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Development of a behavioural welfare assessment tool for routine use with captive elephants

  • Lisa Yon ,

    Roles Conceptualization, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Writing – original draft, Writing – review & editing

    lisa.yon@nottingham.ac.uk

    Affiliation School of Veterinary Medicine and Science, Faculty of Medical & Health Sciences, The University of Nottingham, Sutton Bonington, Leicestershire, United Kingdom

  • Ellen Williams,

    Roles Conceptualization, Data curation, Investigation, Writing – review & editing

    Affiliation School of Animal Rural and Environmental Sciences, Nottingham Trent University, Brackenhurst Campus, Southwell, Nottinghamshire, United Kingdom

  • Naomi D. Harvey,

    Roles Data curation, Formal analysis, Writing – review & editing

    Affiliation School of Veterinary Medicine and Science, Faculty of Medical & Health Sciences, The University of Nottingham, Sutton Bonington, Leicestershire, United Kingdom

  • Lucy Asher

    Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Supervision, Validation, Writing – original draft, Writing – review & editing

    Affiliation Centre for Behaviour and Evolution, Institute of Neuroscience, Newcastle University, Framlington Place, Newcastle, United Kingdom

Development of a behavioural welfare assessment tool for routine use with captive elephants

  • Lisa Yon, 
  • Ellen Williams, 
  • Naomi D. Harvey, 
  • Lucy Asher
PLOS
x

Abstract

There has been much concern in recent years about the welfare of elephants in zoos across North America and Europe. While some previous studies have assessed captive elephant welfare at a particular point in time, there has been little work to develop methods which could be used for regular, routine welfare assessment. Such assessment is important in order to track changes in welfare over time. A welfare assessment tool should be rapid, reliable, and simple to complete, without requiring specialist training and facilities; welfare assessments based on behavioural observations are well suited to this purpose. This report describes the development of a new elephant behavioural welfare assessment tool designed for routine use by elephant keepers. Tool development involved: (i) identification of behavioural indicators of welfare from the literature and from focus groups with relevant stakeholders; (ii) development of a prototype tool; (iii) testing of the tool at five UK zoological institutions, involving 29 elephants (representing 46% of the total UK captive elephant population of 63 animals); (iv) assessment of feasibility and reliability of aspects of the prototype tool; (v) assessment of the validity of each element of the tool to reflect the relevant behaviour by comparing detailed behavioural observations with data from the prototype tool; (vi) assessment of known-groups criterion validity by comparing prototype tool scores in individuals with demographics associated with better or worse welfare; (vii) development of a finalised tool which incorporated all elements of the tool which met the criteria set for validity and reliability. Elements of the tool requiring further consideration are discussed, as are considerations for appropriate application and interpretation of scores. This novel behavioural welfare assessment tool can be used by elephant-holding facilities for routine behavioural welfare monitoring, which can inform adjustments to individual welfare plans for each elephant in their collection, to help facilities further assess and improve captive elephant welfare. This study provides an example of how an evidence-based behavioural welfare assessment tool for use by animal caretakers can be developed within the constraints of zoo-based research, which could be applied to a range of captive species.

Introduction

Modern welfare assessment has placed much focus on providing animal carers or inspectors with the tools to be able to routinely assess welfare in situ (e.g. on farm, in the laboratory, in the field, in a rescue shelter and in zoos [14]). Routine assessment of welfare may be of particular importance for captive elephants. Zoo elephant welfare across North America and Europe has been criticised [59] and in the UK, specific concerns were raised by a report on the welfare of elephants in UK zoos [10]. A review of this report by the government advisory committee, the Zoos Forum [11], suggested that evidence of welfare improvements were needed in order for zoos to continue keeping elephants in captivity. Previous studies have focussed on judging the current welfare state of elephants [5, 10], but few studies have developed methods for routine assessment of elephant welfare. Yet, objective and regular assessment of elephant welfare is needed to be able to monitor and provide evidence of any improvements, as was mandated by the Zoos Forum and the House of Lords [11, 12].

