Environmental Enrichment and Development of Cage Stereotypy in Orange-winged Amazon Parrots (Amazona amazonica)

Transcription

1 C. L. Meehan Animal Behavior Graduate Group/ Department of Animal Science University of California Davis, CA J. P. Garner J. A. Mench Department of Animal Science University of California Davis, CA Environmental Enrichment and Development of Cage Stereotypy in Orange-winged Amazon Parrots (Amazona amazonica) ABSTRACT: Stereotypies are abnormal repetitive behaviors that often develop in animals housed in impoverished environments. Stereotypy represents the interaction of several complex developmental phenomena. To characterize the temporal nature of stereotypy increase (escalation) and decrease (attenuation), we monitored changes in stereotypy performance in young Orange-winged Amazon parrots reared either in barren cages or cages provided with enrichments designed to facilitate foraging and locomotion. Unenriched parrots developed significantly more stereotypy than enriched parrots, and the mean time to stereotypy onset and the rate and magnitude of stereotypy increase also differed between the two groups. We then provided enrichment to the birds that had been reared in the barren cages. Following a 4-week delay, stereotypy was significantly reduced. These results show that stereotypy can be both prevented and reversed with appropriate environmental modification and illustrate how studying this behavior at many points over time can provide insights into its ontogeny. ß 2004 Wiley Periodicals, Inc. Dev Psychobiol 44: , Keywords: parrots; psittacine; Orange-winged Amazon; stereotypy; ontogeny; environmental enrichment; abnormal behaviors INTRODUCTION Stereotypies are abnormal repetitive, unvarying, and functionless behaviors that are often performed by captive and domesticated animals housed in barren environments (e.g., Mason, 1991). These behaviors closely resemble the abnormal repetitive behaviors performed by autistic, mentally handicapped, and unmedicated chronic schizophrenic patients as well the stereotypies induced by amphetamine and certain neurological lesions (for review, Received 20 February 2003; Accepted 9 January 2004 Correspondence to: J. A. Mench Contract grant sponsor: Kenneth A. Scott Charitable Trust Published online in Wiley InterScience ( DOI /dev ß 2004 Wiley Periodicals, Inc. see Garner & Mason, 2002). The precise etiology of these behaviors in captive animals is not yet understood, but stereotypy is often explained as a behavioral response to an inappropriate environment, particularly one in which space and complexity are limited. For example, explanatory models link stereotypy development to captive environments where highly motivated behaviors are frustrated (Mason & Turner, 1993; Rushen, Lawrence, & Terlouw, 1993), functional goals are not attainable (Weidenmayer, 1997), or behavioral competition is low (Mason & Turner, 1993). These models have been influential in providing a framework for the experimental study of stereotypy because they point to environmental restriction as a precursor to stereotypy development and implicate alleviation of environmental restriction as an effective means of reducing stereotypy once it has developed. However, interpretation and application of these models has become narrowly focused such that the emphasis of most studies addressing the impact of specific environmental elements

2 210 Meehan, Garner, and Mench on stereotypy is on endpoint (i.e., whether a particular environmental element affects stereotypy) rather than process (i.e., how a particular environmental element affects stereotypy). It is particularly important to understand the processes involved in the expression of behaviors such as stereotypy since these behaviors develop and change rather than occurring spontaneously and then remaining constant (e.g., Mason, 1991, 1993; Mason & Turner, 1993; Würbel, Chapman, & Rutland, 1998). Examining ontogeny thus allows a greater understanding of how the environment influences the progression of stereotypy. Four distinct categories of behavioral change have been identified that characterize the development of stereotypic behaviors. First, these behaviors become less variable and more stereotypy-like over time (Cronin, Wiepkema, & Hofstede, 1984; Mason, 1993; Meyer- Holzapfel, 1968). This change is known as ritualization (Garner, 1999). Stereotypies may then become elicited by a greater diversity of environmental stimuli, which is known as emancipation (Mason, 1993). As a result of establishment, stereotypies may become more difficult to reverse (Cooper, Ödberg, & Nicol, 1996; Cronin et al., 1984; Kiley-Worthington, 1977) and may become fixed in the behavioral repertoire of the animal such that they remain unchanged, even when the environment is modified. Finally, stereotypies may become