Pain and stress in crustaceans?
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School of Biological Sciences, Queen’s University, MBC, Lisburn Road, Belfast, BT7 9BL, Northern Ireland, UK
1. Introduction
Pain and stress responses are widely used as indicatorsof potential suffering in vertebrates (Dawkins, 1980).However, there has been considerable debate aroundwhich specific vertebrate taxa may suffer (e.g.Broom,2001;Rose,2002),withtheinitialfocusonmammalsbeingextendedtoothergroupssuchasbirds(Gentleetal.,1991),amphibians (Machin, 1999; Stevens, 2004) and fish(Sneddon, 2003; Sneddon et al., 2003). Here, we considerwhether or not pain and stress might affect crustaceans toa degree that would give rise to welfare concerns.
2. Pain
Therearenumerousdefinitionsofpain.Forhumanstheyinvolve some form of self-reporting about the experiencewhilstfornon-humansubjectstheymayincludefeaturesof the behavioural response (Bateson, 1991; Broom, 2001).Defining pain in terms of a specific behaviour, however,poses a problem whenconsidering the taxonomic diversityamong vertebrates, and becomes even more complicatedwhen invertebrates are included. Thus,Broom (2001)described pain as ‘an aversive sensation and feeling,associated with actual or potential tissue damage’, adefinition that focuses on the internal experience ratherthan an external behavioural response. This is importantbecause various taxa differ markedly in their use of particular activities. It may be relatively easy for us tointerpret rapid withdrawal from a noxious stimulus,accompanied by particular vocalizations, postures andrubbing and/or limping as indicating pain when seen in aprimate or dog. However, whilst invertebrates may notshowthesespecificresponsesthisshouldnotbeinterpretedas evidence that they cannot experience pain.Sherwin(2001)noteswithrespecttoanimalpainthatan‘absenceof evidenceisnotevidenceofabsence’.Here,weexaminewhatevidence is available for pain in crustaceans and suggestfurther research that might cast light on the privateexperiences of this large, diverse invertebrate group.Pain has two key components. First, nociception is theability to detect noxious stimuli, which allows for a reflexresponse thatenables theanimal tomoveeitherall,orjust
Applied Animal Behaviour Science 118 (2009) 128–136
A R T I C L E I N F O
Article history:
Available online 17 March 2009
Keywords:
CrustaceaDecapodaWelfarePainStressRubbingAvoidance learningTrade-offsOpioids
A B S T R A C T
We consider evidence that crustaceans might experience pain and stress in ways that areanalogous to those of vertebrates. Various criteria are applied that might indicate apotential for pain experience: (1) a suitable central nervous system and receptors, (2)avoidance learning, (3) protective motor reactions that might include reduced use of theaffected area, limping, rubbing, holding or autotomy, (4) physiological changes, (5) trade-offs between stimulus avoidance and other motivational requirements, (6) opioidreceptors and evidence of reduced pain experience if treated with local anaesthetics oranalgesics, and (7) high cognitive ability and sentience. For stress, we examine hormonalresponses that have similar function to glucocorticoids in vertebrates. We conclude thatthere is considerable similarity of function, although different systems are used, and thustheremightbeasimilarexperienceintermsofsuffering.Thetreatmentoftheseanimalsinthe food industry and elsewhere might thus pose welfare problems.
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2009 Elsevier B.V. All rights reserved.
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This paper is part of a special issue entitled ‘‘Animal Suffering andWelfare’’, Guest Edited by Hanno Wu¨rbel* Corresponding author.
E-mail address:
r.elwood@qub.ac.uk(R.W. Elwood).
