MENTAL ROTATION IN A CALIFORNIA SEA LION (ZALOPHUS CALIFORNIANUS)

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1 The Journal of Experimental Biology, (1997) Printed in Great Britain The Company of Biologists Limited 1997 JEB MENTAL ROTATION IN A CALIFORNIA SEA LION (ZALOPHUS CALIFORNIANUS) B. MAUCK 1 AND G. DEHNHARDT 2, * 1 Universität Köln, Institut für Tierphysiologie, Weyertal 119, D-5931 Köln, Germany and 2 Universität Bonn, Zoologisches Institut, Poppelsdorfer Schloß, D Bonn, Germany Accepted 25 February 1997 Mental rotation is a widely accepted concept that suggests an analogue mode of visual informationprocessing in certain visuospatial tasks. Typically, these tasks demand the discrimination between the image and mirror-image of rotated figures, for which human subjects need an increasing reaction time depending on the angular disparity between the rotated figures. In pigeons, tests of this kind yielded a time-independent rotational invariance, suggested as being the result of a non-analogue information-processing that has evolved in response to the horizontal plane that birds perceive from above while flying. Given that marine mammals use the water surface as the horizontal plane for orientation while diving, the ability of a California sea lion to mentally rotate twodimensional shapes was tested. Using a successive twoalternative matching-to-sample procedure, the animal had to decide between the image and mirror-image of a Summary previously shown sample. Both stimuli were rotated by a multiple of 3 with respect to the sample. The animal s reaction time was measured by a computer-controlled touch-screen device, rewarding the animal for pressing its snout against the stimulus matching the sample. A linear regression analysis of the animal s mean reaction time against the angular rotation of the stimulus yielded a significant correlation coefficient. Thus, the present data can be explained by the mental rotation model, predicting an image-like representation of visual stimuli in this species. The present results therefore correspond well with those found for human subjects, but are inconsistent with the data reported for pigeons. Key words: mental rotation, mental representation, visuospatial information, mirror-image discrimination, California sea lion, Zalophus californianus. Introduction Mental representation is one of the central concepts of comparative cognition. Many researchers have tried to determine how objects in our environment are represented mentally and the nature and structure of these representations. The response behaviour of subjects in appropriate experiments could indicate the type and function of the representations used in different tasks. In a classical study, Shepard and Metzler (1971) found that the time it took human subjects to decide whether two figures were identical or mirror-images of each other was a linear function of the angular disparity between these figures. The interpretation of these results was that the subjects used an analogue transformation process which Shepard and Metzler (1971) called mental rotation, suggesting an image-like representation of visual information. Furthermore, it was argued that the process of imagining the rotation of an object should be equivalent to the process of perceiving the physical rotation of an existing object (Shepard and Cooper, 1982). It was also supposed that the same neural substrate that is involved in the perception of real motion also enables us to imagine the motion of objects retained in our memory (Jolicoeur and Cavanagh, 1992; Corballis and McLaren, 1982). Several studies have shown that factors such as the dimensionality of stimuli (Shepard and Metzler, 1988) or weightlessness (Matsakis et al. 1993) may affect the response characteristics of subjects, but the process of mental rotation has always been confirmed. Nevertheless, the analogue nature of the mental rotation process is still the subject of some debate (the so-called analogue-propositional debate; Pylyshyn, 1973, 1979a,b, 1981). In spite of these doubts, the idea of an imagelike representation has been suggested as the best explanation for such experimental results (Roitblat, 1987). Accepting the model of mental rotation for humans, the question remains whether the same mechanism underlies the visual information-processing of other organisms in such tasks. Hollard and Delius (1982) tested the ability of humans and pigeons to discriminate between the image and mirror-image of rotated two-dimensional stimuli in a matching-to-sample task. Their results indicated that humans used mental rotation, *Author for correspondence.

