A Short-Term Macro and Microevaluation of an Environmental Enrichment Program in a Captive Pride of Southwest African Lions (Panthera Leo Bleyenberghi): Age-Class Differences

Name	Sex	Date of Birth	Place of Birth	Date of Arrival at the Zoo	Parents
Adults
Roque	��?	Jul 1993	unknown	Nov 1993	unknown
Borracha	��?	Oct 1994	unknown	Nov 1995	unknown
Nena	��?	Jul 1997	Barcelona Zoo	-	unknown
Vieja	��?	Aug 1992	unknown	Nov 1993	unknown
Juveniles
Lutecio	��?	Jul 2004	Barcelona Zoo	-	Roque/unknown
Runrún	â�?�?	Jul 2004	Barcelona Zoo	-	Roque/unknown
Nima	��?	Aug 2004	Barcelona Zoo	-	Roque/unknown
Zala	��?	Aug 2004	Barcelona Zoo	-	Roque/unknown

Behaviour	Description
Exploration	The subject is inspecting an area or object, visually, nosily, tastily or listens. It also includes manipulation with the claws
Feeding	The animal is ingesting food or drink
Inactivity	The animal remains immobile, sitting or lying down, with his eyes open or closed and muscles relaxed
Keeper interaction	The lion is sitting or lying down meanwhile looks after zoo keepers
Locomotion	An animal is moving around the facilities (excluding activities forming part of aggressive interactions, play or stereotyped behaviour)
Maintenance	The subject is grooming or scratching itself with its tongue and/or claws. This behaviour also includes: defecating, urinating, scratching, rubbing or scent marking the surface or furniture from the exhibit
Social interaction	Includes behaviour involving two or more interaction individuals, which may be aggressive, parental, sexual or recreational
Solitary play	Includes all vigorous and exaggerated movements, whether or not involving an object but without relations with other individuals
Vigilance	The animal is alert, with his head up, ears pricked and eyes open, standing or lying down
Not visible	The subject or his behaviour is out of the observer's sight

Table 2: Ethogram of the different behaviours observed in Southwest African lions (Panthera leo bleyenberghi) at Barcelona Zoo, Spain.

Enrichment-programme sessions

The sixteen EP sessions were categorized as feeding; occupational or sensory (Table 3). The lions did not have experience with these enrichment items prior to this study. The enrichment micro-evaluation was carried out in July 2005, from Tuesday to Friday at 0800 h when the animals came out from their dens into the outdoor facilities. During these sessions the observer spent 1 h carrying out ad libitum recording (0800 h-0900 h) to determine the ratio of the adult and the juvenile lions that interacted with enrichment devices.

Table 3: Enrichment-device schedule for a pride of Southwest African lions (Panthera leo bleyenberghi) at Barcelona Zoo, Spain: enrichment categories-F: Feeding; O: Occupational; S: Sensory.

Analysis

The Statistical Package for the Social Sciences version 21.0 for Windows (SPSS Inc., Chicago, IL 60606, USA) was used to analyse data.

The categorical data for the daily activity pattern and the use of space were analysed through contingency tables, adjusted residual and Pearson’s X² test. Adjusted residuals (z) had an absolute value of 1.96 for a normal distribution, assuming that the significance level is 0.05 [24]. Moreover, this statistical test permitted to determine exactly which categories of the daily activity pattern and the use of space presented statistically significant differences. Pearson X² was used to determine whether there were statistically significant differences in the two study phases for the two dependent variables in relation to the age class.

The Spread of Participation Index (SPI) was used to analyse the effect of enrichment programme in the use of the space in both age classes. A value of zero (0) indicated a homogeneous use of space while a value of one (1) indicated a use totally heterogeneous [4,9,25,26].

Results

Macro-evaluation

During the EP there was a decrease in ‘vigilance’ and increase in ‘not visible’ in both age classes (Figure 3).

The daily activity pattern for adults showed statistically significant differences between two phases of study (X²=50.2, df=8, P<0.00**). During the EP, adult lions showed a significant increase in ‘inactivity’ and a decrease in ‘locomotion’. No changes were observed in ‘feeding’, ‘maintenance’, ‘exploration’, ‘social interactions’ and ‘keeper interaction’. Moreover, ‘solitary play’ was never observed in adult lions, neither in the BP nor the EP (Figure 3a and Table 4).

