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Effects of environmental enrichment in a captive pair of Golden Parakeet (Guaruba guarouba, Psittacidae) with abnormal behaviors

Effects of environmental enrichment in a captive pair of Golden Parakeet (Guaruba guarouba,... Revista Brasileira de Ornitologia, 23(3), 309-314 ARTICLE September 2015 Eff ects of environmental enrichment in a captive pair of Golden Parakeet (Guaruba guarouba, Psittacidae) with abnormal behaviors 1, 4 2 3 Aryanne Clyvia , Angela Bernadette Faggioli and Cynthia Fernandes Cipreste Conservation, Ecology and Animal Behaviour Group, Programa de Pós-Graduação em Zoologia da PUC Minas, Prédio 41, Avenida Dom José Gaspar, 500 - Coração Eucarístico, CEP 30535-610, Belo Horizonte, MG, Brazil. Bird Section, Fundação Zoo-Botânica de Belo Horizonte, Avenida Otacílio Negrão de Lima, 8000, Pampulha, CEP 30000-000, Belo Horizonte, MG, Brazil. Area of Animal Welfare, Fundação Zoo-Botânica de Belo Horizonte, Avenida Otacílio Negrão de Lima, 8000, Pampulha, CEP 30000-000, Belo Horizonte, MG, Brazil. Corresponding author: aryanneclyvia@yahoo.com.br Received on 10 November 2014. Accepted on 22 June 2015. ABSTRACT: Abnormal behaviors (e.g., feather plucking and pacing) are commonly observed in captive animals. Environmental enrichment techniques have been used to improve animal welfare by promoting the reduction of such behaviors and stimulating the display of typical behaviors. Th e present study examined the eff ects of environmental enrichment techniques in a captive pair of the endangered Golden Parakeet (Guaruba guarouba, Psittacidae), which presented feather-plucking behavior. Different ob jects of environmental enrichment were presented to birds between February and July 2008. Behavioral analyses were performed by comparing pre enrichment, enrichment introduction and after enrichment phases. At each phase, a total of 42 hours of behavioral data were collected through the scan method with instantaneous recording at sampling intervals of 30 seconds. The results showed that the behavioral diversity of the parakeets increased (e.g. “social behavior” 14.00 ± 3.01, df = 2, N = 21, p = 0.19; “locomotion” 25.52 ± 3.14, df = 2, N = 21, p = 0.01) whereas feather plucking (“individual abnormal behavior”) decreased with the use of enrichment (0.10 ± 0.07, df = 2, N = 21, p = 0.78). However, abnormal behavior was again observed after removing enrichment objects. Although environmental enrichment did not eliminate completely the display of abnormal behaviors, the introduction of objects had a positive eff ect on increasing behavioral diversity of the animals and, consequently, improving animal welfare. KE E EY Y Y-WORDS: Animal behavior, animal welfare, captivity, feather plucking, psittacine. INTRODUCTION on captive animals showed that captivity can result in behavioral problems (Bashaw et al. 2001, Bachmann et The life of animals in ca ptivity has many differences when al. 2003, Garner et al. 2004, Torrey & Widowski 2006, compared to animals that live in a natural environment. Clubb & Vickery 2006, Harlander-Matauschek et al. Captive animals are protected from competitive 2007, Dixon et al. 2008) such as feather plucking. Th is interactions, receive adequate food, have sexual partners kind of intensified preenin g can result from chronic stress associated with excessive self-comforting or physical chosen, do not need to escape from predators and are not affected by environmental changes (Young 2003). health disorders (Garner et al. 2003) and a sterile and Th us, captivity becomes an unattractive and predictable predictable environment (van Zeeland et al. 2009). environment for animals, as they must deal daily with Environmental enrichment is a process that creates a the lack of challenges that might affect their welfare, complex and interactive environment, allowing the captive animal to display natural behaviors while promoting which may result in abnormal behaviors such as self- injury (Dixon et al. 2008). The animal has needs to new challenges and off ering opportunity for choice and express its normal behavior but due to the inappropriate control of its environment (Swaisgood & Shepherdson environment it tries to reduce its frustration through the 2005). Environmental enrichment techniques are used repetition of behaviors with no apparent function, called to solve and even prevent the appearance of behavioral disorders (Baer 1998, Meehan et al. 2004, Garner et al. stereotyped behaviors (Meehan et al. 2003, Meehan et al. 2004, Latham & Mason 2007). Numerous studies 2006) by reducing the stress caused by captivity and Eff ects of environmental enrichment in a captive pair of Golden Parakeet (Guaruba guarouba, Psittacidae) with abnormal behaviors Aryanne Clyvia, Angela Bernadette Faggioli and Cynthia Fernandes Cipreste improving physical, mental and social welfare of animals METHODS (Young 2003). Th e Golden Parakeet, Guaruba guarouba, is an This study was conducted from February to July 2008, endemic parrot from Brazil, which inhabits upland with a pair of Guaruba guarouba a kept in an enclosure forests and it is found between northern Rondônia and outside the public view, at Fundação Zoo-Botânica de Mato Grosso, Amazonas, Pará, and western Maranhão Belo Horizonte – FZB-BH, Minas Gerais, Brazil. The (Belmonte & Silveira 2005, Laranjeiras & Cohn-Haft two individuals arrived at FZB-BH in September 2007, 2009). Measuring about 34 cm, it has yellow-golden from a conservationist breeding facility in the state of plumage with green fl ight