Relationships between behaviour and health in working horses, donkeys, and mules in developing countries

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Abstract

Recent studies raise serious welfare concerns regarding the estimated 93.6 million horses, donkeys and mules in developing countries. Most equids are used for work in poor communities, and are commonly afflicted with wounds, poor body condition, respiratory diseases, parasites, dental problems, and lameness. Non-physical welfare problems, such as fear of humans, are also of concern. Interventions to improve working equine welfare aim to prioritise the conditions that cause the most severe impositions on the animals’ subjectively experienced welfare, but data identifying which conditions these may be, are lacking. Here we describe a stage in the validation of behavioural welfare indicators that form part of a working equine welfare assessment protocol. Over 4 years, behavioural and physical data were collected from 5481 donkeys, 4504 horses, and 858 mules across nine developing countries. Behaviours included the animals’ general alertness, and their responses to four human-interaction tests, using the unfamiliar observer as the human stimulus. Avoidance behaviours correlated significantly with each other across the human-interaction tests, with 21% of animals avoiding the observer, but they showed no associations with likely anthropogenic injuries. Over 13% of equids appeared ‘apathetic’: lethargic rather than alert. Measures of unresponsiveness correlated with each other across the five tests, and were associated with poor body condition, abnormal mucous membrane colour, faecal soiling, eye abnormalities, more severe wounds, and older age, depending on the equine species. This suggests that working equids in poor physical health show an unresponsive behavioural profile, consistent with sickness behaviour, exhaustion, chronic pain, or depression-like states.

Introduction

An estimated 39 million donkeys, 40.5 million horses and 12.3 million mules live in developing countries, constituting over 85% of the world's equids (FAOSTAT, 2006). In developing countries, equids are mostly used as working animals, often carrying out tasks under harsh and impoverished conditions for long hours each day. Consequently, previous research has shown that they have many physical and clinical problems, such as wounds, poor body condition, respiratory diseases, high parasite burdens, dental problems, and lameness (de Aluja, 1998, Pritchard et al., 2005, Tesfaye and Curran, 2005, Regan, 2009a, Burden et al., 2010, Burn et al., in press, Saul et al., in press). These problems are likely to reduce the work efficiency of the animals, indirectly reducing the income of the often very poor people who rely on them. The physical/clinical problems are also likely to cause poor welfare for the animals themselves, since similar conditions in humans are associated with pain, weakness, exhaustion, and depression (Kelley et al., 2003). Hence, charities, such as the Brooke Hospital for Animals (‘the Brooke’) who provided data for the current study, work to attempt to improve working equine health and welfare.

To date, despite growing information on working equine health, little is known about the animal welfare implications (in the sense of the animals’ subjective experiences) of the myriad physical conditions these animals accumulate. For example, some physical conditions might be associated with pain (Broster et al., 2009, Regan, 2009b) or exhaustion (the high creatine kinase concentrations in working equids indicates that muscle damage from overwork is prevalent: Tadich et al., 1997, Pritchard et al., 2009), while others may barely be perceived by the animals even if they harm their health and longevity. This is of applied importance because funding and resources to improve animal welfare should ideally be targeted towards problems likely to cause the most suffering as perceived by the animals themselves, which may be those causing deviations from normal behaviour. It would also be of value to have easily observed behavioural welfare indicators, so that the individual animals likely to be in most need of welfare improvement can be identified rapidly before a full assessment is done. Here we describe a stage in the validation of behavioural welfare indicators in working equids to assess their potential for providing information towards these purposes.

The behavioural indicators here formed part of a non-invasive welfare assessment that was developed in 2003 by the University of Bristol in collaboration with the Brooke. It should be noted that the data were not collected for the purposes of this study, but instead for the internal monitoring purposes of the Brooke. The data thus take the form of a series of standardised surveys of working equine populations, and we use an epidemiological approach, exploiting the natural variation within these populations to investigate relationships between variables of interest. The welfare assessment protocol was intended to be brief and appropriate for field conditions, where observers were often interrupting the animals’ work. The welfare indicators were chosen to be simple, to minimise assessment time and to facilitate repeatability between observers. The behaviours included an observation of general alertness versus unresponsiveness to the environment. Unresponsiveness can be a component of chronic pain (Ashley et al., 2005), sickness behaviour (Aubert, 1999, Millman, 2007, Weary et al., 2009), depression (Vollmayr and Henn, 2003, Dunn et al., 2005) and exhaustion; but equally it can be associated with neutral or even good welfare if an animal perceives its situation to be secure enough to allow reduced vigilance (Paul et al., 2005). The human-interaction tests, which were proposed as measures of fear, aversion, or friendliness towards humans, incorporated brief assessments of the animals’ avoidance and other responses when a human approached, and their acceptance of human contact (e.g. for farm animals: de Passille and Rushen, 2005, Waiblinger et al., 2006, and for sports and companion horses: Hausberger et al., 2008). Pain behaviours were not explicitly included in the assessment, since they are highly diverse, differing with the source, nature, and time-scale of the pain (Ashley et al., 2005, Regan, 2009a).

