― Short Report ―

Does oral stereotypy in captive giraffes decrease by feeding them evergreens and barks in winter?

Kota OKABE1＊, Ayumi KAWAMURA1, Hiroki FUKUIZUMI1, Kotone ISHIUCHI2, Chihiro KASE2,3

1Kyoto City Zoo, Okazaki Koen, Okazaki Hoshojicho, Sakyo-ku, Kyoto City, Kyoto 606-8333, Japan 2Chiba Institute of Science, 3 Shiomi-cho, Choshi, Chiba 288-0025, Japan 3Present address: Azabu University, 1-17-71 Fuchinobe, Chuo-ku, Sagamihara, Kanagawa 252-5201, Japan

*Corresponding author. E-mail address: [email protected]

Summary Recently, several zoos have aimed to improve the welfare of captive animals by adopting certain feeding enrichments, particularly to address oral stereotypy in giraffes. Research has revealed that the utilization of certain feeding enrichments, such as browsing enrichment, is effective for preventing oral stereotypy. However, feeding of browsing enrichment may be difficult in winter, although its effect is not evident in this season based on previous studies. Therefore, the weight of tree feed foraged by the giraffes and their behavior, including oral stereotypy, was observed in all seasons of tree feeding. Three giraffes were observed in the Kyoto City Zoo. No significant change was observed in the weight of foraged tree feed throughout the seasons, with a similar weight of food intake observed in all seasons. Although all giraffes expressed oral stereotypy, the behavior increased significantly in winter. Furthermore, the oral stereotypy frequency was not significantly correlated with the weight of foraged tree feed, suggesting that some other factor strongly influenced the frequency, such as the climate differing from that of the giraffes’ original habitat. Therefore, further research is required to elucidate the factors that cause oral stereotypy.

Keywords: giraffe, zoo, feeding enrichment, browsing, seasonal changes

Animal Behaviour and Management, 55 (4): 165-173, 2019 （Received 28 February 2019; Accepted for publication 7 September 2019）

Introduction (2016). Therefore, they must be bred according to a captive management plan, which requires Zoo animals require different stimuli under an appropriate environment to encourage stable captive conditions to prevent stereotypy exhibited captive reproduction. in poor environments (Mason & Latham, 2004). In the wild, giraffes eat trees and bushes of the In general, animals that exhibit stereotypy suffer Acacia spp; however, they forage for various other from lack of welfare. Therefore, zoo experts plants (Lamprey, 1963; Foster, 1966; Leuthold & and researchers are developing environmental Leuthold, 1972; Pellew, 1984a; Ciofolo & Pendu, enrichment, a new method to create more 2002; Parker & Bernard, 2005). A giraffe’s comfortable environments for zoo animals. The prime activity is foraging, which is necessary to method aims to increase behavioral variety, maintain its large body. For example, Leuthold improve the quality of rest, and reduce abnormal and Leuthold (1978) reported that on average, behaviors. eight males and four females foraged for 27% Giraffes are an endangered species native to and 53%, respectively, of each day in the Tsavo Africa declared as a vulnerable species by the East National Park, Kenya. According to Pellew International Union for Conservation of Nature (1984a; 1984b), giraffes forage for more than