Table 4: Adjusted residuals in absolute value for each behavioural category of the daily activity pattern for a pride of Southwest African lions (Panthera leo bleyenberghi) at Barcelona Zoo, Spain: ** statistical significant difference /z/ >1.96, where the z score is a measure of standard deviation of mean.

The daily activity pattern for the juveniles shows statistically significant differences between two phases of study (X²=210.3, df=9, P<0.00**). During the EP, the juvenile lions showed a significantly increase in ‘exploration’, and a decrease in the ‘keeper interaction’ and ‘solitary play’ categories. No changes were observed in ‘feeding’, ‘maintenance’, ‘locomotion’, ‘social interactions’ and ‘inactivity’ (Figure 3b and Table 4).

In relation to the use of space, during the EP both age classes significantly decreased the use of zone 2, and increased the use of zone 1 and zone 4 (Figure 4).

Moreover, during EP only adult lions significantly increased the use of zone 6, zone 7 and the tunnel, whereas the use of zone 5 decreased (X²=231.1, df=7, P<0.00**). However, no change was shown in the use of zone 3 (Figure 4a and Table 5).

Table 5: Adjusted residuals in absolute value for each spatial category of the use of space for a pride of Southwest African lions Panthera leo bleyenberghi at Barcelona Zoo, Spain: ** statistical significant difference /z/ >1.96, where the z score is a measure of standard deviation of mean.

In the case of the juveniles, there was a decrease in the use of zone 3 (X²=281.0, df=7, P<0.00**), whereas no statistically significant differences were found in the use of zone 5, zone 6, zone 7 and the tunnel (Figure 4b and Table 5) during EP.

The SPI index results for the adult lions were 0.55 in the BP and 0.45 in the EP, while for the juveniles the results were 0.45 in the BP and 0.37 in the EP.

Micro-evaluation

Table 6 indicates the ratio of lions that interacted with every enrichment device offered in relation with their age classes. All juveniles (but not all adults) interacted with all enrichment devices. None of adult lions interacted with the scattered dry mint, scattered locks of camel hair and the scattered garlic powder.

Table 6: Ratio of Southwest African lions (Panthera leo bleyenberghi) in each age class at Barcelona Zoo, Spain, that interacted with the different enrichment devices provided during EP micro-evaluation.

Discussion

In this study, the ‘feeding’ category showed no variation in either age classes or study periods like the results observed in McPhee [5] who studied the provision of whole carcasses as a feeding enrichment and found that not all cats responded with increased feeding activity. However, the following publications observed an increase of feeding during enrichment: (1) Bond and Lindburg [12] found as carcass-fed cheetahs showed improved appetites, longer feeding bouts and greater possessiveness of food; (2) Powell [18] found an increase of lick/gnaw with the implementation of a fishsicle in adults and cubs of an African lion pride; (3) Charlton [10] observed that the provision of an environmental feeding-enrichment device increased the total time spent feeding in three jaguars; and (4) Bashaw et al. [11] also determined that the presentation of live fish to African lions increased the variety and frequency of feeding behaviours.

The pride of African lions in this study had no significant variation in the ‘maintenance’ behaviour observed, either in age classes or the two study phases like the results obtained by: (1) Powell [18] did not find significant differences in face rub and back roll in frozen balls of ice containing fish, scents or hanging logs in adult and cub African lions and (2) Charlton [10] who observed no variation in grooming behaviour in three Jaguars. However Walters [6] reported that the time spent grooming increased significantly with the different presentation of food items.

During this study, the ‘social interactions’ of the adult and juvenile lions did not show any variation during the enrichment phase. This may be because the management in this did not allow them to exhibit social species-typical behaviours, such as hunting for prey, searching for a mate or breeding behaviours.

There were two behaviours that had the same result in both age classes during the enrichment phase; that is, a decrease in ‘vigilance’ and an increase in ‘not visible’. The decrease in ‘vigilance’ most probably denoted that the attention of the lions was redirected towards the enrichment devices and that the animals were more entertained and did not pay attention to routine external matters. On the contrary, Powell [18] did not observe variations in alert behaviour for lion adults and cubs during the provision of any enrichment device.

