Distress unites animal conservation and welfare towards synthesis and collaboration

Abstract

An animal's welfare is not inconsequential to conservation and conservation occurs for and in consideration of animal welfare, yet these have historically been reluctant partners (Bradshaw & Bateson, 2000; McLaren, Bonacic & Rowan, 2008). This is surprising, considering, for example, the widespread use of reintroduction and restocking as a conservation tool (e.g. translocation stress, Teixeira et al., 2007; Dickens, Delehanty & Romero, 2010). The apparent dissociation between animal welfare and conservation might be overcome if we could identify at least one mutually agreeable concept, metric and objective – a foundation towards greater collaboration and eventual synthesis. Measures of stress are commonly used to evaluate the welfare of animals when they are subject to conservation actions (Busch & Hayward, 2009). However, conceptual advances in animal welfare have recently redefined the field (Moberg, 2000) in a way that provides a better focus than stress and the antecedents of a synthesis between animal welfare and conservation (McLaren et al., 2008). Here, we describe why the concept and measurement of stress is not as useful to conservation as hoped, the new stress–distress paradigm as a potential solution, and how distress could unite animal welfare and conservation concerns because of its shared currency of biological costs to fitness. Graduates beginning research degrees in conservation should be forgiven for thinking stress is exclusively a bad thing. Not only might they describe their more independent studies as ‘stressful’, but the concept has been defined and applied narrowly in conservation. Stress is generally considered only as the consequence of external threats that are implicitly negative (e.g. stress as an ‘emergency response state’, Busch, 2010, or a ‘fight-or-flight’ response, Nelson, 2005); however, many other non-threatening contexts might also induce a stress response. Increased and intensified activity (e.g. when an animal is mating, hunting or migrating) may also stimulate a stress response, but have neutral or positive outcomes for fitness. Indeed, any temporary context in which the outcome has dramatic implications for fitness is often accompanied by a stress response. The stress response is a generalized reaction to imbalance caused by any factor that activates the hypothalamo–pituitary–adrenal (HPA) axis (Cockrem et al., 2004). Stress, therefore, can be the result of a homoeostatic, not just external, threat or stressor (Sapolsky, 1992) and so can have both positive and negative consequences for animal well-being and fitness (Moberg, 2000). Thus, stress is a concept with ambiguous implications for conservation. Given the conceptual ambiguity, it should not be surprising when commonly used metrics of stress (e.g. blood parameters, heart rate and behaviour) also yield contradictory relationships with fitness (Tarlow & Blumstein, 2007; Busch & Hayward, 2009). Not only might a stress response be the antecedent to improved fitness, but negative feedback also confounds the simple positive relationship between stress and its physiological indicators (i.e. intrinsic control, negative feedback, downregulation, Moberg, 1987; Sapolsky, 1992; Smith & Dobson, 2001; Nelson, 2005; Busch & Hayward, 2009). To cope with this complexity, the terms ‘acute’ and ‘chronic’ stress are often used, but these are difficult to demarcate and measure empirically in ways that can be generalized (Linklater, 2010). The problem is compounded by the intractability of longitudinal measurements of HPA activity (e.g. glucocorticoids) in most wild contexts and animals (Linklater, 2010). Acknowledging the current conceptual and empirical ambiguity of stress is a necessary first step to an animal welfare–conservation synthesis. The challenge to researchers integrating research in animal welfare and conservation is to identify conceptually simple and empirically measurable outcomes of mutual interest, such as distress. Darwinian fitness is the evolutionary ‘strand’ that unites fundamental with applied biology. Conservation biologists working at individual, population and community scales inevitably measure fitness and, in particular, those factors that impact it (i.e. biological costs). Comparative fitness is also an indicator of animal well-being (e.g. reproductive performance, Bradshaw & Bateson, 2000; Tarlow & Blumstein, 2007). Although the fields of animal welfare and conservation have traditionally been divided by their focus on the individual animal versus population (Bradshaw & Bateson, 2000), fitness has a simple and positive relationship with both conservation success and animal welfare. An advance at the intersection of animal welfare and conservation, therefore, must necessarily define itself through fitness and the biological costs that impact it. Distress is the biological cost of cumulative stressors (Moberg, 2000) and is defined and distinguished from stress by its negative consequences for animal fitness. Distress occurs when stress induces allostatic overload (McEwen & Wingfield, 2003) or becomes pathogenic (Sapolsky, 1992; Nelson, 2005). As such, the stress–distress paradigm (Moberg, 2000) is a remarkable advance in animal welfare because it better defines what to measure and when to act. It provides practitioners in animal welfare and conservation with a shared objective (i.e. to minimize distress) and empirical language centred on the measurement and evaluation of biological costs to individual fitness. The stress–distress paradigm will likely redefine the intersection between animal welfare and conservation, but has not as yet been widely applied (but see Wielebnowski, 2003; Linklater et al., 2010). There are some limitations to the application of fitness in the evaluation of animal welfare (Barnard & Hurst, 1996), and animal welfare and conservation advocates are likely to continue disagreeing on many aspects (Bradshaw & Bateson, 2000). Nevertheless, considerable progress might be made where those concerned about animal welfare and conservation agree on the importance of avoiding at least one empirically measurable biological character: distress. This consensus does not require the usual trade-off between welfare and conservation in the management of rare or threatened species. Referring to Bradshaw & Bateson's (2000) graph depicting the integration of welfare and conservation (see fig. 19.1): distress is an empirical measure of when welfare and conservation concerns enter the decision space that describes circumstances considered unacceptable to both. Wildlife managers are under increasing pressure to measure the welfare implications of their work, and the concept of stress and its metrics have been generally accepted as satisfactory, but they are not (Linklater, 2010; Linklater et al., 2010). We advocate a return to what organismal biologists do best: measuring and evaluating biological costs and fitness, and applying the stress–distress paradigm in conservation biology to meet the challenge posed by our concern for animal welfare. Besides, some studies already routinely combine measurements of stress reactivity with biological costs (i.e. distress: e.g. Bateson & Bradshaw, 1997; Waas, Ingram & Matthews, 1999; Zidon et al., 2009; Harcourt et al., 2010), and in our view, such combined measures are more appropriate. Applying the stress–distress paradigm would allow us to transcend the confusion and complications of stress alone as a concept and measurement. It then unites conservation and animal welfare practitioners where their fields overlap but were previously ill-defined. Evolutionary fitness, and the long-term and immediate biological costs to individual animals and populations that it measures, provides the framework and mutual objective necessary to facilitate greater communication between the fields. We thank Heiko Wittmer for comments on a draft paper.