Routine welfare assessment often needs to be rapid, non-invasive and should not require any specialist equipment, facilities or specific training of animals. For this reason routine welfare assessment is often based on observations of behaviour [1315]. Measuring welfare is challenging even without such constraints, there is no single accepted welfare measure; multiple indicators of welfare should be used to surmise if an animal is in a good or bad welfare state [16]. Welfare indicators can nevertheless be objectively evaluated, according to how consistently they can be assessed (reliability), and according to level of evidence that the measurements reflect the construct they were designed to measure (validity). Indicators should differ between animals with better and worse welfare, should be repeatable, and the time frame of change should be known. A fully validated welfare tool will have assessed each type of validity and reliability (see Table 1) against predefined thresholds [17, 18] typically across multiple studies.

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Table 1. Summary of the main types of reliability and validity applied to welfare assessment.

https://doi.org/10.1371/journal.pone.0210783.t001

There are a number of behavioural welfare indicators that might be used to assess the welfare of zoo elephants[19]. Stereotypies are one of those most frequently used [20]. Stereotypies are defined as ‘repetitive, invariant behaviour patterns with no obvious goal or function’ [21] and it is believed they are a way of coping with stress; however, the use of stereotypies as an indicator of current welfare state must be treated with caution, as there is evidence they can persist even after the stressor which caused their development is no longer present, so they may reflect a historical rather than current welfare state [22]. Veasey [23] suggested that documentation of baseline time budgets and comparison with time budgets in new environmental or social conditions, or comparison with wild elephant time budgets may be a valid means of measuring captive elephant welfare. Qualitative behavioural assessment (QBA) has been designed to capture information on the quality of an animal's demeanour. It has been shown to be useful for routine domestic animal welfare assessments [4, 2428], and has been used to assess welfare in free-living African elephants [29]. Furthermore, demeanour was identified by elephant stakeholders as a potential welfare indicator [30]. Night-time and resting behaviour may also be a useful welfare indicator [31, 32]. Wild and captive elephants are known to spend much of the night active [3338]. Many captive elephants do not have access to their outdoor enclosure at night, and are confined to their smaller indoor enclosures [10, 39], particularly during winter months in colder climates. Furthermore, keepers are usually not present during the night time to monitor behaviour; as this unmonitored time period often comprises more than half of each 24 hour period, it might be particularly important to measure welfare during the hours when keepers are not present. All UK elephant-holding zoos now have indoor video cameras to collect footage of their elephants overnight [40], but footage needs to be reviewed and assessed in order to monitor behaviour during this time.

The objective of this study was to develop a routine behavioural welfare assessment tool for keeper assessment of captive safari park and zoo elephants in the UK. Specifically, the aims were to develop and trial a prototype welfare assessment tool for elephants, to assess the reliability of the tool completed at multiple time points by multiple raters, and to assess validity of behavioural indicators in the tool, by comparing each to a more in-depth, objective behavioural assessment measuring the same behavioural welfare indicators. A final aim was to perform a known-groups validation by comparing scores from the tool in individuals with/without health conditions and with/without demographics associated with poor welfare in other studies. This work was undertaken as part of the activities of the British and Irish Association of Zoos and Aquariums (BIAZA) Elephant Welfare Group (see: https://biaza.org.uk/elephant-welfare-group).

Methods

Animals and housing

A prototype tool was tested at five elephant-holding facilities in the UK. These were selected to represent a range of facilities, including safari parks and zoos; different contact systems (free contact and protected contact); group sizes (4, 4, 5, 7 and 9); and levels of herd relatedness. In total the sample comprised 29 elephants (6 male, 23 female): 9 African (Loxodonta Africana) and 20 Asian (Elephas maximus); this represented 46% of the total UK captive elephant population of 63 animals. The elephants ranged from 2–44 years of age and the mean age was 22 years. Twelve were born in the wild, the remaining 17 were born in captivity.

Statement of ethics

The study involved observational assessment of captive elephant behaviour, with no disruption to their behaviour or routine. The project was approved by the Ethics Committee at the University of Nottingham, School of Veterinary Medicine & Science, and by the ethics committees of each of the five participating safari parks and zoos.

Design of the prototype welfare assessment tool

Identification of welfare indicators.

