environments to be more stimulating for specific species and for individual animals.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 42 ) ) References Alford, P. L., Nash, J. F., & Bowen, J. A. (1992). Effects of management practices on the timing of captive chimpanzee births. Zoo Biology, 11 253 260. Baker, K. C. (2004). Benefits of positive human interaction for socially housed chimpanzees. Animal Wel fare, 13 (2), 239 245. Bayne, K. A. L., Dexter, S. L., & Strange, G. M. (1993). The effects of food treat provisioning and human interaction on the behavioral well being of rhesus mon keys ( Macaca mulatta ). Contemporary Topics in Laboratory Science, 32 (2), 6 9. Breland, K., & Breland, M. (1961). The misbehavior of organisms. American Psychologist, 16 (11), 681 684. Carlstead, K. (1998). Determining the causes of stereotypic behaviors in zoo carnivores: Toward appropriate enrichment strategies. In D. J. Sheperd son, J. D. Mellen & M. Hutchins (Eds.), Second nature: Environmental enrichment for captive animals (pp. 172 183) Smithsonian Institution. Carlstead, K., Brown, J., & Seidensticker, J. (1993). Behavioral and adrenocortical responses to environm ental change s in leopard cats ( Felis bengalensis). Zoo Biology, 12 321 331. Chamove, A. S., Hosey, G. R., & Schaetzel, P. (2005). Visitors excite primates in zoos. Zoo Biology, 7 (4), 359 369. Cummings, D., Brown, J. L., Rodden, M. D., & Songsasen, N. (2007). Behavior al and physiological responses to environmental enrichment in the maned wolf

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 43 ) ) ( Chrysocyon brachyurus ). Zoo Biology, 26 331 343. Curtis, D. J., & Zaramody, A. (1999). Social structure and seasonal variation in the behaviour of eulemur mongoz. Folia Primatol ogical, 70 79 96. Dishman, D. L., Thomson, D. M., & Karnovsky, N. J. (2009). Does simple feeding enrichment raise activity levels in ring tailed lemurs ( Lemur catta )? Applied Animal Behaviour Science, 116 88 95. Maier, S. F., & Seligman, M. (1976). Learn ed helplessness: Theory and evidence. Journal of Experimental Psychology, 105 (1), 3 46. Maloney, M. A., & Meiers, S. T. (2006). Effects of three food enrichment items on the behavior of black lemurs ( Eulemur macaco macaco ) and ringtailed lemurs ( Lemur catt a ) at the Henson Robinson Zoo, Springfield I llinois. Journal of Applied Animal Welfare Science, 9 (2), 111 127. Markowitz, H., Aday, C., & Gavazzi, A. (1995). Effectiveness of acoustic "prey": Environm ental enrichment for a captive African leopard ( Pathera pardus ). Zoo Biology, 14 371 379. McPhee, M. E. (2002). Intact carcasses as enrichment for large felids: Effects on on and off exhibit behaviors. Zoo Biology, 21 37 47. Mellen, J., & MacPhee, M. S. (2001). Philosophy of environmental enrichment: Past, p resent and future. Zoo Biology, 20 211 226. Miksis, J. L., Grund, M. D., Nowacek, D. P., Solow, A. R., Connor, R. C., & Tyack. P.L. (2001). Cardiac responses to acoustic playback experiments in the captive

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 44 ) ) bottlenose dolph in ( Tursiops truncatus ). Journal of Comparative Psychology, 115 (3), 227 232. Pizzutto, C. S., Nichi, M., Correa, S. H. R., Ades, C. A.,M., & Guimaraes, D. B. V. (2007). Reduction of a bnormal behavior in a gorilla ( Gorilla gorilla gorilla ) through social interaction with a human being. Lab oratory Primate Newsletter, 46 (3), 6 10. Poole, T. B. (1998). Psychological needs of mammals. In D. J. Sherperdson, J. D. Mellen & M. Hutchins (Eds.), Second nature: Environmental enrichment for captive animals (pp. 83 94) Smithsonian Institution. Ralston, J. V., & Herman, L. M. (1989). Dolphin auditory perception. In R. J. Dooling, & S. H. Hulse (Eds.), The comparative psychology of audition: Perceiving complex sounds (pp. 295 328). Hillsdale, NJ, England: Lawrence Erlbaum Associates, Inc. Reynolds, J. E., Wells, R. S., & Eide, S. D. (2000). The bottlenose dolphin: Biology and conservation Gainseville, Florida: University Press of Florida. Schipper, L. L., Vinke, C. M., Schilder, M. B. H., & Spruijt, B. M. (2008). The effect of feeding enrichment toys on t he behaviour of kenneled dogs ( Canis familiaris ). Applied Animal Behaviour Science, 114 182 195. Seidensticker, J., & Forthman, D. L. (1998). Evolution, ecology and enrichment: Basic considerations for wild animals in zoos. In D. J. Sheperdson, J. D. Mell en & M. Hutchins (Eds.), Second nature: Environmental enrichment for captive animals (pp. 15 29). Washington and London: Smithsonian Institution. Sekiguchi, Y., & Kohshima, S. (2003). Resting behaviors of captive bottlenose dolphins