Contents lists available atScienceDirect
Applied Animal Behaviour Science
journal homepage: www.elsevier.com/locate/applanim
0168-1591/$ – see front matter
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the affected part, of its body away from the source of thestimulus. The concept of nociception does not imply anyadverse ‘feeling’. Second, ‘pain’ is the internal emotionalinterpretation or ‘suffering’ component of that perception.The unpleasant sensory and emotional quality of pain,coupled with the strong motivation to remove the sourceof noxious stimulation, appears to comprise an element of ‘suffering’ (Fiorito, 1986). It allows the animal to learn toavoid the situation that gave rise to the unpleasantexperience (Iggo, 1984). The ability to experience pain isadvantageous to the animal, that is, animals with theability are more likely to survive or maintain good bodycondition, which will enhance their reproductive successcompared to those without the ability. Thus, pain will befavoured by natural selection and may conceivably bewidespread among the animal taxa (Fiorito, 1986; Broom,2001; Sherwin, 2001).Whilstitisclearthathumansexperiencepain,whetheror not animals are capable of a similar experience is oftencontested. It is reasonably well accepted that all mammalshave the capacity to experience pain and there isincreasing acceptance that it occurs in all other vertebratetaxa. Indeed, this thinking forms the basis of legislation inthe United Kingdom where protection from pain duringscientific procedures is afforded to all vertebrates. Basedonthisthereisapresumptionthattheabilitytoexperiencepain had an early appearance in the evolution of thevertebrates. However, what is interesting is that in theUnited Kingdom the Animals (Scientific Procedures) Actwas amended in 1993 to include the common octopus,
Octopus vulgaris
, a mollusc, which has a separate evolu-tionary history of approximately 500 million years fromanimalsthatgaverisetothevertebrates.Iftheoctopuscanexperience pain it is quite possible that this ability couldhave arisen quite separately from that in vertebrates.Alternatively, it is possible that pain has a very earlyevolutionary origin that pre-dates the separation of thevertebrate and mollusc lines. It is also possible that theevolution of pain experience occurred prior to thedivergence of the arthropods from the lines giving riseto the molluscs and vertebrates. Again, however, painexperience could have arisen at some point during theevolution of the arthropods. Here, we examine thepossibility that it occurs within one major group of arthropods, the crustaceans, with some reference to othergroups.Attempting to infer feelings or mental states in animalsis fraught with difficulty (Dawkins, 2006) and the typicalapproach is to use argument by analogy (Dawkins, 1980;Sherwin, 2001). The basic point is that if an animalresponds to a potentially noxious stimulus in a mannersimilar to that observed to the same stimulus in humansthen it is reasonable to assume the animal has had ananalogous experience (Sherwin, 2001). However,Sherwin
(2001)notestherearedifferencesinouracceptanceofthisargument that depend on the species involved rather thanthe behaviour noted. Thus, if we observe a dog or primatewrithinginresponsetoan electricshockwetendtoacceptthat they may have experienced pain, however, much thesame response in an invertebrate is often dismissed asirrelevanttothequestionofpain(Sherwin,2001).Sherwin
(2001)notes the illogical stance that is taken and suggestsa more symmetrical approach when comparing verte-brates with invertebrates. He suggests we should eitherreject the argument by analogy for bothor accept for both.Various criteria have been proposed as demonstratingpain in mammals and these have been used in consideringpain in amphibians (Machin, 1999; Stevens, 2004), fish(Sneddon et al., 2003) and various invertebrates (Fiorito,
1986; Sherwin, 2001; Broom, 2007). Here, we considercriteria that are not dissimilar to those used in previouswork (Sherwin, 2001; Broom, 2007) but are appliedspecifically to the Crusteacea, particularly, but notexclusively, the Decapoda (crabs, lobsters, prawns andshrimps). This group is used extensively in the foodindustry and as such has received much of the attentionregarding potential pain perception. The criteria are: (1) asuitable central nervous system and receptors, (2)avoidance learning, (3) protective motor reactions thatmight include reduced use of the affected area, limping,rubbing, holding or autotomy, (4) physiological changes,(5) trade-offs between stimulus avoidance and othermotivational requirements, (6) opioid receptors andevidence of reduced pain experience if treated with localanaesthetics or analgesics, and (7) high cognitive abilityand sentience.
2.1. Central nervous system and suitable receptors
The central nervous system in crustaceans comprises adouble ventral nerve cord linking a series of ganglia. Theseganglia vary in complexity, with the largest found at theanteriorend,functioningasthebrain.Detailsregardingthenervous system of Crustacea have focused mainly on thelarger Decapoda (Laverack, 1988). These animals have lifespansofmanyyearsandbrainsthatlie,intermsofsizeandcomplexity, somewhere between the octopus and insects(Sandemanetal.,1992).Themotorsystemappearstobeinplaceand fixedwhenthe animalhatches, withthe sensoryunits increasing in number at each moult during growth(Laverack, 1988) under the influence of life-long neuro-genesis (Beltz and Sandeman, 2003). During ecdysis(moult) crustaceans are vulnerable to damage, and aseach stage increases the complexity of the sensoryapparatus, newly added sensors must function immedi-ately (Ali, 1987).In crustaceans, receptor neurons are packaged intocuticular extensions of the exoskeleton called sensilla(Derby and Steullet, 2001). Various receptors are found onthe surface including mechanoreceptive, chemoreceptiveand bimodal sensillae (Ali, 1987). The chemosensilla arepresent on most or all surfaces (Cate and Derby, 2000;Aggio and de Freitas, 2007) and enhance the probabilitythatexternalchemicalchangeswillbedetected(DerbyandSteullet, 2001). By having multiple sensors the animal canminimize the impact of damage by increasing theprobability that some sensors remain undamaged andfunctional (Daniel et al., 1996). To date, however, only theaesthetascs, thin walled chemosensory pegs on theantennules, and associated asymmetric hairs have beenshowntoexclusivelymediatespecificactivities(Aggioandde Freitas, 2007).