165 Does oral stereotypy in captive giraffes decrease by feeding them evergreens and barks in winter?

10 hours and ruminate for more than 6 h a This study was conducted to acquire new day. Furthermore, they adapt to foraging for knowledge regarding giraffe husbandry by secondary branches with smaller leaves and barks evaluating feeding enrichment. Therefore, the (Berry, 1973; Dagg, 2014). Thus, giraffes are present study aimed to evaluate the following: (1) specialized in browsing. whether oral stereotypy in captive giraffes can In a zoo, a giraffe’s appetitive needs cannot be reduced by feeding them with evergreens and be easily fulfilled because it must consume an barks in winter and (2) the association between abundance of different types of leaves. As an oral stereotypy frequency and the weight of alternative to leaves, giraffes may eat food that leaves that a giraffe consumes. To answer these requires little time to consume, such as alfalfa, questions, the effect of feeding enrichment on grass hay, and low-fiber pellets (EAZA, 2006). seasonal change was observed. However, such feeding may increase their oral stereotypy. In a survey conducted in an American zoo, stereotypic behavior was observed in several Materials and Methods giraffes (Bashaw et al, 2001), prompting zoos to implement various environmental enrichments associated with feeding. For example, in the Animals and housing conditions Atlanta Zoo, nine types of enrichment feeders The giraffes at the mixed exhibit grounds of were constructed to slow down the giraffes’ the Kyoto City Zoo (Figure 1) were observed. intake of grain or alfalfa (Fernandez et al, The grounds have exhibited giraffes and 2008), aiming to reduce oral stereotypy. In Grévy's zebras (Equus grevyi) since 2013 and are Paignton Zoo, Baxter and Plowman (2001) surrounded by fences and a visitor area. There investigated the association between rumination is a visitor's passageway to the northeast of the and oral stereotypy in giraffes and showed that ground where visitors can observe at the same environmental enrichment by adding coarse hay height as the giraffes. The grounds have four to their existing diet changed their behaviors. Japanese Zelkova trees (Zelkova serrata) that The study reported that the time spent in oral provide shade and are surrounded by a fence. stereotypy was significantly reduced when the However, the giraffes can eat the leaves of these rumination time was increased. The feeding trees using their tongue. process of giraffes was investigated in Twycross The study subjects were two female (Mirai and Zoo, in the UK, which found that bundles of Mei) reticulated giraffes (Giraffa camelopardalis mature hawthorn branches could increase their reticulata) and one male (Yoshida) reticulated feeding time compared with barks and leaves from giraffe (Table 1). Mirai and Yoshida are related, willow and cherry branches (Dagg, 2014). With whereas Mei is a nonrelative. Yoshida was born regard to seasonal changes, Schmucker et al. in Kyoto City Zoo. The giraffes were exhibited (2010) observed oral stereotypy in four giraffes outdoors from approximately 09:00 to 16:00 by video recording them in the Cologne Zoo h each day and then housed together for the in Germany and found that they exhibited oral remaining day. The feeding enrichment assessed stereotypy at frequencies varying from 4.6% to in this study had been used for approximately 30.7% per winter day. Such activities significantly 10 years at the zoo and incorporated into the decreased in summer when the animals were fed ordinary management of the animals; all three by browsing. This illustrates a major issue for giraffes have been under this feeding management giraffes in European zoos: the leaves that they plan for at least 6 months. usually consume cannot be obtained because of the change in season (EAZA, 2006). Procedure Japanese zoos are currently lagging behind The giraffes were observed for 5 days per with regard to the scientific evaluation of season from May 9 to December 9, 2017 (Table 2). environmental enrichment. However, there have The zoo was open to visitors on all observation been attempts to improve the captive environment days. for zoo animals, including giraffes. Leaves are fed Each period, the type of trees, and the weight to giraffes throughout the year, particularly in of the branches, leaves and barks that were fed some zoos that combine deciduous and evergreen to the animals were recorded (Table 3). The trees. trees utilized in this study were bamboo-leaf

166 OKABE, KAWAMURA, FUKUIZUMI, ISHIUCHI, KASE

Figure 1. Schematic drawing of the mixed exhibit grounds of the Kyoto City Zoo.

