Current Zoology
56 (4): 389−394, 2010
Influence of social upbringing on the activity pattern of captive lion Panthera leo cubs: Benefits of behavior enrichment Sibonokuhle NCUBE 1, Hilton Garikai Taambuka NDAGURWA 2* 1 2
African Lion and Environmental Research Trust (ALERT), P. Bag 1218, Gweru, Zimbabwe Department of Forest Resources and Wildlife Management, Faculty of Applied Sciences, National University of Science and Technology, P.O. Box AC 939, Bulawayo, Zimbabwe
Abstract The influence of social upbringing on the activity pattern of lion Panthera leo cubs was investigated at three sites. In this study, stimulus objects such as sticks, grass, fresh dung (elephant Loxondota africana, zebra Equus quagga, impala Aepyceros melampus, duiker Sylvicapra grimmia, kudu Tragelaphus strepsiceros, giraffe Giraffa camelopardalis and wildebeest Connochaetes taurinus) and cardboard boxes, were utilized in an enrichment program aimed at encouraging active behaviors of captive lion cubs at Antelope Park and Masuwe. Lion cubs at Chipangali were not behaviorally enriched. Activity patterns were recorded for 10 days at each site. We recorded moving, resting, playing, grooming, visual exploration and display of hunting instincts. We found that behavioral enrichment enhanced the active behaviors of captive lion cubs. Orphan-raised cubs spent more time moving, playing and displaying hunting instincts than mother-raised cubs, but the time spent grooming was similar across areas and suggests that grooming is not influenced by enrichment. Mother-raised cubs spent more time engaged in visual exploration than orphan-raised cubs and this could be a behavior acquired from mothers or a result of confidence to explore because of their presence. Activity patterns were different among time treatments across our three study sites. Based on these findings, we suggest that lion cubs raised in captivity could benefit from behavioral enrichment to encourage active behaviors essential for eventual reintroduction into the wild [Current Zoology 56 (4): 389–394, 2010].
Key words
Activity pattern, Panthera leo, Lion cub, Behavioral enrichment, Orphan raised, Mother raised
Lions typically spend 20–21 hours resting (Schaller, 1972), tend to become active during the late afternoon (Estes, 1991), and follow a nocturnal-crepuscular activity pattern (Hayward and Hayward, 2007; Hayward and Slotow, 2009). Grooming is a highly expressed behavior in lions and can involve head rubbing and social licking and has been compared to grooming in primates (Schaller, 1972). Estes (1991) describes head rubbing as a form of closed affectionate contact and Schaller (1972) describes its association with social licking. Small cubs are often groomed by females and especially licked by their mother (Estes, 1991). Play in animals involves running, quick turns, rolling, climbing and wrestling with other objects and each other and is a learning process through which cubs learn how to coordinate, control and develop muscles. Play in lion cubs involves stalking, ambushing, and grappling motor patterns used by adults to capture prey (Bertram, 1978; Estes, 1991) and this behavior is learnt through watching adults hunting (Estes, 1991).Young mammals such as lions
may require familiar surroundings or the presence of the mother or a familiar object before they can engage in play (Estes, 1991). For example, Schenkel (1966) observed lion cubs behaving cryptically and showing no play or exploratory behavior in the absence of the mother. Diverse array of behaviors (active and stereotypic) are exhibited by lion cubs in natural environments where complexities in the environment place physical and cognitive demands on animals. This motivates them to perform behaviors necessary for survival and such behaviors are further reinforced by confidence instilled in cubs by adult lions. Historically, captive animals have been housed in restrictive enclosures without stimuli (Mench and Kreger, 1996), such as those associated with predators, prey, social groups, mates, and environmental stochasticity (White et al., 2003; Wielebnowski, 2003). Several studies have documented the effects of captivity on animal welfare (Carlstead, 1996; Mench and Kreger, 1996; Poole, 1998) and have recognized that captivity can
Received Aug.16, 2009; accepted Feb. 13, 2010 ∗ Corresponding author. E-mail: hgtndagurwa@nust.ac.zw; hgtndagurwa@gmail.com © 2010 Current Zoology