Elephant behavioural welfare indicators were identified from: 1) a rapid review of peer reviewed literature using a systematic search criteria and a critical appraisal tool (see [19]); 2) a review of non-peer reviewed publications on elephant welfare (see [41]); and 3) stakeholder focus groups to identify novel measures (see [30]). Inclusion of keepers in the focus groups meant that some of the indicators included in the tool were suggested by end users; such inclusive participation when developing welfare assessments is considered best practice [17]. Seventy-four potential indicators of welfare were identified by the focus groups, forty one were identified from the peer reviewed literature and a further seventy eight from non-peer reviewed literature. These measures were combined into a summary list for consideration by an external advisory panel, consisting of people working in zoo management, and researchers in animal welfare and in behaviour of captive or free living elephants. Duplicate measures were removed as were those which were not considered behavioural measures of welfare. A list of 76 unique behavioural measures of welfare was produced for potential incorporation in the tool. See Asher and colleagues (2015) for full details of the categories. A full outline of tool development can be found in Appendix A in S1 Appendix, and a brief summary in Fig 1.

Welfare assessment tool.

The list of 76 welfare indicators was then considered for inclusion in the prototype tool. Final selection of measures for inclusion was based on the strength of evidence of their validity or importance as welfare measures (see [19]), their feasibility and practicality for use by elephant keepers and the need to provide a range of measures across different aspects of welfare. The welfare assessment tool was designed to take no longer than 60 minutes to complete.

The prototype welfare assessment tool consisted of three parts (see Appendix B in S1 Appendix for full prototype tool):

  1. 1. Qualitative Behaviour Assessment: Determining the valence of an animal’s emotional or affective state has been identified as an important aspect of welfare assessment [4244]. Qualitative behavioural assessment (QBA) is a methodology which was developed to capture this dimension of animal welfare through assessment of an animal’s demeanour [2629]. Sixteen terms (depressed, active, fearful, indifferent, engaged, distressed, exploratory, social, content, relaxed, uncomfortable, agitated, tense, frustrated, wary, and playful) were scored by participants on a visual analogue scale (VAS) (Table 2), completed four times in the day; each scoring was based on demeanour observed during a one-minute live observation. One 1-minute live observation had to take place in each of four 2-hour time blocks: (1) 9:00–11:00 am; (2) 11:00 am– 1:00 pm; (3) 1:00 pm– 3:00 pm; and (4) 3:00 pm– 5:00 pm) so that observations were spread throughout one full day. A mean score for each term was generated from the ratings of that term at each of the four time points.
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Table 2. QBA terms used in welfare tool and anchors for VAS.

Proposed welfare interpretation, based on valence of term is indicated by a + (positive) or–(negative).

https://doi.org/10.1371/journal.pone.0210783.t002

  1. 2. Daytime behaviour Questions: Keepers were asked to score 35 questions on Likert or VAS (Table 3) following three days of live observations. Five-minute long observations were undertaken four times per day (one 5-minute observation in each of four 2-hour time blocks spread across the day as described above), and were repeated over three consecutive days. The daytime behaviour questions were scored at the end of the third day of live observations. Likert scales for behavioural frequency were used where appropriate, with different numbers of response options based on the expected frequency of that behaviour (based on pilot data and initial keeper feedback).
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Table 3. Prototype Daytime behaviour questions, question text, answer options and indication of proposed relationship to welfare with supporting references.

https://doi.org/10.1371/journal.pone.0210783.t003

  1. 3. Night-time observations: Keepers were asked to score night time behaviour from video footage using scan sampling every 30 -minutes for one night, from 21:00–09:00 (or whatever time keepers arrived in the morning), during the three day observation period. Behaviour was scored as: Feeding, standing or lying (alone or with others), stereotypy, walking, comfort, interaction with environment, social, other (with a space to write in what behaviour, not already listed, was observed), or out of view. Of these measures: feeding, walking, comfort, interaction with environment, social, and standing or lying with others were proposed to indicate positive welfare; standing or lying alone or performing stereotypy were proposed to indicate negative welfare (based on[29, 40])

Welfare assessment tool trial and subsequent development

To test the practicality and feasibility of use the tool was trialled at three time points by a researcher and keeper: Trial 1) by two researchers [including EW]; Trial 2) by a single researcher [EW] and at least one keeper from that zoo (November–December 2014) to test inter-observer reliability (by both people observing the same elephants at the same time); Trial 3) by the same keeper from Trial 2 at each zoo (at least three weeks after Trial 2) to test for intra-observer reliability, as well as one additional keeper at each zoo (to assess inter-observer reliability). After the first trial, the tool was modified; measures which could not be easily rated accurately were removed, and additional options were added in for the answers where required. The tool was then used in Trials 2 & 3 to gather further input from elephant keepers, and to assess the reliability and validity of final measures. All keepers were briefed on use of the tool prior to undertaking these trials.

