Stereotypic Behavior of a Female Asiatic Elephant (Elephas maximus) in a Zoo Andrzej Elzanowski & Agnieszka Sergiel Published online: 04 Jun 2010.

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3 JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 9(3), Copyright 2006, Lawrence Erlbaum Associates, Inc. BRIEF RESEARCH REPORTS Stereotypic Behavior of a Female Asiatic Elephant (Elephas maximus) in a Zoo Andrzej Elzanowski and Agnieszka Sergiel Department of Zoology University of Wroclaw This study recorded daytime behavior of a female Asiatic elephant at the Municipal Zoo, Wroclaw, Poland, in both an indoor pen and an outdoor paddock as continuous scan sampling for 140 hr, over 35 days in 1 year. Stereotypic sequences involved bouts of highly repetitive stereotypic movements and much more variable interbout behavior. The study found both stereotypic movements, nodding and body (corpus) swaying, were asymmetric, accompanied by protraction of the right hind leg and to-and-fro swinging of the trunk. The elephant spent 52% of the daytime in stereotypic movements, 3.5 times the level reported for females in other zoos groups. The share of time devoted to stereotypic behavior was lowest in the summer when the elephant was regularly released to the paddock and highest in the late fall after she had stayed in the pen after months of days outside. This suggests that changes in the management routine enhance stereotypies. Comparing the summer and winter stable management periods, stereotypies were much more frequent in the indoor pen than the outdoor paddock, suggesting that the confinement to a barren pen contributed to the observed levels of stereotypies. Elephants kept in circuses and zoos are known to perform several stereotyped movements described as weaving, swaying back and forth, nodding, head bobbing, trunk (proboscis) swinging, pacing, and occasional lifting of feet (Clubb & Mason, 2002; Friend & Parker, 1999; Gruber et al., 2000; Kiley-Worthington, 1990; Kurt & Garai, 2002; Kurt & Hartl, 1995; Rees, 2004). However, slight bobbing of the head and body, occasionally accompanied by lifting of one leg Correspondence should be sent to Andrzej Elzanowski, Department of Zoology, University of Wroclaw, 21 Sienkiewicz Street, Wroclaw, Poland. elzanowski@biol.uni.wroc.pl

4 224 ELZANOWSKI AND SERGIEL (or sometimes by alternate lifting of a hind leg and a foreleg) but without trunk swinging, was observed in resting, wild, Asiatic elephants (McKay, 1973). Transient weaving was recorded among African elephants in social situations, possibly as an expression of submission and apprehension (Langbauer, 2000). Most of the published descriptions of stereotypies in elephants are lacking in precision, especially with respect to the distinction between weaving and nodding. Although Rees (2004) defined weaving roughly in accord with its usage for equine behavior, as swaying head from side to side while transferring the weight from one fore leg to the other, and swinging the trunk (p. 38), Friend (1999) defined it as swinging to-and-fro movement of body or head (p. 78) and did not record any movement with a transverse component but listed a variety of behaviors (chain pulling and trumpeting) that are seldom, if ever, considered as stereotypies by others. Stereotypies were studied predominantly in the circus elephants who were at least temporarily chained or shackled (Friend, 1999; Gruber et al., 2000; Johnson, 1990; Kiley-Worthington, 1990; Schmid, 1995). Friend (1999) observed weaving in the majority of observed female elephants and head bobbing as an exclusive alternative in a few of them. Kurt and Garai (2002) recorded stereotypies in 44 Sri Lankan elephants who were kept under various conditions (in temples, jungle camps, circuses, and an orphanage), but chained for the night, and described the ontogeny of stereotypic movements that were predominantly to and fro ( parallel to body axis ) in the young and then replaced by predominantly vertical movements and nodding. Friend and Parker (1999) and Gruber et al. (2000) showed that younger elephants are more likely than older elephants to show stereotypic activity. Picketed elephants spend much more time stereotyping than elephants free to move in a paddock (Schmid, 1995) or a pen (Friend & Parker, 1999; Gruber et al., 2000). There are only a few studies of stereotypies in zoo elephants who, in contrast to the majority of circus elephants, are not tethered and thus may be expected to spend less time stereotyping. Koene (1995) studied time budgets in Asiatic elephants in the zoo and observed that stereotypies were more likely to be found in small enclosures with few animals (p. 280). Clubb and Mason (2002) observed stereotypies, mostly weaving, in 9 out of 21 female zoo elephants. They recorded considerable individual variation of stereotypy levels but, on the average, much higher frequency in Asiatic as compared to African elephants. Considerable individual variation of stereotypies has also been reported among zoo elephants by Rees (2004) for Asiatic elephants and by Wilson, Bloomsmith, and Maple (2004) for African elephants. Rees showed that the frequencies of stereotypies are inversely correlated with ambient temperature and body mass. Wilson et al. demonstrated the impact of management schedules on the frequency of stereotypies. In a similar vein, here we present a 1-year study of the impact of alternating housing regimes and feeding schedules on the stereotypic behavior in an Asiatic elephant kept single in a zoo.