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 45 ) ) ( Tursiops truncatus ). P hysiology & Behavior, 79 643 653. Sheperdson, D. J. (1998). Introduction: Environmental enrichment in zoos. In D. J. Sheperdson, J. D. Mellen & M. Hutchins (Eds.), Second nature: Environmental enrichment for captive animals (pp. 1 12) Smithsonian Institut ion. Swaisgood, R. R., White, A. M., Zhou, X., Zhang, H., Zhang, G., Wei, R., et al. (2001). A quantitative assessment of the efficacy of an environmental enrichment programme for giant pandas. Animal Behaviour, 61 447 457. Tarou, L. R., & Bashaw, M. J. ( 2007). Maximizing the effectiveness of environmental enrichment: Suggestions from the experimental analysis of behavior. Applied Animal Behaviour Science, 102 189 204. Tarou, L. R., Bloomsmith, M. A., & Maple, T. L. (2005). Survey of stereotypic behavior in prosimians. American Journal of Primatology, 65 181 196. Trone, M., Kuczaj, S., & Solangi, M. (2005). Does participation in dolphin human interac tion programs affect bottlenose dolphin behavior? Applied Animal Behaviour Science, 93 363 374. Uphouse, L (1980). Reevaluation of mechanisms that mediate brain differences between enriched and impoverished animals. Psychological Bulletin, 88 (1), 215 232. Van de Weerd, H. A., Docking, C. M., Day, J. E. L., Breuer, K., & Edwards, S. A. (2006). Effects of speci es relevant environmental enrichment on the behaviour and productivity of finishing pigs. Applied Animal Behaviour Science, 99 230 247. Van Der Harst, J. E., Fermont, P. C. J., Bilstra, A. E., & Spruijt, B. M. (2003). Access to

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 46 ) ) enriched housing is rewardi ng to rats as reflected by their anticipatory behavior. Animal Behaviour, 66 493 504. Xu, J., Yu, L., Cai, R., Zhang, J., & Sun, X. (2009). Early auditory enrichment with music enhances auditory discrimination learning and alters NR2B protein expression i n rat auditory cortex. Behavioural Brain Research, 196 49 54.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 47 ) ) Figure 6 Lemur vocalizations from left to right: SN= sniff, CR=creak, HM=hmm, SG=soft grunt (S ee Figure 1 for spectrograms) Dolphin vocalizations from left to right: BP= burst pulse, CL=click, W=whistle (S ee Figure 2 for spectrograms) Vocal reperto ire s taken from Curtis & Zaramody (1999) and Ralston and Herman (1989)

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 48 ) ) Figure 7 D = dolphin auditory condition, L= lemur auditory condition, S=silent auditory conditio n. Each auditory condition interval was 2 min long. No subjects were visible for the first 10 min of session 2.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 59 ) ) Figure 8 No interaction with EE was recorded during baseline, because no enrichment was present. Only 16 min (960 sec) of session 2 w as analyzed because of inconsistencies in animal presence. Behavioral repertoire was taken from Curtis and Zaramody (1999). ) ! 9) 09) 19) 29) 39) 49) 59) 69) 79) 89) 099) J#&/) O,<<.) !$#+/)[B,Z%+N) P<$<.
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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 50 ) ) ;.<=8&!> ( ) D= dolphin auditory condition, L = lemur auditory condition, S= silent auditory condition S ilent conditions s panned 14 min; lemur and dolphin conditions each spanned 6 min. The baseline period spanned 26 min. Behavioral repertoire was taken from Curtis and Zaramody (1999).

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 51 ) ) Figure 10 Time spent interacting/oriented with EE was calculated by adding all s ingle instances of interaction/orientation behavior. Silent auditory conditions spanned 14 min. Lemur and dolphin auditory conditions spanned 6 min. All interactions during baseline are recorded as having occurred in the silent condition. Baseline interact ion was determined by dolphin interaction with a nonspecies specific enrichment object (a Frisbee ). The baseline session spanned 26 min. 9) 09) 19) 29) 39) 49) 59) 69) 79) 89) 099) P#.=,) F<;"-%+) !%;#+$#) "./&!0*4! ?=:.-+8@!A+3:.-.+3! Interaction with Objects by Auditory Condition in T. tursiops HB&#;%+#) !#&&%<+)0) !#&&%<+)1)

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 52 ) ) Figure 11 Vocal repertoire based on Ralston and Herman (1989): BP=burst pulses, CL=clicks, W= whistl es See Figure 2 for spectrograms of vocalizations 9D94) 9D43) 1D63) 9D98) 01D18) 9D20) 9) 09) 19) 29) 39) 49) 59) 69) 79) 89) 099) HW) QP) U) "./&!0*4! B+C#%.D#-.+3!"@E&! B+C#%.D#-.+39!$@!F&99.+3!#3:!"@E&!.3! !"#$%&'()*'# HB&#;%+#) !#&&%<+)0) !#&&%<+)1)

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 53 ) ) Appendix A Questions on Enrichment 1. Define enrichment in your own words. 2. Why do you think enrichment is important? 3. Is enrichment an important component of animal caretaking in y our facility? 4. What are some specific enrichment methods utilized? How effective do you perceive those methods to be? 5. What is your perception of the enrichment literature? 6. What is the role of stress in the lives of captive animals? When is it a neg ative influence and when is it positive? 7. Does your institution communicate with other institutions about the effectiveness of different enrichment techniques? 8. Have you seen any evidence of enrichment influencing reproductive success in your facility? 9. How effective are goal based enrichment programs at maintaining the psychological well being of captive animals? How does it compare to an opportunistic approach? 10. How effective is social enrichment in providing meaningful stimulation for an animal? How does it compare to environmental enrichment? 11. Is human interaction used as a form of enrichment in your facility? 12. What's the best way to assess appropriate enrichment for a specific animal? 13. Do you think cognitive research and training are e ffective methods of providing enrichment?