more frequently performed and occupy a greater proportion of the time budget (e.g., Mason, 1993; Powell, Newman, McDonald, Bugenhagen, & Lewis, 2000; Würbel, Chapman, & Rutland, 1998). We have termed this behavioral change escalation. In this study, we sought to examine the effect of environment on stereotypy escalation by characterizing the developmental profiles of this behavioral change in environments of varying complexity. In addition to questions regarding the effect of environmental restriction on stereotypy development, there is significant applied and theoretical interest in the relationship between the environment and the attenuation of stereotypy. Environmental enrichment is widely used as a means of reducing stereotypy performance in captive animals (e.g., Brent & Belik, 1997; Boinski, Swing, Gross, & Davis, 1999; Carlstead, Brown, & Seidensticker, 1993; Forthman et al., 1992; Henderson & Waran, 2001; Swaisgood et al., 2001), but the developmental processes associated with attenuation (decrease in the amount of time stereotypies are performed) are generally not investigated in studies of this nature. Notable exceptions are those studies designed to determine the point at which stereotypy becomes established (e.g., Cooper et al., 1996; Ödberg, 1987; Powell et al., 2000). In this study, we sought to characterize the developmental profile of stereotypy attenuation to reveal how the effect of an enriched environment changes stereotypy over time. By systematically altering the environment, we were able to follow the same population of animals through both the escalation and the attenuation processes. We used Orange-winged Amazon parrots (Amazona amazonica) as our study species. Amazona amazonica is a long-lived species that reliably develops both oral and locomotor stereotypies when housed in impoverished conditions. For example, in the colony from which our animals were sourced, 96% of the parrots perform locomotor and/or oral stereotypies, and different individuals spend between 5 and 85% of their active time performing stereotypies (Meehan, 2002). There is evidence from studies of other avian species that the development of oral stereotypies is related to limited foraging opportunities while the development of locomotor stereotypies is related to lack of space and physical complexity (Keiper, 1969). Since Amazon parrots in the wild spend significant amounts of time in foraging and locomotor activities (Snyder, Wiley, & Kepler, 1987) that are severely restricted in captivity, this also was an ideal species with which to test the efficacy of two specific environmental modifications: introduction of foraging opportunity and physical complexity designed to increase locomotor activity. By closely monitoring the development of stereotypic behaviors over 48 weeks in young parrots that were kept either in control cages or provided with foraging and locomotor opportunities, we were able to examine whether foraging and locomotor opportunities would prevent or reduce the development of stereotypic behavior and determine time to onset, rate of change of performance, and the trajectories of stereotypy escalation (shapes of the developmental curves) in the control and the enriched groups. In addition, by providing the control parrots with physical and foraging enrichments after they had been displaying stereotypic behavior for several months, we were able to determine whether increased foraging and locomotor opportunities would reduce or eliminate the performance of stereotypic behaviors and examine the rate of attenuation. METHODS Subjects and Caging Subjects were 16 (7 male, 9 female) Orange-winged Amazon parrots hatched in the animal colony at the University of California, Davis, from wild-caught pairs imported from Guyana in Housing and experimental procedures were approved by the Animal Use and Care Administrative Advisory Committee. All subjects were parent raised for 18 weeks in m suspended wire cages. At 18 weeks of age, the parrots were moved to individual cages in another room. Individual housing was necessary to avoid confounding environmental and social enrichment. All cages measured m and were suspended 1 m above the ground. Each cage contained one