Recording equipment.

Bespoke video cameras with infrared capability were used to make recordings of both the indoor and outdoor enclosures, except when facilities had existing indoor cameras (in which case these were used for indoor footage). The cameras were high definition Hikvision IR network cameras (Model DS-2CD2632D-IS, Hikvision Europe, The Netherlands), customised to run from battery power (Tracksys, Nottingham, UK) and were mounted on pre-existing structures at each facility when possible, or on bespoke 3 meters steel stands (Oryx Engineering and Installation, UK), at locations which provided fullest visual coverage of the enclosures. Cameras recorded at 20FPS and had a 20m IR light range. Two additional 40 metre, 80 degree angle IR lamps (Camsecure, Bristol, UK) were mounted on the stand for each camera at 90° relative to each other (and 45° to each side of the camera), to provide wider IR coverage at night.

Reliability and validity testing.

Analysis was performed to assess the validity, reliability and feasibility of the prototype monitoring tool, and to identify groupings of elements of the tool in order to reduce the number of measures being analysed. In order to analyse the accuracy of representation of the welfare assessment, during Trials 1 & 2, video footage of the elephants was collected over three consecutive 24 hour periods and was scored using a detailed ethogram (see Appendix C in S1 Appendix). Generally, all behaviours were assessed in both daytime and night time footage. However, there were a few exceptions. Swimming and bathing was only possible during the daytime, so this was only included in the daytime ethogram. Proximity to others (within 3 body lengths of another elephant) was only included in the daytime ethogram, as the size of the night time enclosures may have led to a false interpretation of elephants being proximate to one another when they were just in the same enclosure. Running was also included in the daytime but not the night time ethogram, as smaller night time space often precluded this behaviour. Daytime footage (09:00–17:00) was analysed using five minute scan sampling and night-time footage (18:00–08:00) was analysed using three minute scan sampling for all behaviour except standing and lying rest, which were recorded continuously. Sampling frequency was tested to ensure that timing of scan samplings provided an accurate reflection of behaviour (when it was sampled more frequently) for both daytime and night-time ethogram observations. Five and three minute sampling, respectively, were compared to one minute sampling and found to sufficiently capture frequency of behaviour. The more frequent sampling at night reflected the sampling rate required for capturing social behaviour which was additionally recorded, but is not presented here. While detailed behaviours were captured in the ethograms, analysis of behaviours was made using the higher level behavioural categories of the behaviours from the ethogram, in order to compare the results to the welfare assessment tool.

Face validity and feasibility of the tool were assessed using keeper and expert feedback. Inter-rater reliability was assessed by comparing scores of the researcher and the keeper on Trial 2 at each zoo, for each element of the tool. Test re-test reliability was assessed by comparing scores by the keepers at each zoo involved in Trial 2 assessment with scores by that same keeper at each zoo for Trial 3. Internal consistency and groupings of questions were identified. Concurrent criterion validity was tested to confirm that behavioural indicator of welfare as assessed by the tool did indeed measure the behaviour it was intended to measure. This was achieved by comparing the keeper responses to questions about reported frequency of behaviour in the daytime using the tool with detailed ethogram analysis of video recordings from Trial 2. For night-time observations the frequencies at which behavioural indicators of welfare were observed from night-time observations made by keepers were compared to the proportion of observations of those same behaviours in detailed ethogram analysis of video recordings from Trial 2. Cut-off criteria and analysis performed for each type of reliability or validity were assigned prior to analysis (see Table 4).

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Table 4. Overview of data analysis and criteria for assessing reliability and validity of the welfare tool.

https://doi.org/10.1371/journal.pone.0210783.t004

We collated data from BIAZA’s Elephant Welfare Group on: body condition score (henceforth BCS, noting higher, rather than lower BCS are more generally a welfare concern due to problems with captive elephant obesity); foot health score; gait score; any chronic or acute health conditions experienced in the previous 12 months; whether they were related to any other group members; the number of inter-zoo transfers they had experienced; the elephant’s origin (i.e. captive-born or wild). These variables were used for known-groups criterion validity because welfare manipulation was not possible in this context. Each of these variables is related to health (BCS, foot health, gait score and health conditions) or has been associated with welfare in other studies: the number of inter-zoo transfers [7, 45], relatedness [23], and the elephant’s origin [7, 47].