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 54 ) ) Appendix B Interviews with Animal Caretakers about Enrichment Enrichment interview #1 conducted in person with the Research Manager and the Animal Care Manager of a facility that houses and breeds endan gered prosimians R : Define what enrichment is in your own words: I 1 : In my opinion, it s an item or a situation that adds a level of changes in the animal throughout the day, whether it be positive or negative. There could just be enrichment that happens w ithin their environment, even though it s routine, it could still be enriching. It could just be when a car pulls up, and even though it s not novel it could still be eliciting a response from the animal, positive or negative. I 2 : When I think of enrichme nt, I think of ways of making the animals' enviro n ment and daily life more complex, so that there are more levels to their life. And also, a way of eliciting the full range of natural behaviors and some of those behaviors we think of as stressful or negati ve but it s basically still an experience that we have essentially robbed from them by keeping them in captivity. There is a trade off when you keep an animal in captivity. You keep them from gett ing eaten by the fus a, but their environment is considerably more impoverished than it would be in the wild. So you try and balance that trade off, so that's its more in favor of the animal living as naturally as possible while still being protected for all the reasons that we keep captive animals. Some stress is good. In humans that experience little to no stress, they become in a way autistic people have low stress because they intake low amounts of stimuli and there's no t a lot of interaction. 1 So their cortisol levels would probably very low, we need spikes of stress, that's what we react to. At least in human studies, it s that chronic constant stress that causes all the ideological problems. But interacting with a new mate is stressful, but it s also positive and rewarding as well. Stressful isn't necessarily when we think of the word we associate it with negative things, but it s not. It's not always negative. I 1 : Along with that, it can also bring about cohesion within a group, you know they can all be stressed together or they can all come against some fa ctor that might be stressing. It could elicit something that initially is stressful but then acts as something more cohesive. R : How important do you consider facilitating enrichment or stimulation? How prevalent is it? I2 : Enrichment is really important I think in the traditional cage enclosures. I have never considered enrichment to be a high priority for our animals that are free ranging. There is an enormous amount of environmental and behavioral flexibility out there. It's not that we never do enri chment out there, it s just not as common and I don't feel that it s as )))))))))))))))))))))))))))))) ))))))))))))))))))))))))) ) 0 )L-#)%+>%I%>=B;)%+/#,I%#?#>)%&)+)>=,%+N)/-%&) %+/# ,I%#?)B,#)@B&#>)<+)/-#)"#,&<+B;)<"%+%<+)<()/-#)%+/#,I%#?##D )

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 55 ) ) necessary. But the cages are certainly like simplified environments, and there is not as much opportunity fo r change. And I think its essential for their long term health that we pr ovide enrichment regularly. We have been regular about it, but not very. I 1 : It's very important and it s our responsibility as caregivers to make it not an extra thing, but a routine that we do. R : Can you describe some the techniques you use? I 1 : Brow se not only is it important for their dietary nutrition, but it s also an enrichment item for them. So the browse is very important for them. The toys and things like that, which can be traded throughout the group. Toys can be given to a new group, and th en be haviors are elicited like scent marking and things like that. Also, depending on the weather it s important to give items to the animals. Its important to keep them hydrated, we try and give them ice. We give things within their environment that they are going to benefit from. I 2 : Lemurs have trouble thermoregulating, they are not fabulous at it. Enrichment like ice treats can play dual roles; it s novel it s interesting they can interact with it but it s also.. R : How effective do you think the me thods that you do utilize such as browse and toys are? I 2 : Overall, the cumulative effect of our enrichment is very effective. Our animals are generally very healthy and they show very few stereotypies. But we see very little of that here, so they are psy chologically and socially stimulated enough to avoid normal behaviors. I think that there is always room for improvement, and I think that our weight problem would be easier to control if we increased enrichment that targeted movement. Of course some enric hment is more effective at engaging them than others. I think the hardest thing is to get non food enrichment, they are not often very motivated if it s not food motivated. Our scent marking enrichment has been pretty effective. I 1 : I think it s very effec tive and even if there are items that I don't see them respond to, it s still done. There might initially things that I don't see that they are doing, but even though there are things that I don't see, its still beneficial for them. Again taking that ite m or then putting it in someone else's cage, even if they happen to step on it or accidentally urinate on it, then at least it can be stimulating for someone else. Sometimes we will take towels or sheets and spray it with a scent (ras p berries) and they may never go over to it, they may smell it in the air they may avoid it.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 56 ) ) I 2 : We don't have a feedback loop here. We don't anything formal like that. We talk about it, but that would be a nice improvement and we are working towards it. It's one thing to do e nrichment, it s a whole nother t hing to take data. R : Earlier I remember talking to you about a goal based enrichment program. I am wondering what ideas you have about that at this point? I 2 : What I had in mind was like (facility in central Florida's) nat ural behaviors. Something where you get together as a group and say H ere are our goals for this program.' For us, it would be things like you'd start out with a preliminary activity budget and then see if you could increase the amount of time that they a re active, gearing those parts of the day that they are normally active. If you could extend the active period in the morning and even by an hour, than your animals are more likely to be the appropriate weight and they are less likely to potentially engage in behaviors by picking on. Another thing that would work well for our instit ut ion because we are research oriented, is you have an ethogram for all of our species, t o take data and after the implemen tation of an enrichment program and see how many of t hose behaviors we can actually get them to exhibit. Foraging is tough. Its tough to get animals to forage in a caged setting, but it s not impossible and actually Pattie does a lot of different things that encourage foraging. There are some behaviors that you won't see. Some of our animals are currently on contraceptives so you're not going to see reproductive behaviors. But we have even talked about surrogate infants in the form of stuffed animals for those animals that are breeding. Has never been done w ith lemurs. It was prompted by, one of our females who lost her litter, her triplets, and the first couple of days she was really lethargic and depressed and she took a pine cone and kept trying to hide it and nest with it like she would with her infants. I 1 : I have seen that too with other primates, they take inappropriate objects and have held them and walked around with them. I 2 : So it's a little sad, but I 1 : A grooming board, our lemurs groom with teeth, so you find something they can actually comb through or with chimps you find something they can pick at with their fingers. R : I have some research about the effect of enrichment on reproduction have you had any experience with anything like here? I 2 : without the data We've had decent reproductive success here, but since we give everyone the same level of enrichment, there is no way to really say. I will say that with lemurs weight dramaticall y affects their success of concep tion. Fat lemurs don't conceive; there has been a few articles written abo ut it. And I can certainly see a