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drastically alter an animal’s behavior (Price, 1984; Lickliter and Ness, 1990; Carlstead, 1996; Price, 1998). As a result of a predictable, often unchanging environment, captive individuals may lose the range of behaviors that enable them to respond to a variable and unpredictable environment. Much is currently being done to make improvements in care programs (Hutchins, 2006). Yu et al. (2009) identified low behavioral diversity, abnormal behaviors and excessive inactivity as common problems in captive animals. This has also led to the development of several methods on how to raise lions in captivity and environmental enrichment has been recognized as an effective principle for captive animal management (Yu et al., 2009). The IUCN (2001) recommends a number of guidelines for raising lions in captivity including the need for large natural areas with sufficient drainage. The importance of differences in selective pressures between wild settings and captive ones has been a matter of discussion, especially when considering the release of captive born and reared animals into the wild (Frankham et al., 1986). Behavioral enrichment involves the introduction of toys, play objects and smells into lion enclosures and nature walks to enhance active behaviors and familiarize lion cubs to the natural environment. Behavioral enrichment enables captive animals to exhibit a diverse array of behaviors (Carlstead and Shepherdson, 1994; Shepherdson, 1998) by increasing the complexity of the captive environment (Skibiel et al., 2007). This encourages social interactions, reduces abnormal behaviors, improves health (Carlstead and Shepherdson, 1994), and may also increase the probability of survival when captive animals are reintroduced to the wild (Shepherdson, 1998). Enclosure size and simplicity affect the welfare of captive animals which may result in boredom, an inability to cope with ordinary stressors, lack of motivation, lack of opportunity to perform natural species-specific behaviors (McPhee, 2002), and development of inactive, abnormal, or repetitive behavior (Swaisgood et al., 2003). In the wild environmental complexities stimulate animals to perform behaviors essential for survival (Shepherdson et al., 1993). Thus conservation breeding and reintroduction into the wild can only be an effective management tool if behaviors essential for a life in the wild are maintained in captivity (Hakansson and Jensen, 2008). This study aimed to investigate the influence of behavior enrichment on socially deprived orphan-raised cubs in comparison to mother-raised lion cubs. We used time activity budgets since interrelations between spe-
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cies ecology and behavior are better understood through the analysis of how that particular species allocates time to various activities under a set of defined conditions (Struhsaker and Leland, 1979). We compared the behavior of lion cubs raised differently to ascertain whether behavioral enrichment can compensate for rearing by mothers.
1
Materials and Method
1.1 Site descriptions Chipangali Wildlife Orphanage is 25 km south-east of Zimbabwe’s second largest city, Bulawayo (20°10′S, 28°0 7′E). The mean annual rainfall is 600 mm (40-yr average, 1961–2001) with a range of 325–915 mm and mean annual temperature is 23.6 °C. This facility is dedicated to the rescue and care of orphaned, injured, abused, abandoned and confiscated animals in Zimbabwe. The carnivore research institute at this facility is responsible for research on lions and other carnivores. Antelope Park is located 10 km from Gweru in the highveld of Zimbabwe (19°28′S, 29°09′E). Annual rainfall is 948–1420 mm and mean annual temperature is 24–30oC. The park is a private game reserve involved in animal conservation and has a lion breeding facility. The breeding program is aimed at releasing captive-bred lion cubs equipped with essential behaviors that enable them to survive in the wild. Masuwe is located 7 km from Victoria Falls in the middleveld region of Zimbabwe (18°05′S, 25°45′E). The mean annual rainfall is 700 mm. The mean annual temperature is 24oC (14°C in June, 25°C in October). Masuwe is the second base where lions are used for the lion walk project in preparation for release into the wild. 1.2 Behavioral enrichment The lion cubs at Antelope Park and Masuwe were behaviorally enriched using toys such as sticks, grass and fresh dung from elephant Loxondota africana, zebra Equus burchelli, impala Aepyceros melampus, duiker Sylvicapra grimmia, kudu Tragelaphus strepsiceros, giraffe Giraffa camelopardalis and wildebeest Connochaetes taurinus. The enrichment sessions were replicated three times for each stimuli (Van Metter et al., 2008) alternating the stimulus object between scans. The behavioral enrichment aimed to increase the behavioral repertoire of captive lion cubs and consequently reduce abnormal behavior. We also aimed at encouraging positive utilization of the whole enclosure and in the long term to prepare the lion cubs for eventual introduction to the wild.