2 13 B. MAUCK AND G. DEHNHARDT whereas the reaction times of pigeons showed no linear increase with the angle of rotation. On the one hand, Hollard and Delius (1982) explained this rotational invariance by the pigeons ability to distinguish image and mirror-image as easily as arbitrarily different forms. While Lohmann et al. (1988) could not confirm this hypothesis, Delius and Hollard (1995) found evidence that pigeons discriminate mirror-images, relative to arbitrary shapes, more easily than do humans. On the other hand, Hollard and Delius (1982) as well as Delius and Hollard (1995) argued that the pigeons rotational invariance could have evolved in response to ecological demands. Birds use the ground as the horizontal reference plane while flying. This could have favoured the evolution of a special visual information-processing system that allows birds to recognise the landscape from the bird s-eye view in any orientation without any delay. Conversely, it is speculated that hominids may have secondarily lost this ability of efficient visual recognition regardless of relative orientations. Species living in an aquatic environment could use the water surface as a horizontal reference plane while diving. Pinnipeds, for example, can be observed making use of the dark silhouettes of prey contrasting with the bright water surface while hunting (Hobson, 1966). Furthermore, in visual discrimination experiments, seals and sea lions are often described as swimming upside down and on their side, which does not affect their choice accuracy. On the basis of such observations, Schusterman and Thomas (1966) hypothesized that visual perception in these marine mammals might be different from that of terrestrial mammals. We therefore wondered whether, during the course of evolution, ecological demands could have triggered an information-processing system similar to that suggested for pigeons, resulting in an equivalent rotational invariance in mental rotation tasks. Results that coincided with those found by Hollard and Delius (1982) would indicate a convergent evolution of informationprocessing systems. Materials and methods Subjects Owing to the scant availability of suitable test animals as well as the lengthy preparation period required for such animals, the present investigation is a case study. It was conducted at the Dolphinarium Münster, Germany, using a 6-year-old male California sea lion (Zalophus californianus Lesson). The animal was experimentally naive but, apart from the experiments, it was trained for the daily shows at the dolphinarium. Experiments were performed during the morning hours in two sessions, before and after the first show. Because the animal was fed for the last time each day in the late afternoon, there was a natural food deprivation of approximately 16 h before the first session started. Experiments were performed in a resting pool that allowed the separation of the subject from the other sea lions and dolphins kept at the dolphinarium. Stimuli and test apparatus Twelve two-dimensional stimuli similar to those of the study by Hollard and Delius (1982) were used for testing reaction times, and ten additional stimuli were used in the course of acquisition (Fig. 1). A test stimulus consisted of nine black squares (27 mm 27 mm) attached to each other at their sides and forming an asymmetrical shape. These shapes and their mirror-images were computer-designed, rotated by various multiples of 3, and printed in the centre of a white stimulus card (21 cm 25 cm). A diameter of 17 cm was not exceeded when shapes were rotated, and each shape occupied 12 % of the area of the stimulus card. The stimulus cards were shrinkwrapped in foil to protect them from water. In contrast to the study of Hollard and Delius (1982), stimuli were rotated both clockwise and counter-clockwise with respect to the previously shown upright sample shape; rotations of more than 18 are therefore regarded as smaller angles of the opposite direction. The computer-controlled experimental device was designed to present stimuli in a successive two-alternative matching-tosample procedure. The apparatus was positioned on a dry platform at the edge of the pool and could easily be reached by the animal (Fig. 2). At a distance of 1.5 m from the platform, a stationing hoop was installed immediately above the water surface. The test apparatus consisted of a black polyvinylchloride (PVC) board with three Perspex windows side by side in the lower part. The bottom edge of each window was approximately cm above the water surface. Behind each window was a halogen light (75 W) installed in a box constructed of opaque PVC. Stimulus cards could be mounted reversed in front of the windows. A stimulus was only visible when the respective stimulus card was illuminated from behind. With the light in the box turned off, the window appeared to be a white sheet. Above the right-hand and lefthand windows, light barriers were installed, with their infrared beams running vertically at a distance of approximately 1 cm in front of the stimulus cards. Breaking of the light barrier was detected by the computer and was used during a trial to switch off the stimuli and to record the animal s reaction time and choice, thereby functioning as a touch-screen device. The test apparatus was connected to a control unit sited in the vicinity of the experimenter. The control unit was used to start a trial and revealed information about the animal s response (correct choice or error). The control unit was connected to a portable PC set up in a room next to the experimental chamber. Customdesigned software was used to control the hardware and to record the animal s reaction time and response. Reaction time could be measured with an accuracy of.5 s. Experimental procedure At the beginning of a trial, the stimulus cards were mounted reversed in front of the three windows of the apparatus. Following a hand gesture, the animal positioned its head in the stationing hoop, facing the apparatus (Fig. 3A). In order to avoid giving the animal any cues, the experimenter hid behind the apparatus as soon as the animal reached its position in the