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 57 ) ) correlation between weight and enrichment, which would then contribute to reproduction. But like a direct correlation, there is no way we can say, but I wouldn't rule it out. I 1 : After our female lost her litter we put he r next to a mother who had appropriate behavior, so it was as if the daily visual of how a mongoose reacted with her infant hopefully would give her some indication of the appropriate behavior. I 2 : And ther e was a lot of visual interest; she spent a lot o f time s taring at the mother and infant. S he would sit up on nest box and the mother and infant would sit on the other side. She would sit and was quite tolerant. There was no aggression. I 1 : They were in a fairly large cage and they chose to be right next to each other. I 2 : We have a lot of social enrichment, that's probably our most common form of enrichment. We have a singly house primate out there, but he hasn't gotten crazy behaviorally. We have increased his enrichment. But he is very enriched, simpl y by the lemurs. R : Have you identified any behaviors that are different between the free ranging and the caged species? I 1 : I think vocalizations, there are much more vocalizations in the free rangers. I don't know if it s because of the species, but I d o notice that when the free rangers are in there are less vocalizations from them. Also, unfortunately the cages that we do have are not as high as the forest canopy. So their ability to lope about the forest is not the same. R : What is your perception o f the enrichment literature? I 2 : It's sort of impoverished I would say. Most the readings you find on enrichment are informal things from people who work in the field. There's always been an attitude about captive research, about how captive data collectio n is not as valid as data collected in the field. There's absolutely that prejudice. You encounter it at every conference that you go to. Those people whose job it is to research are less attracted to those kinds of research questions, because there is jus t this attitude. So then it remains for those of us who are taking care of captive animals and know how important it is, but don't have the time to get that data. I definitely think that taking data in captivity can inform us about animals in the wild. But that is not the generally held view at all, although that's changing. I think it's changing. I think that our academic generation is making that transition of more interdisciplinary. I 1 : I agree with you, it is fairly informal. Sometimes there is no foll ow up. It's great for novel ideas, but it doesn't really have a scientific approach to it. I 2 : It's more qualitative than quantitative. I 1 : And I have not iced more in the past few years that the veterinary community is taking on enrichment as a source of t reatment. To actually find out if enrichment or enriching