3 Stereotypy, Ontogeny, and Enrichment 211 wooden perch at a height of 1.75 m above the ground, a metal L-shaped feeder, and a nipple drinker. Water and pellets (Roudybush low-fat maintenance pellets; Roudybush Inc., Sacramento, CA) were available ad libitum. Other food items (fruits, vegetables, seed, and nuts) were presented daily in limited quantities. Parrots in both treatment groups received the same amounts of these additional food items; only the manner of presentation differed since enriched birds received the items in their foraging enrichment devices (discussed later). Lights went on at 0800 hr and off at 1900 hr, but there was a window that allowed in some natural light, creating seasonal dawn and dusk periods. The study was completed over a 64-week period. No seasonal differences in behavior were observed. We created treatment groups by randomly dividing the parrots into two groups of 8, balanced (as much as possible) for sex and parentage. Each group was then randomly assigned to either the control or the enriched condition. The control group had 4 males and 4 females, and the enriched group had 3 males and 5 females. The control and the enriched cages were spaced in the room to control for position effects. Visual barriers were installed between cages so that each parrot only had visual contact with the parrot in the adjacent cage; adjacent cages were assigned to the same condition. Vocal contact was possible between all birds in the room. After 2 days of habituation to the new surroundings, the enrichment protocol was implemented in the enriched cages. Enrichment Protocol Two categories of enrichments were used: physical and foraging. Examples of the enrichments used are listed in Table 1. Physical enrichments were chosen to increase the physical complexity of the cage. They provided alternate perching sites, climbing or swinging opportunities, or movable objects that could be manipulated with the beak, feet, or both. Foraging enrichments were chosen to provide an opportunity for the parrots to perform some amount of work to receive foods such as seeds, fruits, and nuts. These enrichments required that the parrots chew through barriers, manipulate objects through holes, sort through inedible material, or open containers to obtain food items. Foraging enrichments were refilled daily at 0900 hr. Twenty-four different enrichments (12 foraging, 12 physical) were used over the course of the entire study, and eight different enrichments (4 foraging, 4 physical) were chosen for each of the three 16-week periods. All parrots in the enriched condition received one foraging and one physical enrichment in one of 16 possible combinations each week for 16 weeks. The order in which the combinations were presented was balanced using a Latin square design. Behavior Observations To avoid observer effects on behavior, we conducted all observations via videotape. Parrots in the enriched condition were observed three times weekly to monitor enrichment use. To account for changes in enrichment use relative to the length of time the parrot had been exposed to the pair of enrichments, enrichment use observations were conducted on Day 0 (new pair of enrichments introduced), Day 3, and Day 6 (last day with pair of enrichments) each week. To account for changes in enrichment use relative to the length of time since the foraging enrichments had been refilled, observations were scheduled at 0930 and 1200 hr (either 30 min or 3 hr after the foraging enrichments were refilled). Each observation lasted 20 min, during which time all occurrences of physical contact, excluding incidental contact, with enrichments were recorded using Hewlett Packard HP 48 Gþ graphing calculators programmed for data collection. Since there has been little published work on stereotypy performance in psittacines, these behaviors had not been Table 1. Descriptions of Some of the Enrichment Items Used in the Experiment Enrichment Item Description Foraging Enrichments T-shirt bags a Fruit cage Toy box Treat basket Physical Enrichments Boing b Diamonds b Spring b Bridge b Foraging enrichments were chosen to provide an opportunity for the parrots to perform some amount of work to receive foods such as seeds, fruits, and nuts. These enrichments required that the parrots chew through barriers, manipulate objects through holes, sort through inedible material, or open containers. All foraging enrichments were filled with both edible and inedible items. Sack of cotton cloth hung on a rope from the top of the cage. Cylindrical metal cage (height 15 cm, diameter 7 cm) hung with a chain from the top of the cage. Plastic cube (25 cm 3 ) with holes and doors of various sizes and shapes hung from the top of the cage. Enclosed woven basket hung from the top of the cage. Physical enrichments were chosen to increase the physical complexity of the cage. They provided alternate perching sites, climbing or swinging opportunities, or movable objects that could be manipulated with the beak, feet, or both. 2.5 cm diameter cotton rope wound around a spiral spring (.75 m long) hung from the top of the cage. Two plastic diamonds and lengths of plastic chain (.5 m long) connected end to end and hung from the top of the cage. Flexible plastic coil (.75 m long) connected horizontally to opposite ends of the cage. Swinging ladder (.75 m long) made of wood and rope connected horizontally to opposite ends of the cage. Source: a Bird Brain Toys; b Birds and Branches.

