Gender differences, responsiveness and memory of a potentially painful event in hermit crabs Mirjam Appel, Robert W. Elwood * School of Biological Sciences, Queen’s University, Belfast article info Article history: Received 9 June 2009 Initial acceptance 30 July 2009 Final acceptance 4 September 2009 Available online 12 October 2009 MS. number: 09-00379R Keywords: avoidance crustacean hermit crab memory nociception Pagurus bernhardus pain Nonreflexive responses to a noxious event and prolonged memory are key criteria of a pain experience. In a previous study, hermit crabs, Pagurus bernhardus, that received a small electric shock within their shell often temporarily evacuated the shell and some groomed their abdomen and/or moved away from their vital resource. Most, however, returned to the shell. When offered a new shell 20 s later, shocked crabs were more likely than nonshocked crabs to approach and move into a new shell and did so more quickly (Elwood & Appel 2009, Animal Behaviour, 77 , 1243–1246). Here we examined how increasing the time between the shock and the offering of a new shell influences the response. There was evidence of a memory of the aversive shock that lasted at least 1 day. Crabs tested after 30 min and 1 day were more likely to approach the shell and new shells were more likely to be taken 30 min after the shock. Shocked crabs approached the new shell more quickly and used fewer probes of the chelipeds prior to moving in and these results were stable over time and significant for specific times up to 1 day. Females were more likely than males to evacuate shells and did so after fewer shocks. These results extend previous work and demonstrate an extended memory of having been shocked. The findings are consistent with respect to criteria for pain that are accepted for vertebrates. Ó 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Nociception is the ability to detect and respond to noxious stimuli (Sneddon 2004). It is easy to demonstrate in humans and nonhuman animals because a consistent response to a noxious stimulus, by withdrawing all or just the afflicted part of the body, indicates detection and protection. Pain is an internal, aversive experience or feeling that is often associated with nociception (Broom 2007). Pain may be demonstrated in humans because they can self-report on whether or not the experience is unpleasant and they may also indicate the level of unpleasantness on a scale. Determining whether animals experience pain, however, is more difficult and various criteria have been suggested that might indi- cate pain (Bateson 1991; Broom 2001; Elwood et al. 2009). Pain provides a strong motivation for learning so the animal reduces future tissue damage and thus enhances fitness (Broom 2001). For example, conditioned place avoidance is seen in rats, Rattus norvegicus, when acetic acid is repeatedly injected in the same section of the test apparatus and this is suggested to demonstrate a negative affective state (Johansen et al. 2001). Thus avoidance learning, coupled with prolonged memory, is expected to be shown if pain is experienced. Second, we may expect to see a change in behaviour directly associated with reduced use of the afflicted part of the body. For example, an animal may protect the afflicted area by reducing the load placed on a limb and the animal may limp. It may avoid use of a forelimb in handling tasks or it may hold, rub or groom the afflicted area (Weary et al. 2006). Third, we expect to see analgesics and local anaesthetics reduce the responses to a noxious, potentially painful stimulus such that treatment with these substances will reduce avoidance learning and reduce limping and rubbing, etc. (Bateson 1991; Sneddon 2003). Fourth, because pain may be viewed as a motivation and because different motivations compete centrally for overt behav- ioural expression (McFarland & Sibly 1975), we would expect to see specific pain responses to be traded off against other motivational requirements (Millsopp & Laming 2008; Elwood et al. 2009). For example, a noxious stimulus delivered when the animal is feeding might completely inhibit feeding if the animal has fed recently but there may be less inhibition if the animal had been food deprived (Millsopp & Laming 2008). Coupled with this expectation is the requirement for the response to be more than a simple reflex and to involve the brain in mediating the response. Clearly, the behav- ioural responses noted above would normally fulfil this expecta- tion. Other expectations of pain include suitable receptor systems and central nervous systems (CNS), even if these are not identical to those of humans (Elwood et al. 2009), possible physiological changes such as a shift in ventilation rate and heart rate and * Correspondence: R. W. Elwood, School of Biological Sciences, Queen’s Univer- sity, Belfast, MBC, 97 Lisburn Road, Belfast BT9 7BL, U.K. E-mail address: r.elwood@qub.ac.uk (R.W. Elwood). Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav 0003-3472/$38.00 Ó 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2009.09.008 Animal Behaviour 78 (2009) 1373–1379