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 58 ) ) the animal's life more affects the animal's life or their rate of healing. They get a better response with animals who are less stressed. I 2 : There is definitely not a lack of emphasis on psycholo gical well being in the caretaking community. But its not something that is discussed very often in the research community, particularly in terms of animal behavior, or abnormal behavior because they're captive. But what drives me crazy is that "they could be a resource for wild animals at some point in the future," They are a resou rce now! They are in is impoverished in the form of horizontal structures. Many different species of lemurs prefer large sweeping and moving branches. And we have a slash pine f orest. So one of the things that Savannah is looking at is their behavior, and where they are spending their time and what they are spending their time on before and after we supplement that forest with more horizontal structures. And while that is powerfu l for use in captivity, it s also something that can be powerful in the wild when doing translocations or trying to encourage survival. Most of Madagascar is, if you are lucky, a rainforest. You have these scraggly much smaller, much less complication in ideal environments for the lemurs. Increasing survival by putting in horizontal structures is a small investment for the output. But it s something that they won't actually unless they have demonstrated that they will use them. Wild data giv e us feedback f or captive studies which can then be used in conservation studies. R : Are there a lot of reintroductions? I 2 : No, there has been one. But there are more translocations within Madagascar. Reintroductions are really controversial. It's really hard to take an animal that is born in captivity and have it succeed in the wild. The one introduction that they did, the black and white ruffed lemurs, most of those animals were taken from zoos. Some of those animals did interact with wild animals and have offspring. S o, from that point of view it was a success. But most of them bred with each other and not with wild animals, with is only helpful if the offspring then breed with wild animals. And there is a lot of concern now about disease transfer. Translocations are t aking wild animals from one place and moving them to an area that used to be in their home range but isn't now. Translocations are somewhat more successful because the animals at least were wild born. There's still a lot of complications. If you haven't de alt with the reason that they went extinct in that area then they are just going to go extinct again. But there's been some very successful translocations in Madagascar. There's a rumor that they are.. Reintroductions, if you have to do a reintroduction t hen you are on your last leg. It's not very promising and it s enormously expensive. R : So how do you guys feel about training and cognitive research as forms of enrichment for captive animals? I 1 : I think that training is enrichment for them. And it help s to build the bond between trainer and animal, at times if they want. It gets them active within their enclosure. I have seen s uccessful laser target training; that can be beneficial for their health.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 69 ) ) I 2 : From what we have seen here, it has been enormou sly enriching. I 1 : They look forward to it. I 2 : Absolutely, they practically line up. I 1 : One of the training sessions involves them being inside to crate train. And some days when it takes a little longer, the days that they are not fed earlier, they al l come inside thinking it's a training day.. well I don't know what they are thinking I 2 : They also spend more time inside their crates. At least with the infant mongoose that we have, she sees people and immediately investigates them, sometimes to the po int of being problematic. I have worked with quite a few mongoose lemurs now, and that seems to be directly a result of her training. She sees people and thinks positive things will happen. R : Do you think that human interaction is a positive experience f or most lemurs? I 1 : If you don't have a net I think it s overall positive and I think that lemurs as a whole have the uncanny ability to forget a little easier than other species of primates. So I think they definitely associate human interaction with pos itive. R : Do you have any sense that they associate specific experiences with you and specific experiences with I1? I 1 : I1 claims that there's one who doesn't prefer her at some points. I 2 : She hates me! She is an aggressive animal in general. But she bo nded with our last keeper to the point that the keeper could go in with her and could get on her knee and habituating her.. When I go to the cage wall she immediately jumps over and tries to grab at me. I definitely couldn't go into the cage with her. Patt ie is starting to make progress and is able to make some contact through the cage wall. But I am always the one who catches her up for physical. And once that pattern was established, the other keeper wasn't even allowed to do restraint. So that the other keeper couldn't be associated with those negative experiences. But she is an extreme example. R : In general, you don't see a long term effect? I 2 : No I don't. I also have positive interactions with them as well, even though I feel like I am the one that d oes the negative things and not the positive things. We had a bamboo lemur that had a negative association with hats, with an object. They participated in a study that was looking to correlate testicle size with testosterone. The man, the researcher, wore a baseball cap. Kevin always wore a baseball cap. Kevin doesn't do a lot of lemur care there. That's his job basically. R : As far as health of the animals in this facility, is the main problem weight gain? I 1 : Weight gain as well as some intestinal para sites.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 60 ) ) I 2 : Weight is something we are always conscious of and aware of but it has been a huge problem here. I 1 : It'd be nice to have the lemurs trained for routine medical husbandry. It might even be possible in the future to anesthetize them for injecti ons. R : So when you take blood you anesthetize them? I 1 : Yeah in general, we do have individuals that we can grab. R : In general are they pretty fragile? I 2 : They are pretty robust. There is a species variation; we don't keep fragile species here. One of the reasons we started was to get those adaptive generalists that aren't a pretty color but that tend to be really robust. They usually recover just fine from anesthesia. Lemurs, for the most part, are not very breakable. R : I am wondering if there is a ny kind of communication between facilities about enrichment ideas. What have you guys learned from other places? I 2 : Almost everything! This was my first keeping job. What I didn't learn from the keeper who trained me, I learned from other keepers. Either from forums or I 1 : Going there and seeing the platforms or what the inside holding looks like and how they do their routine. I think that's the best to see how other people are doing things. I 2 : It's often depending on the conference you are going to, the last conference I went to, one of the topics was on enrichment. R : Are there many new ideas at workshops like that? I 2 : Yeah! Absolutely! Like fish, we still haven't done that. I was at this conference and one of the keepers said they would put a litt le covered fish tank in with their lemurs and the lemurs were intensely fascinated with the fish tank. And I was like Dude! Betas are like a dollar I think that the mongoose lemurs in particular would be riveted by it. I think they would spend a while trying to get the fish out. We should hide eggs! I wonder if we could get little unfertilized quail eggs. I bet the mongoose lemurs would go crazy. R : Any other ideas? I 1 : Trying to get away from food enrichment to visual, maybe a tv. I 2 : We do have a lo ng term enrichment plan. We are still fleshing it out. Ultimately we want more fruiting in there. I 1 : We talked about increasing the browse for the guys on the inside, both the variety and frequency.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 61 ) ) I 2 : Browse takes time actually. It's one of the more t ime intensive things, but it s so rewarding. One of the things we are working on it make it easier. There is a master gardener who approached Penelope, and the two of them are planning to plant the browse garden so it will be really close and the keepers w ill know that everything there will be safe to take from and put in the cages. It takes time (comes from the forest). I 1 : I think the variety too. Just knowing where it is and getting there I 2 : I am excited about your project and I would like to see more students doing enrichment research. I am curious to know if enrichment done ad hoc is more or less effective. Because if it s as effective, then why go through all the trouble of creating an enrichment program. Because it s pretty time consuming to set it up. Everyone just assumes that a program would be effective, but that's a pretty big leap. I mean if you are already doing, do the animals care. I 1 : T hat was a topic of discussion. Every Wednesday they get grape vine, so what does Wednesday mean to them? R : It seems like if you are giving enrichment, even if it is opportunistic, there is some kind of enrichment program there it s just the degree to which I have thought about this some and thinking about intention and maybe if there is more thought put i nto it, maybe then just because you are calling it a program it becomes this greater thing that is more important within the institution. I 2 : It also has more to do with institutional support. R : Because it's the same kinds of things, the same kinds of o bjects. It's just how much time you are thinking about it. I 2 : And how much administrative support it. But if it s programmatic But it would be powerful data. I 1 : In my community, enrichment is very important. We welcome any involvement. I 2 : It's a rea lly fabulous and positive part of the job. I 1 : We gave them pumpkins last night. I 2 : We were talking about trying to get free items. It seems unfair that we don't have a budget for enrichment. It's a really cool way to reuse and recycle. We have a bunch of kids toys out there; you can't recycle kids toy plastic. We are probably doubling its life, at a minimum. I 1 : They don't care if it doesn't have wheels anymore.

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 62 ) ) Enrichment Interview #2 conducted by phone with the Curator of Behavioral Husbandry of a z oo with a large collection of diverse species R: Define enrichment in your own words. I 3 : In my own worlds, I feel like its providing animals with opportunities to, creating homes for them where they have opportunities to express their natural abilitie s in their behaviors and mainly to live a life where they can be comfortable and where they can feel safe but also by safe, I am not trying to say that its this life where things aren't exciting. Where there are things of interest and unique and novel expe riences happen but it s done in a way that they can also cope with those experiences and still feel like they can handle them. And i t's not done in a way where its shocking or they can't have the environmental sort of support to go out and to escape or to get away from various stimuli. R: Is enrichment an important component of animal caretaking in your facility? I3: Absolutely. It's actually very difficult because you know when you look at it traditionally; enrichment was always sort of this add on. B ut as designs of exhibits get better and better it s very difficult to say what is enrichment because as we do better with social structure that we put together for the animals. What do you add on when you have this giant beautiful savannah in a social gro up of T hompson's gazelles? Well, truly the exhibit itself and the opportun i ties you've provided through the home that they live in is their enrichment program and a lot of it is looking at your output instead of your input. Looking at, what is behavior tha t we have seen in these animals and is it what we would like to see and what is it that we should change or do differently to get us where we need to go in terms of augmenting that particular environment. It s not so much about these small little add ons a nymore. Enrichment is critical, hugely important, a huge focus at (the zoo) but I would say that its definitely evolving based on the kinds of exhibits that we are able to provide right now. R: What are some specific enrichment methods utilized? How effe ctive do you perceive those methods to be? I3: I think that all of the enrichment programs are designed based on both the individual history and the natural history of individual anima ls because individual animals are what welfare is about. Your first loo k from a species level about what the needs are but then you have to look at the individual needs. So when we go about the task of designing a program we first start by trying to identify: what are the behaviors that the species would be exhibiting or wou ld be highly motivated to exhibit and also what are the outcomes of those behaviors. If a particular animal does a lot of digging, what is the outcome of that digging? Is it to make a burrow? Is it to get cool? Because if they can t be able to answer that need, you might be able to give them an opportunity to do it. But if they can t

