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Revista Brasileira de Ornitologia 25(1): 1–11. ARTICLE March 2017 Important tools for Amazon Parrot reintroduction programs 1,3 2 1,2 Cristiano Schetini de Azevedo , Lívia Soares Furtado Rodrigues & Julio Cesar Rodrigues Fontenelle Programa de Pós-graduação de Ecologia em Biomas Tropicais, Universidade Federal de Ouro Preto, Campus Morro do Cruzeiro s/n, Instituto de Ciências Exatas e Biológicas, Bauxita, 35400-000, Ouro Preto, MG, Brazil. Laboratório de Pesquisas Ambientais, Instituto Federal de Minas Gerais, Rua Pandiá Calógeras, 898, Bauxita, 35400-000, Ouro Preto, MG, Brazil. Corresponding author: firstname.lastname@example.org Received on 03 June 2016. Accepted on 23 April 2017. ABSTRACT: Anti-predator behavior and personality have important consequences for the survival of captive-bred animals after reintroduction in the wild. The personality of an animal can be defined as low within-individual variation in behavior relative to between-individual variation in behavior. Mortality caused by predation is the main reason for reintroduction failure, and training captive-born animals to avoid predators can solve this problem. However, how anti-predator training affects the personality of animals is uncertain. The objective of this study was to test the behavioral responses of captive Amazon Parrots (Amazona aestiva, Psittacidae) submitted to an anti-predator conditioning protocol, and to evaluate if anti-predator training affects parrot personalities. Twenty-six parrots were trained against predators using taxidermized models; their personalities were evaluated by calculating boldness scores before and after anti-predator training sessions. Parrots increased the expression of anti-predator behaviors when tested with all models; control groups behaved in a more relaxed way. The anti-predator responses persisted for 60 days after the end of the training sessions. Boldness scores increased in 50% of cases after anti-predator training sessions, and in only 33% of cases did parrots become shyer after anti-predator training. The tendency of parrots to exhibit bold behaviors in the personality tests, even after the training sessions, may be explained by their early experiences, low behavioral plasticity or high cognitive ability. Training naive parrots was an effective tool to enhance behavioral responses against predators before reintroduction. The study of personality is of great importance in reintroduction and translocation programs to determine the position of each individual in the shy-bold continuum and to help select individuals more suited for reintroduction. KEY-WORDS: anti-predator training, captivity, conservation, personality, Psittacidae. INTRODUCTION 1991, Short et al. 1992, Miller et al. 1994). Death of captive-born animals soon after reintroduction can be Predation is one of the most important factors that affect minimized by releasing the animals in predator-free areas, by building fences to avoid the entrance of predators, species distribution and abundance (McLean et al. 1999, by eliminating the local predators by translocations or Begon et al. 2006). Anti-predatory behavior has important consequences for the survival and population dynamics hunting, or by training naïve animals to recognize and of prey, and in the stability of predator-prey interactions to avoid predators (Griffin et al. 2000). The use of anti- (Stankowich & Blumstein 2005). Anti-predator behavior predator conditioning has increased in the last decade (Miller et al. 1994, Maloney & McLean 1995, McLean has been studied mostly in fish, birds and mammals 1996, Richards 1998, McLean et al. 1999, Azevedo & (Griffin et al. 2000), and the most commonly performed strategies by animals include hiding, escaping, freezing Young 2006, Specht 2007, Miles et al. 2013). or fighting (Sanz & Grajal 1998, E ilam 2005, Rosier Many species, from humans to arthropods, differ & Langkilde 2011, Yorzinski & Platt 2012, Miles et individually in how they respond to environmental stimuli such as novelty, risk, and sociability (Lendvai et al. 2013). Captive-born animals or animals reared in al. 2011). These differences are determined by behavioral predator-free territories may lose their anti-predator skills (Curio 1988), and because it is energetically costly and physiological traits, and can be described by their to maintain these behaviors, they tend to disappear over personalities (Groothuis & Carere 2005). The personality time (Ryer & Olla 1998). of an animal can be defined as the low within-individual variation in behavior relative to between-individual Mortality caused by predation has been critical in variation in behavior (Carter & Feeney 2012), i.e. some reintroduction/translocation attempts (Beck et al. Important tools for Amazon Parrot reintroduction programs Azevedo et al. individual behaviors