3 Mental rotation in a sea lion 1311 stationing hoop. A trial was started by the experimenter by pressing a button at the control unit, whereupon the computer switched on the light behind the sample in the middle of the apparatus. After the sample had been shown for 5 s, the computer switched it off and the two comparison stimuli were presented without delay. One comparison stimulus represented the image of the previously shown sample, while the other was its mirror-image. In mental rotation trials, both comparison stimuli were rotated in the same direction by a multiple of 3. The sea lion was rewarded for responding to the image of the sample. The appearance of the two comparison stimuli was the signal for the sea lion to choose. At the same time, the computer started to measure the reaction time. After leaving the hoop, the animal was asked to approach the apparatus and to press its snout against one stimulus card, thereby breaking the infrared light beam (Fig. 3B). The computer switched off all stimuli and recorded the animal s reaction time, while the control unit showed whether the response was correct. Correct choices were rewarded by a fish (Sprattus sprattus), but there was no punishment for incorrect choices. Sessions were composed according to pseudorandom schedules (Gellerman, 1933) concerning the presentation of comparison stimuli at both positions of the apparatus and the sequence of test stimuli. A session consisted of 24 trials. Learning criterion was defined as the animal s performance of at least 8 % correct choices (χ 2 -test, P<.1) in at least two successive sessions. Nevertheless, in order to establish the sea lion s performance during acquisition, more sessions were sometimes conducted after the animal had reached the criterion. Since the animal was experimentally naive, it had to become acquainted with the matching procedure as well as with image/mirror-image discriminations before tests with rotated shapes could be performed. For this reason, the study was subdivided into various phases of acquisition and testing. Results Acquisition of matching and image/mirror-image discriminations Training on the matching procedure was started by presenting the animal with two shapes (circle versus angular shape, nos 1 and 2 in Fig. 1) that were judged to be highly discriminable from each other. After a strong side bias during the first four sessions (resulting in 5 % correct choices, Fig. 4A), the sea lion showed a steady improvement in performance and exceeded 8 % correct choices in the tenth session. After the twelfth session, the animal s performance remained stable at greater than 85 % correct choices. The addition of a third stimulus (no. 3, triangle), which was paired against each of the initial stimuli, had only a minor effect on the animal s performance (Fig. 4B). The results of the next phase of acquisition, in which the animal was required for the first time to perform image/mirrorimage discriminations, are shown in Fig. 5. Two asymmetrical shapes (nos 4 and 5) and their mirror-images were used as stimuli in their normal upright orientation, both resembling those used later in tests with rotated shapes. With these new discrimination requirements, choice accuracy fell to chance level during the first two sessions, but then (with one exception) showed a steady increase until the sea lion reached criterion in sessions /11 and, after a small decline, in sessions 13/14 (Fig. 5A). We then replaced shapes 4 and 5 by eight novel ones (nos 6 13, Figs 1, 5B), all being equally represented during a session. As before, these shapes were paired against their mirror-images and were shown only in their normal upright orientation. This increase in complexity of the discrimination task again led to a decline in choice accuracy (Fig. 5B). Only after the nineteenth session did the sea lion s performance remain consistently above 8 % correct choices. Up to this stage of the experiment, the animal had seen all shapes and their mirror-images in their normal upright orientation. Before tests with rotated stimuli could be started, the sea lion had to become acquainted with the discrimination of such stimuli. For this purpose, shape no. 6 was presented not only in the orientation but also rotated by 3 and in both directions. The other seven stimuli (nos 7 13) continued to be shown exclusively in their normal upright orientation. While performance in non-rotation trials generally surpassed that of rotation trials during the first five sessions, this discrepancy in choice accuracy disappeared during the next five sessions (Fig. 6). Finally, the sea lion performed at greater than 87.5 % correct choices in both types of discrimination task. Subsequently, in addition to shape 6, Fig. 1. The stimuli used in the course of acquisition and during testing.