4 212 Meehan, Garner, and Mench previously identified and defined. Thus, we began this study by developing an ethogram of stereotypy performance in this species (Table 2). We used the widely accepted definition of stereotypy a behavior that is repetitive, invariant, and has no apparent purpose or meaning to identify the stereotypies performed by the parrots in this study. We watched hundreds of hours of videotapes from a pilot study as well as all videotapes from the current study to develop the ethogram. This ethogram included clear descriptions of each of the stereotypies, but did not have precise performance parameters. For example, to address individual differences in patterns of stereotypy, a route trace was defined as an invariant, repetitive pattern through space, but the pattern itself could vary between individuals. In addition, while all stereotypies were measured with respect to duration of performance, there were no rules for duration of performance built into the ethogram. To monitor stereotypy performance, all birds in both conditions were observed for 2 hr every 4 weeks. One hour of video was collected in the morning ( hr), and 1 hr of video was collected in the afternoon ( hr). The videotapes were later viewed and analyzed using a datacollection program written in Microsoft Access (2002) Microsoft Corporation. Durations of performance of the following behaviors were recorded: general locomotion, preening, feeding/drinking and enrichment use, locomotor stereotypy, and oral stereotypy. For each parrot, the amount of active time (time not sleeping or resting) was calculated from each tape. Enrichment of Control Group After three 16-week periods, the parrots from the control group began receiving enrichments. The enrichment protocol described earlier was repeated, and behavioral observations continued as described previously. This phase of the study continued for additional 16 weeks, after which all parrots from both treatment groups were adopted into private homes. Statistical Methods Repeated measures mixed-model GLM was used throughout. The model tested for the effects of treatment, sex, and week. Week was treated as a continuous variable. The assumptions of parametric methods were confirmed from plots of residuals versus fitted values, and suitable transformations were applied where required. All analyses were performed using MiniTab12 Statistical Software (2000) MiniTab, Inc. To ensure that any decrease in stereotypy was not solely due to an increase in enrichment use, we subtracted the amount of time the enriched group spent interacting with enrichments from the total time active to arrive at a measure of activity corrected for enrichment use. We used this measure of activity to calculate the percent of active time each parrot spent performing stereotypy. We then calculated the average percent active time spent stereotyping during each observation week. Data from Table 2. Behavior Descriptions of Behaviors Classified as Locomotor and Oral Stereotypies Description Locomotor Stereotypies Pacing Perch Circles Corner Flips Route Trace Oral Stereotypies Wire Chewing Sham Chewing Food Manipulation Dribbling Locomotor stereotypies involve the repetition of an identical pattern of movement. The pattern of foot and body movements is identical on each repetition of the behavior. This pattern had to be repeated two or more times for the bout of behavior to be classified as a stereotypy. The parrot walked back and forth across the perch, turning around upon reaching either end of the perch. Alternatively, the parrot faced the front of the cage and side stepped from one end of the perch to the other. Pacing can be performed along the entire length of the perch or just for a few steps. The parrot walked the length of the perch, climbed up the sidewall of the cage, climbed across the top of the cage, down the opposite sidewall to the perch, completing a vertical circle across top of cage and down sidewall. The parrot turned in small circles in a top corner of the cage. The parrot walked and/or climbed a repeated identical route around the cage. Oral stereotypies involve the repetition of an identical pattern of oral movements. Oral stereotypies also may be performed in an identical location in the cage. This pattern had to be repeated two or more times for the bout of behavior to be classified as a stereotypy. The parrot gnawed repeatedly on the wire bars of the cage. While gnawing, individual parrots may pull violently on the wire, making a snapping sound. These movements involve identical body postures or identical locations within the cage. The parrot made chewing movements with nothing in its mouth. The parrot picked up a food item (usually a pellet) in the mouth. The food item is not chewed, but is instead turned around in the mouth repetitively. The parrot dropped and picked up an object repeatedly usually with beak while on perch. In each case, the behavior involved the repetition of an invariant pattern of motor output that lacked any goal or function. All behaviors were scored with respect to duration of performance.