can consistently differ across of establishment of viable parrot populations after situations or contexts, and these differences tend to be reintroductions. stable over time (Sih et al. 2004, Bell & Stamps 2004, Despite the importance of reintroduction as a Dingemanse & Réale 2005, McDougall et al. 2006, tool for species conservation (Foose 1986, Cade 1988), Stamps & Groothuis 2010, Wolf & Weissing 2012). without behavioral interventions in captivity, such as Personality traits, such as the shy-bold continuum anti-predator conditioning, individuals can show high (Wilson et al. 1994, Kurvers et al. 2010), can be used mortality rates after release in the wild, especially due to describe and measure behavioral variation in humans to predation (Macias et al. 2003, White-Jr. et al. 2005, and other species (Wilson et al. 1994, Watters & Powell Valle et al. 2010, Veloso-Júnior et al. 2010, Alonso et 2012). A bold animal is one inclined to take risks, al. 2011). Psittacines, as an example, were predated by especially in novel situations, and a shy animal is one snakes, hawks and ocelots in reintroduction programs not inclined to take risks (Toms et al. 2010). Personality with no pre-release anti-predator conditioning (Macias traits can be partly heritable (10–50%, van Oers et al. et al. 2003, Valle et al. 2010, Veloso-Júnior et al. 2010). 2004, 2005, Taylor et al. 2012), and the topic of how Anti-predator conditioning for an Amazon parrot species personality is maintained in animal populations across is only known for Amazona vittata (Boddaert, 1783), time (evolutionary patterns) and had been subject of reintroduced in Puerto Rico by the Puerto Rican Parrot recent under study (Wolf & Weissing 2012). Recovery Program, which reports a strong positive The assessment of animal persona lity traits has some response of the parrots to the predator-aversion training practical applications, especially for captive animals, since (White-Jr. et al. 2005). it can help keepers in the selection of the most suitable Few studies have evaluated if anti-predator training animals for exhibition, reproduction and handling, for can change personality traits. Among these, the results are instance (Carlstead 1999). Behavioral assessment can also ambiguous, with some studies showing that personality be a tool for the selection of the best animals to reintroduce was altered after anti-predator training sessions (Azevedo into the wild in conservation programs (Azevedo & Young & Young 2006, Specht 2007), with bolder animals 2006), since the reintroduction of captive-bred animals becoming less bold, and other showing that personality is an alternative approach to species conservation (Foose was not altered after anti-predator training sessions 1986, Cade 1988). For instance, bold individuals should (Smith & Blumstein 2012). not be reintroduced since they may suffer a high-risk of The aim of this study was to test behavioral death due to their propensity to take risks (Bremner- responses to an anti-predator conditioning program for Harrison et al. 2004). Alternatively, shy individuals should captive Amazon Parrots, using A. aestiva as a model. We not be reintroduced since they may show reduction in hypothesized that the predator-aversion behaviors would foraging and growth rates (Biro & Stamps 2008). The be enhanced after consecutive training sessions, helping ideal scenario would be the reproduction of individuals the naive parrots (those living for longer periods in occupying intermediate positions in the shy-bold captivity that had no previous experiences with predators) continuum, i.e. neither too bold or too shy; this would to recognize and avoid predators. This study also intended enable the correct response when individuals are exposed to evaluate the personality of captive-bred A. aestiva to a threat, such as a predator, or when searching for food individuals and tested the hypothesis that individuals or partners (Azevedo & Young 2006). become shyer after being trained against predators, due The Turquoise-fronted Parrot [Am azona aestiva to increased fearfulness caused by predator visualization. (Linnaeus, 1758); hereafter Amazon parrot] is one of the most common Brazilian parrots (Béjcek & Stastný 2002), occurring in all biomes, except the Pampas (Schunk et al. METHODS 2011). Although A. aestiva are not considered threatened by extinction (IUCN 2015 – “Least Concern”; MMA Animals 2014 – not threatened), chicks are frequentely captured in the wild and traded illegally (Beissinger & Bucher 1992, We randomly selected thirty adult Amazona aestiva Seixas & Mourão 2002, Schunk et al. 2011), mainly due individuals spontaneously returned to the Brazilian to their capacity to imitate the human voice (Ribeiro Environmental Agency (Instituto Brasileiro do Meio & Silva 2007). Many specimens are rescued annually Ambiente e Recursos Naturais Renováveis - IBAMA) at a 1:1 by governmental agencies and are sent to rehabilitation sex ratio (parrots were sexed through DNA analysis). All centres for future reintroduction (Beissinger & Bucher parrots had lived for at least 5 years in captivity. The study 1992, Seixas & Mourão 2002). Consequently, testing was conducted in the IBAMA facilities, at Belo Horizonte, an anti-predator conditioning protocol for this species Minas Gerais state, southeastern Brazil. Parrots were held is important because this could increase the chances in two enclosures measuring 7.10 m length × 1.8 m width Revista Brasileira de Ornitologia 25(1): 2017 Important tools for Amazon Parrot reintroduction programs Azevedo et al. × 2.45 m height (15 parrots in each enclosure), placed 2 not displayed in predatory situations) categories, based m apart, away from human interferences and surrounded on the preliminary observations and in the studies of by natural habitat. Two parrots died during the study due Andrade & Azevedo (2011). to injuries caused by fights inside the aviaries, thus data from only 28 individuals were included in the study. All Anti-predator training protocol experiments were approved by IBAMA's Animal Ethics Committee. Anti-predator training was done using two taxidermized The birds were fed twice daily, in the morning models of potential predators – an Ocelot [Leopardus (around 08:00 h) with Psittacidae feed (Evicanto pardalis (Linnaeus, 1758)] and a Harris's Hawk [Parabuteo Papagaios ) and in the afternoon (around 14:00 h) with unicinctus (Temminck, 1824)] – and an adult human; a fruits and seeds. Water was provided ad libitum. Birds chair was used as a control model. The presentation of were marked with colored rings on their legs to facilitate models was followed by an aversive stimulus (chasing by individual recognition. an unfamiliar human). All training sessions were done in groups of three parrots each (except two groups with two Anti-predator training ethogram parrots; the parrots remained in the same group during the entire experiment): two groups were trained against An ethogram for the Turquoise-fronted parrots (Table the three predator types (mixed group); two groups were 1) was compiled based on 20 h of ad libitum sampling trained against the ocelot model (ocelot group); two groups during 20 days of preliminary observations (Altmann were trained against the hawk model (hawk group); two 1974) and previous studies (Prestes 2000, Andrade & groups were trained against the human (human group), Azevedo 2011). Behaviors were classified into aversion totaling six groups (two groups per predator type); and (anti-predator behaviors) and relaxing behavior (those two groups received no training (control) (Table 2). Table 1. Behavioural ethogram of Amazona aestiva individuals kept at IBAMA/BH with behavior description used during anti-predator training sessions and classification used to calculate boldness scores. BehaviorAcronym Description Category Classification Self or Allopreening PREE Parrot preens own feathers or feathers of other individuals. Relax Boldness Nodding head ND Parrot nods its head. Anti-predator - Aggression AGR Parrot pecks conspecifics aggressively. Relax Boldness Yawning YA Parrot yawns. Relax - Walking on perch WP Parrot walks on the perch.Relax Boldness Walking on the floor WF Parrot walks on the floor. Relax Shyness Walking on wire WW Parrot walks on the enclosure's wiremesh.Relax Shyness Inactive IN Parrot remains inactive or sleeping. Relax Boldness Inactive on wire IW Parrot remains inactive on the wiremesh.Relax Shyness Alert AL Parrot adopts an alert posture (head up, looking fixedly Anti-predator Shyness towards something). Hiding behind the shrub HID Parrot hides behind the shrub, avoiding the predator models. Anti-predator Shyness Sleeping SLEE Parrot sleeps. Relax - Pacing PAC Parrots walks from one side to another on the perch, on Abnormal Shyness the wiremesh or on the floor, using the same route for no apparent reason. Flying FLY Parrot flies away from the predator models. Anti-predator Shyness Vocalizing VOC Parrot emits social vocalizations. Relax Shyness Pecking on feather/leaf PF Parrot pecks on free feathers or tree leaves on the ground.Relax Boldness Head scratching HS Parrot scratches its head with its feet. Relax Boldness Wing/leg stretching WS Parrot stretches its wings or legs. Relax Boldness Pecking on plastic Parrot pecks plastic markings of the perches or the perches -Boldness markings or on perch inside the enclosure. Pecking on the platform Parrot pecks the wooden platform of the novel objects. - Boldness Playing with object Parrot plays with the novel object. - Boldness Cleaning the beak Parrot scratches its beak on the perch to clean it. - Boldness Not visible NV Parrot is not visible. - - Some behaviors were observed only during anti-predator training sessions and others only during