4 1312 B. MAUCK AND G. DEHNHARDT Control unit Mirror A Detector of infrared barrier Reflector of infra-red beam Presentation of the sample Stationing hoop Computer connection Box with halogen lamp Fig. 2. Schematic drawing of the experimental apparatus. B shapes 4, 5 and 14 were also rotated by 3,, 9 and 1. In the course of sessions, the animal was presented with tasks of increasing difficulty with regard to the angle of rotation (results not shown). The final performance of % correct choices in rotation as well as non-rotation trials was considered to be a good basis for the subsequent measurement of reaction times. Measurement of reaction times Testing was subdivided into six test series of 8 12 sessions each (Fig. 7). In each series, two stimuli were used which were unknown to the animal except in their normal upright orientation. The animal was familiarised in a few sessions before testing started with the normal upright orientation of novel stimuli, which had been presented neither at orientation nor rotated (nos 12, 13, 17 22). Sixty-one test sessions were performed, each consisting of trials. Rotation of stimuli in both possible directions (clockwise and counterclockwise) was well-balanced and the sequence of test stimulus presentation was determined according to pseudorandom schedules (Gellerman, 1933). In order to determine a mean reaction time as reference in every series, up to trials with stimuli in the normal orientation ( ) were interspersed in every session. The animal s performance was above chance (χ 2 -test, P<.5) in of 61 sessions; in 5 sessions, performance was 8 % or greater of correct choices (χ 2 -test, P<.1, Fig. 7). In all but one test series, performance was worst in the first session, but clearly improved in the second session. No significant preference for one direction of rotation could be detected from the number of correct choices (χ 2 -test, P<.5). Mean error rates and mean reaction times with standard deviations for correct responses were analysed for every test series and summarised in an overall evaluation as a function of the absolute angle of rotation (Fig. 8A,B). In spite of the increasing mean error rate from less than % at 3 to Fig. 3. The experimental procedure. During presentation of the sample, the animal was stationed in a hoop (A). After being presented with the comparison stimuli, the animal made its choice by pressing its snout against one of the shapes (B). Photograph taken by H. Müller-Elsner. approximately 3 % at 9, before it decreased again at higher angles of rotation (Fig. 8A), performance was always significantly above chance (χ 2 -test, P<.5). Mean reaction times were calculated from correct choices in 439 trials ( ), 126 trials (3 ), 125 trials ( ), 126 trials (9 ), 281 trials (1 ), 283 trials (15 ) and 88 trials (18 ). Although data points indicate a sigmoid curve with a slight decline in reaction time for rotations of 15 and 18, linear regression analysis yielded a significant correlation (r=.873, P<.5) between mean reaction time and absolute angle of rotation (Fig. 8B). This correlation was unaffected in separate analyses of reaction times for clockwise and counterclockwise rotations (clockwise, r=.76, P<.5; counterclockwise, r=.9, P<.1). Discussion The first basic requirement for testing the model of mental rotation was the animal s success in performing matching-tosample tasks. The sea lion mastered the initial training problems with little difficulty, and its performance remained

5 Mental rotation in a sea lion 1313 Correct choices (%) A Number of sessions Fig. 4. The animal s acquisition of the matching rule. (A) Performance during training with two stimuli. (B) Performance after adding a third stimulus. well above chance in sessions with novel stimulus configurations and comparable with that of the pigeons in the study by Hollard and Delius (1982). Unlike Hollard and Delius, we do not conclude from this performance that the sea lion applied a concept-like matching rule (same different or identity concept) for solving mental rotation problems. For the interpretation of such a generalised matching concept, a sufficiently large sample size of first-trial data is necessary (Thomas and Noble, 1988; Oden et al. 1988; Schusterman and Kastak, 1993), which most experiments on mental rotation do not provide. Although California sea lions have been shown to fulfil this first-trial criterion in concept formation experiments (Hille, 1988; Kastak and Schusterman, 1994), this ability is not essential for solving mental rotation problems. On the contrary, the constant use of the images of the test shapes as sample and S+, while their mirror-images were always designated as S, may have favoured the formation of stimulus-specific rules rather than a concept of same or different. Furthermore, the use Correct choices (%) A B Number of sessions Fig. 5. Acquisition of mirror-image discriminations. (A) Performance during training with two asymmetrical shapes. (B) Performance after replacing the two initial shapes with eight new ones. B Correct choices (%) Number of sessions Fig. 6. Performance after introducing a rotated stimulus., correct choices in all trials;, correct choices in rotation trials only;, correct choices in non-rotation trials only;, stimulus