1. Environmental Enrichment of Captive Primates: a Research for Welfare at Maia’s Zoo DEPARTAMENTO DE CIÊNCIAS DA VIDA FACULDADE DE CIÊNCIAS E TECNOLOGIA UNIVERSIDADE DE COIMBRA Raquel Costa 1, Cláudia Sousa 2,3, Miquel Llorente 4,5 1 Faculdade de Ciências da Universidade de Coimbra, Coimbra, Portugal 2 Departamento de Antropologia Faculdade de Ciências Sociais e Humanas Universidade Nova de Lisboa, Lisboa, Portugal 3 Centro em Rede de Investigação em Antropologia, Lisboa, Portugal 4 Unitat de Recerca i Laboratori d’Etologia, Fundació Mona, Girona, Spain 5 Institut Català de Paleoecologia Humana i Evolució Social – IPHES, Universitat Rovira i Virgili, Tarragona, Spain CIP Girona, 2012/2013

2. Resume 1. Introduction 1.1. Aim 2. Methodology 2.1. Sample 2.2. Apparatus 2.3. Data collection 3. Predictions 4. Results 4.1. Gibbon 4.2. Brown lemur 4.3. Mona monkey 4.3. Main behaviour comparison 5. Discussion 6. Conclusion 6. References 7. Acknowledgments

3. Introduction As highly social and intelligent beings, primates need, when in captivity, a great level of social and environmental complexity in order to bring their behavioural repertoire and activity budget as close as possible to their wild conspecifics. (Celli et al., 2003). “We should be beyond attempts to repairing, or limiting the damage, and proactively be providing a life worth living (…) Permanently removing ingrained abnormal stereotypic behaviours is rare so prevention is far better than cure.” (Buchanan-Smith, 2010: 45) Environmental enrichment (EE) promotes a stimulating background to confined individuals using strategies that encourage activity, as well as induces behaviors similar to those exhibited by conspecifics in the wild. (Márquez-Arias et al., 2010:32)

4. Aim Assess behaviourIntroduce enrichmentCompare welfare “To confirm enrichment actually occurred, evaluation is required to determine whether the well-being of the animals improved and thus whether the strategy was actually effective enrichment” (Hoy et al., 2010: 304).

5. Methodology: sample ® Raquel Costa Fig.2. Brown lemurs (E. fulvus) at Maia’s zoo. Fig.3. Mona monkeys (C. mona) at Maia’s zoo. Fig.1. Gibbons (H. lar) at Maia’s zoo.

6. Methodology: apparatus 2 different devices Fig. 4. EE consisting in bamboo pieces filled with food Fig. 6. Mona monkey with the bamboo. Fig. 5. EE consisting in a wire box filled with fruits and straw. Fig. 7. Gibbon with the wire box. ® Raquel Costa

7. Methodology: data collection TopicStartingEnding Volunteer workOctober, 8thOctober, 20th Searching for literature/writingOctober, 21stDecember, 24th Topic Hylobates lar Cercopithecus mona Eulemur fulvus Baseline, 40 sessions (Bl) December, 26th February, 5thDecember, 26th Bamboo, 40 sessions (Bb)January, 30thFebruary, 6thJanuary, 30th First Immediate Effect Baseline, 15 sessions (1CEI) March, 3rdFebruary, 27th Wire Box, 40 sessions (WB)March, 20th March, 13th Second Immediate Effect Baseline, 15 sessions (2CEI) April, 14thApril, 10th Post-Baseline, 40 sessions (PB) Results analysis April, 19th April, 30 th April, 16th April, 30 th April, 16th May, 1 st Total (hours)95 Total observation: 285h Tabela 2. Observation’s distribution concerning the phase of the study and the number of hour of observation. Table 1. Chronogram, indicating study dates appointments.

8. Methodology: data collection Recording behaviour:. Ethogram: 20 behaviours. scan sampling : 30 minutes (30s) Frequency: session by session analysis Kruskal-Wallis and Mann-Whitney U test (SPSS 20)

9. Predictions With the EE’s introduction, foraging should increase, reducing inactivity, locomotion and interaction with the public. Regarding social interactions between individuals, affiliation, grooming and agonism should increase during WB (proximity). As for stereotypic behavior observed in two groups (brown lemurs and Mona monkeys) should decrease.

10. Results: gibbon Chart 1.Total sum per phase of relative frequency per session in Gibbons’ behaviour observed in the experiment (BL – Baseline; Bb – Bamboo; 1CEI – First Immediate Effect Baseline; WB – Wire Box; 2CEI – Second Immediate Effect Baseline; PB – Post-Baseline).

11. Results: brown lemur Chart 2. Total sum per phase of relative frequency per session in Brown lemurs’ behaviour observed during the experiment (BL – Baseline; Bb – Bamboo; 1CEI – First Immediate Effect Baseline; WB – Wire Box; 2CEI – Second Immediate Effect Baseline; PB – Post-Baseline).

12. Results: Mona monkey Chart 3. Total sum per phase of relative frequency per session in Mona monkey's group during the study (BL – Baseline; Bb – Bamboo; 1CEI – First Immediate Effect Baseline; WB – Wire Box; 2CEI – Second Immediate Effect Baseline; PB – Post- Baseline).