All analysis was conducted in the statistical programme R [48] using packages stats: BlandAltmanLeh, psy, psych, polcor, lme4.0, and lmerTest.

Final welfare assessment tool

Identification of indicators.

Final selection of indicators for inclusion in the welfare assessment tool was based on the strength of evidence of their validity as welfare indicators, their feasibility and practicality for use by elephant keepers, their accuracy as compared to thorough behavioural analysis and the desire to include a range of measures across different areas of welfare to create a more robust tool. A few questions were included for future interest but not analysed. These were questions on vocalisations (because stakeholders and expert panel believed they were reflective of welfare but there was little current evidence to support this in elephants) and an overall welfare assessment score (scored on a VAS from Worst imaginable and to Best imaginable for any elephant anywhere). The purpose of the overall welfare assessment score was to provide information on individual welfare for zoo records which may not have been captured by the other aspects of the tool.

Results

Qualitative behaviour assessment

Some QBA terms could be combined into component groupings, but terms ‘Playful’ and ‘Wary’ did not group easily with other terms. One component which emerged was labelled: At ease in the environment which was comprised of higher ratings on ‘Content’ and ‘Relaxed’, and lower ratings of ‘Uncomfortable’, ‘Agitated’, ‘Tense’ and ‘Frustrated’. Cronbach’s alpha revealed good internal reliability for this grouping component (0.90). This component was found to be reliably completed on different occasions and by different raters, as were two additional QBA terms, ‘Playful’ and ‘Wary’ (see Table 5). The QBA terms were not validated against detailed behavioural recordings, but they were analysed for known-group validity. Using this analysis elephants were found to be rated as more wary if they had experienced a health problem in the previous 12 months (by 0.77±0.38, t = 2.03, P = 0.05).

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Table 5. Reliability statistics for the three parts of the behavioural welfare tool.

https://doi.org/10.1371/journal.pone.0210783.t005

Daytime behaviour questions

Three groupings of daytime behaviour questions were identified. The first grouping, labelled Dependence on routine, comprised questions on: Feeding frequency (higher), Feeding at scheduled time only (higher), Waiting for scheduled events (higher) and Playing with others. (lower) The internal reliability of this grouping of questions as assessed by Cronbach’s alpha was 0.67. Based on proposed interpretation of the individual items, higher dependence on routine was proposed as a negative welfare indicator. A second grouping labelled Positively engaging with the physical and social environment consisted of: Wallowing frequency, Interactions with the environment, and Affiliative behaviour (all higher). This grouping’s internal reliability, as assessed by Cronbach’s alpha, was 0.68. Based on proposed interpretation of the individual items, higher positive engagement was proposed as a positive welfare indicator. A final grouping related to Activity consisted of: Walking frequency (higher) and Standing still frequency (lower) and the internal reliability, as assessed by Cronbach’s alpha, was 0.82. Based on proposed interpretation of the individual items, higher activity was proposed as a positive welfare indicator.

Out of twelve questions assessed for test-retest/intra- and inter-rater reliability, four questions did not reach an acceptable level of reliability (see Table 5). These were Interaction with water, Walking frequency, Dustbathing and Standing still frequency.

The majority of questions were found to be associated with the relevant behaviour observed in the ethogram analysis of behaviour, providing concurrent criterion validity for these questions to confirm they are measuring the behaviour they were designed to measure (see Table 6). Exceptions to this were Sand rolling and Object play.

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Table 6. Concurrent validity statistics for the daytime and night-time behavioural observations part of the behavioural welfare tool.

https://doi.org/10.1371/journal.pone.0210783.t006

Dependence on routine (which included answers to questions on Feeding frequency, Feeding at scheduled times, Waiting for scheduled events and less playing with others) was positively associated with (worse) foot health scores (0.45 ±0.09, t = 4.84, P<0.001) and gait scores (0.016±0.05, t = 3.27, P = 0.003). The question on stereotypy frequency, which had a binomial distribution, was associated with gait score and whether elephants were related to other members of the herd. Elephants were more likely to show more stereotypy if: (i) they had higher (worse) gait scores (OR = 1.66, CI = 1.01–2.74, P = 0.047); (ii) they were not housed with related herd members (OR = 22.97 CI = 1.53–34.37, P = 0.02).