Table 1. Details of the three giraffes observed estimated from day 2 to day 5 according to the in this study. length of the observer’s stay. When the giraffes were placed outside enclosure, besides branches, they were freely fed dry Lucerne hay and restrictedly fed a hay cube; when placed inside enclosure, they were oak (Quercus myrsinifolia), locust tree (Robinia restrictedly fed dry Lucerne hay, hay cube, and pseudoacacia), cherry blossom (Prunus yedoensis), dry pellets (Mazuri® Wild Herbivore Diet Hi- lacebark elm (Ulmus parvifolia), red bayberry Fiber, St. Louis, Missouri, USA); however, hay (Morella rubra), and glossy privet (Ligustrum was never completely eaten at night. The forages lucidum). The tree species that were fed varied were distributed among several places and were according to the season. While none of the never occupied by any particular giraffe. Water trees flowered in all seasons, the locust tree was available ad libitum. bore no leaves in winter. Before the tree feed The observation times were 09:00–11:00, was presented to the giraffe, its weight was 11:30–13:30, and 14:00–16:00 h. The behaviors measured on a spring balance scale. All tree recorded (Table 4) are the result of direct feeds were divided into two halves for daytime visual scans of all giraffes at 3-min intervals. feeding outside enclosure and nighttime feeding Furthermore, the oral stereotypy at 1-min inside enclosure. The weights of branches were intervals was recorded by the 1/0 sampling measured again after feeding and the weight method. The proportion of each behavior and the of tree feed eaten in a day was calculated. The frequency of oral stereotypy were calculated per weight of tree feed foraged by the giraffes was day; the mean proportion and frequency for each

Table 2. Details of the observation days periods.

167 Does oral stereotypy in captive giraffes decrease by feeding them evergreens and barks in winter?

season were used as the mean proportions and oral stereotypy frequencies, respectively.

Statistical analysis Significant changes in behavioral patterns, the oral stereotypy frequency per day and the percentage of foraged tree feed were evaluated by Steel–Dwass analysis. In addition, partial Pearson’s product–moment correlations were calculated to evaluate the association between the oral stereotypy frequency and the weight of foraged tree feed, obtained from only 12 days of observation data because of the corruption of the spring data. It is preferable to compare the weight of foraged tree feed and the oral stereotypy frequency per giraffe. However, the weight of foraged tree feed per giraffe was not measured, and the weight of foraged tree feed was calculated from weights measured before and after the giraffes were fed. Therefore, oral stereotypy frequency rate for each giraffe were summed for each day and compared with the total weight of foraged tree feed per day. All data are presented as means with 95% confidence intervals.

Results No significant change was observed in the weight of foraged trees throughout the seasons, with a similar weight of food intake observed in all seasons (Table 3). The utilization of each tree species changed according to the season; however, the weight of feeding did not significantly differ among each tree species. The change in behavioral patterns per day of each giraffe is reported in Tables 5-7. The resting behavior of all giraffes increased in summer. The feeding behavior of Mirai significantly changed only between spring and summer, whereas no significant change was observed in the other giraffes. Oral stereotypy was expressed by all giraffes. Using the 1/0 sampling method of oral stereotypy per day, significant differences were Table 3. Weights and types of tree species that were provided f or foraged by the giraffes. observed in all giraffes (Figure 2). Similar to behavioral patterns, the oral stereotypy frequency rate increased significantly in winter. No significant correlations were found between the oral stereotypy frequency rate and the weight of foraged tree feed (Figure 3).

Discussion The preferences of giraffes with regard to leaves were reported by Sauer et al. (1982). The browsing of leaves of different plant species

168 OKABE, KAWAMURA, FUKUIZUMI, ISHIUCHI, KASE

Table 4. Recorded behaviors and their definitions.

Table 5. Mean seasonal differences in the behavioral patterns of the giraffe Mirai assessed per day of each season using the scan sampling method

Table 6. Mean seasonal differences in the behavioral patterns of the giraffe Mei assessed per day of each season using the scan sampling method

Table 7. Mean seasonal differences in the behavioral patterns of the giraffe Yoshida assessed per day of each season using the scan sampling method

169 Does oral stereotypy in captive giraffes decrease by feeding them evergreens and barks in winter?

Figure 2. Oral stereotypy frequencies per day by 1/0 sampling method. Means followed by the same letters are not significantly different, based on P < 0.05.