personality tests. Revista Brasileira de Ornitologia 25(1): 2017 Important tools for Amazon Parrot reintroduction programs Azevedo et al. Table 2. Identification number and sex of parrots submitted to anti-predator training sessions and to the personality tests before and after the application of the anti-predator training sessions, and the predator stimuli used. Anti-predator training sections Hawk Ocelot Human Mixed (Hawk/Ocelot/Human)Control 7 13 19 1 24 8 14 20 2 25 9 15 21 3 26 10 16 22 4 27 11 17 23 5 28 12 18 29†6 30† † Parrots that died during anti-predator training sessions. Training sessions were run in an enclosure similar birds were never caught). After the capture simulation, to the maintenance aviary (50 m from the maintenance the predator appeared again to the parrots for more 15 s aviaries), but with its laterals covered by an opaque black (Fig. 1). plastic to prevent birds from seeing outside surroundings. The roof of the aviary was not covered by a black plastic. A circular opening of 0.3 m in diameter in the black plastic in the front of the enclosure allowed the researcher to video record all training sessions using a webcam COMPAQ. The enclosure's door was also covered with the black plastic and during the experiment was opened to show the models to the parrots inside. A bush at the end of the enclosure provided the parrots with shelter. Figure 1. Protocol used in the anti-predator training of the Amazon Each parrot group received three training sessions, parrots. except the mixed group, who received nine training sessions (three with each predator model); control The ocelot, human and chair stimuli appeared to groups, although not trained with predator models, also the parrots through the frontal enclosure's door; the received three sessions with a chair. Training sessions were hawk appeared to the parrots through the enclosure's run in four consecutive days of February 2012, always roof. The costume used by the man had the objective to between 08:00–09:00 h and 16:00–17:00 h, since these camouflage his silhouette, i.e. for the parrots, the chaser birds are diurnal and inactive in the hottest periods of was not a human. Control groups received the same day (Collar 1997, Pitter & Christiansen 1997, Gilardi & training protocol used for the other groups, but the Munn 1998). human persecution never occurred. Data were collected Parrots were captured in the maintenance enclosure using focal sampling with instantaneous recordings in 15 and then transferred to the test enclosure each day, and s intervals (Altmann 1974). a 15-min period was adopted for birds' acclimation and relaxing. All captures were done quietly, with Memory tests minimal interference to avoid stressing the parrots and no influences of this procedure were detected during Memory tests were performed 30 and 60 days after the data analysis. When in the test enclosure, parrots in the anti-predator training session. These tests consisted in maintenance enclosures could not see or hear the test showing the predator models to all groups of parrots groups. Each trial lasted 18 min, which consisted of 2 (trained and controls) similar to that of the anti-predator min filming before the presentation of the predator training sessions, except that the chasing simulation did (phase 1), 1-min of conditioning (phase 2), and 15 min not occur. of filming after the end of conditioning (phase 3), thus, more than one group received anti-predator training in Personality tests the same day, but not simultaneously. The 1-min of conditioning was adapted from Griffin Behaviors recorded in the ethogram representing et al. (2001): the stimulus (predator) was shown to the boldness and shyness were identified (Ta ble 1). Risk- animals for 15 s before a human dressing a costume (see taking behaviors, normally expressed during encounters below) and carrying a net entered the enclosure and began with predators or in stressful situations, were considered a 30 s simulated capture procedure (aversive experience; shy behaviors (van Oers & Naguib 2013), and Revista Brasileira de Ornitologia 25(1): 2017 Important tools for Amazon Parrot reintroduction programs Azevedo et al. aggression, exploratory and maintenance behaviors, Data analysis of personality tests exhibited during calm, non-stressful events, were selected as bold (Smith & Blumstein 2013). A boldness score Using an Anderson-Darling test we determined that was calculated for each individual following Bremner- our data did not meet the requirements for parametric Harrison et al. (2004). Boldness scores were calculated statistics, so the data were square-root transformed and per individual before and after anti-predator training parametrical statistical tests were used throughout. sessions, during the novel object trials (personality tests; A paired t-test was used to test whether boldness see below). The