13. Results: comparison Inactivity: decreased in WB; Feeding: increased in WB; Hum 0: increased in Bb. Inactivity: decreased in Bb, WB and PBL; Hum 0: increased in Bb and WB; Other: increased in WB. Inactivity: decreased in Bb; Feeding: increased in WB; Stereotypy: decreased in WB; Hum 0: increased in Bb and decreased in WB; Vocalization: increased in Bb and WB; Self-grooming: increased in WB; Sex: decreased in WB ® Raquel Costa Fig.8. Mona monkey at Maia’s Zoo. Fig.9. Brown lemur at Maia’s Zoo. Fig.10. Gibbon at Maia’s Zoo.

14. Discussion High inactivity, abnormal behaviours (stereotypy) present Baseline: Poor welfare!! manipulation of the devices resulted in decreased inactivity in the three species, which may indicate that the increased activity in general may represent a welfare improvement. No changes in social behaviours. Introduction of EE devices Bamboo had a “smother" effect than the wire box, perhaps because it represents only a small reward unlike the box that contained the entire first meal. Further, the fact that it is an opaque object, which may have been too complex to individuals not accustomed to such devices (Clark and Smith, 2013). It is necessary to balance: the enrichment should be stimulating and of possible resolution to prevent habituation (Grönqvist et al., 2013). This notion is fundamental as challenge contributes to the individuals’ "fitness" and even to decrease stereotypic activity (Meehan and Mench, 2007)

15. Discussion Detail… Gibbons: individuals had different responses to enrichment (Agile was less inactive WB and Maya in PB; Agile interact with the public, Maya hid), which may indicate individuality: two individuals of the same species, with the same background, the same habitat demonstrate different personality traits with implications for the design of enrichment to implement. ® Raquel Costa Fig.11. Maya with the bamboo cane

16. Discussion Detail… Brown lemurs: maintained high inactivity, explained perhaps by the low metabolic rate of lemurs in response to harsh and volatile habitats (Simmen et al., 2010), a feature perpetuated in captivity. However, this group was the one that showed the largest number of significant changes in their behavior. In particular, reducing the stereotypical behaviours. ® Raquel Costa Fig.12. Miss Piggy with the bamboo cane.

17. Discussion Mona: with no significant decrease in stereotypy, perhaps because this behaviour has become a "habit" difficult to remove from the routine (Mason and Latham, 2004). However, this were the group that showed the most significant decrease in inactivity (Longa) and increased foraging (both). To detail… ® Raquel Costa Fig.13. Longa with the bamboo cane.

18. Conclusion We suggest that the wire box should be part of the routine while Bamboo can be used as a casual EE (complement). This can prevent habituation, while contributing to a rich and diverse diet which can in turn prevent the abnormal behaviour’s development. At the same time we are improving animal welfare, we are contributing for a proper education and public awareness for wildlife conservation. The results show that the subjects did, indeed, need EE intervention. It is clear that the effect of enriching feeding strategy depends on the species and the individual’s personalities. Enrichment effect may not be immediate, so we must be "patient" with its use (Mason and Latham, 2004). Future projects will include a greater number of individuals.

19. Conclusion “Captive conservation breeding programs should not be wholly concerned with maintaining a diverse gene pool – they should also be concerned with conserving species-typical behaviors, especially if they are to produce behaviorally intact captive animals that can be reintroduced to the wild with minimal training, financial resources, and loss of individuals” (Kerridge, 2005: 71).

20. References Buchanan-Smith, H. M. 2010. Environmental enrichment for primates in laboratories. Advances in Science and Research, 5: 41-56. Celli, M.L.; Tomonaga, M.; Udono, T.; Teramoto, M.; Nagano, K. 2003. Tool use task as environmental enrichment for captive chimpanzees. Applied Animal Behaviour Science, 81: 171-182. Clark, F. E.; Smith, L. J. 2013. Effect of a Cognitive Challenge Device Containing Food and Non Food Rewards on Chimpanzee Well-Being. American Journal of Primatology, 9999: 1-10. Gronqvist, G., Kingston-Jones, M. and Lehman, J. 2013. The effects of three types of environmental enrichment on the behaviour of captive Javan gibbons (Hylobates moloch). Applied Animal Behaviour Sciences, 147(1): 214-223. Hoy, J. M.; Murray, P. J.; Tribe, A. 2010. Thirty years later: Enrichment practices for captive mammals. Zoo Biology, 29: 303-316. Kerridge, F. J. 2005. Environmental enrichment to address behavioral differences between wild and captive black- and-white ruffed lemurs (Varecia variegata). American Journal of Primatology, 66(1): 71-74. Márquez-Aris, A.; Santillán-Doherty, A. M.; Arenas-Rosas, R. V.; Gasca-Matías, M. P.; Muñoz-Delgado, J. 2010. Environmental enrichment for captive stumptail macaques (Macaca arctoides). Journal of Medical Primatology, 39: 32-40. Mason, G. J.; Latham, N. R. 2004. Can’t stop, won’t stop: is stereotypy a reliable animal welfare indicator? Animal Welfare, 13: S57-S69. Meehan, C. L.; Mench, J. A. 2007. The challenge of challenge: Can problem solving opportunities enhance animal welfare? Applied Animal Behaviour Science, 102: 246-261. Novak et al., 2006 Simmen, B.; Bayart, F.; Rasamimanana, H.; Zahariev, A.; Blanc S.; Pasquet, P. 2010. Total Energy Expenditure and Body Composition in Two Free-Living Sympatric Lemurs. PLoS ONE, 5(3): 1-10.

21. Acknowledgments Contact: raquelberingei@gmail.com I thank Dr. Cláudia Sousa and Dr. Miquel Llorente for their valuable methodological suggestions throughout the research, Zoo staff and keepers for their assistance in enrichment task preparations and reliability procedures, as well as to all volunteers and interns for their support.