Evidence for pain in decapod crustaceans
RW Elwood 2012.
Pain and stress in crustaceans?
RW Elwood, S Barr, L Patterson 2009.
There is now good evidence that crustaceans can experience pain, argues Professor Robert Elwood of Queen’s University, Belfast. Pain in crustaceans is an important area of animal welfare research because, as Professor Elwood states in the above 2012 research paper1:
| “The substantial numbers of them used in the food industry and the extreme treatments to which they are exposed should indicate the potential for improved welfare if evidence of pain is found.” |
Extreme treatments are not confined to methods of killing, such as boiling lobsters alive, but also include mutilations and long distance transport. In some crab fisheries, the claws are pulled off and retained whilst the animal is thrown back to the sea alive but unable to feed (2 cited in 1).
The current author notes that a panel of scientists, commissioned by the European Food Safety Authority (EFSA), has similarly concluded that the evidence indicates decapod crustaceans (crabs, lobsters, crayfish and prawns etc) can feel pain3. In its Scientific Opinion on animals used for scientific research purposes, EFSA therefore recommended that only the most humane methods should be used when killing these animals since:
| “The largest of these animals [decapod crustaceans] are complex in behaviour and appear to have some degree of awareness. They have a pain system and considerable learning ability. Little evidence is available for many decapods, especially small species. However, where sub-groups of the decapods, such as the prawns, have large species which have been studied in detail they seem to have a similar level of complexity to those described for crabs and lobsters.3“ |
It is elsewhere reported that crustaceans are beginning to be included in animal welfare regulation in some countries, such as Norway4 and New Zealand3. This web page describes some of the evidence presented in Professor Elwood’s 2012 paper, as well as some presented previously in a 2009 paper that he co-authored5 with Stuart Barr and Lynsey Patterson. For greater explanation and more descriptions of studies, please refer to the two papers at the top of this page.
Researching pain in crustaceans.
As has been discussed in Do fish feel pain? the key question, when researching pain in animals, is whether the animal’s response to a noxious, i.e. harmful, stimulus (“nociception”) entails an unpleasant feeling (pain). Does the animal’s response to harmful stimuli, such as heat (moving either all, or just the affected part of its body away from the source of the heat), involve pain or is it merely a reflex response without feeling? The following criteria have been suggested by various authors that might indicate the ability to feel pain. Professor Elwood’s 2012 paper discusses the last 4 while the first 4 were discussed in the 2009 paper5.
- The presence of nociceptors
- A ‘suitable’ central nervous system
- Decreased responses with analgesics or opioids;
- High level of cognitive ability
- Avoidance learning;
- Physiological changes;
- Protective motor reactions;
- Motivational trade-offs between pain and other requirements.
Nociceptors and a central nervous system.
The 2009 paper describes the central nervous system in crustaceans5. Crustaceans possess nociceptors which are packaged into cuticular extensions of the shell, called sensilla. They have a central nervous system which comprises a double ventral nerve cord linking a series of ganglia. The largest ganglia is found at the anterior end (head) and functions as the brain.
While the crustacean brain is small and differs from the vertebrate brain, this does not preclude the possibility of experiencing pain. Small brain size does not necessarily mean there is no complexity of brain function (6 cited in 1) and it is known that the same function may be performed by different anatomical structures in different types of animal. For example, crustaceans do not possess any of the visual systems found in humans, yet they have a well developed visual ability based on an entirely different CNS and receptors.
Effects of analgesics or opioids.
The 2009 paper describes the effects of opioid analgesics (pain killers) as similar to those observed in vertebrates. For example, in a study of the crab (Chasmagnathus granulatus), the animals were given an electric shock which caused a defensive threat display. Morphine injections reduced the sensitivity to electric shocks in a dose-dependent manner7. Opioids appear also to reduce the fear response in crustaceans. In another study, the normal response of escape running from a novel stimulus (a dark moving screen) was lessened by morphine8. The action of morphine on crustaceans indicates the possibility that crustaceans, like vertebrates, possess endogenous analgesics (pain killers) to regulate pain.
Cognitive ability.