S. NCUBE, H. G. T. NDAGURWA: Behavior of captive lion cubs
1.3 Experimental design and data collection Three study sites were selected (Chipangali, Antelope Park and Masuwe). Lions are raised in captivity at these three sites and the only difference is in social upbringing. Cubs at Masuwe and Antelope Park are raised as orphans and cubs at Chipangali are mother-raised. The cages measured 15 × 16.4 m with a management enclosure measuring 15 × 8.6 m at Masuwe, and 15 × 15 m with a management enclosure attached measuring 7 × 6 m at Antelope Park and Chipangali. Scan sampling was used to record time spent on different activities (Altmann, 1974) of four cubs aged between 2–2.5 months (mean: 2.13± 0.04 SE) at each location. Data were collected at 5 min intervals on activity pattern during three time periods, early morning (07:00–09:00), mid-morning (10:00–12:00) and late afternoon (16:00–18:00). The cubs were watched for 10 d at each site and activity pattern was recorded as locomotion, resting, playing, grooming, visual exploration and display of hunting instincts. Observations were carried out from left to right and right to left alternating between scans recording the behavior of each cub during every round of scan. The observer had no interaction with the animals and there was no public viewing of cubs during data collection. All other conditions such as feeding were similar across the study areas. 1.4
Data analysis
Time spent on a particular activity was calculated as the number of individuals engaged in that activity in each scan as a proportion of the total number of animals in each scan. These scan budgets were then used as individual data points in calculating overall estimates of time spent on activities. This method is particularly useful when different numbers of individuals are seen each scan (Clutton-Brock, 1977; Martin and Bateson, 1993) or when behavior is synchronized such that the behavior of a few individuals recorded in each scan can be used to represent a group’s overall behavior (Clutton-Brock, 1977). Activity patterns were compared between locations and three time periods using one-way ANOVA (n = 30). Differences between means were tested using Tukey’s HSD post hoc test with a level of significance of P < 0.05. Data were arcsine-square root transformed before analysis to normalize distributions (Zar, 1984). Data were statistically analyzed using SPSS 14 for Windows (SPSS Inc., Chicago, USA).
2
Results Activity patterns were different between Chipangali
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and Antelope Park and between Chipangali and Masuwe, except for grooming which was similar among the three locations (Table 1). Locomotion was significantly higher (F2, 87 = 46.66, P < 0.01) in orphan-raised cubs than in mother-raised cubs. There was significantly more resting among mother-raised cubs than orphan-raised cubs at Antelope Park and Masuwe (Table 1). Mean time spent playing by orphan-raised cubs at Antelope Park (11.92±0.85 SE; n =10) and Masuwe (10.94±0.89 SE; n =10) was higher than for mother-raised cubs at Chipangali (3.89±0.55 SE, n=10). There was no significant difference (F2, 87=1.39, P>0.05) in time spent grooming by lion cubs among the three locations. Lion cubs raised by their mother engaged in more (F2, 87 = 121.64, P < 0.01) visual exploration than orphan-raised lion cubs. Finally, hunting instincts were more pronounced in orphan-raised cubs than mother-raised cubs (Table 1). There was a difference in activity pattern among the time treatments at all locations (Table 2). Locomotion was significantly different among time treatments at all locations and occurred mainly during early morning and late afternoon. Time spent resting was significantly higher during mid-morning than during early morning and late afternoon at all locations. At Chipangali, among mother-raised lion cubs, playing significantly declined (F2, 27 = 35.63; P < 0.01) from early morning to mid-morning to late afternoon. Amongst orphan-raised lion cubs at Antelope Park (F2, 27 = 92.46, P < 0.01) and Masuwe (F2, 27 = 10.87, P < 0.01) playing was significantly higher during the late afternoon than early morning and mid-morning. Mother-raised cubs at Chipangali spent more time grooming in the morning than during mid-morning and late afternoon. Amongst orphan-raised cubs grooming was confined to the mid-morning and late afternoon at Antelope Park (F2, 27 =14.84, P < 0.01) and Masuwe (F2, 27 = 53.39, P < 0.01) respectively. Although there was a significant difference (F2, 27 = 13.95, P < 0.01) in visual exploration among the time treatments by mother-raised lion cubs, the cubs visually explored throughout the day, in contrast to orphan-raised cubs at Antelope Park and Masuwe where the activity was greatest in mid-morning. Amongst orphan-raised cubs at Antelope Park (F2, 27 = 34.68, P < 0.01) and Masuwe (F2, 27 = 17.60, P < 0.01) the display of hunting instincts occurred mostly during late afternoon and was significantly higher (F2, 87 = 53.17, P < 0.01) than in mother-raised cubs at Chipangali.