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 63 ) ) actually build a burrow that could cause them to have a lot of frustration. So you have to make sure that you can provide the opportunities as far as the behav ior but also sort of the satisfi er at the end of the behavior. You kind of look at creating the opportunity for the behavior and the outcome. If you are talking about a rhino, wallowing would be a highly motivating behavior for them. For creating a coating on their bodies that is like a sunscreen but also it cools them off, but you have to look at the substrate that you are providing: is it desirable, wallowable material? Is it something the an imals would like to wallow in? A nd you can provide that. Then the next question i s: do they actually wallow in it? You might have certain animals that do wallow in it, so you say h ey, you know they are wallowing in it. But then you have to look, do all of the animals have an opportunity to wallow? Are dominant animals keeping that res ource from other animals or is the location not a good location? All of the animals should be able to have the opportunity to take advantage of that wallow. It s not just about giving them something, you have to really make sure that you can have a goal, b ut you have to make sure that all of the animals have an opportunity to take advantage of it and that it really works and you have to make sure that over time, that's also successful. For example, with a wallow, they kind of lose their gas over time and th ey are more effective if you change around the substrate every few months. And in the case of our animals, we put a few differe nt wallows in different locatio n s to make sure that animals are not left out. R: What is your perception of the enrichment lite rature? I3: I think in general with zoos, its always hard because the size of the studies are very small in terms of the animals and it 's just how.... it's hard because usually they don't relate enrichment to an animal's overall welfare and usually their r elated to x behavior. So they are very narrow for the most part. I think it s challenging because it's a bit of the nature of science and the nature of collections in zoos. People trying to cut down the number of variables that they can have in the study a nd make the study able to pass the peer review process and then I think the studies become so over generalized or so diluted that I think then the question is : how useful are they really? In terms of information that could be applied at another zoo. And t hen the re are completely areas of void; in training they're looking at the interaction between training the keepers and the animals. It's very difficult to find anything that is substantial about the benefits of training. R: Can you talk about training a s a form of enrichment? I3: There is a lot of anec dotal but not a lot of scientific objective stuff in the literature. And that's one of the things that I have been trying move into our institution to figure out how to do more of. And for many years I ha ve been doing presentations (I haven't the past two years) but for five years before that, doing stuff at C harles R iver labs, to encourage them to do training with those animals. The reason why is because they will scientifically measure the effect of trai ning on their collection because that's something that they are dedicated to doing with all aspects of the ir husbandry, is measurement. T h a t s what a lot of the enrichment lit comes from, is from the laboratory community and

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 64 ) ) measuring the benefits of speci fic enrichment devices so my hope is while they start training they could measure the value of training. We view training as a tool that could potentially be used for any animal within our collection, for day to day husbandry and for medical care. Everyt hing from animals just walking from in the barn to out in the savannah to hopping on the scale to crazy cool things like ultrasounds, drawing blood samples, rectal ultrasounds for reproductive assessment. These are all things that many animals can be train ed to do voluntarily and cooperate with their own care. And our feeling is that, by animals doing things voluntarily and cooperatively decreases the amount of immobilization that you have to do and every time you immobilize an animal there is more risk tha t the animal will risk the caregivers. It can potentially be a stressor to the animal to be immobilized, esp ecially depending in how they are immobilized, esp ecially if they're darted there can be a risk to the anim a l through the darting process as well. W e just feel that there is tremendous benefit to training animals just from that alone, but also, our tigers are trained for blood draws. The fact that we can get blood from them at anytime means that we can be really proactive about it in our medical care. Because they are voluntary, they can they tend to overdose animals, just the injection itself can cause inflammation or a reaction inside the body, they can get tumors from them. So by being able to dose them appropriately, the animals don't have those side effects and you treat them much more appropriately. You can also know if an animal is getting sick by looking at their blood, you can track things like hormone levels, so there's huge benefits just from getting a regular blood sample and on top of it you don't have to immobilize the animal. If you think somebody is getting sick or ill you can pretty much give them their full physical without having to do an immobilization. Even if you do have to immobilize, the animal can take a voluntary injection, (a ll of our primates do this) the amount fo r the drug will be far less than if the animal was darted because the animal sees a vet and a dart gun their adrenaline shoots up, so you need a lot more of an immobilizing drug to have them go to sleep. There's thi ngs like immobilizing drugs can cause, like lowering your immunity. The fact that you got excited while being given an immobilizing drug can make your white blood cell count go up, so when the vet then looks at your numbers it s difficult to tell whether y our white blood cell count goes up because you got excited or because you are getting sick. We can respond to emergencies much better with training. F or example one of the gorillas got their hand accidentally closed in a door, and the keepers were able to train him to put that hand out and get an x ray voluntarily, so without having to cause any more stress on the animal. Therapy can be trained, if an animal has surgery or gets a wound from another animal. The keepers can train them to move that limb or whatever to get full mobility back. I think that it's a huge area, where it s just hard to get I am finally now starting to get one of our scientists to be interested in trying to get some stuff into the lit erature. I t s just very difficult. They all sa y, oh the sample size, the variability. It s hard because you have to make these conditions, control conditions and they need to have it set up in a certain way to be able