number of occurrences for shyness and scores differed significant ly between treatments (before boldness behaviors was counted to calculate the score. and after anti-predator training) and to test if displayed The number of shyness behaviors were multiplied by 1 behaviors differed between distances (less than 1.3 m and the number of boldness behaviors were multiplied and more than 1.3 m) (Zar 1998). One-way ANOVA by 2, and the higher the score, the bolder the individual was used to test for differences in boldness score variation was considered (Bremner-Harrison et al. 2004, Kurvers between treatments [Boldness Score after anti-predator et al. 2010). training minus Boldness Score before anti-predator Personality tests consisted in presenting two training (BSa - BSb)] (Zar 1998)]. unknown objects to the parrots: a traffic cone and a The correlation between mean percentage of pot of potato chips connected to a bottle of milk; one predator aversion behaviors (= average of 30-day and object was shown to the birds before the anti-predator 60-day shy behaviors × 100 / total recorded behaviors) training sessions and the other object was shown to the and personality was tested using non-linear correlation birds after the anti-predator training sessions. The objects analysis with quadratic function. Cluster analysis was were presented to the birds on a platform at the centre of used to determine the similarity in personality between the enclosure. Four perches, with markings indicating the individuals before and after anti-predator training distances to the object (less than 1.3 m and more than 1.3 sessions. The distance measure used was the difference m), were connected to the platform. between boldness scores and amalgamation rule was The tests were conducted in the maintenance aviaries UPGMA (Zar 1998). Statistical tests were run using at 08:00 h and each group of parrots participated in only Minitab 12, Mystat 12 and Past. For all statistical analyses, one test before and only one test after anti-predator the confidence level was 95% ( = 0.05). training sessions. The behaviors and t he distance of the birds to the objects (approach distance) immediately after RESULTS its presentation were recorded for 60 min for each object, using the instantaneous focal-animal sampling method with 1-min intervals (Martin & Bateson 2007). The tests Anti-predator training were fi lmed using the webcam of a COMPAQ notebook. Personality tests after anti-predator training sessions Parrots behaved similarly during the conditioning phase occurred before the memory tests, in the day following 2 of the anti-predator training sessions, only differing in the end of the anti-predator training sessions. the expression of inactivity, with the parrots of the control group more inactive than the parrots of the hawk and Data analysis of anti-predator tests ocelot groups (Fig. 2). Parrots trained with the ocelot hid more than the control group, and parrots trained against Data normality was evaluated using the Anderson-Darling all predators (mixed group) flew more than the parrots of test. Since the data did not meet the requirements for the control group (Fig. 2). Parrots of the control group normality, we used Friedman's non-parametrical ANOVA paced and slept more than the other groups; parrots test, with Dunn's post-hoc, to evaluate differences between of the mixed group nodded their heads more than the parrots' responses to the different predator models (control, parrots of the hawk group (Fig. 2). Relaxing behaviors, ocelot, hawk, mixed, mixed hawk, mixed ocelot, mixed like yawning, self and allopreening, were not exhibited human, and human), between phases (before, during and during the conditioning phase. after the appearance of the predator model). Wilcoxon's Parrots expressed more anti-predatory behaviors test was used to compare the parrots' behaviors between with all predator models during phase 3 (hiding behind 30 and 60 days after training (memory tests). The results the shrub, and flying). The control group behaved in a for the mixed group were evaluated pooled (data from more relaxed way, expressing more behaviors like walking the tests with all predator models together) and separated on the perch, inactivity, and sleeping (Fig. 3). (with only the responses showed for each predator model; Aversion behaviors increased significantly after the hawk, ocelot and human). For all statistical analyses, the presentation of the predator models, including with the confidence level was 95% ( = 0.05) (Zar 1998). human model (Fig. 3). Relaxing behaviors decreased Revista Brasileira de Ornitologia 25(1): 2017 Important tools for Amazon Parrot reintroduction programs Azevedo et al. during the presentation of the predator models, but in the hawk group, and walking on perch in the mixed increased significantly during phase 3, especially during group. Parrots