Night-time observations

Ten elements of the night-time observations section of the welfare tool could be assessed for reliability; of these, seven met the criteria for being reliable (see Table 5). Some behaviour types recorded in the night-time observations (Comfort behaviour and Interactions with the environment) were so rare that they could not be assessed for reliability. Standing rest alone, Walking and Social behaviour, which were recorded as part of the prototype welfare tool, were not reliable between or within raters. Feeding, Standing rest with others, Lying rest (alone or with others), Stereotypy and Length of the longest lying bout, could be assessed reliably.

The relative proportion of eight out of eight behaviour types at night assessed using the welfare tool were representative of the relative proportions of these same behaviours using detailed ethogram video analysis (see Table 6).

The length of the longest lying bout was more likely to be shorter if elephants (i) did not have any health problems (more likely to score in 1st Quartile, 5.67, CI = 1.73–18.6, P = <0.001); (ii) had a lower BCS (more likely to score in 1st Quartile, OR = 1.61, CI = 1.02–2.56-, P = 0.05); or (iii) had a higher foot score (more likely to score in 2nd Quartile OR = 1.35, CI = 1.82–3.30, P = 0.01 and in 1st Quartile, OR = 4.75, CI = 2.31–9.76, P<0.001).

Finalised tool

Based on the results from the prototype tests, a finalised Elephant Behavioural Welfare Assessment Tool was developed for use by captive elephant managers (see Appendix D in S1 Appendix). All those elements of the tool which met the criteria for reliability and validity were included (see Tables 5 and 6 and Table 7). The finalised tool is presented to keepers in an Excel sheet in which they enter the raw data and see the final scores. Those questions which can be grouped together to form a single score are automatically rotated as necessary and averaged to form a single score for each component (Positively engaging with the physical and social environment; Dependence on routine; At ease in the environment) which is then presented to the keepers as an outcome of the tool alongside the single scores for all other non-groupable questions.

Discussion

This project involved the development of a novel, evidence-based, behavioural welfare assessment tool for use in evaluating the welfare of captive elephants. The behavioural welfare assessment tool developed in this project was designed to address a specific need in the elephant-holding zoo community in the UK: the need for a validated (as far as possible in the time available and constraints of research in a zoo environment), relatively rapid, easy-to-use tool that could be regularly used by elephant keepers to make behavioural assessments of welfare. The results of the study suggest that this aim was successfully met, as many behavioural indicators of welfare, previously validated as such from other studies, could be reliably scored using the tool designed. Furthermore, many of the indicators measured using the tool were representative of that behaviour measured using a gold standard ethological method of scoring behaviour every 3–5 minutes for 72 hours. A number of behavioural indicators of welfare assessed during the day using the tool were closely matched to the ethological behaviour scoring; these included: feeding, wallowing, stereotypy and play behaviour. At night, agonistic behaviour and lying rest, particularly when the lying rest occurred near others, were both measured accurately using the tool, as these measures also closely matched the results from the ethological behaviour scoring. An excel spreadsheet with pre-designed formulae, and drop down boxes, has been designed and distributed to the zoos for ease of data entry and collation and interpretation of results. This will allow zoos to assess the impact of changes in management and husbandry, to facilitate evidence-based management of their elephants, and is available from the authors on request.

The aim of this study was not dissimilar to those of the AssureWel and AWIN projects [49, 50], both of which involved development of practical on-farm welfare assessments of farmed species. Like the current study, the AWIN project also used behaviour as a central part of their welfare assessments and used stakeholder input to develop more user-friendly protocols [50]. Similar to the current project, AWIN also incorporated QBA in their welfare assessment for some species. Unlike the current study, both AWIN and AssureWel included assessments of health and physical condition in addition to behaviour. There are other projects and protocols developed by BIAZA’s Elephant Welfare Group (EWG) which have been designed to assess these aspects of welfare [51]. Used together it is hoped that these tools will provide a more complete overview of UK zoo elephant welfare.

A number of approaches have been suggested for assessing animal welfare, and it was possible to incorporate some, but not all, of these considerations in the newly developed tool described here. This new tool will provide some preliminary indications of elephant preferences: in where, how and with whom they choose to spend their time, within the constraints of their environment. This may help elephant-holding facilities to identify with which, of the resources elephants have available, they most interact. Facilities can share best practise, however, this will always be limited to what is available to elephants across different facilities, and time spent interacting with resources does not always indicate preference for that resource.