5 Stereotypy, Ontogeny, and Enrichment 213 Weeks 4, 16, 32, and 48 were used in the analyses. Prior to the start of the study (Week 0), all parrots were observed and determined not to perform any stereotypic behaviors. To preserve homogeneity of variance, data from this period were not included in the analyses. We performed an angular transformation of the stereotypy scores to try to resolve a floor effect and to preserve error homogeneity. The data for stereotypic behavior development were analyzed using repeated measures GLM as well as Mann Whitney and Wilcoxon nonparametric tests. To avoid pseudoreplication, nonparametric tests were performed on within-animal differences so that each parrot was represented by a single data point. We used the nonparametric tests as secondary analyses to GLM because the floor effect could not be resolved by transformation. Using repeated measures polynomial regression, we analyzed the developmental trajectories of the control and the enriched groups to determine if the curves were different shapes or if they were two portions of the same curve. To model S-shaped curves, we included quadratic and cubic terms for week. To examine whether the developmental trajectories of the two treatment groups were merely portions of the same curve, we included only the Treatment Week interaction in the model. This term effectively allows the curve to shift along the x-axis (week) for each treatment group. However, excluding Treatment Week 2 and Treatment Week 3 from the model forces the shape of the curve to remain constant. We also constructed a model including a Treatment Week 2 interaction to determine if the two curves were of different shapes. In this model, a significant Treatment Week 2 interaction confirmed that the shapes of the two curves were different. To determine the rate of change of stereotypy performance of parrots in the control group before and after receiving enrichments, we broke the experiment down into four time periods: early control (Weeks 4 16), midcontrol (Weeks 16 32), late control (Weeks 32 48), and enrichment (Weeks 48 64). We then calculated the rate of change in stereotypy performance during each of these periods. We analyzed these data using a repeated measures mixed model GLM and used Bonferronicorrected t tests to make post hoc pairwise comparisons between periods. RESULTS Description of Responses to Enrichment All parrots in the enriched group interacted with all the enrichments. They would approach the objects 1 to 20 min after presentation and then proceed to investigate them with their beaks and feet. The physical enrichments elicited balancing, swinging, and climbing behaviors while the foraging enrichments elicited chewing, object manipulation, sorting inedible material, and food-selection behaviors. The physical enrichments were often used to access the foraging enrichments. Use of both enrichment types remained stable during the first two 16-week periods and declined during the third 16-week period, repeated measures GLM: F(2, 35) ¼ 7.56, p ¼ (Fig. 1). In all periods, foraging enrichments were used more than physical enrichments, repeated measures GLM: F(1, 35) ¼ 44.34, p > (Fig. 1). Stereotypy Development Patterns of stereotypy development in the control and the enriched birds are presented in Figure 2. Over the 48 weeks of the experiment, the parrots in the control FIGURE 1 Mean ( SEM) enrichment use during the three 16-week enrichment periods. In all periods, foraging enrichments were used more than physical enrichments.

6 214 Meehan, Garner, and Mench rose slightly from Week 16 to Week 32 and showed its greatest rate of increase from Week 32 to Week 48. FIGURE 2 Residual plot (residuals plotted from least squares mean line where data points represent the y-value corrected for individual and sex) of the percent of active time (activity time spent interacting with enrichments) parrots in the enriched () and the control (o) group spent stereotyping over the course of the 48-week study. Measurements of stereotypy are reported for Weeks 4, 16, 32, and 48. condition developed significantly more stereotypy than the parrots in the enriched condition, Treatment Week repeated measures GLM: F(3, 42) ¼ 15.02, p < (Fig. 2). The repeated measures Wilcoxon analysis showed that overall stereotypy increased from Week 4 to Week 48 in both groups, (T ¼ 78.0, N ¼ 16, p < 0.005). Mann Whitney analysis confirmed that the increase from Week 4 to Week 48 was greater in the control treatment (W ¼ 96.5, N 1 ¼ N 2 ¼ 8, p < 0.005). In the control group, stereotypy was first observed in 1 parrot at Week 4 (5% of active time). By Week 16, 7 of the 8 parrots in the control