1. Introduction

Zoos and aquariums aim to preserve wildlife through research, education, and conservation activities, while simultaneously providing good welfare conditions to the animals in their care [1]. Advances in husbandry practices and zoo animal welfare science are key to guaranteeing that zoological institutions work as scientific and ethical conservation centres [2].

According to Mellor and colleagues [3], an animal’s welfare state can be described as the balance between its negative and positive subjective experiences. Nonhuman animals (hereafter, referred to as animals) are deemed to reach a positive welfare state when they mostly experience positive affects (e.g., a sense of security, sometimes indicated by playfulness), when their physical and behavioural needs are met, and when they can exert choice and control over resources and the environment.

Many studies have tried to evaluate animal welfare by verifying whether and how environmental and human stimuli (e.g., ambient temperature and visitor presence, respectively) affect animal behaviour [4]. Nevertheless, only a few researchers have examined the combined impacts of these stimuli in an attempt to obtain a clearer picture of animals’ experiences and welfare state (see for example: [5-9]). Interestingly, some of these studies detected an overestimation of the visitor effect (i.e., the positive or negative influence exerted by visitor presence) when other parameters, such as temperature and time of day, were included in the analysis [5, 6, 7].

In this study, we aimed to assess the integrated effects of environmental conditions (i.e., ambient/water temperature, relative humidity, and background noise level) and caregiver/visitor presence on the behaviour of a pair of captive Asian small-clawed otters (hereafter, referred to as ASCOs) through the application of multivariate research methods. In particular, we investigated the subjects’ behavioural time budget, and the occurrence and potential causes of abnormal repetitive behaviour (ARBs), and evaluated whether and how the otters’ behaviours were affected by selected environmental and human-related parameters.

2. Material and methods

This study focused on a pair of ASCOs housed at the Giardino Zoologico di Pistoia (GZP), Pistoia, Italy. We collected data during 14 sampling days selected within a two-month period (from 19th July to 6th September 2020). We videoed the otters to ensure comprehensive monitoring of their behavioural patterns [10]. We conducted six one-hour observations daily (S1: 9:15–10:15 am; S2: 10:45–11:45 am; S3: 12:15–1:15 pm; S4: 2:45–3:45 pm; S5: 4:15–5:15 pm; S6: 5:45–6:45 pm) to record data evenly across the public opening hours (9:00 am–7:00 pm), and to include feeding sessions and enclosure cleaning in the data collection periods. Each observation session was based on a 30-minute recording of each otter. We conducted a total of 84 focal sessions for each subject, resulting in 40 hours and 18 minutes of observation material for the male and 39 hours and 25 minutes of observation material for the female. The order of the subjects was alternated to monitor them in both the first and second 30-minute portion of each one-hour observation session. Based on other similar studies [5-7, 11-12], we selected the following parameters to be included in the analyses: weather conditions, ambient and water temperature, wind speed, relative humidity, background noise level, number of visitors, and caregiver presence. Weather conditions, wind speed, humidity, and ambient and water temperature were recorded at the beginning of each observation session. We recorded caregiver presence in and around the enclosure while recording visitor numbers and background noise every five minutes (seven times per focal observation). To test the effect of the selected parameters on behaviours, we ran generalised linear mixed models (GLMMs) [6-8].

3. Results

Both otters performed a wide array of species-specific behavioural patterns [13], with a limited occurrence of aggressive and avoidance behaviours, which are usually associated with negative emotional states, such as fear and anxiety [14]. Moreover, the presence of potential ARBs, which usually indicate poor welfare conditions, was limited. The otters could also exercise control and choice over the environment, choosing where to perform behaviours almost 24 hours a day.

Focusing in detail on the otters’ time budgets, the dominant category was out of sight, accounting, on average, for 41.59% of the subjects’ time budgets. This was consistent with the results reported for breeding pairs kept with offspring in outdoor naturalistic enclosures [11, 15-16]. Conversely, pairs and triplets of siblings held in indoor enclosures with limited natural vegetation and shelters have been reported to spend less time out of sight [12, 17]. Thus, the results of this study seem to confirm that different and enriched hiding options are key requirements in captive settings, in line with husbandry guidelines [18]. Nevertheless, a larger sample size is needed to exclude the influence of group composition.

When visible, the subjects mainly engaged in resting and vigilance behaviours. The percentage of time allocated to resting was similar to that reported for breeding pairs in family groups [11, 15-16]. Vigilance performance was, instead, slightly higher in comparison with the available literature, in which ASCOs were estimated to spend less than 15% of their time budget checking the surrounding environment [12, 17]. The otters engaged less in land locomotion and affiliative interactions compared to the breeding pairs of two family groups studied by Cuculescu-Santana et al. [11] and Owen [15]. This discrepancy could be due to the absence of offspring in this study that could have stimulated affiliative interactions, and the overall increased activity level of the adults involved in providing parental care (i.e., carrying, following, and feeding cubs) [6].

Notably, the family group analysed by Gothard [16] allocated 20% of its time budget to foraging and feeding, with a 13% increase when enriched with crickets and mealworms scattered in the enclosure. All the other studies, including the present research, reached a maximum of half of that percentage used for foraging and feeding. Since the species spends 40 to 60% of its waking time foraging in the wild [19], a greater use of food-based enrichments [1] is highly recommended.

As hypothesised, we did not detect an influence of visitor numbers, noise, or visitor interaction on behavioural responses, confirming the finding of recent studies indicating that visitor presence tends not to be the main factor affecting behaviours when other parameters are taken into consideration [5-7]. Our results mainly showed an effect of time of day (i.e., observation session) on the individuals’ behaviours, as previously reported for other species [5-7, 9]. Individual identity was a significant predictor of the level of juggling (i.e., fast, erratic movements that pass an object between the forepaws and sometimes the mouth), vigilance, and visitor–animal interaction, in accordance with results reported by other scholars studying bird species [18]. An analysis of the otters’ personality traits could be useful to pinpoint better the individual specific traits that should be considered when applying changes to the enclosure and to husbandry and care procedures. Indeed, personality influences how animals cope with their environment and interact with humans [20-22].

4. Conclusion

In conclusion, to our knowledge, this study was the first to investigate the integrated influence of environmental and human-related stimuli on the welfare of captive otters. Our results suggest that the otters involved in this study mainly experienced positive welfare states, indicating that they were likely provided with good welfare conditions. Enclosure design and husbandry practices were found to allow the subjects to perform a variety of species-specific behaviours, and to exert choice and control over their environment. Due to the small sample size, the results cannot be generalised, and the limited number of video recording devices might have led to an underestimation of resting and affiliative behaviours. The COVID-19 pandemic and associated restrictions caused a reduction in visitor numbers, meaning re-evaluation of the visitor effect in relation to other parameters taken into consideration in this study is warranted in the future. Moreover, further studies, aimed at investigating how the subjects’ behaviour varies during the day, across seasons, and with personality, are also recommended, to evaluate how otters’ needs change over time, and how this could alter visitor effects. This understanding could be used to optimise their husbandry routines and maximise positive experiences.

Despite the limitations acknowledged previously, this study increases the understanding of a scarcely researched topic and confirms the effectiveness of applying multivariate research methods to better analyse the array of lived experiences of captive animals. It also suggests suitable areas for further research and provides recommendations, such as the implementation of new enrichments, for improving the welfare of the studied subjects.

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This entry is adapted from the peer-reviewed paper 10.3390/ani13132228