QBA was used in the tool and may have potential to capture the valence of the elephants’ emotional state. Although we were not able to validate this, we have demonstrated that some QBA terms can be rated reliably by keepers and some terms are associated with physical welfare state. Further validation is needed against other measures or manipulations of emotional state. Indeed, complete validation of a welfare tool is an extensive process and cannot be completed in a single study. Future work should explore potential links between behavioural scores made in this tool in better and worse environments and in comparison against specific positive or negative welfare outcomes (e.g. health parameters, or reproductive activity).

One other aspect of welfare which is sometimes considered to be important is telos, which has been defined as ‘nurturing and fulfilment of the animal’s nature’ [52]. Assessment of telos, or of natural behaviour, in captive elephants might best be accomplished through comparisons with wild elephant behaviour (time budgets, physical activities, social groups) [23], although others argue against this approach, favouring instead a focus on the consequences of behaviour [53]. This newly developed tool assesses a wide range of natural elephant behaviours seen in both captive and wild elephants (including comfort behaviour, sleep, foraging, social interactions, exploratory behaviour).

Proposed welfare tool elements: Elements requiring further consideration

Overall, the sample size was sufficient to allow assessment of validity and reliability against pre-determined criteria (without correction for multiple testing). There were a small number of males in the the dataset (20%), however, this is largely reflective of the UK elephant population where only ~25% are adult males. Whilst our sample was highly representative, covering 49% of the UK elephant population, the numbers are still relatively small from a statistical testing perspective. As a result it was not felt appropriate to correct for multiple testing, and as different comparisons explore different aspects of validity/reliability, the number of tests conducted within a single comparison were reduced to the minimum needed. Although the number of comparisons made here were extensive, this is in line with guidelines for the development of new psychometric tools [54], which require testing for internal consistency, criterion validity, and reliability. If correction for multiple testing had been used, wallowing measured during the daytime and stereotypy and lying near others at night-time as measured by the tool would have remained significantly associated with ethological measurements of this same behaviour. Evidence of replication of the results with a new dataset will be tested in the coming years as the tool is used over time.

In general, the majority of the elements tested in the prototype tool met the criteria for reliability and validity, and were therefore included in the final version of the tool (see Appendix D in S1 Appendix). There were, however, some measures which were not reliable or not valid in all contexts, and further work is needed to either investigate other ways to assess those particular aspects of behaviour, or to determine the meaning or significance of variations in the expression of these behaviours. There was poor agreement between reports of water interaction and object play recorded using the tool, and ethological assessments of these behaviours. It is possible that this is because these behaviours occurred rarely, so the less frequent behavioural assessments made when using the tool were less likely (by chance) to occur at the right time to detect the performance of such behaviour. Movement or activity levels (walking or standing still) were not accurately assessed in the prototype tool and questions on these were therefore removed from the final tool. Alternative methods for assessing this behaviour should be sought in the future, as activity can be an important part of physical welfare [55, 56]. The proposed QBA term ‘depressed’ was not used reliably by different assessors and feedback by keepers indicated that they found it a difficult term to use. Alternative terms such as ‘lethargic’ or ‘apathetic’ have been suggested to capture this dimension. It is not entirely clear how to best collect data on night time behaviour; a number of measures were reliable and reflected behaviour measured on that particular night, but did not necessarily reflect behaviour over a longer time frame (such as the three nights across which the tool was validated). It may be worth extending the night time observations over more nights, but more would need to be known about the consistency of such behaviour at night before this could be recommended.

