Elsevier

Animal Behaviour

Volume 97, November 2014, Pages 201-212
Animal Behaviour

Review
Defining and assessing animal pain

https://doi.org/10.1016/j.anbehav.2014.09.007Get rights and content

Highlights

  • Assessing pain in animals is problematic without a distinct definition.

  • We provide clear criteria for animal pain that can be used to evaluate if pain occurs.

  • The empirical evidence for pain is reviewed over a wide range of species.

  • By fulfilling all criteria, a given species can be considered as experiencing pain.

The detection and assessment of pain in animals is crucial to improving their welfare in a variety of contexts in which humans are ethically or legally bound to do so. Thus clear standards to judge whether pain is likely to occur in any animal species is vital to inform whether to alleviate pain or to drive the refinement of procedures to reduce invasiveness, thereby minimizing pain. We define two key concepts that can be used to evaluate the potential for pain in both invertebrate and vertebrate taxa. First, responses to noxious, potentially painful events should affect neurobiology, physiology and behaviour in a different manner to innocuous stimuli and subsequent behaviour should be modified including avoidance learning and protective responses. Second, animals should show a change in motivational state after experiencing a painful event such that future behavioural decision making is altered and can be measured as a change in conditioned place preference, self-administration of analgesia, paying a cost to access analgesia or avoidance of painful stimuli and reduced performance in concurrent events. The extent to which vertebrate and selected invertebrate groups fulfil these criteria is discussed in light of the empirical evidence and where there are gaps in our knowledge we propose future studies are vital to improve our assessment of pain. This review highlights arguments regarding animal pain and defines criteria that demonstrate, beyond a reasonable doubt, whether animals of a given species experience pain.

Section snippets

Pain: a complex issue

Nociception, the capacity to respond to potentially damaging stimuli, is a basic sensory ability (Purves et al., 2012), and even occurs in bacteria (Berg, 1975). Testing whether animals are able to respond to noxious stimuli is typically straightforward, even though many nociceptors are multifunctional (Tsagareli, 2011). Philosophers and scientists, however, make a distinction between pain and nociception (Allen, 2011) because pain is primarily a subjective experience of anguish, despair and

Function of pain

Nociception is a fundamental sensory system that alerts an animal or human to potential damage. Nociceptive pathways connect with brain areas important for motivation, and animals are motivated to avoid the injurious stimulus and protect themselves from further damage (Bateson, 1991). Therefore, it would be adaptive to evolve such a system and many diverse taxa possess specific receptors, i.e. nociceptors that detect damaging stimuli, for example Drosophila melanogaster and Caenorhabditis

Definition of animal pain

Because it is impossible to know how other humans feel when they are in pain, we rely upon their ability to communicate their experience of pain. This illustrates how difficult it is to measure pain in humans that cannot speak (e.g. neonates) or animals that do not share our language. Therefore, the commonly used definition of human pain cannot be directly applied to animals because it relies on either knowing how animals feel or requiring them to be able to communicate their subjective

The neural apparatus

Nociceptors (A and C fibres) are found in most groups of vertebrates, including mammals (Carstens and Moberg, 2000, Weary et al., 2006), birds (Breward and Gentle, 1985, Gentle et al., 2003, Gentle and Tilston, 2000, Gentle et al., 2001, Hothersall et al., 2011, McKeegan, 2004, McKeegan et al., 2002), reptiles (Liang and Terashima, 1993, Terashima and Liang, 1994), amphibians (review in Guénette, Giroux, & Vachon, 2013) and fish (e.g. Roques et al., 2010, Sneddon, 2002). However, the proportion

Whole Animal Response

Stimuli that are considered painful in humans have been shown to induce similar physiological and behavioural changes in other nonhuman mammals. The majority of physiological changes associated with potentially painful stimuli are mediated by the sympathetic nervous system and hypothalamic–pituitary–adrenal axis (HPA). The sympathetic responses can be determined either directly by measuring the circulating catecholamines, adrenaline and noradrenaline (e.g. Mellor et al., 2002, Raekallio et al.,