feathers (Sick 1997). Th e Maranhão, Brazil, already showing feather plucking species is considered vulnerable and is a common target behavior. The enclosure measured 3.82 m long, 2.94 m for illegal trade (IUCN 2014). According to the Golden wide and 1.91 m high with cemented walls and floor, Parakeet Management Plan (RIOZOO 1998) proposed front and roof of wire mesh and 1/3 covered with asbestos by IBAMA - Instituto Brasileiro do Meio Ambiente e tile. There were also two perches and some strings for Recursos Renováveis, captive individuals can present locomotion within the enclosure. certain infectious and parasitic diseases, nutritional and The birds’ diet was balanced and included fruits , behavioral problems. One of the most common abnormal vegetables (such as apple, banana, papaya, carrots, behaviors in captive parrots is feather plucking (Garner et peppers and others) and free access to water. Individuals al. 2006, Lumeij & Hommers 2008, Jayson et al. 2014), received food twice a day, at 08h30min and 13h30min, which may be a result of social isolation, poor diet, but no food was available after 15h30min. According diseases, infections or lack of stimuli in the environment to veterinarians of FZB-BH, the pair had good physical (Young 2003, Rubinstein & Lightfoot 2012). health without any disease or infection. Th is study aimed to evaluate the eff ects of An ethogram was created to include behavioral data environmental enrichment techniques in a pair of displayed by parrots (Table 1) after observing animals Guaruba guarouba, which exhibited abnormal behavior through the ad libitum sampling method (Martin & of feather plucking, in order to decrease or eliminate this Bateson 2007), for 10 hours, during a week. behavior and consequently improve their welfare. As the birds had a high degree of feather plucking, we T T TABLE 1. Ethogram of behaviors performed by a pair of Golden Parakeet (Guaruba guarouba) at the Fundação Zoo-Botânica de Belo Horizonte, Brazil. Behavior Descriptions Resting Bird remains in resting position, alone or side by side with its partner. Social behavior Bird cleaning feathers of the other. Bird offerin g his head to the other or feeds the partner with its beak. Vigilance Bird is alert, guiding his head in sideways movements directing towards sounds or stimulus. Exploring Bird walking in over stimulus object. Bird trying to catch something like twigs, objects and other environmental stimuli without eating. Pecking Bird gnawed repeatedly, chewing the ID ring itself or components of the environment as the canvas enclosure, rope, perch, walls or feeder. Manipulating and feeding Bird holding some object, food, branch, etc. Bird watching and/or eating the object. Locomotion Bird moving by any form of locomotion from one place to another (walking or flyin g). Vocalization Bird performing any type of vocalization. Preening Bird cleaning and arranging its feathers using the beak. Bird passing beak alternately and repeatedly against the substrate. Scratching the beak or other body parts with its feet. Individual Abnormal Behavior Bird showing excessive feather preening (tearing off ). Mutual Abnormal Behavior Bird showing excessive partner’s feather preening (tearing off ). Not Visible Bird is not visible to the observer. Others Other behaviors not described in the ethogram. Revista Brasileira de Ornitologia, 23(3), 2015 Eff ects of environmental enrichment in a captive pair of Golden Parakeet (Guaruba guarouba, Psittacidae) with abnormal behaviors Aryanne Clyvia, Angela Bernadette Faggioli and Cynthia Fernandes Cipreste chose to use an environmental enrichment methodology as, most of the time, the parrots remained inactive and developed in FZB-BH. The methodolo gy consists in frequently the social interactions resulted in feather presenting several diff erent stimuli over 4 consecutive plucking. days, in consecutive weeks, resulting in a rapid increase Due to the non-normality of the data generated in behavioral diversity, and the possible solution for by the behavioral samplings (tested with the Anderson- displaying abnormal behaviors of self-mutilation such as Darling test; Zar 1999), we compared the occurrence feather plucking (C. Cipreste pers. comm.). of behaviors through means among the three phases of We collected behavioral data using the scan method the study using the Friedman Test, with a post-hoc c Tukey with instantaneous recording at sampling intervals of 30 Test (Zar 1999). For each phase, the mean of a given seconds. Data collection were carried out from Monday behavior was calculated as the total number of records to Friday, only once a day, in alternating times between obtained with that type of behavior by the total number 07h30min and 16h00min, so they could cover all periods of records obtained for all types of behavior. Standard of the individuals’ activity. The stud y was divided into errors were also estimated among the three phases of the three phases: pre enrichment (before the presentation of study. All analyzes were performed by the Minitab v.12 environmental enrichment), enrichment introduction and BioEstat v.3 programs, at significance level of 95 %. (during the introduction of enrichment items), and after enrichment (after the removal of environmental stimuli from the enclosure). According to methodology R R RESULTS developed in FZB-BH and previously applied to other species (C. Cipreste pers. comm.), the study was conducted All behavioral data collected in 126 hours of study and over 21 consecutive weeks without interval between the statistical