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 65 ) ) to truly prove their point. One of things is that there has been great record keepin g at (the zoo) over the past ten years and I think we are sitting on 12 years of a gold mine, just in our records that we could be using. But we are starting to peel back some of the layers there. So we are looking at some things and I am just very hopeful that, I think that we can do some of these really nice case studies, but I think that if we can get some numbers out there it would get zoo directors more commited to these programs. Because I think that even though people will agree that there are benefi ts to them, they are still some of the first programs that get unfunded when budgets get t ight. And I think t h a t s not the integration we are looking for. I think they are so important that we can t have them go O h well, we don't have the money. That's n ot what we are going to do. R: Does your institution communicate with other institutions about the effectiveness of different enrichment techniques? I3: There are some ways that information is shared, the sh ape of enrichment is one tool. The Fort Worth Z oo has an enrichment w ebsite where people share ideas; we have ideas on our enrichment website. We are always calling and talking to people about their ideas. We probably have many time s a year, people from different institutions shadow at least twice a month, we probably have someone coming to shadow our program. They have really cut back on travel though because of our budget so the last couple of years we haven't been going to as many conferences and doing as much as we used to do, but we still spen d a lot of phone time or time on list serves sharing ideas back and forth. It's a critical thing to be sharing ideas back and forth because we are sort of a brain trust for each other. When you add other perspectives that is how you can really get your pr oblem solving or an individual that sort of perplexes you and you kind of put your feelers out there, hopefully someone else has had some ideas before or had some experiences. R: Is human interaction used as a form of enrichment in your facility? Like an ything it can be something that is good and something that is used incorrectly in any facility. I think the first thing is knowing the individual history and the natural history of your animals and knowing what is appropriate and what isn't. Y ou always ha ve to make sure that your snapshot is going to get you to what your movie is at the end. For example, if you are playing around too much with your bongos, that he doesn't turn into a monster even if he is parent reared. If there is too much interaction wh en he is younger, your snapshot may be cool as a younger but when he gets sexually mature he might try to mount keepers. So you just have to be really judicious in understanding what is appropriate and what is not appropriate. I think given that, if these things are put into context. I think it s very important for us to recognize that we are part of t h ese animals lives; it s important for us to make sure that we are always respectful of the animals and their environment and that we are putting

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 66 ) ) ourselves appropriately within those contexts. In some cases, I think we can be a great form of interaction with them and we can be a very positive force in terms of making the animals day more interesting and exciting and I think that we have many examples at (the zoo) where that's the case in terms of I think there are some animals where that game of training and interaction is something that the animals are all over. For example, our red river hog, some of the animals will just go in and rub down and scratch an d get a massage as part of their sessions. Many of the primates, the keepers will groom them as part of the session. Obviou s l y the training itself can be very enriching in terms of it being a puzzle or a game to figure out and some of the cognitive trainin g that it was like a computer game that he did with the animals, and the animals would continue to do it whether food was involved or not. I think the animals themselves sort of tell us that those interactions are desirable based on their behaviors. R: What's the best way to assess appropriate enrichment for a specific animal? I3: We have a list of questions tha t we go to on website. It sort of goes through, we do it in the group. We have a team that will answer the questions ahead of time and then we di scuss the individual animal and kind of talk through things case by case, because the facility itself might have constraints or certain members of the group might have some constraints. Or the question also changes over time. O ur tigers when we first had t hem were young enthusiastic tigers and they are an aging collection and now we are looking at more geriatric. Your program has to evolve with the needs of your collection as well. In terms of making it appropriate, I think it's a constant assessment of th e animals and how they're reacting and responding. Sometimes we have brilliant ideas in our office that are completely wrong when it comes to the animals reactions and response. R: Do you deal with a lot of abnormal behaviors? And if so, does the enrichm ent you provide have any effect on them? I3: We're very lucky. In our case we haven't had a lot of abnormal behaviors to work on. Usually we can catch them early on, sometimes they are due to new introductions where animals might be initially uncomfortable in an exhibit space. If so, you can figure out how to amend. It's sort of a test and adjust period. And if you can notice right behaviors th at you can keep from becoming stereotypic behaviors. But if you can notice animals doing some small behaviors, diff erent changes to their exhibit you can keep them from becoming pattern behaviors. Enrichment is a huge help in that, but also recognizing the behaviors quickly is a huge help in that. We have had animals that have come in with some behaviors that enrichmen t has been a huge help with, but when I talk about enrichment its in a very broad sense big changes in their environment and big changes in their social grouping have helped. We had a llama who had a head twirling behavior, that through enrichment the team was able to eliminate. Sometimes you have some repetitive pacing of animals before they eat. It s common with carnivores when they are getting ready to get something to eat. Sometimes you can reduce it by changing the time

