AnimalSentience2016.X:BrownCommentary2onKeyonFishPain Fishpain:aninconvenienttruth CommentaryonKeyonFishPain CulumBrown BiologicalSciences MacquarieUniversity Abstract:Whetherfishfeelpainisahotpoliticaltopic.Theconsequencesofourdenialare huge given the billions of fish that are slaughtered annually for human consumption. The economic costs of changing our commercial fishery harvest practices are also likely to be great. Key outlines a structure-function analogy of pain in humans, tries to force that templateontherestofthevertebratekingdom,andfails.Histargetarticlehassofarelicited 34 commentaries from scientific experts from a broad range of disciplines; only three of these support his position. The broad consensus from the scientific community is that fish mostlikelyfeelpainanditistimegovernmentsdisplaycourageenoughtoact. Culum Brown [email protected] studies the behavioural ecology of fishes with a special interest in learning and memory. He is Associate Professor of vertebrate evolution at Macquarie University, Co-Editor ofthevolumeFishCognitionandBehavior,andEditorfor Animal Behaviour of the Journal of Fish Biology. https://sites.google.com/site/culumbrown/ Key(2016,2016a,2016b)hasputforthastructure-functionanalogyofpaininhumansand thensetsouttodiscoverhowfaronemighttakethattemplatewhenappliedtotherestof thevertebratekingdom–well,fishandtheoddrodentatanyrate.Morethan30 commentersrespondedtothearticleandthisclearlyshowsthatthistopicisstill controversial.Ofthese,three(Rose;Hart;Diggles)supportKey’sposition.Thevastmajority ofcommentaries,however,donot,andarguethatfishmostlikelyfeelpain.Mostagreethat Key’sargumentisflawedatbestandhisevidenceofhowpainworksinhumansisselective, simplistic,misleadingandoutdated(Damasio&Damasio;Merker;Panksepp;Shriver).One emergingconsensus,however,isthatnosinglelineofscientificevidenceshouldover-rule anyotherandmanyoftherespondentsagreethatbehaviouralstudies,suchasconditioned placeaversion,areanimportantcomponenttounderstandingpaininhumanandnonhumanvertebratesalike. TheprimarymessagefromthesecommentariesisthatKey’sargumentisfundamentally flawedfromanevolutionaryperspective.Heargues(althoughlaterdeniesit)thathuman brainarchitectureisrequiredtofeelpain.Themechanisticapproachcentresaroundthe roleofthecortexinhumanpain.ButasDinets,Brown,Ngandotherspointout,thehuman cortexhastakenonahugenumberofrolesthatoncewerethedomainofotherbrain regions.Tosuggestthatfishdon’tfeelpainbecausetheylackacortexonewouldalsohave towrite-offconsciousness(Seth)orindeedanycognitivefunctionthatoccursinthehuman AnimalSentience2016.X:BrownCommentary2onKeyonFishPain cortex.Oneexampleofapplyingthislogicwouldbetoconcludethatfisharenotcapableof learningeither.Clearlythisargumentisabsurd(seeBrownetal2011;Brown2015for reviews).Jones,Mather,Striedter,ElwoodandEdelmanallpointoutthatKey’sapproach alsodeniesanypossibilityofconvergentevolution,butsurprisinglyKeyacceptsthatbirds mightprovideanexampleofanindependentevolutionofacortex-likestructure.Haikonen, Manzotti,andSethtakeitonestepfurtherandsuggestthatwedon’tevenunderstandpain inhumansyetanditisfartooearlytobemakingjudgementcallsonothertaxa.Theroleof thecortexinhumanpainisstilldebated(Stevens;Damasio&Damasio)andismostlikely notthe“on-offswitch”forconsciousness(Segner).Waltersarguesthathighlevelsof consciousnessarenotrequiredforpainperception,aviewwhichisconsistentwith evolutionbeingagradualprocessratherthanoccurringasallornothingleapsandwiththe notionthatpainislikelyanancientevolutionarytrait. Broom,Sneddon&Brownstatedthattheseparationofnociceptionfromtheemotional responsetoit(pain)isoldfashionedandsomewhatcounter-productive.Theyarguethat nociceptionandpainarepartandparcelofthesamesystem,andgiventheimportant natureofitsfunction(harmavoidance),thissystemislikelyevolutionarilyancient.Itshould hardlybesurprisingifthissystemishighlyconservedacrossallvertebratesgiventhe associatedfitnessadvantages(Seth;Striedter;Elwood).Thefactthatthebrainregionsthat areresponsiblevaryacrosstaxaisconsistentwithwhatweknowtobethecasewithmany otherbrainfunctions. Digglesclaimsthatthecheerleadersoffishpainperception(andwelfaregenerally) intrinsicallylinkpainwithwelfare.Herightlypointsoutthatothermeasuresofwelfareare availableandarefarlesscontroversial.Ofcoursethereasonwearenottalkingaboutthese othermeasureshereisbecausetheyhavebeenthefoundationoffishwelfarefordecades (seeHuntingfordetal2006).Thereisnoargumenttobehadthere.Thequestionweare addressinghereiswhetherfishfeelpainandwhetherweshouldincludeitinourwelfare frameworkaswedowithothervertebrates.Everyoneagreesthatcurrentcommercial harvestingmethodsarehighlystressfulforfish.Sadly,wecurrentlylackthepoliticalwillto doanythingaboutit.Ihopethatgiventheknownrelationshipbetweenstresslevelsand filetquality,theaquacultureindustrywillmovetolimitpainandstressinfishesinthe absenceofanylegislation(i.e.,self-regulationdrivenbyeconomics).Unfortunately,Diggles alsoneedsarefreshercourseinvertebrateevolutionsincehewronglystatesthatfishare morecloselyrelatedtosharksthantheyaretomammalsandusesthatasabasisfor likeningpaininfishtosharksratherthantomammals.Itistruethat“human-like” nociceptorshavenotbeenidentifiedinelasmobranchsyet,butthatisnottosaythatthey donotexist.Science101:Absenceofevidenceisnotevidenceofabsence. Hartrightlypointsoutthatthereareissueswithterminologyandthathumansareselfobsessed.Frankly,Ithinkthewholeconsciousnessdebateisdistractingandisnotlikelyto besolvedanytimesoon.Westilldon’treallyknowwhatitisorhowitisgeneratedin humansletaloneinanimals.Nevertheless,recentpapers(e.g.,Reyetal2015)certainly suggestthatfishareconsciousbeingsbasedonanycriteriacurrentlyinuse.Wadiwel suggestsweshouldjustacceptthatwecannotexperiencewhatotheranimals(orpeople) AnimalSentience2016.X:BrownCommentary2onKeyonFishPain arefeelingandthatthequestionofpaininfishishenceoneofmakingcautiousethical decisionsunderconditionsofuncertainty:theweightoftheevidenceforandagainstpainin fish,andtheweightoftheconsequencesofafalsenegative(inferringfishdonotfeelpain wheninrealitytheydo). Thevastmajorityofcommentaries–expertsinawidespectrumofrelevantscientificand ethicalspecialities--accepttheaccumulating,multi-disciplinaryevidencethatitislikelythat fishfeelpain;moreover,eveninthecaseofthefence-sitters(includingoptimistic agnostics),itisquiteapparentthattheprecautionaryprinciplesapply,giventhe monumentalnumberoffishkilledeachyearincommercialfisheries.Indeed,Jonessuggests thatsuchapositionisnotonlyprudent,butethicallyobligatory.Weshouldnotallow conclusionsdrawnfromscientificevidencetobetaintedbythepotentialcommercial consequences,asKeyseemstorecommend. 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