The results of the not visible reported here are in accord with: (1) McPhee [5] that studied the ‘hiding on exhibit’ behaviour in large felids increased significantly during three trials of carcass provision and (2) Walters [6] also observed that a male tiger was ‘out of sight’ on a greater number of occasions during the week when multiple enriched feeding was provided. However, Bashaw et al. [11] did not find significant differences in ‘not visible’ behaviour in large felids during an enrichment programme. May be the animals decide to go into not visible places in order to avoid negative external stimulus like the visitors or climatic conditions. It is obviously necessary a balance between animal necessity to privacy and zoo visitors’ expectations. Therefore, it is necessary to design new enclosures with privacy places but with visibility for the visitors using plants, rocks, nets, etc. in combination with cameras and monitors of new technology in order to see the animals in any condition (extreme climatic conditions, breeding season or indoor enclosures) [2].

During the EP, the ‘locomotion’ decreased significantly in the adult lions but it did not vary in the juvenile lions. On the contrary, follow studies observed an increase in ‘locomotion’ during the implementation of enrichment: (1) Powell [18] observed a significantly increase in the ‘stand/locomote’ category in the adults and the cubs when frozen balls of ice containing fish and various scents where presented in the enclosure; (2) Charlton [10] denoted a significant increase in the ‘move’ category in a jaguar; and (3) Walters [6] observed a significant increase in ‘locomotion’ in a male tiger.

In the case of the ‘exploration’ behavioural category, this did not vary for adults during the EP but it increased in juveniles during the same phase. Powell [18] also observed a significant increase of ‘paw manipulation’, which in the study reported here is included in ‘exploration’ category, in adult lions and cubs when a fishsicle, various scents and hanging logs were provided.

‘Keeper interaction’ did not vary for adults but it decreased in the juveniles during EP. When the juvenile lions were interacting with enrichment items may be they were less susceptible to look out keepers’ movements because they consider enrichment more interesting. The latest and interesting studies in relation to keepers try to evaluate the effect of keepers’ personality on felid welfare [27,28].

The ‘solitary play’ behavioural category was not observed in adult lions in either phase; however, this behaviour decreased in the juveniles during the EP may be due to that the juvenile lions preferred interacting with the enrichment items. It is also important to consider the function of play during the juvenile period because this behaviour is widely assumed to be a juvenile activity, crucially involved in the development of adult behavioural skills and exerting major beneficial effects on behaviours required later in ontogeny [29]. Schaller [30] determined that the type of play demonstrated by lions depends on the state of development: cubs are more playful than sub-adult or adult lions, coinciding with the results observed in the adults in this study.

When visitors walk around the facilities for lions in zoological institutions there is a general feeling that the low activity that these felids show is due to lack of space and boredom [31]. What not all visitors know, however, is that one of the natural behavioural characteristics of lions is inactivity. In the wild, lions remain inactive for 20 h to 21 h a day; spend 2 h travelling across their territory and 40-50 min eating, provided that hunting has gone well although they can have several days without eating [30]. For this reason, it is important to avoid a possible stress by over increasing lions’ activity through enrichment programmes and to work hardly in the educational programmes for zoo visitors [32].

The final behavioural category in this study was ‘inactivity’, which increased in adult lions but did not vary in the juveniles during the EP. Margulis et al. [33] determined a relationship between inactivity and season (i.e. spring: 85% inactivity; summer: 90% inactivity) in lions. Further studies would be necessary to determine the influence of temperature on the daily activity pattern and use of space for lions in zoological institutions. It is also important to take into account whether the provision of environmental enrichment causes stress to those animals that generally demonstrate high percentages of rest or inactivity, thereby unbalancing their species-typical behaviour ratio. In this case, it is important to distinguish between the time spent resting as a naturally predominant state, and apathy as a result of boredom and an inadequate environment. Perhaps the enrichment programmes implemented for animals such as lions, should aim to reduce undesirable behaviours (e.g. stereotypies or aggression) rather than increasing activity. Moreover, the study reported here corroborates the enrichment-evaluation strategies found in the literature; that is, large felids benefit from the implementation of environmental-enrichment programmes although they spend the most amount of their time resting. Various publications have concluded that there is no significant variation in inactivity during the implementation of a feeding-enrichment programme; for example, Powell [18] for African lion adults or cubs, McPhee [5] with large felids, Charlton [10] with jaguars, and Walters [6] with a male tiger. It would be interesting to understand whether environmental enrichment with the aim of increasing activity in animals that have naturally high levels of speciestypical inactivity, would really improve the welfare of these subjects. This point has implication of for visitors to zoological institutions who become frustrated when they do not see the animals during their visit. Good signage can be used to educate the public about the natural behaviours of such species and alleviate these problems [34].