significance of all behavioral categories during three phases. the three phase of study are shown in Table 2. Th e most First phase data were collected on Mondays for 120 frequent behaviors displayed during the pre-enrichment phase were (mean ± standard error of the number of minutes. Second phase data were collected from Monday to Th ursday with duration of 30 minutes per day. Th ird records): “resting” (345.40 ± 12.10), “manipulating phase data were collected on Fridays for 120 minutes. and feeding” (43.62 ± 7.20) and “vigilance” (26.76 Th e birds did not receive environmental enrichment from ± 3.74). Th e less frequent behaviors displayed at the Friday to Sunday. Th is study resulted in 42 hours of data same phase were: “exploring” (0.00 ± 0.00), “individual abnormal behavior” (0.29 ± 0.14) and “mutual abnormal collection in each phase, totaling 126 hours of behavioral data. behavior” (1.29 ± 1.05). In the second phase, during the Some environmental enrichment items used were: introduction of environmental enrichment, the most tree branches with leaves; cinnamon pendants; pendants frequent behaviors displayed were: “resting” (252.50 ± of rawhide chew bone with edible aniline; branches 20.60), “exploring” (60.70 ± 11.40) and “manipulating and feeding” (54.14 ± 7.05). The less frequent behaviors with fruit kebabs; coconut bowls with dry grass and fig ; zucchini filled with fruit pieces; ice blocks with fruit juice displayed at this phase were: “individual abnormal and/or gelatin and fruit pieces; pineapple leaves with/ behavior” (0.10 ± 0.07), “others” (0.24 ± 0.14) and without fruit pieces; hollowed wooden wheel fill ed with “mutual abnormal behavior” (0.29 ± 0.21). Finally, after mashed banana and honey; baskets of twisted popsicle the enrichment phase the most frequent behaviors were: “resting” (326.20 ± 12.20), “manipulating and feeding” sticks dyed with edible aniline with mashed fruits, honey or vanilla essence, hanging cardboard boxes with dry grass (38.95 ± 6.91) and “locomotion” (26.24 ± 2.45). The and one of the following: fruit, clove, walnuts, hazelnuts less frequent behaviors were: “exploring” (0.00 ± 0.00), or Brazil nuts. Other fruits used in enrichments depended “individual abnormal behavior” (0.14 ± 0.08) and on the availability of the FZB-BH kitchen and fruiting “mutual abnormal behavior” (0.33 ± 0.25). Only fi ve behaviors diff ered signifi cantly among period. Usually, they were not part of the diet of birds (such as persimmon, strawberry, kiwi, grape and others) the three phases of study. The behavior “restin g” but were used to improve the attraction degree for the had the highest frequency displayed during the pre- enrichment items. enrichment phase, decreasing signifi cantly during the Enrichment was done as follows: from Monday to use of enrichment and increased back again during the third phase (Friedman = 12.67, p < 0.01, Table 2). Th e Thursday several tree branches with leaves, accom panied by some of the other items mentioned above were inserted pair did not exhibit the behavior “exploring” in the pre- in the enclosure. Th e sequence of use of each item was enrichment but this behavior was significantly expressed random, but no item was repeated during the week. All during the enrichment and, after removing the stimuli, items were chosen to stimulate foraging behavior and this behavior was not displayed anymore (Friedman = 31.50, p < 0.01, Table 2). Th e behavior “locomotion” locomotion besides providing positive social interactions Revista Brasileira de Ornitologia, 23(3), 2015 Eff ects of environmental enrichment in a captive pair of Golden Parakeet (Guaruba guarouba, Psittacidae) with abnormal behaviors Aryanne Clyvia, Angela Bernadette Faggioli and Cynthia Fernandes Cipreste was less expressed in the first phase of the study, increased behavior” decreased over the use of enrichment stimuli significantly durin g the use of environmental enrichment and increased slightly after the withdrawal of stimulus and also after its removal (Friedman = 9.02, p < 0.01, Table (Friedman = 0.17, p = 0.92 / Friedman = 0.50, p = 0.78 2). The behavior “vocalization” was displayed durin g the respectively, Table 2). The behaviors “manipulatin g and stimuli phase, decreasing by almost half after removal of feeding” and “vigilance” increased during the phase of the enrichment items, but remained higher when compared stimulus and fell after removal of the items (Friedman = to the first phase (Friedman = 7.12, p < 0.01, Table 2). 2.17, p = 0.34 / Friedman = 5.02, p = 0.08, respectively, The behavior “preening”, decreased on the second phase Table 2). The behavior “pecking” decreased after removal but increased after the removal of stimulus (Friedman = of enrichment items and had a larger drop during the 8.02, p = 0.02, Table 2). stimuli (Friedman = 3.88, p = 0.14, Table 2). Finally, All other behaviors were not significantly different the behavior “social interaction” increased during the among the three study phases. However, we observed that use of environmental enrichment and even more after “mutual abnormal behavior” and “individual abnormal withdrawal (Friedman = 3.31, p = 0.19, Table 2). T T TABLE 2. Mean ± standard error of the number of behavioral records and Friedman Test results for the exhibited behaviors of a pair of Golden Parakeet (Guaruba guarouba) during three phases: pre enrichment, enrichment introducing and after enrichment, at FZB-BH, along 21 weeks between February and July 2008 (df = 2, N = 21,  = 0.05). Enrichment Behavior Pre enrichment After enrichment