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Table 1
Current Zoology
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Mean (± SE) behavioral values for lion cubs raised at three locations
Chipangali
Locomotion
Resting
Playing
Grooming
Visual exploration
Display of hunting instinct
9.83 ± 0.78 a
68.03 ± 3.11 a
3.89 ± 0.55 a
7.57 ± 0.84 a
30.09 ± 0.88 a
0.62 ± 0.14 a
32.70 ± 2.43 b
39.63 ± 2.92 b
11.92 ± 0.85 b
6.27 ± 0.49 a
8.29 ± 1.59 b
21.21 ± 2.75 b
36.82 ± 2.66 b
36.55 ± 3.17 b
10.94 ± 0.89 b
6.57 ± 0.22 a
6.72 ± 0.95 b
22.39 ± 0.92 b
**
**
**
ns
**
**
46.66
31.96
31.73
1.39
121.64
53.17
MR
Antelope Park OR
Masuwe OR
F2, 87
Results of significance tests are shown for differences among means (ns, P > 0.05; ** P <0.01). Different superscript letters (a and b) in the same column indicate significant differences between means (Tukey’s HSD, P < 0.05). MR, mother raised, OR, orphan raised † Mean behavioral values were calculated for each time of day (n = 30) Table 2 Mean (± SE) behavioral values for lion cubs in the early morning, mid-morning and late afternoon at Chipangali, Antelope Park and Masuwe Locomotion
Resting
Playing
Grooming
Visual exploration
Display of hunting instinct
36.22 ± 0.07 a
1.66 ± 0.01 a
Chipangali Early morning
14.65 ± 0.01a b
46.13 ± 0.33 a
8.06 ± 0.03 a
b
b
13.22 ± 0.06 a b
b
Mid morning
4.45 ± 0.02
Late afternoon
10.40 ± 0.03 c
71.21 ± 0.03 c
1.75 ± 0.01 c
7.30 ± 0.05 c
29.36 ± 0.04 c
0.00 ± 0.00 c
**
**
**
**
**
**
73.37
11.20
35.63
86.24
13.95
15.18
Early morning
49.95 ± 0.01 a
28.35 ± 0.01 a
8.90 ± 0.01 a
6.62 ± 0.02 a
2.21 ± 0.03 a
24.00 ± 0.52a
Mid morning
18.26 ± 0.01 b
61.89 ± 0.03 b
8.45 ± 0.01 b
c
c
F2, 27
86.75 ± 0.04
1.85 ± 0.01
2.19 ± 0.07
24.70 ± 0.03
0.20 ± 0.00
b
Antelope Park
Late afternoon
F2, 27
29.90 ± 0.28
28.65 ± 0.01
18.40 ± 0.03
b
9.31 ± 0.03 c
2.89 ± 0.03
c
b
20.40 ± 0.03 2.25 ± 0.01
a
1.85 ± 0.13
b
37.79 ± 0.03
c
**
**
**
**
**
**
10.01
10.13
92.46
14.84
20.63
34.68
Masuwe Early morning
52.95 ± 0.01a
26.49 ± 0.03 a
10.70 ± 0.05 a
b
b
b
5.30 ± 0.03 a
1.65 ± 0.01a b
22.90 ± 0.05 a b
16.06 ± 0.02 b
Mid morning
18.15 ± 0.01
Late afternoon
39.35 ± 0.01c
22.55 ± 0.01 c
16.90 ± 0.08 c
8.17 ± 0.00 c
4.76 ± 0.01c
28.22 ± 0.06 c
**
**
**
**
**
**
18.45
36.48
10.87
53.39
25.32
17.60
F2, 27
60.60 ± 0.05
5.21 ± 0.03
6.26 ± 0.02
13.75 ± 0.01
Results of significance tests are shown for differences among means (** P <0.01). Different superscript letters (a and b) in the same column indicate significant differences between means (Tukey’s HSD, P < 0.05). † Mean behavioral values were calculated for each time of day (n = 10 or ten observations per time of day)
3
Discussion
Generally lions spend a greater proportion of their time resting (Schaller, 1972; Estes, 1991). In a similar manner, mother-raised cubs were found to spend more time resting and they also spent relatively little time moving, which could be due to confinement in cages. Consistent with findings by Schaller (1972), Bertram