Cognition is the ability to acquire and manipulate information9 cited in 5 and animals with particularly good abilities are often assumed to be more likely to experience pain6,10 cited in5. The 2009 paper 5 argues that hermit crabs:
| “show an excellent ability to gather, manipulate and use information from multiple sources, indicating a higher cognitive ability than generally recognised.” |
These crustaceans gather information about potential new shells and integrate that with information they have about the shell they currently occupy before deciding which is the better of the two. They use several sources of information, such as external and internal shape and size, using visual and tactile information. The following short clip shows a hermit crab move into a new shell.
Hermit crabs may also fight over the possession of shells, where one crab tries to evict another from its shell. In deciding whether or not to do this, the hermit crab uses information about its own shell, the other shell and the other shell’s occupier. Defenders assess the vigour of an attack and make decisions about whether or not to resist the attacker.
Avoidance learning.
Shore crab (Carcinus maenas). In experiments, this species rapidly learned to avoid one of two dark shelters if they had previously received a shock there
Credit: Jean-Michel Bernard.
The 2012 paper1 discusses the role of pain in learning. A reflexive response to a harmful stimulus can give an immediate protection from it. For example, when a human hand touches a hot object, the hand is involuntarily withdrawn instantly in a reflex action. Where pain is involved in a response to harmful stimuli, this is presumed to have developed to provide a longer term protection. Through an unpleasant experience of pain, an animal learns to avoid the same stimulus in future. The ability of an animal to learn to avoid something unpleasant therefore suggests that pain is involved.
Several studies described in the 2012 paper demonstrate the ability for avoidance learning in decapods:
- Crabs (Chasmagnathus granulatusability) were less likely to enter a light compartment if they had previously received an electric shock there11
- Shore crab (Carcinus maenas) were less likely to enter a one of two dark shelters if they had previously received a shock there12
- Crayfish (Procamarus clarki) learned to associate a light signal with a shock and to avoid the shock by walking forward to the other end of a box13.
Physiological changes.
According to the 2012 paper5, decapods have a stress hormone called the Crustacean Hyperglycaemic Hormone (CHH) that functions in a way similar to corticosteroids in vertebrates. It causes glycogen to be converted to glucose and elevates levels of lactate.
Protective motor reactions.
Glass prawn (Palaemon elegans). After scientists brushed acetic acid onto one antenna, this species showed a marked increase in grooming and rubbing of the area.
Credit: Christophe Quintin.
In a study of glass prawn (Palaemon elegans)14, the animals showed a marked increase in grooming of the affected antenna after scientists brushed acetic acid (or sodium hydroxide) onto one antenna, as compared to control animals brushed with water. Rubbing the antenna against the wall of their tank also increased. This type of behaviour, in response to a noxious stimulus on an area of the body, is similar to that seen in vertebrates. This behaviour, argues Professor Elwood in the 2012 paper, suggests an awareness of the specific site and is not easily explained as a reflex.
Motivational trade-offs.
Hermit crab (Pagurus Bernhardus). These crabs are extremely vulnerable when outside of their shell but will choose to leave the shell to avoid an electric shock. The strength of shock required for them to vacate partly depends on how much they value the shell compared to other shells.
Credit: David Spreekmeester.
An animal that experiences pain will be motivated to avoid it. However, the animal may have other competing needs that motivate the animal to behave in a way that does not avoid the pain. For example, fish subjected to an electric shock whilst feeding are less likely to give up feeding to avoid the shock if they have been deprived of food. Motivational trade-offs imply a central decision process that is more than simple reflex and indicate the relative value to the animal.
Some studies have tested for motivational trade-off in hermit crab between the motivation to avoid an electric shock inside their shell and the motivation not to leave the protection of the shell15 & 16 cited in 1. Hermit crabs show strong preferences for particular species of shell as determined by shell choice experiments. Those in the less preferred species got out of their shell at a lower voltage than did those in the preferred species15.
A number of crabs that evacuated the shell then felt deep into the shell as if searching for the source of the noxious stimulus15 & 16 cited in 1. Some crabs walked away from their shells, leaving themselves naked and therefore vulnerable, in order to escape the noxious stimulus. They were prepared to pay this price in order to avoid being shocked.
Conclusion.