Friedman p introducing RE 345.40 ± 12.10 252.50 ± 20.60 326.20 ± 12.20 12.67 < 0.01* SB 10.48 ± 1.97 14.00 ± 3.01 18.43 ± 3.11 3.31 0.19 VI 26.76 ± 3.74 35.67 ±3.95 26.52 ± 2.98 5.02 0.08 EX 0.00 ± 0.00 60.70 ± 11.40 0.00 ± 0.00 31.50< 0.01* PE 13.10 ± 2.35 8.05 ± 1.09 11.19 ± 1.82 3.88 0.14 MF 43.62 ± 7.20 54.14 ± 7.05 38.95 ± 6.91 2.17 0.34 LO 17.81 ± 2.05 25.52 ± 3.14 26.24 ± 2.45 9.02 0.01* VO 3.00 ± 0.77 12.14 ± 2.45 6.38 ± 1.35 12.07 <0.01* PR 16.67 ± 2.62 16.52 ± 2.30 25.19 ± 2.77 8.02 0.02* IAB 0.29 ± 0.14 0.10 ± 0.07 0.14 ± 0.08 0.50 0.78 MAB 1.29 ± 1.05 0.29 ± 0.21 0.33 ± 0.25 0.17 0.92 NV 0.10 ± 0.10 0.14 ± 0.14 0.00 ± 0.00 0.07 0.96 OT 1.48 ± 1.38 0.24 ± 0.14 0.38 ± 0.33 0.02 0.99 RE = resting, SB = social behavior, VI = vigilance, EX = exploring, PE = pecking, MF = manipulating and feeding, LO = locomotion, VO = vocalization, PR = preening, IAB = individual abnormal behavior, MAB = mutual abnormal behavior, NV = not visible, OT = others * = Significant differences, p < 0.05. (The means obtained for each behavior was the number of behavior’s records divided by the number of all behavioral records. Th e standard error was the sample standard deviation divided by the square root of the sample size.) DISCUSSION Some studies have demonstrated that the use of environmental enrichment techniques reduces In pre enrichment phase, birds remained inactive most of stereotyped behaviors and increases behavioral repertoire the time but a reduction in such inactivity was noticeable of captive birds (Mason 1995, Meehan et al. 2003, Meehan et al. 2004, Andrade & Azevedo 2011). In the present after insertion of enrichment items, since the birds began to interact with stimuli, a pattern that has been observed study, environmental enrichment increased behavioral in other captive birds (Azevedo & Faggioli 2001, Meehan diversity of birds, although they continued showing & Mench 2002, Andrade & Azevedo 2011). The birds feather plucking behavior. According to Swaisgood increased movement because of their interaction with & Shepherdson (2005), sometimes environmental enrichment techniques cannot fix com pletely but enrichment items and kept moving even after removal. Th is suggests that they might keep seeking for novelties just reduce the display of abnormal behaviors, as such in the enclosure once stimulated. behaviors can be persistent, depending on how long they Revista Brasileira de Ornitologia, 23(3), 2015 Eff ects of environmental enrichment in a captive pair of Golden Parakeet (Guaruba guarouba, Psittacidae) with abnormal behaviors Aryanne Clyvia, Angela Bernadette Faggioli and Cynthia Fernandes Cipreste have been in place or what stimulus was applied (Mason enclosure’s location, once individuals have reached the et al. 2007). FZB-BH already with this behavioral problem. Other An increase of the category “preening” was signifi cant individuals of the same species have been previously after removing the stimulus and birds started plucking maintained in the same enclosure without presenting feathers again even before the study completion. Feather feather plucking. Dixon et al. (2008), studying Gallus plucking may be considered an exaggerated kind of gallus s (Galliformes: Phasianidae), described that a small preening (Meehan et al. 2003). Thus, results suggesting a and sterile enclosure results in the incidence of abnormal small increase in abnormal behaviors, both individual and behaviors. For Gaskins & Hungerford (2014) sometimes mutual, could have been caused by increased “preening” the enclosure size is less important than cage complexity carried out by birds after removing enrichment from the for maintaining the animal welfare. enclosure. We used an overexposure stimuli technique that At the present study we focused on attempting might have over-stimulated the “preening” behavior and to eliminate abnormal behaviors of a captive pair of according to Newberry & Estevez (1997), overstimulation parakeets using environmental enrichment techniques can produce stronger responses than natural stimulation. that increased their behavior diversity. Even though the Despite a few records of positive social interactions abnormal behavior of feather plucking was not eliminated, before the introduction of enrichment, most of the the increased activity of the animals helped on reducing interactions shown by the Golden Parakeets resulted in the display of such behaviors, which characterizes a mutual mutilation. However, the number of positive social possible improvement of the pair’s welfare. We suggest interactions increased with the introduction of stimulus that these individuals continue to participate in a weekly and after its removal. Th e use of social enrichments in environmental enrichment program that creates variations environments with individuals of the same or different on their normal routine and allows them to express more species can result in positive interactions (Bayne 2005). natural and diverse behavior. For Sandos (1999), the use of environmental enrichment techniques for captive birds decreases the attacks among A A ACKNOWLEDGMENTS individuals, since they spend more time interacting with the enrichment. We would like to thank the Fundação Zoo-Botânica de It was noticed an increase of alert behaviors during Belo Horizonte for allowing us to conduct this study. the exposure of the stimuli, whereas this situation was We appreciate all the help given by: João Bosco, Lucia, different from the birds routine. 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Effects of environmental enrichment in a captive pair of Golden Parakeet (Guaruba guarouba, Psittacidae) with abnormal behaviors