5 ZOO BEHAVIOR OF AN ASIATIC ELEPHANT 225 The Subject and Her Housing METHOD Observations were carried out in the Municipal Zoological Garden of Wroclaw, Poland, from December 2002 through December The subject was a female Asiatic elephant (Elephas maximus) born in She has lived here since 1981 and has remained single for about the last 3 years. She is kept in an indoor pen and, weather permitting, released for the day to an outdoor paddock. She may leave the pen spontaneously but has to be lured back to the pen with food. When moving between the pen and the paddock, she has no choice of backing off because the pen door is shut behind her. Feeding time was about 1:00 p.m. (with up to 1-hr delays) when she stayed indoors 24 hr per day, and at 3:00 p.m. or later when she was let outside for the day. She was fed when she returned to the pen. The indoor pen of 30 m 2 has a floor of bricks, walls of iron bars, and no elements of environmental enrichment. It is separated from visitors by a system of heating pipes and an iron railing. There was no possibility of contact with the neighboring animals as the next pen was kept empty to serve as a spare space. The elephant was exposed to acoustic and olfactory stimuli only. The temperature was maintained in the range of 15 to 18 C. The paddock of 650 m 2, with a northwest exposure and thus afternoon sunshine, has ground covered by sand; only concrete covers the periphery. The paddock is surrounded by a dry moat with iron spikes and electric wire and is separated from one enclosure by a high wall and from another by a wire fence permitting a view of the neighboring white rhinoceros and dwarf hippopotamus. The paddock is equipped with a log for play and manipulation. Data Collection All the elephant s activities were scan-sampled at constant intervals (Martin & Bateson, 1993). As stereotypic behavior, we recorded sequences of bouts of rhythmically repeated movements together with the intervening short breaks (up to a few seconds) for relaxed interbout behavior (see Results), as long as the elephant remained on the same spot. Moving to another spot ended a stereotypic sequence. Stereotypic behaviors were videotaped with a Sony CCd TR501E camera and then analyzed in slow motion. The observations were carried out from 9:00 a.m. until 1:00 p.m. for 35 days, which amounts to the total observation time of 140 hr. The observations were scheduled as five 7-day samples, each representing a unique combination of the season and housing:

6 226 ELZANOWSKI AND SERGIEL 1. Spring in the pen (S/I). 2. Spring in the paddock (S/O). 3. Early fall in the paddock (F/O). 4. Late fall in the pen (F/I). 5. Winter in the pen (W/I). The early fall, late fall, and winter samples were taken on 7 consecutive days (F/O: September 20 to October 20; F/I: October 23 to November 14; W/I: December 2 to December 19). In the spring (March 12 to April 14), when the weather-dependent choice of the keepers between the paddock and the pen was unpredictable, the observations were carried out intermittently to obtain a 7-day sample for each the paddock (S/O) and the pen (S/I). Statistical Analyses The results were analyzed using the STATISTICA 6.0 package (Statsoft, 2001) with respect to the total duration of stereotypic behaviors at various times of the day (min/hr), the duration of single bouts of a stereotypic movement (minimum, maximum, and modal value), and the incidence of each stereotypic movement throughout the entire observation period. Statistical interpretation was based on nonparametric tests. The Friedman test, which verifies the variation in a group by the scheme of tied variables, was used to analyze the differences between medians from the sums of minutes devoted to stereotypic behaviors in each hour of observation. We applied a post-hoc analysis multiple comparisons (Nemenyi test for Friedman s analysis of variance) to determine which periods differ in a statistically significant way (Friedman s test alone shows that some differences are significant but does not specify them). The amount of time devoted to stereotypic movement at specific times of the day was analyzed for each sample separately (S/I: p =.02000; S/O: p =.01654; F/O: p =.82811; F/I: p =.30584; W/I: p =.00081). The p values show that the differences in frequency between consecutive hours of observation were statistically significant in samples S/I, S/O, and W/I. Following Rees (2004), a possible correlation between mean hourly temperatures and stereotypy levels in the two outdoor samples (S/O and F/O) was checked using the Spearman rank-order correlation test. RESULTS The observed stereotypic behavior involved bouts of complex asymmetric movements, rhythmically repeated about 18 times in one bout, and much more