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The crustacean brain is quite unlike that described invertebrates, and thus, some might dismiss the idea of painexperience in the same way that that the possibility of fishexperiencing pain has been dismissed (Rose, 2002). Therationalefordismissalisthathumanpainisexperiencedinparts of the cerebral cortex and thus animals lacking thisstructurecannotexperiencepain(Rose,2002).Crustaceanshave no cerebral cortex, and thus this argument is used.Using the same logic it could be suggested that becausecrustaceans lack any of the visual systems found inhumans they must be blind. This is not the case ascrustaceans have a well developed visual ability, althoughbased on an entirely different CNS and receptors. Clearlythe same function can arise in different animal taxa, usingdifferent morphology, and it appears to be illogical toaccept this reasoning for some experiences but to dismissit for pain.A second suggestion for rejecting a pain experience incrustaceans is that the brain might be too small. However,Broom (2007)notes that brain size does not necessarilyequate to complexity of function so that the argumentshould not be based on size
per se
. For example, the smallbrain of many small fish has not excluded them fromprotectivelegislation. Nevertheless,we note thatthe brainof large crustaceans, such as a lobster, is likely to beconsiderably larger than that of many vertebrates. There-fore it is the complexity of function rather than the size of the brain that should be an indicator of welfare concernsand it must be noted that complexity may not alwayscorrelate with size (Broom and Zanella, 2004).
2.2. Avoidance learning
There seems to be no selective advantage in sufferingfrom pain
per se
so the advantage must arise from theanimal taking more effective measures to avoid thatspecific experience in the future. Thus, swift avoidancelearning is a central test for the hypothesis of a painexperience.Thiswasexaminedinthecrab,
Chasmagnathus granulatus,
by placing the animals in a dark compartmentof a double-chamber device and allowing them to movetowards a light compartment (Denti et al., 1988). Experi-mental crabs received a shock in the light compartment,whilst controls were not subjected to the stimulus. After1 min both experimental and control crabs were free toreturn to the dark compartment. A single trial was enoughto establish an association between light and shock thatwasdetectedupto3 hlater,butnotafter24 h.Subsequentexperiments involving multi-trial training showed reten-tion of learned behaviour after a 24 h rest interval in adifferent environment from that used in training (Fernan-dez-Duqueetal.,1992).Thecrabswereshowntoavoidthelight chamber indicating that they associated it with anaversive situation. The learned outcome was not a fasterescape response to the stimulus but rather refraining fromentering the light compartment (Fernandez-Duque et al.,1992).Similarexperimentswithcrayfish(
Procambarusclarkia
)also demonstrate that they learn to associate the turningon of a light with a shock that was given 10 s later. Theylearned to respond by walking to a safe area in which theshockwasnotdelivered(Kawaietal.,2004).However,thisonlyoccurredifthecrayfishwasfacingtheareatowhichitcould retreat to avoid the shock. If it was facing away fromthe safe area the animal did not walk but responded to theshock by a tail-flick escape response. Despite repeatedpairingsoflightandshocktheanimaldidnotlearntoavoidthe shock by tail-flicking in response to light. Curiously,when the animals that had experienced shocks whilstfacing away from the safe area were subsequently testedfacing towards the safe area they showed a very rapidavoidance of the shock upon the onset of the light. Thus,theyseemedtohavelearnedtheassociationalthoughtheyhadnotpreviouslyusedittoavoidtheshock.Thesestudiesshow ability in decapods that fits the minimum criterionfor pain experience.
2.3. Protective motor reactions that might include reduceduseoftheaffectedarea,limping,rubbing,holdingorautotomy
Zimmerman (1986)defined a pain experience, in part,as eliciting‘protective motor andvegetative reactions’ andguarding or rubbing of affected areas is observed invertebrates (Stasiak et al., 2003).Weary et al. (2006)
arguedthatrubbingdenotedanawarenessofthesiteofthenoxious stimulus andSneddon et al. (2003)noted thatrainbow trout (
Oncorhynchus mykiss
) that had noxiouschemicalsinjectedintothelipshowedrubbingoftheliponthesubstrate.Inrats,groomingactionsfollowinganoxiousstimulus appear to be aimed at removing the cause of painand use a different organisation than those related to themaintenance of the pelage, thermoregulation, socialsignalling, or arousal reduction (Vos et al., 1998).Furthermore, in vertebrates, rubbing may activate fibresthat inhibit nociceptor afferents, that is, it activates part of the endogenous analgesic system.The rubbing or grooming of specific areas has beenrecently investigatedin the glass prawn,
Palaemon elegans
,a small littoral decapod crustacean (Barr et al., 2008).When sodium hydroxide or acetic acid solution wasapplied to one antenna there was a significant increase,compared to water control, in grooming of that antennaduring which it was pulled though the small pincers andmouth parts of the animal. Furthermore, there was anincrease in rubbing of the antenna against the side of thetank. These grooming and rubbing activities were specificto the treated antenna with no increase seen with theuntreated antenna. The animal seemed to be aware of thespecific location of the noxious stimulus and directed itsattention to that specific location. Pinching an antennawith forceps elicited a higher level of rubbing of theantenna against the tank wall but had no effect on theamount of grooming. Furthermore, when acetic acid wasapplied to an eye of a glass prawn there was a markedincrease in grooming, compared to water control treat-ment, which often involved both pincers moving simulta-neously but the two being moved in very different andcomplex ways. The grooming was directed specifically tothat eye, again demonstrating that the animal is aware of the locationofthenoxiousevent(Barret al.,unpublished).Whether this involves the activation of an endogenousanalgesic system has yet to be investigated, indeed, it is
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