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 67 ) ) of day or adding enrichment thro ughout times of the day. We still do see some repetitive door checking by some of the animals. We have a process at (the zoo) and if any keepers or managers or actually anybody that notices any behaviors that they think look strange or weird or out of pla ce, that they can report the behavior and then it s looked into. If it is considered that is not in the normal range for those animals, we have a whole step by step process that we go through to assess the behavior and then to try to work on that behavior. So I think that's really helpful in terms of trying to work on something The process does work, they thing that we are working on right now is a welfare assessment and that is something we would do with the whole collection. The thing that I don't like about the other pro cess is that it's reactionary. "O h, I've noticed something." It would be great to notice as you go, looking at positive behaviors and not just undesirable behaviors. There is a lot of work now about measuring positive signs of welfare n ot just negative signs of these sort of suspect behaviors. So what I am interested in, what if we had a thing where we were measuring positive signs and things that could be suspect all along and kind of always looking at our collection and randomly testin g our collection, because then that way we can get a really nice baseline of what we want to be seeing. And if for example, you should expect to see x amount of play behavior or certain types of positive behaviors and you are actually seeing decreases in t hose, that would be actually a first sign before you ever see some sort of suspect behavior. So hopefully we could catch things much earlier and also have a really nice baseline of what we would like to be seeing. For example the ones that we are looking at and piloting now is we will identify physical and behavioral indicators of things, for example, grooming each other is a behavior that is positive and something that we would like to see. These things they would be based on the hierarchy, and like anyt hing when you are an animal keeper, things are in trend. We would be looking at assessing if we started seeing him not grooming as much as he used to groom. Everything is in combin ation. You have to look at the big picture, it s not just one behavior. On e of the top positive indicators that we look for, one of the top suspect behaviors, would make us take another look. And then there is this other thing called a pig plotter that just helps us look at the group as a whole. 11. How effective do you think y our attempts at enrichment are generally? I think that we are really lucky to work for (the zoo) because they are willing to put the resources into our program and we have the ability to try new things with the animals, so we are given the time to, cause time is a huge resource. I feel very excited and proud with our program in terms of what we are able to pr ovide and I also think that the team of people that we have are very attentive to the welfare of the collection. I feel really good about what we are able to do. But I don't really think welfare of the collection is a journey that happens with a clear destination. I think that all of us are trying to continue to do things better. That's why I want us to figure out this other welfare assessement

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 68 ) ) I thi nk that the future holds a lot of learning. I think that maybe we should have more objective studies of how we are doing, I think that we will assess welfare. I think the field is big, wide and open. I think that we have a lot to hear. Enrichment Intervi ew #3 conducted by email by a researcher who has worked on enrichment with pigeons R: Define enrichment in your own words. I4: Enrichment is a way to give captive animals opportunity to express normal, species specific behaviors. It provides them with bo th mental and physical stimulation and activity, with the goal of increasing their well being. R: Why do you think enrichment is important? I4: I think that in return for utilizing and keeping animals captive, and using them to learn more about behavior, learning and biology, it is the responsibility of laboratories to provide the animals in their care with a quality of life. I also believe that barren and confining housing will affect both the physiology and performance of laboratory animals. R: Is enri chment an important component of animal caretaking in your facility? I4: I do not feel like there is a consistent practice across the different labs that house animals. In our laboratory, we are slowly trying to address some of these questions. R: What a re some specific enrichment methods utilized? How effective do you perceive those methods to be? I4: Currently, with our laboratory pigeons, we provide them with the opportunity to fly, interactions with conspecifics and opportunities to water bathe on a d aily basis. We are in the process of exploring other types of enrichments for our laboratory pigeons such as toys and mirrors. Access to their aviary has been difficult to assess. It seems that there is initial burst of activity, but activity levels thems elves may not be the best way to assess whether or not an aviary is an effective type of enrichment. It can also pose a few problems, such as when some of the birds get territorial and start fighting. With our laboratory fish, we have seen some increased breeding behavior when they are provided with plants and stones in their tanks. R: What is your perception of the enrichment literature? I4: There have been so many different approaches to enrichment! I did enjoy Robert

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 79 ) ) Young's book. I think there have been some really well designed studies, and like any other subject out there, there is some variation in how well enrichment is designed and evaluated. I also don't think that enrichment should be discounted just because a researcher does not get the ant icipated response. I think regardless of animals temperament, genetics, or behavior, that different forms of enrichment that allow natural behaviors should be offered. Also, the behavior of animals and humans are present can be quite different as to how they act in the presence of their conspecifics or when alone, so evaluation of enrichment needs to take that into consideration. R: What is the role of stress in the lives of captive animals? When is it a negative influence and when is it positive? I4: I' m not sure that I see a positive role of stress in the lives of captive animals. R: Does your institution communicate with other institutions about the effectiveness of different enrichment techniques? I4: Not formally we have certainly talked to other p eople who housed pigeons. In general, my experience has been that psychology labs in the United Kingdom are much more progressive about housing pigeons than many laboratories in the United States. R: Have you seen any evidence of enrichment influencing re productive success in your facility? I4: See above about the fish, and a few of our pigeons have laid eggs since they have had access to social contact with other birds. We have been actively trying to breed the zebrafish, but we are not breeding the pige ons and have destroyed any eggs that were laid. R: How effective are goal based enrichment programs at maintaining the psychological well being of captive animals? How does it compare to an opportunistic approach ? I4: I am not sure what you mean by an oppo rtunistic approach? R: How effective is social enrichment in providing meaningful stimulation for an animal? How does it compare to environmental enrichment? I4: I see social enrichment as a type of environmental enrichment. I think it depends on the spec ies and what their natural behaviors are are they social? Do they pair bond? Are they territorial? How much space do they have? Do they have hiding spaces? R: Is human interaction used as a form of enrichment in your facility?

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!"#$%#& !"#$%(%$)*+,%$-.#+/)))) 70 ) ) I4: Not intentionally. A few of our pigeons are pretty social and cuddly. We do some hand feeding to try to get them used to being held to make other husbandry techniques easier, such as weighing and moving. R: What's the best way to assess appropriate enrichment for a specifi c animal? I4: I think the best way is to assess several different responses to an enrichment and also to consider the natural behaviors of the animal. If you look at only one measure (such as activity level or time spent interacting with a novel object) I don't think you can really get a good sense as to how enrichment adds to a captive animal s life. R: Do you think cognitive research and training are effective methods of providing enrichment? I4: Not in and of itself. It also depends on what other techn iques are employed are the animals used to handling? How food deprived are they? What if they do not perform well on the cognitive research? I do think it can provide some mental stimulation, but that is not necessarily a "natural" behavior for the an imal, and I do not think it is sufficient to enrich a captive animal s life. ) ) ) ) ) ) ) ) ) ) ) ) )

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