7 ZOO BEHAVIOR OF AN ASIATIC ELEPHANT 227 variable, casual-looking, interbout behavior (Figure 1). A bout involved asymmetric nodding and body (corpus) swaying with a protraction of the right hind leg and to-and-fro trunk swinging. In the asymmetric nodding, the head was always tilted to the left while being raised and tilted to the right while being lowered. The body swayed to the right and slightly to the rear while the head was raised; the recovery movement of the body to the midline and slightly forward was accompanied by lowering of the head. The body swaying was apparently effected by asymmetric bowing (possibly with some torsion) of the presacral backbone with the hindquarters remaining stationary except for a slight leaning to the right. The latter may have been facilitated by the protraction of the right hind leg, which usually occurred after a few initial movements. The right, protracted leg showed slight flexion and extension movements in concert with the right-leaning and straightening of the back. The trunk was swung FIGURE 1 The studied female elephant engaged in the bout (top) and the interbout behavior (bottom) of a stereotypic sequence. Note the protracted right hind leg allowing her to sway the corpus to the right during the bout and the ample swaying with the trunk during the interbout.

8 228 ELZANOWSKI AND SERGIEL backward while the head was raised and forward while the head was lowered. In the paddock, the stereotypic to-and-fro movement of the trunk was combined with some tossing of sand over the back, making the trunk swinging wider and less regular than in the pen. The bouts of stereotypy were interrupted by variable interbout behavior that usually started with straightening (retraction) of the protracted hind leg, then stepping either forward or backward, followed by some turning around and, sometimes, by raising and protracting the front foot. In the paddock, the interbout behavior involved a lot of wide movements of the trunk with generous sand tossing. In the pen, the trunk movements were directed mostly at the door. Overall, the observed elephant spent 52% of the total observation time in stereotypic movements. However, the share of time devoted to stereotypic behavior varied significantly between the samples and was lower for the outdoor than for the indoor samples (Figure 2). The time devoted to stereotypic behavior was by far the lowest in the early fall (F/O) when the elephant was regularly released to the paddock, and much higher close to the lowest indoor value in the S/O sample when the releases to the paddock were irregular. There are also highly significant differences (p =.01701) between the three indoor samples. The highest levels of stereotypy occurred in the S/I sample when the elephant had to stay in the pen on some days but not on others, depending on the weather. The second highest levels were observed in the F/I sample, when she had to stay in the pen after a long summer period of going out to the paddock. The lowest hourly share of stereotypies performed indoors was observed in the winter (W/I) after the elephant got used to staying in the pen all the time. The daily dynamics of observed stereotypies were similar in all three indoor samples (S/I, F/I, W/I) with highest frequency between 10:00 a.m. and 1:00 p.m. In contrast, the two outdoor samples differ dramatically in this respect. In the spring (S/O), when the days outdoors alternated with the days indoors, the maximum amount of time spent on stereotypies was between 12:00 p.m. and 1:00 p.m., immediately before the feeding time on the indoor schedule (Table 1). In the fall (F/O), after the entire summer of spending daytime outdoors, the maximum hourly median value was between 2:00 p.m. and 3:00 p.m., within 1 hr immediately preceding the return to the pen and feeding. The difference between the two outdoor samples in the amount of stereotypies from the fourth hour of observation (12:00 p.m. to 1:00 p.m.) is statistically significant (Wilcoxon signed ranks test: Z = 2.201,p= ). There was no correlation between mean hourly temperatures and stereotypy levels for these two samples (Spearman rank-order correlation test: S/O: r = , p = ; F/O: r = , p = ). The duration of single stereotypic sequences (Table 2) roughly correlated with their overall share in the time budget except for a slightly shorter duration in the W/I sample than on the days spent outdoors in the spring (S/O), when the elephant had to wait through the feeding time as expected on the indoor schedule.