trained against the hawk were more the last 5 min of phase 3 (Fig. 3). Although aversion inactive 30 days after the end of the anti-predator training behaviors increased in phase 3 in the control group, sessions (mean ± SE: 30 days: 25.22 ± 6.14; 60 days: 9.39 it showed the lowest increase when compared to the ± 4.11; Z = 2.29, P = 0.01, n = 18; df = 1). Parrots trained predator models (Fig. 3). in the mixed group walked more on the perch 30 days No differences in the behaviors of the parrots were after the end of the anti-predator training sessions (mean observed 30 and 60 days after the anti-predator training ± SE: 30 days: 1.94 ± 0.57 records; 60 days: 0.83 ± 0.35; for all predator models, except for the behaviors inactive Z = 2.37, P < 0.01 n = 18; df = 1). Figure 2. Behaviors displayed by Amazon Parrots during phase 2 of the anti-predator training sessions. IN = inactive; HID = hiding behind tree; FLY = flying; ND = nodding head; PAC = pacing; SLEE = sleeping; Superscript letters: CD = P < 0.05; AB = P < 0.01. Figure 3. Behaviors displayed by the Amazon Parrots during phases 1, 2 and 3 of the anti-predator training sessions. Avr = aversion behaviors; Rel = relaxing behaviors; b = before the appearance of the predator model (phase 1); d = during the appearance of the predator model (phase 2); a = after the appearance of the predator model (phase 3); AB P < 0.05; CD P < 0.01; EF P < 0.001. Revista Brasileira de Ornitologia 25(1): 2017 Important tools for Amazon Parrot reintroduction programs Azevedo et al. Personality tests and 12), and exhibited a higher boldness score (BSa = 205). Parrots that exhibited intermediate boldness scores Boldness scores of parrots ranged between 178 and 240. after training belonged mostly to the group trained with the Harris's Hawk (9, 11, and 12), but also to the control The personality of most individuals changed after the treatments. The scores increased significantly in 50% of (25), ocelot (18), and mixed groups (4). cases (t = -4.47, n = 16, df = 15, P < 0.001) and decreased Boldness scores after training had a significant significantly in 33% of cases (t = 2.35, n = 16, df = 15, P quadratic relationship with mean percentage of predator = 0.02). aversion, measured 30 and 60 days after the treatments (Aversion = -16.0 + 0.16 × BSa – 0.0004 x BSa ) (Fig. The most fearful individuals before training based on boldness scores were those that were trained against 5), which means that parrots with intermediary boldness the Harri's Hawk (boldness score's mean: 224; Fig. 4), scores showed higher aversion to the predators. and the most fearful individuals after training were 1,2 those that were trained against the Ocelot (boldness 1,1 score's mean: 212; Fig. 4). In general, there was a O O C Ha H O u Ha 1,0 tendency of increased boldness after training, except in Ha Hu O Ha parrots trained against ocelots, where the boldness score 0,9 Ha M C M Hu decreased (Fig. 4). 0,8 0,7 C Ha H M u 0,6 O Hu 0,5 0,4 0,3 0,2 170 180 190 200 210 220 230 240 250 Bol dness score after treatment Figure 5. Relationship between boldness scores after anti-predator 200 training and average aversion to three predator types 30 and 60 days after training. Bolder individuals only exhibited lower aversion values. The box indicates the region of the graph with intermediate and bold individuals that exhibited high aversion to predators and that would be Before good candidates for release. The letters indicate the different training Mixed Hawk Ocelot Human Control After regimes: C – control, Ha – trained against Harris's Hawk, O – trained T reatment Figure 4. Means and confidence intervals (95%) of B lue-fronted against ocelot, Hu – trained against human, and M – mixed training Parrot boldness scores before and after anti-predator training sessions. against all predator models. All individuals underwent anti-predator training (except control ones), either against all models (mixed) or one predator only (hawk, DISCUSSION ocelot, and human). There were no significant differences in the Anti-predator training modified t he behaviors of the personality of parrots that underwent different training parrots, increasing their awareness about their predators and controls (F = 1.7, n = 28, df = 4, P = 0.177), before and diminishing relaxing behaviors. Additionally, the and after treatment (F = 0.1, n = 28, df = 4, P = 0.814), anti-predatory behaviors persisted for at least 60 days and no significant interaction between these factors was after the end of the anti-predator training sessions. Anti- observed (F = 1.7, n = 28, df = 4, P = 0.186). Additionally, predator behaviors have to be effective in the very first there were no significant differences in mean differences time a prey encounters its predator, but these responses of boldness scores (BSa - BSb) between treatments (F = can be improved with experience (McLean & Rhodes 