Results from this study suggested the interpretation of one of the behavioural indicators of welfare used in the tool may need to be reconsidered. Prior to undertaking the study, it had been assumed that longer bouts of lying rest were indicative of better welfare, as an absence of lying rest is associated with poor welfare [57]. However, it is possible that longer, uninterrupted bouts of lying rest might also be an indicator of poor welfare since in the current study, this was associated with health problems, and with poorer foot and gait scores (and associated with higher BCSs, suggesting that higher body weight may have contributed to these issues). In general, the known-groups analysis conducted was not used to select measures for inclusion in the tool, however this analysis provided some interesting initial results. Only four of the items in the tool (including one composite measure of four questions) were associated with the known-groups which were health related measures or circumstances which had previously been related to welfare (relatedness of herd, zoo transfers, origin). The fact that more items were not associated with these variables is not unexpected due to small sample sizes, large individual variance between elephants, and the known groups being related only to certain aspects of welfare (hence why known-groups was not a criteria for inclusion in the tool). However, it must be noted that many of the items still require criterion validation from more suitable measures (e.g. ideally a welfare manipulation within an individual). The items for which known-groups validation was supported generally fitted expectations with regard to direction of relationships with welfare. The QBA component ‘wary’ was higher in elephants that had experienced a health problem in the past 12 months; although it is important to note that keepers would have had knowledge of this and this may have influenced their QBA rating. Stereotypic behaviour was higher in animals which were not housed with related herd mates. More stereotypy was also associated with worse gait which could either be explained by stereotypy influencing gait, or some shared experience which influenced both gait and stereotypy. Higher ‘Dependence on routine’ was associated with poorer foot and gait health. This mirrors findings in dairy cows, which show higher levels of routine (i.e. visiting the same feeder and stall every day) when they are lame [58].

This tool was not intended to compare welfare of different elephants at different facilities; it would not be appropriate to do so for a number of reasons. A number of the measures in this tool, including most notably stereotypies, represent an animal’s cumulative welfare state, rather than their current welfare. Furthermore, there are a range of individual factors, such as life history, health status, age, and reproductive status among many others, which can influence the results from this welfare tool, and it is important to take these into account when interpreting results. This tool has instead been designed to monitor changes in an individual elephant’s behavioural welfare over time, and to assess the impact of changes in management and husbandry. Changes in husbandry and management might include, for example, access to a new enclosure or environmental enrichment, a new type of flooring, a new elephant added to the collection, or a move of an elephant to a new facility.

Conclusions

This study describes the development of a new elephant behavioural welfare assessment tool designed to be relatively rapid, reliable and easy to use, to facilitate regular use by elephant keepers. To date the tool has been used by 11 UK and Irish facilities, and many of these facilities have used it multiple times to begin to track possible changes in welfare over time. The tool comprises three sections: (1) Qualitative behaviour assessment, rating demeanour of the elephant on 12 terms, scored after four sets of 1-minute observations across one day; (2) A series of questions answered after four sets of 5-minute daytime behaviour observations across three days; (3) Night-time observations, consisting of reviewing overnight footage, and recording behaviour using 30 minute scan sampling for one night.

Regular use of this tool by captive elephant facilities is recommended (e.g. quarterly) to facilitate assessment and monitoring of elephant welfare over time. This information can be used to determine the impact of any changes in husbandry and management of elephant welfare, and can help facilities to develop and adjust individual elephant welfare plans to optimise the welfare for each elephant in their care.

We would suggest that the methodology used for this project could similarly be employed to develop and validate behavioural welfare assessment tools to evaluate welfare in a wide range of species in a zoo or aquarium setting. This would enable a more comprehensive approach to monitoring the welfare of these species over time, and determine response to changes in management and husbandry, to better understand the impact of management decisions and to better inform policy to support optimal zoo animal welfare.

Acknowledgments

The authors would like to thank the staff at all the UK elephant holding zoos for their suggestions and input in the stakeholder focus group teleconferences. A special thanks to the managers and keepers at Twycross Zoo, Knowsley Safari Park, Colchester Zoo, Chester Zoo and ZSL Whipsnade Zoo for all of their kind assistance in helping develop and trial the prototype behavioural welfare assessment tool. Thanks to BIAZA’s Elephant Welfare Group (EWG) for their support throughout the project. Grateful thanks to the members of our Expert Advisory Panel, Oliver Burman, Samantha Bremner-Harrison, Ros Clubb, Francoise Wemelsfelder, Charlotte Macdonald and Phyllis Lee. A huge thank you to Chantelle Whelan, Emma Mellor, Ana Maria Martos Martinez-Caja, James Mursell, Chelsea Terry and Esme Taylor-Roberts for their assistance in analysing video footage. Thanks to the Defra members of the project Steering group from the policy and evidence team: Jane Withey, Helen Pontier and Margaret Finn, and to the external experts on the project Steering Group, John Eddison and Matt Hartley.

The project was funded by the Department for Environment, Food and Rural Affairs (Defra) (WC1081) UK.

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