9 FIGURE 2 The share of time devoted to stereotypic movements in each of the five 7-day samples (5 42 hr): S/I = spring/indoors; S/O = spring/outdoors; F/O = fall/outdoors; F/I = fall/indoors; W/I = winter/indoors. A post-hoc analysis to Friedman s analysis of variance confirmed significant differences for F/O vs. F/I, S/O vs. S/I, S/I vs. F/O, and S/O vs. F/I. The module of difference was greater than C kw value in all these samples. Sample TABLE 1 Time Used for Stereotypic Sequences by the Female Elephant 9:00 to 10:00 10:00 to 11:00 11:00 to 12:00 12:00 to Averaged 13:00 a Mdn S/I F/I W/I S/O F/O Note. Time in medians givein in minutes. Based on Friedman s analysis of variance. All differences between samples are highly significant (p <.00). S/I = spring/indoors; F/I = late fall/indoors; W/I = winter/indoors; S/O = spring/outdoors; F/O = early fall/outdoors. a Indoor feeding time. 229

10 230 ELZANOWSKI AND SERGIEL TABLE 2 Duration of Single Stereotypic Sequences Observed in the Female Elephant in 7-Day (42-Hour) Sample Hour S/I S/O F/O F/I W/I Averaged Mdn 9:00 to 10: :00 to 11: :00 to 12: :00 to 13:00 a Averaged Mdn Note. Duration in medians given in minutes. S/I = spring/indoors; S/O = spring/outdoors; F/O = early fall/outdoors; F/I = late fall/indoors; W/I = winter/indoors. a Indoor feeding time. DISCUSSION There are two novelties in comparison to a few published descriptions in the stereotypic behavior of elephants (Friend, 1999; Kiley-Worthington, 1990; Kurt & Hartl, 1995; Rees, 2004). One is a clear distinction between the bouts and the interbout behavior (Figure 1) that explains inconsistencies in the published descriptions. In addition, we observed the raising of the front leg (Kurt & Hartl, 1995) or engaging in two activities simultaneously (Friend, 1999) only during the interbouts. The other is a pronounced asymmetry of the stereotypic bout movements that makes such descriptive terms as weaving and nodding inaccurate without a qualifier. Although speculative interpretations of a behavior observed in just one individual would not be warranted, we believe that further detailed descriptions of elephant stereotypies will help compare them to natural behaviors and thus better explain their causation. The figure of 52% of the total observation time spent in stereotypic movements is high. It is close to that observed in the neonates who were kept for at least 3 months in a Sri Lankan orphanage tethered for most of the time (Kurt & Garai, 2002) and much higher than 14.8% calculated for Asiatic elephant females kept in groups in various zoos (Clubb & Mason, 2002). The lowest contribution of stereotypies to the daily time budget we recorded in the F/O sample amounted to 24%. Several factors probably contributed to the observed high levels of stereotypy. We have no data on social deprivation (Clubb & Mason, 2002) and fixed management schedule per se (Wilson et al., 2004). Our data suggest the impact of changes in the management schedule that occurred within our observation period and of the confinement to a barren indoor pen through the winter. The highest levels of stereotypic behavior in the S/I and F/I samples occurred concomitant with(s/i) or after(f/i) the changes of both the housing regime and feed-