In relation to the use of space, the results of this study indicate that during the enrichment phase in both age classes, use of space was fairly consistent and comparable with three studies: (a) a male tiger whose enclosure utilization was greatest on the days which food presentation was varied [6]; (b) a fishing cat with live-fish that showed greater enclosure utilization [9]; and (c) Powell [18] determined the adult SPI did not show significant changes between the BP and EP, meanwhile the use of space in the juveniles was more homogeneous during EP.

In relation to the environmental-enrichment micro-evaluation, the results of this study concluded that all juveniles but not adults interacted with all enrichment devices. There are also other studies in some species of mammals [20], Japanese macaques [21], and bottlenose dolphins [22] whose results showed that the juveniles tend to interact with enrichment devices more than adults.

In this study, none of the adult lions interacted with scents (i.e. mint and garlic powder). It seems to be that sensory enrichment in adults has less effect than feeding ones. These results had also been observed in: 1) Powell [18] observed that frozen balls of ice containing fish elicited most of the changes in the lions’ behaviour and could thus be said to be most effective than scents (musk cologne, peppermint, allspices and almond extract) and 2) Skibiel et al. [13] observed that the proportion of time spent pacing significantly decreased more during presentation of frozen fish (-26.58%) than during spices (-21.25%).

The welfare of felids in captivity is very difficult to achieve because the hunting -considered as one of the most important species-typical behaviour is not being reproduced totally and it provokes stereotyped behaviours and digestive problems. It will be important to know how the absence of this behaviour affect to their welfare and to consider what kind of species are less susceptible to maintain in captive conditions. It includes: 1) enclosure design (climatic conditions, size and furniture); 2) diet (type, presentation, frequency and seasonal variation); 3) social requirements (solitary, social, breeding programme and multispecies exhibit); 4) enrichment programmes (design, evaluation, type and efficacy); 5) training sessions with veterinary aims; 5) veterinary treatment (breeding control, congenital illness and vaccines); and 6) visitors’ effect on welfare [34].

One of the most limitations of this study is the few studied enrichment sessions and the few published studies about enrichment response between the adults and the juveniles. Future studies should include microevaluation variables (the number of interaction/animal, the number of animals interacting with enrichment, the time spent interacting with enrichment, the enrichment item latency, and so on) in order to know more details about the efficacy of enrichment items and how each animal interact with them. This evaluation should be useful to increase the enrichment efficacy and as a consequence animal welfare.

Acknowledgements

This study could not have been carried out without the help and active participation of the team of keepers at Barcelona Zoo: Miquel Griñó, Óscar Quílez, Oriol Borrut, Ramón Cardona and Maribel Moragas. Finally, thanks to Carlota Curriu, Marc Escobar and Agnès Collia for their cooperation.