Figure 3. Evaluation of associations between the oral stereotypy frequency rate per day and weight of foraged tree feed per day. by the giraffes is most significantly correlated 26.4%. Therefore, feeding on secondary branches with the crude protein content in both dry and and bark may be effective for foraging in a wet samples. The nutritional value of leaves of captive environment. certain tree species in Japan has been reported Oral stereotypy was expressed in all giraffes previously (Shiota et al., 2017), and the data at degrees that changed with the seasons. In shows that the crude protein content in the winter, oral stereotypy changed significantly locust tree and glossy privet are significantly in all giraffes based on 1/0 sampling. Previous higher than those in the bamboo-leaf oak and research (Schmucker et al. 2010) showed that oral red bayberry. Moreover, the nutritional value stereotypy frequencies decrease when giraffes of leaves does not significantly change between can browse in summer. Although, in winter, seasons. In the present study, the giraffes feeding and rumination did not significantly were fed leaves, secondary branches, and decrease in the present study. Furthermore, bark; therefore, it was difficult to compare the in the present study, the degrees of browsing results with those of previous studies about did not significantly change, and the weights of the nutritional value of leaves. However, the the browsed feed were similar throughout all utilization of the locust tree and glossy privet, seasons. These results shows may influence not which are high in crude protein, was relatively only browse feeding activity on the behavior of high, particularly in winter, when the trees had the giraffes. However, in this study, it was not no leaves. Moreover, the giraffes consumed the possible to completely assess the association barks of the locust tree, at rates that approached between the weight of foraged tree feed per

170 OKABE, KAWAMURA, FUKUIZUMI, ISHIUCHI, KASE day and daytime behavior because nocturnal Conservation, pp.260. Cambridge University behavior was not observed; therefore, this Press, Cambridge. should be examined in the future. Furthermore, EAZA Giraffe EEPs. 2006. EAZA husbandry rumination can be influenced because Baxter and and management guidelines for Giraffa Plowman (2001) reported that oral stereotypy is camelopardalis. pp.132. Arnhem, Netherlands. significantly reduced when rumination increases Fernandez LT, Bashaw MJ, Sartor RL, Bouwens by adding coarse-cut meadow hay to the daily feed N, Maki TS. 2008. Tongue twisters: feeding for giraffes. However, there were no significant enrichment to reduce oral stereotypy in giraffe. changes in rumination in all giraffes throughout Zoo Biology, 27, 200-212. all seasons; therefore, no evidence was found to Foster JB. 1966. The giraffe of Nairobi National confirm that the degree of rumination influences Park: home range, sex ratios, the herd, and giraffe behavior in this study. Therefore, it food. African Journal of Ecology, 4, 139-148. is indicated that some other factor may have International Union for Conservation of Nature had a strong influence on the incidence of oral (IUCN). 2016. The IUCN Red List of stereotypy in these giraffes. Rees (2004) reported Threatened Species. [homepage on the Internet] that when elephants were exposed to cold International Union for Conservation of Nature, weather, the frequencies of their stereotypies Gland, Switzerland; [cited 20 November 2018]. increased. Therefore, a possibility is that the Available from URL: https://www.iucnredlist. increase in the frequency of oral stereotypy in org/species/9194/136266699 winter was caused by the difference between Lamprey HF. 1963. Ecological separation of the environmental conditions (such as temperature large mammal species in the Tarangire Game and humidity) in the captivity and those in the Reserve, Tnaganyika. African Journal of Ecology, original habitat of the giraffes. However, in 1, 63-92 giraffes, further research is required because Leuthold BM, Leuthold W. 1972. Food habits of some factors cause the oral stereotypy is unclear. giraffe in Tsavo National Park, Kenya. African Therefore, to clarify the association between a Journal of Ecology, 10, 129-141. cold climate and oral stereotypy in giraffes, the Leuthold BM, Leuthold W. 1978. Daytime effect of environmental enrichments that warm the activity patterns of gerenuk and giraffe in body, such as provision of outdoor spot heating Tsavo National Park, Kenya. African Journal of and increasing heat owing to rumination, should Ecology, 16, 231-243. be investigated in the future. Mason GJ, Latham N. 2004. Can’t stop, won’t stop: is stereotypy a reliable animal welfare Acknowledgements indicator? Animal Welfare, 13, 57-69. The authors would like to thank Enago (www. Parker DM, Bernard RTF. 2005. The diet and enago.com) for the English language review. ecological role of giraffe (Giraffa camelopardalis) introduced to the Eastern Cape, South Africa. Journal of Zoology, 267, 203-210. Pellew RA. 1984a. Food consumption and energy References budgets of the giraffe. Journal of Applied Baxter E, Plowman AB. 2001. The effect of Ecology, 21, 141-159. increasing dietary fibre on feeding, rumination Pellew RA. 1984b. The feeding ecology of and oral stereotypies in captive giraffes (Giraffa a selective browser, the giraffe (Giraffa camelopardalis). Animal Welfare, 10, 281-290. camelopardalis tippelskirchi). Journal of Zoology, Bashaw MJ, Tarou LR, Maki TS, Maple TL. 202, 57-81. 2001. A survey assessment of variables related Rees PA. 2004. Low environmental temperature to stereotypy in captive giraffe and okapi. causes an increase in stereotypic behaviour Applied Animal Behaviour Science, 73, 235-247. in captive Asian elephants (Elephas maximus). Berry PSM. 1973. The Luangwa valley giraffe. Journal of thermal biology, 29, 37-43. Puku, 7, 71-92. Sauer JJC, Skinner JD, Neitz AWH. 1982. Ciofolo I, Le Pendu Y. 2002. The feeding Seasonal utilization of leaves by giraffes Giraffa behaviour of giraffe in Niger. Mammalia, 66, camelopardalis, and the relationship of the 183-194. seasonal utilization to the chemical composition Dagg AI. 2014. Giraffe: Biology, Behaviour and of the leaves. African Zoology, 17, 210-219.