11 ZOO BEHAVIOR OF AN ASIATIC ELEPHANT 231 ing schedule. This suggests an aggravating influence of the unfulfilled expectation of being released. In addition, the surge of stereotypies before the indoor feeding time (1:00 p.m.) in the S/I sample (Table 1) is best explained by the expectation of food that was delivered on this hour throughout the winter. There is good evidence that an expectation of feeding (Friend, 1999; Kurt & Hartl, 1995; Rees, 2004) or other events (Friend, 1999; Kurt & Garai, 2002) may evoke stereotypies in captive elephants probably because a captive individual has nothing to do about it due to restraint, artificial environment, or the individual s own impairment. No changes of management schedule were at play during the summer, ending with our F/O sample, and during the W/I stay. A comparison of samples from the two stable periods (Table 1) with dramatically different housing regimes suggests that the confinement to a small, barren, indoor space contributed to the observed levels of stereotypies in the W/I sample. However, the impact of winter confinement may have been aggravated by the lasting memories of having been released in the past. ACKNOWLEDGMENTS We gratefully acknowledge the cooperation of the Wroclaw Zoo personnel: Antoni Gucwinski, Director; Miroslaw Piasecki, Head of the Ungulate Section; Ewa Piasecka, Senior Assistant for Education; and the rest of the staff. We also thank L. Pasko for expert advice in statistics, A. Kowalski for discussion, and two anonymous reviewers for criticisms. The temperature data were provided by the Meteorological and Climatological Laboratory and Observatory of the University of Wroclaw. REFERENCES Clubb, R., & Mason, G. (2002). A review of the welfare of elephants in European zoos. Horsham, PA: RSPCA. Friend, T. H. (1999). Behavior of picketed circus elephants. Applied Animal Behaviour Science, 62, Friend, T. H., & Parker, M. L. (1999). The effect of penning versus picketing on stereotypic behaviour of circus elephants. Applied Animal Behaviour Science, 64, Gruber, T. M., Friend, T. H., Gardner, J. M., Packard, J. M., Beaver, B., & Bushong, D. (2000). Variation in stereotypic behaviour related to restraint in circus elephants. Zoo Biology, 19, Johnson, W. (1990). The rose-tinted menagerie. London: Heretic. Kiley-Worthington, M. (1990). Animals in circuses and zoos: Chiron s world? Essex, England: Little Eco-Farms. Koene, P. (1995). The use of time budget studies in captive propagation and zoo biology. In U. Gansloßer, J. K. Hodges, & W. Kaumanns (Eds.), Research and captive propagation (pp ). Fürth, Germany: Filander Verlag.

12 232 ELZANOWSKI AND SERGIEL Kurt, F., & Garai, M. (2002). Stereotypies in captive Asian elephants A symptom of social isolation. In H. M. Schwammer, T. J. Foose, M. Fouraker, & D. Olson (Eds.), A research update on elephants and rhinos (pp ). Münster, Germany: Schüling Verlag. Kurt, F., & Hartl, G. B. (1995). Asian elephants (Elephas maximus) in captivity A challenge for zoo biological research. In U. Gansloßer, J. K. Hodges, & W. Kaumanns (Eds.), Research and captive propagation (pp ). Fürth, Germany: Filander Verlag. Langbauer, W. R. (2000). Elephant communication. Zoo Biology, 19, Martin, P., & Bateson, P. (1993). Measuring behaviour: An introductory guide (2nd ed.). Cambridge, England: Cambridge University Press. McKay, G. M. (1973). Behavior and ecology of the Asiatic elephant in southeastern Ceylon. Smithsonian Contributions to Zoology, 125, Rees, P. A. (2000). Are elephant enrichment studies missing the point? International Zoo News, 47, 303. Rees, P. A. (2004). Low environmental temperature causes an increase in stereotypic behaviour in captive Asian elephants (Elephas maximus). Journal of Thermal Biology, 29, Schmid, J. (1995). Keeping circus elephants temporarily in paddocks: The effect on their behaviour. Animal Welfare, 4, StatSoft. (2001). STATISTICA Version 6 [Data analysis software system]. Tulsa, OK: Author. Wilson, M., Bloomsmith, M., & Maple, T. (2004). Stereotypic swaying and serum cortisol concentrations in three captive African elephants (Loxodonta africana). Animal Welfare, 13,