The studies noted above are consistent with the concept of pain and demonstrate that the responses to noxious, potentially tissue damaging stimuli go beyond that predicted by nociceptive reflex. Elwood argues the evidence shows there is a “strong possibility” that decapods, as well as fish, do experience pain and that
| “both taxa should be treated as though they are able to experience the negative affective state of pain”. |
A Mood. January 2014.
1. Elwood, R.W., 2012. Evidence for pain in decapod crustaceans. Animal Welfare, Volume 21, Supplement 2, June 2012 , pp. 23-27(5). Universities Federation for Animal Welfare.
2. Patterson, L., Dick, J.T.A. and Elwood, R.W., 2009. Claw loss and feeding ability in the edible crab, Cancer pagurus: implications of fishery practice. Applied Animal Behaviour Science 116: 302-305.
3. The EFSA Journal (2005) 292, 1-46 – Opinion on the “Aspects of the biology and
welfare of animals used for experimental and other scientific purposes”. Accessed on 16 November 2013 at: http://www.efsa.europa.eu/en/efsajournal/doc/292.pdf.
4. Electrical stunning of edible crabs, Report no: 18/2013, Nofima, ISBN 978-82-8296-0279-3 (pdf). Accessed on 16 November 2013 at: http://www.nofima.no/filearchive/Rapport%2018-2013.pdf.
5. Elwood, R.W., Barr, S. and Patterson, L., 2009. Pain and stress in crustaceans? Applied Animal Behaviour Science 118 (2009) 128–136.
6. Broom, D.M., 2007. Cognitive ability and sentience: which aquatic animals should be protected? Diseases of Aquatic Organisms 75: 99-108. http://www.int-res.com/articles/dao_oa/d075p099.pdf
7. Lozada, M., Romano, A., Maldonado, H., 1988. Effects of morphine and naloxone on a defensive response of the crab Chasmagnathus granulatus. Pharm. Biochem. Behav. 30, 635–640.
8. Maldonado, H., Romano, A., Lozada, M., 1989. Opiate action on response level to danger stimulus in the crab Chasmagnathus granulatus. Behav. Neurosci. 103, 1139–1143.
9. Dukas, R., 1998. Introduction. In: Dukas, R. (Ed.), Cognitive Ecology: The Evolutionary Origin of Information Processing and Decision Making. Chicago University Press, Chicago, pp. 1–19.
10. Dawkins, M.S., 2006. Through animal eyes: what behaviour tells us. Appl. Anim. Behav. Sci. 100, 4–10.
11. Denti, A., Dimant, B. and Maldonado, H. 1988. Passive avoidance learning in the crab Chasmagnathus granulatus. Physiology & Behavior. Volume 43, Issue 3, 1988, Pages 317–320 http://www.sciencedirect.com/science/article/pii/0031938488901941.
12. Magee, B. and Elwood, R.W. 2013. Shock avoidance by discrimination learning in the shore crab (Carcinus maenas) is consistent with a key criterion for pain. http://jeb.biologists.org/content/216/3/353.full.pdf+html.
13. Kawaia, N., Konob, R. and Sugimotob, S., 2004. Behavioural Brain Research. Volume 150, Issues 1–2, 2 April 2004, Pages 229–237Avoidance learning in the crayfish (Procambarus clarkii) depends on the predatory imminence of the unconditioned stimulus: a behavior systems approach to learning in invertebrates. http://www.sciencedirect.com/science/article/pii/S0166432803002614.
14. Barr, S., Laming, P.R., Dick, J.T.A. and Elwood, R.W., 2008. Nociception or pain in a decapod crustacean? Animal Behaviour 75: 745-751. http:/www.researchgate.net/publication/222668013_Nociception_or_pain_in_a_decapod_crustacean/file/9c960519cb4de4647e.pdf
15. Appel, M. and Elwood, R.W., 2009. Motivational trade-offs and potential pain experience in hermit crabs. Applied Animal Behaviour Science 119: 120-124.
16. Appel, M. and Elwood, R.W., 2009. Gender differences, responsiveness and memory of a potentially painful event in hermit crabs. Animal Behaviour 78: 1373-1379.
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