Like many large-scale, multi-centre epidemiological studies, data were collected by a number of trained observers (e.g. Waters et al., 2002, Dawkins et al., 2004, Rutherford et al., 2009). The observers in the current study were only those attaining ≥80% agreement with the trainer for all indicators, but the more general inter- and intra-observer reliability of the physical and behavioural indicators in the welfare assessment have also been tested (Burn et al., 2009): the population was too homogenous to conclusively test all the indicators, but while alertness showed acceptable intra-observer reliability, it showed poor reliability between observers. This suggests that some observers have different thresholds or use different cues for deciding when equids are alert or not, despite having been trained using the same guidance notes and photographs. These differences will have added unsystematic noise to the data analysed here, but the variable was included because so little is currently known about working equine behaviour, and measures of general alertness could be important in future equine welfare assessments. The responses to the four human-interaction tests did show acceptable reliability between observers. The only physical indicator in the current study that attained poor reliability was mucous membrane colour, but it was included here because of its clinical relevance as a field test for endotoxaemia or gastrointestinal illness (Hailat et al., 1997, Thoefner et al., 2001, Hillyer, 2004).

In the current study, we investigated how the behaviours related to each other, and how they related to potentially relevant physical measures. Our hypotheses were broadly that (a) unresponsiveness should correlate across the tests and (b) unresponsiveness should be associated with an overall reduced prevalence of physical problems if it signifies good welfare, or with an increased prevalence of physical problems if it indicates negative welfare (i.e., we tested whether responsiveness in these animals had a relationship in either direction with physical problems). Also, if aversion to humans is consistent within individual animals, animals that show aversion to humans in one of the tests should (c) show aversion to humans in the three other human-interaction tests, and (d) have more physical signs of anthropogenic harm e.g. wounds on the hindquarters, potentially indicating beating.

Section snippets

Animals and observers

Non-invasive behavioural and physical data were collected from 5481 donkeys, 4504 horses, and 858 mules across 60 locations in nine developing countries: Afghanistan, Egypt, Ethiopia, Guatemala, India, Jordan, Kenya, Pakistan and The Gambia. The data were collected over a 4-year period (March 2003–February 2007). The locations were areas where the Brooke was working or considering working in the future, or where a collaborating organisation was working (see Acknowledgements for collaborating

Correlations between behaviours

The prevalences of each behaviour for the three species are given in Table 2, showing that over 13% of equids appeared apathetic or depressed (the two categories are combined in the current study because only 0.6% of the animals (70 individuals) appeared depressed). Measures of unresponsiveness correlated positively with each other across the behavioural tests (Table 3). For example, in all three species, apathy correlated with a lack of response to the observer walking beside the animal, and

Discussion

The results suggest that the behavioural tests incorporated into this welfare assessment have potential as welfare indicators for identifying individual animals with negative welfare, in an unresponsive state, or that consistently show behavioural aversion to unfamiliar humans.

Summary

In summary, behavioural unresponsiveness correlated across the behavioural measures in the current study, and was associated with more numerous or severe physical conditions. The strongest associations were found between an apathetic general attitude and lower BCS, abnormal mucous membrane colour, older age, and (in horses) eye abnormalities; apathy/alertness may therefore provide a useful – if non-specific – indicator for rapidly identifying animals most in need of welfare interventions.

Acknowledgements

This study was supported and funded by the Brooke Hospital for Animals. Many thanks to all the owners who kindly permitted their animals to be used in this study, and to the observers who collected the data. We are grateful for Dr. Joy C. Pritchard's constructive comments on the manuscript. We would also like to thank the Kenya Network for Dissemination of Agricultural Technologies, Equinos Sano para El Pueblo (ESAP, Guatemala), Gambia Horse and Donkey Trust, and the Aga Khan Rural support

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