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Revista Brasileira de Ornitologia, 23(3), 309-314 ARTICLE September 2015 Eff ects of environmental enrichment in a captive pair of Golden Parakeet (Guaruba guarouba, Psittacidae) with abnormal behaviors 1, 4 2 3 Aryanne Clyvia , Angela Bernadette Faggioli and Cynthia Fernandes Cipreste Conservation, Ecology and Animal Behaviour Group, Programa de Pós-Graduação em Zoologia da PUC Minas, Prédio 41, Avenida Dom José Gaspar, 500 - Coração Eucarístico, CEP 30535-610, Belo Horizonte, MG, Brazil. Bird Section, Fundação Zoo-Botânica de Belo Horizonte, Avenida Otacílio Negrão de Lima, 8000, Pampulha, CEP 30000-000, Belo Horizonte, MG, Brazil. Area of Animal Welfare, Fundação Zoo-Botânica de Belo Horizonte, Avenida Otacílio Negrão de Lima, 8000, Pampulha, CEP 30000-000, Belo Horizonte, MG, Brazil. Corresponding author: aryanneclyvia@yahoo.com.br Received on 10 November 2014. Accepted on 22 June 2015. ABSTRACT: Abnormal behaviors (e.g., feather plucking and pacing) are commonly observed in captive animals. Environmental enrichment techniques have been used to improve animal welfare by promoting the reduction of such behaviors and stimulating the display of typical behaviors. Th e present study examined the eff ects of environmental enrichment techniques in a captive pair of the endangered Golden Parakeet (Guaruba guarouba, Psittacidae), which presented feather-plucking behavior. Different ob jects of environmental enrichment were presented to birds between February and July 2008. Behavioral analyses were performed by comparing pre enrichment, enrichment introduction and after enrichment phases. At each phase, a total of 42 hours of behavioral data were collected through the scan method with instantaneous recording at sampling intervals of 30 seconds. The results showed that the behavioral diversity of the parakeets increased (e.g. “social behavior” 14.00 ± 3.01, df = 2, N = 21, p = 0.19; “locomotion” 25.52 ± 3.14, df = 2, N = 21, p = 0.01) whereas feather plucking (“individual abnormal behavior”) decreased with the use of enrichment (0.10 ± 0.07, df = 2, N = 21, p = 0.78). However, abnormal behavior was again observed after removing enrichment objects. Although environmental enrichment did not eliminate completely the display of abnormal behaviors, the introduction of objects had a positive eff ect on increasing behavioral diversity of the animals and, consequently, improving animal welfare. KE E EY Y Y-WORDS: Animal behavior, animal welfare, captivity, feather plucking, psittacine. INTRODUCTION on captive animals showed that captivity can result in behavioral problems (Bashaw et al. 2001, Bachmann et The life of animals in ca ptivity has many differences when al. 2003, Garner et al. 2004, Torrey & Widowski 2006, compared to animals that live in a natural environment. Clubb & Vickery 2006, Harlander-Matauschek et al. Captive animals are protected from competitive 2007, Dixon et al. 2008) such as feather plucking. Th is interactions, receive adequate food, have sexual partners kind of intensified preenin g can result from chronic stress associated with excessive self-comforting or physical chosen, do not need to escape from predators and are not affected by environmental changes (Young 2003). health disorders (Garner et al. 2003) and a sterile and Th us, captivity becomes an unattractive and predictable predictable environment (van Zeeland et al. 2009). environment for animals, as they must deal daily with Environmental enrichment is a process that creates a the lack of challenges that might affect their welfare, complex and interactive environment, allowing the captive animal to display natural behaviors while promoting which may result in abnormal behaviors such as self- injury (Dixon et al. 2008). The animal has needs to new challenges and off ering opportunity for choice and express its normal behavior but due to the inappropriate control of its environment (Swaisgood & Shepherdson environment it tries to reduce its frustration through the 2005). Environmental enrichment techniques are used repetition of behaviors with no apparent function, called to solve and even prevent the appearance of behavioral disorders (Baer 1998, Meehan et al. 2004, Garner et al. stereotyped behaviors (Meehan et al. 2003, Meehan et al. 2004, Latham & Mason 2007). Numerous studies 2006) by reducing the stress caused by captivity and Eff ects of environmental enrichment in a captive pair of Golden Parakeet (Guaruba guarouba, Psittacidae) with abnormal behaviors Aryanne Clyvia, Angela Bernadette Faggioli and Cynthia Fernandes Cipreste improving physical, mental and social welfare of animals METHODS (Young 2003). Th e Golden Parakeet, Guaruba guarouba, is an This study was conducted from February to July 2008, endemic parrot from Brazil, which inhabits upland with a pair of Guaruba guarouba a kept in an enclosure forests and it is found between northern Rondônia and outside the public view, at Fundação Zoo-Botânica de Mato Grosso, Amazonas, Pará, and western Maranhão Belo Horizonte – FZB-BH, Minas Gerais, Brazil. The (Belmonte & Silveira 2005, Laranjeiras & Cohn-Haft two individuals arrived at FZB-BH in September 2007, 2009). Measuring about 34 cm, it has yellow-golden from a conservationist breeding facility in the state of plumage with green fl ight feathers (Sick 1997). Th e Maranhão, Brazil, already showing feather plucking species is considered vulnerable and is a common target