1.7, P = 0.186). However, parrots displayed behaviors 1991, Griffin et al. 2000). Although the parrots of this more frequently in the distances greater than 1.30 m study responded to the predators in the first session, they from the objects (t = -6.45, P < 0.001, n = 56, df = 1). exhibited stronger responses after two training sessions; Cluster analysis did not group parrots from different a similar result was observed for the Noisy Friarbird treatments or separate control parrots from individuals Philemon corniculatus (Latham, 1790) trained by Curio who underwent anti-predator training. For instance, et al. (1978). before the treatment, bird 18 was separated from the Relaxing behaviors were more frequent in the parrots other individuals and had a boldness score indicative of the control group during phase 2 (predator model of shyness (BSb = 188). After the treatment, the same appearance), and this response reflects the fact that the individual was grouped with other parrots (27, 4, 9, 11, parrots were able to recognize that the model of a chair Revista Brasileira de Ornitologia 25(1): 2017 Boldness score Average predator aversion Important tools for Amazon Parrot reintroduction programs Azevedo et al. was not a threatening stimulus. New Zealand Robins habituation (Griffin et al. 2000, Hemmi & Merkle 2009). [Petroica australis (Sparrman, 1788)], Greater Rheas [Rhea For example, Houbara Bustards [Chlamydotis undulata americana (Linnaeus, 1758)] and Tropical Screetch-owls (Jacquin, 1784)] habituated to a fox model after two [Megascops choliba (Vieillot, 1817)] also responded to a training sessions (van Heezik et al. 1999), and Greater control stimulus expressing relaxing behaviors (Maloney Rheas habituated to predator models after five training & McLean 1995, Azevedo & Young 2006, Specht 2007). sessions (Azevedo & Young 2006). Parrots in this study The abnormal behavior pacing was exhibited by one did not show signs of habituation since the responses parrot of the control group (number 26); this individual to the predator models were consistent over all trials; in displayed such behavior in all phases of the study, and fact, in the first two trials they were alrea dy responding should be eliminated from the group of parrots destined strongly to the predators. to be reintroduced. Anti-predator training changed the personality The behavior hiding behind the shrub was more of Blue-fronted Amazon Parrots, and in most cases it frequently exhibited in response to the mixed hawk promoted an increase in the boldness scores. A study group. This response was also observed in a study with with Greater Rheas, a study with tropical Screech-owls, Hispaniolan Amazon Parrots [Amazona ventralis (Müller, and a study with Trinidadian Guppies [Poecilia reticulata 1776)] trained against falcons (White-Jr. et al. 2005), (Peters, 1859)] found significant decreases in the boldness and when training owls against hawks (Alonso et al. scores of the individuals after anti-predator training 2011). Nodding head was exhibited mainly against the sessions (Azevedo & Young 2006, Specht 2007, Smith hawk model. The most frequent anti-predator response & Blumstein 2012). In the present study, boldness scores of Rock Partridges [Alectoris graeca Meisner, 1804)] to a decreased after anti-predator training sessions in only hawk model was to crouch (Zaccaroni et al. 2007) which, 33% of sampled parrots. according to the authors, is a cryptic behavior, very effective It is known that fear responses can vary according against predatory birds. Maybe this behavior, associated to the personality of the individuals (Verbeek et al. 1994, to the green plumage of the parrots (they become cryptic Wilson 1998, Carere et al. 2005), and according to the immerse in the vegetation), constitute a good way to avoid individual's life history (early experiences) (Levine et al. being located by flying predators (Alcock 2013). 1993, Fox & Millam 2004). For instance, bolder Rainbow Inactive and flying were the most recorded behaviors Trout [Onchorhyncus mykiss (Walbaum, 1792)] became displayed by parrots in association with Ocelot and shyer after watching shy individuals being presented to human models. Possibly, the best tactic against terrestrial novel objects (Frost et al. 2007). In the current study, the predators, which use a silent and furtive approach early experiences of the parrots could not be determined, toward prey, is to remain inactive in order to monitor since all individuals were recovered from traffic. Although and evaluate the behavior of the predator (Zaccaroni et interviews were conducted with the parrot owners, they al. 2007). This strategy allows prey to save energy, since did not provide any information about the origins of the it will only exhibit escape behaviors if necessary (risk- birds, fearing legal punishment. The only information disturbance