used in rotation trials. of a generalised matching concept and the use of stimulusspecific rules are not mutually exclusive (Roitblat and von Fersen, 1992), so that the sea lion could have used both strategies simultaneously. Whichever discrimination rule a subject applies to a mental rotation task, as long as it maintains a high level of performance, the nature of the rule should not affect reaction times. The sea lion also complied with the second basic requirement for this study in reliably performing image/mirrorimage discriminations, which cannot be taken for granted in animals. Pigeons have much more difficulty in discriminating mirror-image patterns than discriminating arbitrarily different pairs of patterns (Lohmann et al. 1988). They find mirrorimage patterns especially difficult to discriminate if the patterns are reflected along their vertical axis (Todrin and Blough, 1983). However, Delius and Hollard (1995) found evidence that pigeons at least in comparison with humans have less difficulty with mirror-images than with arbitrary shapes. Regarding primates, bushbabies (Galago senegalensis) have been shown to be greatly confused by mirror-image discriminations (Sanford and Ward, 1986), whereas baboons (Papio anubis) have little difficulty in solving such tasks (Hopkins et al. 1993). Our sea lion also had little difficulty in performing mirror-image discriminations. Nevertheless, during testing with rotated stimuli, which can be assessed as an additional source of difficulty, performance was worst in the first session in all but one series. According to D Amato et al. (1985), low performance levels in first sessions in matching-to-sample tasks can be explained by the so-called novelty effect, a disruptive, neophobic response of subjects. Transfer criterion is therefore often determined as in the

6 1314 B. MAUCK AND G. DEHNHARDT 9 Correct choices (%) 8 7 Fig. 7. Performance during the six test series. Rotated test shapes and angles of rotation are shown below the respective data curves. 5, 3, 3, 1, 1, 1, 1, 9, , 18 15, 18 3 Number of sessions 4 5 study by Hollard and Delius (1982) neglecting the first session after a change of stimuli. Although our sea lion s performance seems to be impaired by a novelty effect, choice accuracy differed significantly from chance level in all but one of the first sessions with novel stimulus configurations. While Schusterman and Thomas (1966) demonstrated, even before the phenomenon of mental rotation had been described, that a California sea lion readily recognizes shapes irrespective of their spatial orientation, the present results show that this ability remains unaltered when complex image/mirror-image discriminations are required. As predicted by the model of mental rotation, the animal s mean reaction times increased linearly with angular disparity. The overall reaction time is composed of both the time it takes the animal to approach the apparatus and the time used in decision-making. Since our sea lion had to cover a comparatively long distance from its stationing hoop to the test board, its overall reaction times compared with those of human subjects or pigeons (Hollard and Delius, 1982) were rather long. However, since the time it took the sea lion to approach the apparatus can be assumed to be relatively constant, the increase in overall reaction time may be ascribed to an increasing time required to make a decision. As in many other studies on mental rotation (Just and Carpenter, 1976; Shepard and Cooper, 1982; Folk and Duncan Luce, 1987; Kail, 1991; Corballis and Manalo, 1993; Corballis and Sidey, 1993), the sea lion s reaction times deviate from linearity at some angles of rotation. Although, at first glance, a sigmoid curve seems to provide a better fit to the data presented in Fig. 8B, a decrease in reaction time at angles of 15 and 18 can be explained by the model of mental rotation. Shepard and Cooper (1982) reported that, beyond 18, reaction times are bimodally distributed, with the upper mode corresponding to the linear extrapolation of the reaction-time function to angles larger than 18 and the lower mode corresponding to the linear extrapolation of that function backwards to a point at the same distance from 18. This suggests that reaction time is not necessarily determined by the angular disparity between two stimuli but rather by the particular direction the long or the short way that the subject takes to mentally rotate a stimulus. Furthermore, a subject might change its direction of mental rotation during a trial for two reasons: either when it recognises that the other way round would be shorter, or when it recognises that mental rotation of a particular asymmetrical stimulus would be easier in one of two possible directions. Taking this into consideration, reaction times that are shifted upwards are to be expected, especially for higher angles (below 18 ), while a switch in direction of mental rotation would seldom occur at 18, because at this angle it takes the same Errors (%) Time (s) A B Angle of rotation (degrees) Fig. 8. Overall evaluation of the animal s performance and reaction time. (A) Mean error rate as a function of the angle of rotation. (B) Mean reaction times (±S.D., N= ) as a function of the angle of rotation.