behavior. The enclosure measured 3.82 m long, 2.94 m for illegal trade (IUCN 2014). According to the Golden wide and 1.91 m high with cemented walls and floor, Parakeet Management Plan (RIOZOO 1998) proposed front and roof of wire mesh and 1/3 covered with asbestos by IBAMA - Instituto Brasileiro do Meio Ambiente e tile. There were also two perches and some strings for Recursos Renováveis, captive individuals can present locomotion within the enclosure. certain infectious and parasitic diseases, nutritional and The birds’ diet was balanced and included fruits , behavioral problems. One of the most common abnormal vegetables (such as apple, banana, papaya, carrots, behaviors in captive parrots is feather plucking (Garner et peppers and others) and free access to water. Individuals al. 2006, Lumeij & Hommers 2008, Jayson et al. 2014), received food twice a day, at 08h30min and 13h30min, which may be a result of social isolation, poor diet, but no food was available after 15h30min. According diseases, infections or lack of stimuli in the environment to veterinarians of FZB-BH, the pair had good physical (Young 2003, Rubinstein & Lightfoot 2012). health without any disease or infection. Th is study aimed to evaluate the eff ects of An ethogram was created to include behavioral data environmental enrichment techniques in a pair of displayed by parrots (Table 1) after observing animals Guaruba guarouba, which exhibited abnormal behavior through the ad libitum sampling method (Martin & of feather plucking, in order to decrease or eliminate this Bateson 2007), for 10 hours, during a week. behavior and consequently improve their welfare. As the birds had a high degree of feather plucking, we T T TABLE 1. Ethogram of behaviors performed by a pair of Golden Parakeet (Guaruba guarouba) at the Fundação Zoo-Botânica de Belo Horizonte, Brazil. Behavior Descriptions Resting Bird remains in resting position, alone or side by side with its partner. Social behavior Bird cleaning feathers of the other. Bird offerin g his head to the other or feeds the partner with its beak. Vigilance Bird is alert, guiding his head in sideways movements directing towards sounds or stimulus. Exploring Bird walking in over stimulus object. Bird trying to catch something like twigs, objects and other environmental stimuli without eating. Pecking Bird gnawed repeatedly, chewing the ID ring itself or components of the environment as the canvas enclosure, rope, perch, walls or feeder. Manipulating and feeding Bird holding some object, food, branch, etc. Bird watching and/or eating the object. Locomotion Bird moving by any form of locomotion from one place to another (walking or flyin g). Vocalization Bird performing any type of vocalization. Preening Bird cleaning and arranging its feathers using the beak. Bird passing beak alternately and repeatedly against the substrate. Scratching the beak or other body parts with its feet. Individual Abnormal Behavior Bird showing excessive feather preening (tearing off ). Mutual Abnormal Behavior Bird showing excessive partner’s feather preening (tearing off ). Not Visible Bird is not visible to the observer. Others Other behaviors not described in the ethogram. Revista Brasileira de Ornitologia, 23(3), 2015 Eff ects of environmental enrichment in a captive pair of Golden Parakeet (Guaruba guarouba, Psittacidae) with abnormal behaviors Aryanne Clyvia, Angela Bernadette Faggioli and Cynthia Fernandes Cipreste chose to use an environmental enrichment methodology as, most of the time, the parrots remained inactive and developed in FZB-BH. The methodolo gy consists in frequently the social interactions resulted in feather presenting several diff erent stimuli over 4 consecutive plucking. days, in consecutive weeks, resulting in a rapid increase Due to the non-normality of the data generated in behavioral diversity, and the possible solution for by the behavioral samplings (tested with the Anderson- displaying abnormal behaviors of self-mutilation such as Darling test; Zar 1999), we compared the occurrence feather plucking (C. Cipreste pers. comm.). of behaviors through means among the three phases of We collected behavioral data using the scan method the study using the Friedman Test, with a post-hoc c Tukey with instantaneous recording at sampling intervals of 30 Test (Zar 1999). For each phase, the mean of a given seconds. Data collection were carried out from Monday behavior was calculated as the total number of records to Friday, only once a day, in alternating times between obtained with that type of behavior by the total number 07h30min and 16h00min, so they could cover all periods of records obtained for all types of behavior. Standard of the individuals’ activity. The stud y was divided into errors were also estimated among the three phases of the three phases: pre enrichment (before the presentation of study. All analyzes were performed by the Minitab v.12 environmental enrichment), enrichment introduction and BioEstat v.3 programs, at significance level of 95 %. (during the introduction of enrichment items), and after enrichment (after the removal of environmental stimuli from the enclosure). According to methodology R R RESULTS developed in FZB-BH and previously applied to other species (C. Cipreste pers. comm.), the study was conducted All behavioral data collected in 126 hours of study and over 21 consecutive weeks without interval between the statistical significance of all behavioral categories during three phases. the three phase of study are shown in Table 2. Th e most First phase