hypothesis; Frid & Dill 2002). The Ocelot about the early experiences of parrots was that all and the human models elicited both behaviors, but for individuals studied had lived in captivity for at least five the human model, these responses were stronger than for years. The boldness of the parrots trained against humans the Ocelot, where parrots flew away in almost all sessions. achieved the highest mean-scores and the minimum Perhaps this stronger response to the human model could treatment variation (236 before training to 237 after be a result of the perception of a greater risk of predation training; corroborating the hypothesis that they may be by the parrots, which corroborates the risk-disturbance hand-reared. This result indicates that these individuals hypothesis of Frid & Dill (2002). may not be ideal for reintroduction, since the chance of Memory tests showed that the responses of parrots being recaptured by humans may be great or that training to the predators lasted for at least 60 days after the against humans should be more intense. Feenders et end of the training sessions. Similar results were found al. (2011) showed that hand-reared Starlings [Sturnus in a study of Greater Rheas (Azevedo & Young 2006). vulgaris (Linnaeus, 1758)] had greater latency time to Predator encounters probably occur within a period of move in novel environments than wild-caught ones, but two months in the wild, and the persistence of the proper found no difference in the behavioral responses between anti-predatory responses is important, since it can increase both groups of birds in a novel object experiment. the survival rate of the parrots when reintroduced. The later experiences of the parrots, however, could It is difficult to establish t he exact number of training be determined since the parrots stayed in the IBAMA sessions necessary to elicit the right anti-predatory facilities for at least four months prior to experiments. All behaviors and to avoid habituation, but it is suggested parrots received a routine of environmental enrichment, that the least number of training sessions is best to avoid and it has been shown that environmental enrichment Revista Brasileira de Ornitologia 25(1): 2017 Important tools for Amazon Parrot reintroduction programs Azevedo et al. Alonso R., Orejas P., Lopes F. & Sanz C. 2011. Pre-release training diminishes neophobia in Amazon Parrots (Meehan et of juvenile Little Owls Athene noctua to avoid predation. Animal al. 2003, Fox & Millam 2007). The consistency of lack Biodiversity and Conservation 34: 389–393. of variation in responses of parrots to the novel objects Altmann J. 1974. Observational study of behavior: sampling methods. before-after-anti-predator training may be reflecting this Behaviour 49: 227–267. Andrade A.A. & Azevedo C.S. 2011. Efeitos do enriquecimento routine. ambiental na diminuicão de comportamentos anormais exibidos The tendency of parrots to exhibit bold behaviors in por Papagaios-verdadeiros (Amazona aestiva, Psittacidae) cativos. the personality test even after the training sessions may Revista Brasileira de Ornitologia 19: 56–62. be explained by their remarkable cognitive ability (Emery Azevedo C.S. & Young R.J. 2006. Behavioural responses of captive- 2006). The ability to differentiate non-predators from born Greater Rheas Rhea americana Linnaeus (Rheiformes, Rheidae) submitted to antipredator training. Revista Brasileira de predators ensures that animals do not generalize their Zoologia 23: 186–193 responses to non-predators (Griffin e t al. 2000, Azevedo Azevedo C.S., Young R.J. & Rodrigues M. 2012. 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Washington: National Academic Press. select accurately the individuals more suited for release, Carere C., Drent P.J., Privitera L., Koolhaas J.M. & Groothuis T.G.G. and intermediate individuals or bold ones that recognize 2005. Personalities in Great Tits, Parus major: stability and consistency. Animal Behaviour 70: 795–805. potential predators and exhibit aversive behaviors toward Carlstead K. 1999. Constructing behavioural profiles for zoo animals: predators should be preferred. incorporating behavioral information into captive population management. Oregon: AZA Behaviour and Husbandry Advisory Group and Oregon Zoo. ACKNOWLEDGEMENTS Carter A.J. & Feeney W.E. 2012. Taking a comparative approach: analysing personality as a multivariate behavioural response across species. PLoS ONE 7: e42440. We thank IBAMA for loaning the animals and enclosures, Collar N.J. 1997. Family Psittacidae (parrots), p. 280–479. In: del and for the support provided throughout the study. 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Ornithology Research – Springer Journals
Published: Mar 1, 2017
Keywords: anti-predator training; captivity; conservation; personality; Psittacidae
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