References

1. Mellen JD, MacPhee MS (2001) Philosophy of environmental enrichment: past, present and future. Zoo Biol 20: 211-226.
2. Hosey G, Melfi V, Pankhurst S (2013) Zoo animals: behaviour, management, and welfare. Oxford, England, UK.
3. Shepherdson DJ (2003) Environmental enrichment: past, present and future. Int Zoo Yb 38: 118-124.
4. Soriano AI, Vinyoles D, Maté C (2016) Long-term macroevaluation of environmental enrichment in three brown bears (Ursus arctos) at Barcelona Zoo. J Appl Anim Welf Sci 19:1-13.
5. McPhee MS (2002) Intact carcasses as enrichment for large felids: effects on on- and off-exhibit behaviors. Zoo Biol 21: 37-47.
6. Walters T (2003) Observations of the short-term behavioural response of a captive male tiger (Panthera tigris) to changes in feeding enrichment. Ratel 30: 29-47.
7. Ruskell AM, Meiers ST, Jenkins SE, Santymire RM (2015) Effect of bungee-carcass enrichment on behaviour and fecal glucocorticoid metabolites in two species of zoo-housed felids. Zoo Biol 34: 170-177.
8. Quirke T, O’ Riordan RM (2012) Evaluation and interpretation of the effects of environmental enrichment utilizing varying degrees of sampling effort. Zoo Biol 32: 262-268.
9. Shepherdson DJ, Carlstead K, Mellen J, Seidensticker J (1993) The influence of food presentation on the behavior of small cats in confined environments. Zoo Biol 12: 203-216.
10. Charlton N (1998) The effects of an environmental enrichment device on the behaviour of captive jaguars. Ratel 25: 178-188.
11. Bashaw MJ, Bloomsmith MA, Marr MJ, Maple TL (2003) To hunt or not to hunt?: A feeding enrichment experiment with captive large felids. Zoo Biol 22: 189-198.
12. Bond JL, Lindburg DG (1990) Carcass feeding of captive cheetahs (Acinonyx jubatus): the effects of a naturalistic feeding program on oral health and psychological well-being. Appl Anim Behav Scie 26: 373-382.
13. Skibiel AM, Trevino HS, Naugher K (2007) Comparison of several types of enrichment in captive felids. Zoo Biol 26: 371-381.
14. Van Metter JE, Harriger MD, Bolen RH (2008) Environmental enrichment utilizing stimulus objects for African lions (Panthera leo leo) and Sumatran tigers (Panthera tigris sumatrae). Bios 79: 7-16.
15. Quirke T, O’ Riordan RM (2011) The effect of a randomised enrichment treatment schedule on the behaviour of cheetahs (Acinonyx jubatus). Appl Anim Behav Sci 135: 103-109.
16. Markowitz H, Aday C, Gavazzi A (1995) Effectiveness of acoustic “prey”: environmental enrichment for captive African leopard (Panthera pardus). Zoo Biol 14: 371-379.
17. Damasceno J, Genaro G, Quirke T, McCarthy S, McKeown S, et al. (2017) The effects of intrinsic enrichment on captive felids. Zoo Biol 36: 186-192.
18. Powell DM (1995) Preliminary evaluation of environmental enrichment techniques for African lions (Panthera leo). Anim Welf 4: 361-370.
19. Kendal RL, Coe RL, Laland KN (2005) Age differences in neophilia, exploration, and innovation in family groups of Callitrichid monkeys. Am J Primatol 66: 167-188.
20. Glickman SE, Sroges RW (1966) Curiosity in zoo animals. Behav 26: 151-188.
21. Jaman MF, Huffman MA (2011) Age class differences in the feeding behaviour of captive Japanese macaques (Macaca fuscataia) in the forested and nonvegetated enclosure groups. Zoo Biol 30: 260-274.
22. Eskelinen HC, Winship KA, Borger-Turner JL (2015) Sex, age, and individual differences in Bottlenose dolphins (Tursiops truncatus) in response to environmental enrichment. Anim Behav and Cogn 2: 241-253.
23. Altmann J (1974) Observational study of behavior: sampling methods. Behav 49: 227-267.
24. Haberman SJ (1978) Analysis of qualitative data 1. Academic Press, New York, USA.
25. Dickens M (1955) A statistical formula to quantify the “spread-of-participation” in group discussion. Speech Monographs 22: 28-31.
26. Soriano AI, Ensenyat C, Serrat S, Maté C (2006) Introducing a semi-naturalistic exhibit as structural enrichment for two brown bears (Ursus arctos). Does this ensure their captive well-being? J Appl Anim Behav Scie 9: 299-314.
27. Phillips C, Peck D (2007) The effects of personality of keepers and tigers (Panthera tigris tigris) on their behaviour in an interactive zoo exhibit. Appl Anim Behav Scie 106: 244-258.
28. Carlstead K (2009) A comparative approach to the study of keeper-animal relationships in the zoo. Zoo Biol 28: 589-608.
29. Martin P, Caro TM (1985) On the functions of play and its role in behavioural development. Adv Study Behav 15: 59-103.
30. Schaller GB (1972) The Serengeti lion: A study of predator-prey relations. The University of Chicago Press, Chicago, USA.
31. Mellen JD, Shepherdson DJ (1997) Environmental enrichment for felids: an integrated approach. Inter Zoo News 35: 191-197.
32. Law G, Macdonald A, Reid A (1997) Dispelling some common misconceptions about keeping of felids in captivity. Inter Zoo Yb 35: 197-207.
33. Margulis S, Hoyos C, Anderson M (2003) Effect of felid activity on zoo visitor interest. Zoo Biol 22: 587-599.
34. Irwin MD, Stoner JB, Cobaugh AM (2013) Zookeeping: An introduction to the science and technology. The University of Chicago Press, Chicago, USA.