171 Does oral stereotypy in captive giraffes decrease by feeding them evergreens and barks in winter?

Schmucker SS, Kolter L, Nogge G. 2010. 2017. Weight estimation and seasonal change of Analysis of the fine structure of oral activities nutrients content in tree leaves fed in Japanese in captivity unravels control of food intake in zoos. Nihon Chikusan Gakkaiho. 88, 9-17 (in giraffe (Giraffa camelopardalis). Giraffa,4 , 73. Japanese) Shiota Y, Yayota M, Kawamura A, Tanaka M.

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キリンへの冬季の樹木給餌は口の常同行動を減少させるか？

岡部光太 1＊、河村あゆみ 1、福泉洋樹 1、石内琴音 2、加瀬ちひろ 2,3

1 京都市動物園 606-8333 京都府京都市左京区岡崎法勝寺町岡崎公園 2 千葉科学大学 288-0025 千葉県銚子市潮見町 3 3 現所属：麻布大学 252-5201 神奈川県相模原市中央区淵野辺 1 丁目 17 − 71

*Corresponding author. E-mail address: [email protected]

要 約

近年、動物福祉の観点から飼育動物の環境の改善が多くの動物園で行われている。特にキリンでは、 口の常同行動の減少のために複数の採食エンリッチメントの実施が行われている。先行研究では、複数 の給餌器の設置や乾草の給餌量の変更、樹木給餌の実施が常同行動の減少に効果があったとされている。 しかし、樹木給餌は冬季の実施が困難であり、冬季においてはその効果も明らかとはなっていなかった。 そこで今回、全ての季節において樹木給餌を行い、樹木摂食量と口の常同行動の調査を行った。観察に は京都市動物園で飼育する 3 頭のキリンを供試した。その結果、樹木摂食量は季節間で有意な変化は見 られず、ほぼ同量の摂食が確認された。一方、全ての個体で口の常同行動が観察され、有意に冬に増加 する結果となった。樹木摂食量と口の常同行動の発現量には相関は見られなかった。そのため、今回の 観察において、樹木摂餌量ではない、例えば本来の生息地との間に生まれる気候的なギャップが要因と なっている可能性が考えられた。それゆえ、口の常同行動に与えるその諸要因は未だは明らかではない ため、今後さらなる研究が必要である。

キーワード：キリン , 動物園 , 採食エンリッチメント , 樹木給与 , 季節変化

Animal Behaviour and Management, 55 (4): 165-173, 2019 （2019．2．28 受付；2019．9．7受理）

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