(1978) and Estes (1991) orphan-raised lion cubs spent considerable time playing, mostly during midday. Grooming was similar in both groups, contrary to expectations of increased grooming in mother-raised cubs as lion cubs are licked by their mother (Estes, 1991). However, grooming in orphan raised cubs was relatively low, although not different, because small cubs are groomed heavily by females but do little grooming
S. NCUBE, H. G. T. Ndagurwa: Behavior of captive lion cubs
themselves (Bertram, 1978). There was also a significant distinction in the preferred grooming time and was confined to the morning, midday and late afternoon at Chipangali, Antelope Park and Masuwe, respectively. Visual exploration was more pronounced in motherraised cubs and probably a result of local traditions based on learning from the mother than in orphan-raised cubs. Imprinting usually takes place soon after birth and is a unique form of learning acquired from the mother or mother figure by the young animal (Manning, 1979) and this could also explain higher rate of visual exploration in mother-raised lion cubs (Schenkel, 1966). Contrary to Schenkel (1966), however, who described lion cubs as cryptic and showing no play in the absence of the mother, orphan-raised lion cubs were more playful than mother-raised cubs and could be due to behavioral enrichment. Orphan-raised cubs at Antelope Park and Masuwe displayed hunting instincts more frequently than mother-raised cubs and this could be attributed to behavioral enrichment that takes place in the former. This study shows that behavior enrichment can have profound effects on the activity patterns of captive lion cubs. Several studies show that animals express more natural behaviors when given the opportunity (Bond and Lindburg, 1990; Carlstead et al., 1991; Powell, 1995; McPhee, 2002). The lack of hunting instinct displayed and the reduced locomotion for mother-raised cubs could be the result of a lack of behavioral enrichment. Chipangali lion cubs spend most of their time inactive (or resting) but they can benefit from behavioral and environmental enrichment as it increases their activity as in Antelope Park and Masuwe lion cubs. Our study also showed that mother-raised cubs benefit from learning from their mother and visually scan their environment. While behavioral enrichment had a sustained impact on lion cubs, our interpretation of these results and conclusions remain conservative since we could not provide data on non-enriched lion cubs. In future studies we recommend the inclusion of non-behaviorally enriched lion cubs to differentiate between the behaviors of mother-raised and orphan-raised lion cubs. However, our study does highlight the importance of behavioral enrichment on captive bred orphan-raised lion cubs. Acknowledgements The authors thank Chipangali Wildlife Orphanage (CWO) and the African Lion and Environmental Research Trust (ALERT) for allowing research at Antelope Park and Masuwe. Special thanks to PJ Mundy, A Sebata and two anonymous reviewers for comments on an earlier version of this paper.
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