condition were performing stereotypies. For these 7 parrots, the range of time spent performing stereotypy at Week 16 was 6 to 21% of active time. By Week 32, the range of stereotypy performance for these 7 parrots was 4 to 28% of active time. By Week 48, all 8 parrots in the control group were performing stereotypy, and the range of performance was 6 to 25% of active time. Of the total time spent stereotyping, 67% was spent in locomotor stereotypy and 33% in oral stereotypy. In the enriched group, 1 parrot performed stereotypy at Week 4 (3.5 % of active time). This same parrot also was the only one to perform stereotypy at Week 16 (5% of active time). By Week 32, 2 parrots were performing some stereotypy (1.5 and 9% of active time, respectively), and by Week 48, 4 of the 8 parrots in this condition were performing stereotypy. The range of stereotypy performance for these 4 parrots at Week 48 was 4 to 10% of active time. Of these stereotypies, 92% were locomotor and 8% were oral. Duration of stereotypy performance Analysis of Developmental Curves For the repeated measures GLM model with only a Treatment Week interaction, the cubic week term was nonsignificant [repeated measures GLM: F(1, 30) ¼ 1.35, p ¼ 0.254], showing that the developmental trajectories of the two treatment groups were not regions of the same curve. We constructed a new model removing the cubic week term and adding a Treatment Week 2 interaction. In contrast, this term was significant at p < [repeated measures GLM: F(1, 15) ¼ 19.40], confirming that the developmental trajectories were different shapes in the two treatment groups (Fig. 2). Enrichment of the Control Group All parrots in the control group began interacting with the enrichments within 2 days of introduction. Although some parrots avoided the enrichments for the first several hours, by the second day, interactions with the physical enrichments were prolonged. By the following day, most of the parrots had figured out how to successfully utilize the foraging enrichments. In all periods, foraging enrichments were used significantly more than physical enrichments [repeated measures GLM: F(1, 49) ¼ 12.87, p ¼ 0.001] (Fig. 3). The control parrots performed significantly less stereotypy after receiving enrichments in the final phase of the study than they did during the earlier periods. Baseline and enriched levels of stereotypy were similar, but differed significantly from levels during the control periods, period main effect [Mixed Model Comparison of Means: F(4, 24) ¼ 15.17, p < 0.001] (Fig. 4). The rate of change in stereotypy performance for each time period is presented as the slope of the corresponding line in Figure 4. The rate of increase in stereotypy performance during the early control period was significantly greater than the rate of increase during the late control period (post hoc t test on the slope coefficients: t ¼ 3.44, df ¼ 40, p ¼ 0.001). However, the rate of increase during the early control period was statistically similar to the rate of decline in stereotypy performance during the enriched period (post hoc t test on the slope coefficients: t ¼ 0.284, df ¼ 40, p ¼ 0.777). Post hoc tests revealed that the significant decrease in stereotypy performance during the enriched period was due to changes that occurred between Weeks 52 and 64 and that no significant decrease in stereotypy performance occurred between Weeks 48 and 52 (t test, p ¼ 0.056). Of the total stereotypy performed by these parrots at Week 64, 90% were locomotor and 10% were oral.

7 Stereotypy, Ontogeny, and Enrichment 215 FIGURE 3 Mean ( SEM) enrichment use by the original control group during four 4-week enrichment periods. In all periods, foraging enrichments were used more than physical enrichments. DISCUSSION Enrichment and the Development of Stereotypy As predicted, parrots that received foraging and physical enrichments spent significantly less of their active time performing stereotypic behaviors than did parrots in the control group, providing empirical evidence for the role of these specific environmental factors in the development of stereotypy in this species. The role of specific environmental factors on stereotypy development has been demonstrated with mammals such as voles (Ödberg, FIGURE 4 Rates of change in stereotypy performance during the early control (Weeks 4 16), mid-control (Weeks 16 32), late control (Weeks 32 48), and enriched (Weeks 48 64) periods. Differences in stereotypy performance at each period are indicated by different superscripts at each period marker. Slopes are below each line. Differences in slopes (independent of direction) are indicated by different superscripts.