7 Mental rotation in a sea lion 1315 time to rotate the shape in either direction. Although these arguments could explain deviations from linearity for some angles, a case study such as this one cannot prove these considerations. The rotational invariance found in pigeons and the nonincreasing reaction time function of baboons when they see shapes in their left optical hemifield (Vauclairs et al. 1993) are assumed to be adaptations which have arisen phylogenetically because of the demand to operate visually on a horizontal reference plane (Hollard and Delius, 1982; Delius and Hollard, 1995). In spite of similar ecological demands on pinnipeds, which use the water surface as the horizontal reference plane, we could detect no rotational invariance in our sea lion. In fact, our data can be explained assuming a mental rotation of an image-like representation of visual stimuli, a result that is normally obtained in experiments with human subjects. An image-like representation of visual information in California sea lions has also been concluded from artificial language comprehension tests (Schusterman and Krieger, 1986), in which the animals transformed gestural signs referencing specific object properties into image-like representations of those objects. Obviously, ecological demands such as a horizontal reference plane are not necessarily correlated with the evolution of information-processing systems that facilitate a rotational invariance. However, given the variety of methods used in studies on mental rotation, it should be asked whether certain methodological details could trigger a rotational invariance. Besides differences in the intensity of training, our study differed from that of Hollard and Delius (1982) in the way in which the stimuli were rotated. We demanded from our animal mental rotation in both possible directions by presenting it with stimuli which were rotated clockwise as well as counterclockwise with respect to the previously shown sample shape. In contrast, the stimuli used in the study of Hollard and Delius (1982) were rotated only clockwise with respect to the sample. Assuming that the comparison stimuli are to be rotated back to the normal upright position of the sample, the pigeons would have had to perform a counterclockwise mental rotation. Delius and Hollard (1995) also varied the angle of the sample shapes, whereas the comparison shapes were presented in the normal upright orientation. At first glance, this suggests that subjects in this case would have had to perform a clockwise mental rotation, rotating the comparison stimuli back to the sample s orientation. Nevertheless, the use of a simultaneous testing procedure as well as the growing familiarity with stimuli in their normal upright orientation may have favoured the opportunity to mentally rotate the sample instead of the comparison stimuli, resulting in a counterclockwise rotation as well. With regard to these differences concerning the direction of mental rotation it is interesting to consider the extent to which both cerebral hemispheres are involved in visuospatial processes. While, in general, studies which tried to estimate the nature of human hemispheric specialisation for mental rotation have produced inconsistent results (e.g. Ornstein et al. 198; Deutsch et al. 1988; Fischer and Pellegrino, 1988; Dittuno and Mann, 199), the results from those that examined the involvement of both hemispheres in clockwise and counterclockwise mental rotation are more consistent. Burton et al. (1992) showed that counterclockwise rotation was processed more efficiently by the left hemisphere/right visual field, coinciding with the results of Corballis and Sergent (1989). Cook et al. (1994) found a more efficient hemispheric cooperation with the left hemisphere taking the part of active manipulation of a mental image, while the reference role is performed by the right hemisphere. During the past two decades, various studies have also shown a strong cerebral lateralization in the visual system of pigeons. In most cases, a dominance of the left hemisphere/right visual field was found for certain visual tasks (Güntürkün, 1985; Güntürkün and Kesch, 1987; von Fersen and Güntürkün, 199). However, until now, there has been no study that examined the influence of this visual lateralization in pigeons on the ability to perform mental rotation tasks. Certainly, it would be interesting to determine whether the pigeons dominance of the left hemisphere favours performance in tasks that demand counterclockwise rotation, as might be supposed bearing in mind the results of Burton et al. (1992). If this hypothesis were to be confirmed, it could explain the consistently fast reaction times found for pigeons. In the present study, we provide the first evidence for mental rotation in a non-primate species. The appearance of this mental rotation effect in spite of similar ecological demands for birds and pinnipeds could also be ascribed to the fact that the horizontal reference plane is not as important to pinnipeds as has been concluded from their aquatic life-style. However, if ecological demands are responsible for the phenomenon of rotational invariance in pigeons, it should also be detected in other avian species. Appropriate experiments are currently being carried out. 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