Enriching the lives of reptiles: an ethologically informed approach
- Autores: Alicia Bartolomé
- Directores de la Tesis: Pau Carazo Ferrandis (dir. tes.), Enrique Font Bisier (codir. tes.)
- Lectura: En la Universitat de València ( España ) en 2025
- Idioma: inglés
- Tribunal Calificador de la Tesis: Clifford Warwick (presid.), Isabel Damas Moreira (secret.), Fay Clark (voc.)
- Programa de doctorado: Programa de Doctorado en Biodiversidad y Biología Evolutiva por la Universitat de València (Estudi General)
- Materias:
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- Resumen
Environmental enrichment, defined as a change in an animal's captive environment that seeks to improve its physical and behavioural well-being, has become a popular tool for promoting animal welfare. Public concern for animal welfare has been accompanied by a growing demand to improve the living conditions of captive animals, and enrichment has emerged as an essential tool for this. It is widely used in various settings, from homes to research labs, farms, and zoos. Environmental enrichment also represents a growing field of research, drawing from disciplines such as ethology, veterinary science, and animal welfare, among others. However, despite the increasing research and interest in environmental enrichment, its implementation and assessment remain challenging, particularly for certain taxa such as reptiles.
In this thesis, we intended to contribute to the advancement of environmental enrichment research for reptiles from both theoretical and practical perspectives. We first evaluated the status of environmental enrichment for reptiles, focusing on zoos as one of the main places where reptiles are kept in captivity. Although zoos and aquaria are paying increasing attention to environmental enrichment, several ongoing barriers hamper its widespread implementation and research progress. Foremost among these is the taxonomic bias which entails that information and research is biased towards some taxa (mainly mammals and birds), which may limit our understanding of enrichment's value for neglected groups such as reptiles. We conducted a qualitative survey study (Chapter 3) to investigate which types of enrichment are used and for which species. The survey also explored issues such as sources of enrichment ideas, barriers to implementation, enrichment goals, and specific techniques employed. Results showed that enrichment use was biased towards nutritional and structural types, with tortoises and monitor lizards being the most frequently enriched groups. While most respondents employed behavioural assessments, nearly 20% reported no method for evaluating enrichment effectiveness. This lack of assessment hinders the development and refinement of species-appropriate, goal-directed interventions. Additional barriers included insufficient knowledge, lack of resources, and confusion between enrichment techniques and basic husbandry practices. Despite these challenges, respondents overwhelmingly recognised enrichment as an integral aspect of reptile husbandry. Overall, our results indicate that although interest in enrichment is widespread in European zoos, proper techniques and programs to ensure effective implementation remain are still somewhat lacking due to different biases and barriers affecting environmental enrichment and animal welfare sciences.
Next, we aimed to highlight the importance of grounding enrichment practices in ethologically informed methods, considering the behaviour and life history of the species to be enriched. We proposed and evaluated specific enrichment methods for two species of wall lizards (Podarcis muralis and P. liolepis), based on current knowledge and our experience with these species. Lacertid lizards from the genus Podarcis are emerging as a prominent group in research in different fields, particularly P. muralis. P. liolepis has received less attention, but its chemosensory abilities have been well studied. Despite chemoreception being fundamental to reptilian biology, sensory enrichment with chemical stimuli has rarely been applied to reptiles. In Chapter 4, we evaluated the use of chemosensory enrichment as a method to enhance the welfare of P. liolepis. We chose male conspecific odours as stimuli for the enrichment based on the species' chemosensory behaviour. Behavioural observations during the enrichment period showed a long-term reduction in abnormal behaviours compared to control groups. In the exploration tests, enriched lizards showed reduced locomotion and more time perching between trials, suggesting faster habituation to a novel environment. Taken together, our results suggest improved welfare of enriched animals. Given the positive outcomes using a simple strategy, this method could be broadly applied to improve the welfare of captive lizards and reptiles in general.
We then decided to further explore enrichment in the European common wall lizard (P. muralis), incorporating non-invasive measures of stress-related hormones alongside behavioural assessments. Before employing any such technique, it is crucial to validate the use of the appropriate tests to ensure accurate measurement of glucocorticoid levels, in our case, through faecal metabolites corticosterone metabolites (FCMs). Therefore, in Chapter 5, we validated two enzyme immunoassays (EIAs: 5alpha-pregnane-3ß,11ß,21-triol-20-one and 11-oxoaetiocholanolone) for monitoring FCMs in male and female P. muralis. We collected daily faecal samples before (baseline) and after (post-treatment phase) inducing elevated corticosterone levels using transdermal administration of corticosterone (pharmacological treatment) and handling/confinement (biological treatment). Both treatments elevated FCM levels, though pharmacological treatment produced larger increases, with a higher response in females. In contrast, the biological treatment yielded smaller FCM peaks, with no significant sex differences. Overall, 5alpha-pregnane-3ß,11ß,21-triol-20-one EIA appeared to be more sensitive in detecting these effects. Regarding lizard behaviour, both treatments led to increased hiding and decreased basking compared to baseline. The effects were more pronounced in animals subjected to handling/confinement, despite smaller FCM increases. Altogether, our results confirmed the suitability of the EIAs for non-invasive FCM monitoring and underscored the importance of using multiple validated measures in welfare assessment and the need for further research on direct measures to evaluate reptile welfare.
Finally, we evaluated the effects of three types of enrichment on the behaviour and FCMs of P. muralis (Chapter 6). We used chemosensory (conspecific scents), thermal/structural (basking platforms), and nutritional (a feeding device) enrichment providing ethologically relevant challenges. All enrichment interventions yielded a significant decrease in abnormal behaviour (interaction with transparent boundaries) and a significant increase in exploration compared to baseline, changes that are considered indicative of improved welfare. FCM levels increased throughout the experiment (i.e., there was a significant effect of time spent in captivity), but this increase was less acute during enrichment phases, suggesting that enrichment attenuated the increase of FCMs. Our results emphasise the importance of using an integrated approach to evaluate enrichment effects, paying attention to the necessary prior validation of the welfare indicators employed, and the need for an ethologically informed design. We believe that the enrichment strategies we propose in this thesis could be beneficial for other reptiles, provided that species-specific and individual differences are considered, and the strategies are incorporated within a program that ensures efficacy assessment.