data were collected on Mondays for 120 frequent behaviors displayed during the pre-enrichment phase were (mean ± standard error of the number of minutes. Second phase data were collected from Monday to Th ursday with duration of 30 minutes per day. Th ird records): “resting” (345.40 ± 12.10), “manipulating phase data were collected on Fridays for 120 minutes. and feeding” (43.62 ± 7.20) and “vigilance” (26.76 Th e birds did not receive environmental enrichment from ± 3.74). Th e less frequent behaviors displayed at the Friday to Sunday. Th is study resulted in 42 hours of data same phase were: “exploring” (0.00 ± 0.00), “individual abnormal behavior” (0.29 ± 0.14) and “mutual abnormal collection in each phase, totaling 126 hours of behavioral data. behavior” (1.29 ± 1.05). In the second phase, during the Some environmental enrichment items used were: introduction of environmental enrichment, the most tree branches with leaves; cinnamon pendants; pendants frequent behaviors displayed were: “resting” (252.50 ± of rawhide chew bone with edible aniline; branches 20.60), “exploring” (60.70 ± 11.40) and “manipulating and feeding” (54.14 ± 7.05). The less frequent behaviors with fruit kebabs; coconut bowls with dry grass and fig ; zucchini filled with fruit pieces; ice blocks with fruit juice displayed at this phase were: “individual abnormal and/or gelatin and fruit pieces; pineapple leaves with/ behavior” (0.10 ± 0.07), “others” (0.24 ± 0.14) and without fruit pieces; hollowed wooden wheel fill ed with “mutual abnormal behavior” (0.29 ± 0.21). Finally, after mashed banana and honey; baskets of twisted popsicle the enrichment phase the most frequent behaviors were: “resting” (326.20 ± 12.20), “manipulating and feeding” sticks dyed with edible aniline with mashed fruits, honey or vanilla essence, hanging cardboard boxes with dry grass (38.95 ± 6.91) and “locomotion” (26.24 ± 2.45). The and one of the following: fruit, clove, walnuts, hazelnuts less frequent behaviors were: “exploring” (0.00 ± 0.00), or Brazil nuts. Other fruits used in enrichments depended “individual abnormal behavior” (0.14 ± 0.08) and on the availability of the FZB-BH kitchen and fruiting “mutual abnormal behavior” (0.33 ± 0.25). Only fi ve behaviors diff ered signifi cantly among period. Usually, they were not part of the diet of birds (such as persimmon, strawberry, kiwi, grape and others) the three phases of study. The behavior “restin g” but were used to improve the attraction degree for the had the highest frequency displayed during the pre- enrichment items. enrichment phase, decreasing signifi cantly during the Enrichment was done as follows: from Monday to use of enrichment and increased back again during the third phase (Friedman = 12.67, p < 0.01, Table 2). Th e Thursday several tree branches with leaves, accom panied by some of the other items mentioned above were inserted pair did not exhibit the behavior “exploring” in the pre- in the enclosure. Th e sequence of use of each item was enrichment but this behavior was significantly expressed random, but no item was repeated during the week. All during the enrichment and, after removing the stimuli, items were chosen to stimulate foraging behavior and this behavior was not displayed anymore (Friedman = 31.50, p < 0.01, Table 2). Th e behavior “locomotion” locomotion besides providing positive social interactions Revista Brasileira de Ornitologia, 23(3), 2015 Eff ects of environmental enrichment in a captive pair of Golden Parakeet (Guaruba guarouba, Psittacidae) with abnormal behaviors Aryanne Clyvia, Angela Bernadette Faggioli and Cynthia Fernandes Cipreste was less expressed in the first phase of the study, increased behavior” decreased over the use of enrichment stimuli significantly durin g the use of environmental enrichment and increased slightly after the withdrawal of stimulus and also after its removal (Friedman = 9.02, p < 0.01, Table (Friedman = 0.17, p = 0.92 / Friedman = 0.50, p = 0.78 2). The behavior “vocalization” was displayed durin g the respectively, Table 2). The behaviors “manipulatin g and stimuli phase, decreasing by almost half after removal of feeding” and “vigilance” increased during the phase of the enrichment items, but remained higher when compared stimulus and fell after removal of the items (Friedman = to the first phase (Friedman = 7.12, p < 0.01, Table 2). 2.17, p = 0.34 / Friedman = 5.02, p = 0.08, respectively, The behavior “preening”, decreased on the second phase Table 2). The behavior “pecking” decreased after removal but increased after the removal of stimulus (Friedman = of enrichment items and had a larger drop during the 8.02, p = 0.02, Table 2). stimuli (Friedman = 3.88, p = 0.14, Table 2). Finally, All other behaviors were not significantly different the behavior “social interaction” increased during the among the three study phases. However, we observed that use of environmental enrichment and even more after “mutual abnormal behavior” and “individual abnormal withdrawal (Friedman = 3.31, p = 0.19, Table 2). T T TABLE 2. Mean ± standard error of the number of behavioral records and Friedman Test results for the exhibited behaviors of a pair of Golden Parakeet (Guaruba guarouba) during three phases: pre enrichment, enrichment introducing and after enrichment, at FZB-BH, along 21 weeks between February and July 2008 (df = 2, N = 21,  = 0.05). Enrichment Behavior Pre enrichment After enrichment Friedman p introducing RE 345.40 ± 12.10 252.50 ± 20.60 326.20 ± 12.20 12.67 < 0.01* SB 10.48 ± 1.97 14.00 ± 3.01 18.43 ± 3.11 3.31 