Behavioural Processes 130 (2016) 31–35 Contents lists available at ScienceDirect Behavioural Processes jo ur nal homep ag e: www.elsevier.com/locate/behavproc Trade-offs between predator avoidance and electric shock avoidance in hermit crabs demonstrate a non-reﬂexive response to noxious stimuli consistent with prediction of pain Barry Magee, Robert W. Elwood ∗ School of Biological Sciences, Queen’s University Belfast, Belfast BT9 7BL, UK a r t i c l e i n f o Article history: Received 19 March 2016 Received in revised form 31 May 2016 Accepted 30 June 2016 Available online 1 July 2016 Keywords: Hermit crab Pain Predator odour Reﬂex Trade-off a b s t r a c t Arthropods have long been thought to respond to noxious stimuli by reﬂex reaction. One way of testing if this is true is to provide the animal with a way to avoid the stimulus but to vary the potential cost of avoidance. If avoidance varies with potential cost then a decision making process is evident and the behaviour is not a mere reﬂex. Here we examine the responses of hermit crabs to electric shock within their shell when also exposed to predator or non-predator odours or to no odour. The electric shocks start with low voltage but increase in voltage with each repetition to determine how odour affects the voltage at which the shell is abandoned. There was no treatment effect on the voltage at which hermit crabs left their shells, however, those exposed to predator odours were less likely to evacuate their shells compared with no odour or low concentrations of non-predator odour. However, highly concentrated non-predator also inhibited evacuation. The data show that these crabs trade-off avoidance of electric shock with predator avoidance. They are thus not responding purely by reﬂex and the data are thus consistent with predictions of pain but do not prove pain. © 2016 Elsevier B.V. All rights reserved. 1. Introduction Pain in animals has been deﬁned as ‘an aversive sensory experi- ence caused by actual or potential injury that elicits protective and vegetative reactions, results in learned behaviour, and may modify species speciﬁc behaviour’ (Zimmerman, 1986). The initial percep- tion involves nociceptors and it is possible for these to trigger a reﬂex response to move part or the whole of the organism away from the stimulus without the emotional experience (Elwood et al., 2009). Thus, mere withdrawal from the stimulus is not evidence of pain because it is easily explained as a nociceptive reﬂex. There- fore other approaches are required by which various behavioural and physiological criteria (Bateson 1991; Elwood 2012; Sneddon et al., 2014) may be tested and only if fulﬁlled can pain be deemed a possibility. In particular, responses that cannot be just a reﬂex are required before the idea of pain can be entertained. For example, octopus show prolonged, apparently non-reﬂexive activities directed at the site of a wound (Alupay et al., 2014). Squid show greater responsiveness to approaching stimuli after an experimentally induced localised injury (Crook et al., 2011). Fur- ∗ Corresponding author. E-mail address: r.elwood@qub.ac.uk (R.W. Elwood). ther, squid that have the sensory input of a localised injury blocked by local anaesthetic do not survive an interaction with a predator as well as those not blocked. However, just the local anaesthetic without the wound had no detrimental effect (Crook et al., 2014). That is, perception of the input provides long-term protection and increases survival. With respect to decapod crustaceans, long term rubbing in prawns (Barr et al., 2008) and hermit crabs (Appel and Elwood, 2009a,b) indicates an awareness of the location of the wound site (Weary et al., 2006) and the prolonged, complex rubbing appears to be beyond a reﬂex (Elwood, 2011). Further, avoidance and dis- crimination learning has been demonstrated in shore crabs where they avoided a shelter in which they received a noxious stimu- lus and developed a preference for a similar shelter, in which no shock was given, offered during the same trial (Magee and Elwood, 2013). This long-term reduction of tissue damage by avoiding the noxious stimuli in the future is a key criterion for pain (Bateson, 1991). Further, hermit crabs that have been shocked within their shell show an increased likelihood of changing shells that lasts at least 24 h (Appel and Elwood, 2009a; Elwood and Appel, 2009) indi- cating a long-term shift in motivation to avoid the shell in which shock was experienced. Further evidence consistent with pain is a general anxiety after noxious stimuli, as evidenced by crayﬁsh avoiding brightly lit areas of a maze after being repeatedly subject http://dx.doi.org/10.1016/j.beproc.2016.06.017 0376-6357/© 2016 Elsevier B.V. All rights reserved.