8 216 Meehan, Garner, and Mench 1987), deer mice (Powell et al., 2000), and laboratory mice (Würbel, Chapman, & Rutland, 1998); our study is the first to illustrate that the response shown by an avian species to the lack of specific important environmental elements is similar to the response shown by mammals. However, the degree of environmental modification used in our study was not sufficient to completely prevent the development of stereotypic behavior. At the end of 48 weeks, the parrots in the enriched condition performed stereotypies an average of 4% of their active time. This is a common outcome of studies examining the role of specific environmental factors in stereotypy development (e.g., Ödberg, 1987; Powell et al., 2000; Würbel et al., 1998). For example, increasing the physical complexity of cages with twigs prevents most, but not all, stereotypy development in young voles (Ödberg, 1987). Similarly, the combination of feeding sunflower seeds and increasing physical complexity has a significant effect on the amount of time deer mice spend performing stereotypy, but does not eliminate the development of these behaviors altogether (Powell et al., 2000). Weidenmayer (1997) was successful in preventing nearly all development of stereotypy in gerbils reared with access to a burrow, but only if the burrow was paired with a tunnelshaped entrance. Weidenmayer s results suggest that not only a species-specific approach but also an iterative one is necessary to isolate the specific aspects of the environment that are critical to the absolute prevention of stereotypy. Forms of Stereotypy Parrots in the control condition developed both locomotor and oral stereotypies while those in the enriched condition developed almost exclusively locomotor stereotypies. This suggests that specific stereotypic topographies may be associated with the absence of specific environmental elements (Mason & Mendl, 1997). In this case, if oral stereotypies are associated with frustration of foraging behaviors, then the foraging enrichments may have successfully eliminated this frustration. If the development of locomotor stereotypies is associated with limited space, prevention of flight, or lack of social contact, then this would explain why these behaviors were not prevented by the physical enrichments we provided. In another study, we found that raising parrots in pairs in double-sized cages provided with the physical and foraging enrichments used in the current study completely prevented the development of stereotypic behaviors (Meehan et al., 2003), but because all enrichments were presented simultaneously the effects of each different type of enrichment on locomotor stereotypies could not be determined. Additional experiments assessing the effectiveness of increased flight space and social housing on locomotor stereotypy development would address this issue. There is evidence from other avian species that the development of oral stereotypies is related to lack of opportunity to perform foraging behaviors while the development of locomotor stereotypies is related to a lack of space and physical complexity (Keiper, 1969). Since we introduced foraging and physical enrichments together rather than separately, it is difficult to determine the relative importance of each enrichment category from our study. It is possible that the combination of physical and foraging enrichments is necessary for the preventative effects on stereotypy development we observed and that neither of the enrichments alone would have had that effect. Evidence from Developmental Trajectories By analyzing the trajectories of stereotypy development, we found that the timing of onset, rate of escalation, and the shape of the developmental curves all differed between the control and the experimental groups. None of the parrots in either condition displayed any stereotypy immediately following transfer to the experimental cages. After 4 weeks of exposure to the experimental condition, only 1 parrot in the control condition displayed any stereotypic behavior. A delay in stereotypy onset also is seen in bank voles (Ödberg, 1987), gerbils (Weidenmayer, 1997), deer mice (Powell, Newman, Pendergast, & Lewis, 1999), and domestic mice (Würbel, Chapman, & Rutland, 1998). The length of the delay varies between species, but a period of time separating exposure to a barren environment and stereotypy onset in naïve animals is a common feature of stereotypy development. However, we found that the control and the enriched groups differed with respect to the length of the delay of onset of stereotypy performance. After Week 16 of the experiment, 7 of the 8 parrots in the control group were performing stereotypies compared with only 1 parrot in the enriched group. By Week 48, all 8 parrots in the control condition were performing stereotypies compared with 4 of the 8 parrots in the enriched condition. These results indicate that conditions in the enriched cages were sufficient to delay the onset of stereotypy performance. This result is similar to that found by Powell et al. (1999), who reported that stereotypy onset for deer mice in standard cages preceded onset in enriched cages by 3 weeks. These data suggest that there is a phase preceding the manifestation of the stereotypic behavior, the length of which can be modified by environmental quality. We call this phase the inception phase of stereotypy development. Escalation of stereotypy performance also was affected by enrichment. The amount of time spent performing sterotypies increased over the course of the study in both groups, but the magnitude, rate, and timing of this increase differed. In the control group, the duration of stereotypy