0.19 VI 26.76 ± 3.74 35.67 ±3.95 26.52 ± 2.98 5.02 0.08 EX 0.00 ± 0.00 60.70 ± 11.40 0.00 ± 0.00 31.50< 0.01* PE 13.10 ± 2.35 8.05 ± 1.09 11.19 ± 1.82 3.88 0.14 MF 43.62 ± 7.20 54.14 ± 7.05 38.95 ± 6.91 2.17 0.34 LO 17.81 ± 2.05 25.52 ± 3.14 26.24 ± 2.45 9.02 0.01* VO 3.00 ± 0.77 12.14 ± 2.45 6.38 ± 1.35 12.07 <0.01* PR 16.67 ± 2.62 16.52 ± 2.30 25.19 ± 2.77 8.02 0.02* IAB 0.29 ± 0.14 0.10 ± 0.07 0.14 ± 0.08 0.50 0.78 MAB 1.29 ± 1.05 0.29 ± 0.21 0.33 ± 0.25 0.17 0.92 NV 0.10 ± 0.10 0.14 ± 0.14 0.00 ± 0.00 0.07 0.96 OT 1.48 ± 1.38 0.24 ± 0.14 0.38 ± 0.33 0.02 0.99 RE = resting, SB = social behavior, VI = vigilance, EX = exploring, PE = pecking, MF = manipulating and feeding, LO = locomotion, VO = vocalization, PR = preening, IAB = individual abnormal behavior, MAB = mutual abnormal behavior, NV = not visible, OT = others * = Significant differences, p < 0.05. (The means obtained for each behavior was the number of behavior’s records divided by the number of all behavioral records. Th e standard error was the sample standard deviation divided by the square root of the sample size.) DISCUSSION Some studies have demonstrated that the use of environmental enrichment techniques reduces In pre enrichment phase, birds remained inactive most of stereotyped behaviors and increases behavioral repertoire the time but a reduction in such inactivity was noticeable of captive birds (Mason 1995, Meehan et al. 2003, Meehan et al. 2004, Andrade & Azevedo 2011). In the present after insertion of enrichment items, since the birds began to interact with stimuli, a pattern that has been observed study, environmental enrichment increased behavioral in other captive birds (Azevedo & Faggioli 2001, Meehan diversity of birds, although they continued showing & Mench 2002, Andrade & Azevedo 2011). The birds feather plucking behavior. According to Swaisgood increased movement because of their interaction with & Shepherdson (2005), sometimes environmental enrichment techniques cannot fix com pletely but enrichment items and kept moving even after removal. Th is suggests that they might keep seeking for novelties just reduce the display of abnormal behaviors, as such in the enclosure once stimulated. behaviors can be persistent, depending on how long they Revista Brasileira de Ornitologia, 23(3), 2015 Eff ects of environmental enrichment in a captive pair of Golden Parakeet (Guaruba guarouba, Psittacidae) with abnormal behaviors Aryanne Clyvia, Angela Bernadette Faggioli and Cynthia Fernandes Cipreste have been in place or what stimulus was applied (Mason enclosure’s location, once individuals have reached the et al. 2007). FZB-BH already with this behavioral problem. Other An increase of the category “preening” was signifi cant individuals of the same species have been previously after removing the stimulus and birds started plucking maintained in the same enclosure without presenting feathers again even before the study completion. Feather feather plucking. Dixon et al. (2008), studying Gallus plucking may be considered an exaggerated kind of gallus s (Galliformes: Phasianidae), described that a small preening (Meehan et al. 2003). Thus, results suggesting a and sterile enclosure results in the incidence of abnormal small increase in abnormal behaviors, both individual and behaviors. For Gaskins & Hungerford (2014) sometimes mutual, could have been caused by increased “preening” the enclosure size is less important than cage complexity carried out by birds after removing enrichment from the for maintaining the animal welfare. enclosure. We used an overexposure stimuli technique that At the present study we focused on attempting might have over-stimulated the “preening” behavior and to eliminate abnormal behaviors of a captive pair of according to Newberry & Estevez (1997), overstimulation parakeets using environmental enrichment techniques can produce stronger responses than natural stimulation. that increased their behavior diversity. Even though the Despite a few records of positive social interactions abnormal behavior of feather plucking was not eliminated, before the introduction of enrichment, most of the the increased activity of the animals helped on reducing interactions shown by the Golden Parakeets resulted in the display of such behaviors, which characterizes a mutual mutilation. However, the number of positive social possible improvement of the pair’s welfare. We suggest interactions increased with the introduction of stimulus that these individuals continue to participate in a weekly and after its removal. Th e use of social enrichments in environmental enrichment program that creates variations environments with individuals of the same or different on their normal routine and allows them to express more species can result in positive interactions (Bayne 2005). natural and diverse behavior. For Sandos (1999), the use of environmental enrichment techniques for captive birds decreases the attacks among A A ACKNOWLEDGMENTS individuals, since they spend more time interacting with the enrichment. We would like to thank the Fundação Zoo-Botânica de It was noticed an increase of alert behaviors during Belo Horizonte for allowing us to conduct this study. the exposure of the stimuli, whereas this situation was We appreciate all the help given by: João Bosco, Lucia, different from the birds routine. 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Journal

Ornithology ResearchSpringer Journals

Published: Sep 1, 2015

Keywords: Animal behavior; animal welfare; captivity; feather plucking; psittacine

References