Whole Animal Response

Potentially painful stimuli influence a range of physiological responses in birds (review in Prunier et al., 2013), for example plasma corticosterone and heart rate increase after beak trimming and feather removal (Davis et al., 2004, Gentle and Hunter, 1991, Glatz, 1987, Glatz and Lunam, 1994). Birds also exhibit withdrawal responses to a variety of noxious treatments that are used as standard in mammalian pain studies, for example foot withdrawal in response to high temperature in parrots,

Whole Animal Response

Amphibians show a classic wiping response to application of acetic acid as well as a withdrawal response to noxious heat and mechanical stimulation (Willenbring & Stevens, 1996). Both responses are attenuated by administration of compounds with analgesic properties (Kanetoh et al., 2003, Mohan and Stevens, 2006, Stevens et al., 2009). Similarly, reptiles display characteristic responses to painful stimulation (e.g. limb retraction in response to formalin in Speke's hinged tortoise, Kinixys

Whole Animal Response

Teleost fish move away from noxious stimuli that would cause pain in mammals. For example, koi carp, C. carpio, move away from a clamp exerting high mechanical pressure to the lip and tail and this withdrawal response is decreased when the fish are lightly anaesthetized (Stockman, Weber, Kass, Pascoe, & Paul-Murphy, 2013). Classical conditioning studies using the negative reinforcement of electric shock is a popular paradigm in fish experiments (e.g. Yoshida & Hirano, 2010). Rainbow trout and

Molluscs

Molluscs include bivalves, gastropods, nudibranchs and cephalopods, which differ markedly in morphology, behaviour and neural complexity (Crook & Walters, 2011). Various species respond to noxious stimuli and show associative learning (Kavaliers, 1988; Crook & Walters, 2011). Cephalopods are highly mobile with a large, complex brain and good learning ability (Mather, 2011) and they have recently been included in the European Union Directive (2010/63/EU) that provides protection from suffering

Arthropods: decapods

Various decapod crustaceans have been investigated to determine whether responses to noxious stimuli are merely nociceptive reflexes, with no short-term or long-term effects on CNS function. Shore crabs, Carcinus maenas, show rapid (two-trial) discrimination avoidance learning when shocked in one of two dark shelters (Magee & Elwood, 2013). Further, hermit crabs, Pagurus bernhardus, that received a single shock within their shell showed a prolonged increase in motivation to leave that shell and

Arthropods: insects

Insects respond vigorously to noxious stimuli, but these responses can be suppressed (e.g. during sexual cannibalism, Sakaluk, Campbell, Clark, Johnson, & Keorpes, 2004) or intensified (e.g. after ultraviolet exposure, Babcock, Landry, & Galko, 2009). The molecular mechanisms mediating these behaviours are at least partially known in some species (e.g. D. melanogaster) and appear to be homologous to the molecular mechanisms mediating nociception in mammals (Johnson & Carder, 2012). Nociception

Principle of triangulation

Pain in animals has been assessed using a wide range of indices, and it has been argued that none of these indices when taken in isolation can be considered as definitive evidence of ‘pain’ in animals (e.g. Rose et al., 2014). However, we, along with other authors, (e.g. Bateson, 1991, Mason and Mendl, 1993, Nicol et al., 2009, Sneddon, 2004, Sneddon, 2009, Sneddon, 2011, Sneddon, 2013, Weary et al., 2006; Elwood, 2012, Flecknell et al., 2011) are advocating not that these individual isolated

Conclusions

Our summary of the evidence supports the conclusion that many animals can experience pain-like states by fulfilling our definition of pain in animals, although we accept that 100% certainty cannot be established for any animal species. Nevertheless, the ‘precautionary principle’, the idea that it is better to err on the side of more protection for a group of animals if it is beyond reasonable doubt that they experience pain (e.g. Andrews, 2011), proposes that we should act as if at least some

Acknowledgments

We are grateful for comments from the Executive Editor, Ana Sendova-Franks, and two anonymous referees. L.U.S. is grateful for funding from EU FP7, National Centre for the 3Rs, UK (NC3Rs), Society of Biology, Society for Endocrinology and Universities Federation for Animal Welfare (UFAW), UK; M.L. is grateful to NC3Rs, UK and S.A.A thanks the Natural Sciences and Engineering Research Council of Canada (NSERC) for funding.

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