9 Stereotypy, Ontogeny, and Enrichment 217 performance increased by 13.25% over 48 weeks, with the greatest rate of increase occurring during the early control phase. The rate of increase of stereotypy duration slowed during the late control phase and leveled between Weeks 32 and 48. In contrast, stereotypy performance in the enriched group increased by 3.75% over the course of the experiment and showed its greatest rate of increase from Week 32 to Week 48. Like the control parrots, performance peaked at 48 weeks, but we can infer from the rate of escalation between Weeks 32 and 48 that performance may have continued to increase had the study continued. This difference in the rate of escalation also is seen in deer mice: The percent time mice spend performing stereotypy increases at a significantly faster rate among animals housed in barren cages than among those housed in enriched cages (Powell et al., 1999). Enrichment of Control Birds In the second part of this study, we sought to characterize the profile of stereotypy attenuation by providing foraging and physical enrichments to parrots that had developed stereotypy during the previous 48 weeks. All parrots responded to the enrichments, such that over the 4 months of the experiment stereotypy performance decreased from 13 to 3% of active time. In other studies that have demonstrated a decline in stereotypy with enrichment, these declines may be explained by a shift in the time budget where less time is available for stereotypy performance (e.g., Boinski et al., 1999; Carlstead et al., 1991; Forthman et al., 1992). However, because the stereotypy measures we used were corrected for time spent with the enrichments, we are confident that the reduction in stereotypy we observed is not an artifact of behavioral competition for space in the time budget. The fact that we monitored behavior at multiple points over a 16-week enrichment period allowed us to characterize the effects of enrichment on stereotypy performance over time. This is a departure from the methods commonly employed in research of this type. For example, enrichments are sometimes only available to the animals for hours or days before final measurements of stereotypy are taken (e.g., Carlstead et al., 1991; Henderson & Waran, 2001; Swaisgood et al., 2001). In other cases, the animals are housed in the modified environment for weeks or months, but behavior is either observed only at the very end of this period (e.g., Powell et al., 2000) or the data are lumped into pre- and postenrichment categories for analysis (e.g., Brent & Belik, 1997; Forthman et al., 1992; Grindrod & Cleaver, 2001). Thus, because of these methods, it is often impossible to tell how the effects of enrichment on stereotypy change over time and if they are temporary or persistent. We addressed this issue by following the course of stereotypy attenuation for 16 weeks following the presentation of enrichments. Interestingly, while the parrots began to utilize the enrichments regularly after 2 to 3 days, a significant reduction in stereotypy performance did not occur during the first 4 weeks of enrichment. Once stereotypies began to decline, they continued to do so at a rate similar to the rate of escalation during the early control phase of the study. These data suggest that declines in stereotypy performance are delayed and gradual rather than immediate and abrupt. They also suggest that there is a stage that precedes significant decreases in stereotypic behavior performance, thus representing another silent phase in stereotypy development. We call this phase the reversal phase of stereotypy development. Developmental Profile of Stereotypy Our study reveals that analysis of the temporal nature of stereotypy development can contribute to an understanding of the relationship between environment and the progression of stereotypic behaviors. We characterized two stages of stereotypy development, inception and reversal, which occurred without significant changes in behavior. We also characterized two developmental phases, escalation and attenuation, defined by significant changes in behavior. More work is needed to determine the processes underlying each of these stages; however, our study showed that in parrots, inception can be prolonged by the use of foraging and physical enrichments, and that the length of the inception and reversal stages is similar. This study clearly shows that in young parrots stereotypies can be nearly completely prevented through the use of an enrichment protocol designed to facilitate foraging and locomotor behaviors; however, it is important to note that all the parrots in this study had not yet reached sexual maturity. The effectiveness of environmental enrichment on stereotypy prevention might be altered by the age of the animals when enrichment is introduced. Thus, further studies are needed to examine the impact of enrichment on stereotypy throughout the life span. In addition, stereotypies that were performed for many months declined to negligible levels of performance when parrots received consistent, long-term exposure to a varied enrichment protocol such as the one we employed. However, it is important to note that a reversal stage of variable length might precede noticeable declines in stereotypy performance. It is possible that reversal periods will vary according to the species in question, the age of the animal, and the length of time the animal has performed stereotypies. Examining patterns of stereotypy reversal presents an excellent area for future study with various species.

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