dissolved oxygen.Theamount of Water containsonlysmallamountsof flow. flow ofwatercountercurrenttogillblood maintain aunidirectionalbutoscillating recorded andanalyzed,showingthatfish buccal andopercularchamberswere of fishtoday. Pressurechangesinthe detailed knowledgeofanextensiverange mechanism, remainsthebasisforamore and musculaturethepumping apparatus, intermsofboththeskeleton Their descriptionoftherespiratory framework forfutureworkinthearea. respiration infishthatformeda observations intoasummaryof bringing togetheradisparatesetof of respiratorymechanismsinfish, a majorstepforwardinourunderstanding is stillrefreshingtoreadandwasclearly review isnowmorethan50 approach tobiologicalproblems.The more mechanisticandanalyticalinhis classical biologistwhereasSheltonwas Hughes was,inmyopinion,themore CLASSICS each classic paper’s impactonthefieldofbiology andtheirownwork. each classicpaper’s Classics isanoccasionalcolumn, featuringhistoricpublicationsfromtheliterature.Writtenthese articlesdiscuss bymodernexpertsinthefield, published theirreview‘ and Sheltonwasminewhenthey Hughes wasShelton’s PhDsupervisor understanding ofbiologicalfunction. physical andchemicalprinciplestothe group ofexperimentalbiologistsapplying members oftheCambridgeUniversity George HughesandGrahamSheltonwere Biochemistry Advances inComparativePhysiologyand nervous controlinfish’,published ‘Respiratory mechanismsandtheir and GrahamShelton’s classicpaper David RandalldiscussesGeorgeHughes fathers offishrespiration Hughes andShelton:the fish’ in1962(HughesandShelton,1962) mechanisms andtheirnervouscontrolin Fish Respiration © 2014.PublishedbyTheCompanyofBiologistsLtd|JournalExperimentalBiology(2014)217,3191-3192doi:10.1242/jeb.095513 in 1962. Respiratory years oldbut . exchange inbonyfish(Piiperand Scheid, Subsequent modelanalysisof gas symmorphosis (Weibel etal.,1998). development ofconceptssuch as Hughes andSheltondidfacilitate the the systemsapproachpromulgatedby exchange acrosstheirskin.Despitethat, fish supplementoxygenuptakeby its mouthopen,andinaddition,many due toforwardmovementofthefishwith ventilation, i.e.theventilationofgills water. Also,theydidnotconsiderram maintain oxygenpercentutilizationfrom too highandactivefishareableto assumption ofthecostsbreathingwas swimming activity. However, their breathing couldlimitmaximum oxygen percentutilization,thecostof ventilation andtheassociateddecreasing concluded thatwithincreasinggill ventilation, HughesandShelton might increasewithincreasesin total energy outputinrestingfishand breathing mightbeashigh20%of removed. Assumingthatthecostof decrease intheamountofoxygen across thegillswereassociatedwitha showed thatincreasedflowsofwater Experiments presentedinthereview high as70–80%inrestingfish. utilization) hadbeenobservedtobeas water flowingoverthegills(percent The amountofoxygenremovedfrom blood andwater. as wellthecountercurrentflowof the conditionsfortransferacrossgills capacity rateratioofbloodandwater that effectiveness dependedonthe analysis, butwhattheypointedoutwas were insufficient dataforadetailed maximum possiblerateoftransfer. There oxygen transferinrelationtothe definedastheactualrateof transfer’, introduced theterm‘effectiveness of this onoxygentransfer. Theyalso and water)analyzedtheeffects of (ratio offlow×oxygencontentblood introduced theterm‘capacityrateratio’ metabolism. HughesandShelton the requiredrateofoxygentransferfor blood flowthroughthegillstodeliver over thegillsmustbemuchhigherthan concluded, therefore,thatwaterflow volume ofwater. HughesandShelton far greaterthanthatinanequivalent oxygen carriedinthebloodisusually understanding ofCO would seealarge increaseofour gases atthattime.Thenext50 the paucityofdataontransferthese third respiratorygas,ammonia,reflecting CO only limiteddiscussioninthereviewof maintain capacityrateratio.Therewas have averyhighcardiacoutputto icefish, whichlackhaemoglobinand observation presagedthediscoveryof without theuseofhaemoglobin.This consumption atlowtemperatures could maintainstandardoxygen Hughes andSheltonconcludedthatfish the water. Fromtheseexperiments, blocked byaddingcarbonmonoxideto even ifhaemoglobinoxygenationwas almost alloftheoxygenfromwater water assessed.Goldfishcouldremove oxygen couldberemovedfromthe chambers andtheextenttowhich limited. Fishhadbeenplacedinsealed of thebloodcirculationinfishwas At thetimeofreview, knowledge exchange. disappeared fromdiscussionsofgas ‘effectiveness oftransfer’ havelargely the terms‘capacityrateratio’,and different gasexchangesystemssothat adopted tofacilitatecomparisonbetween Q (bloodflow)andtheV/Qratiowere mammalian termssuchasV (ventilation), better understoodanddescribed, As fishgasexchangesystemsbecame to theanalysisbyHughesandShelton. elasmobranchs andbirdsalsoowemuch 1984) andstudiesofgasexchangein recording activityfromafish brain and a graduatestudent,Sheltonand Iwere problem. Intheearly1960s,when Iwas investigator. Signaltonoisewasalarge equipment wasoftenmadeby the system wasdifficult and,at that time,the Recording fromthecentralnervous important componentofthereview. across thegills,isprobablymost with themodellingofoxygenexchange the neuralcontrolofbreathing,along The extensiveandelegantdiscussionof between bloodandwater. complex structure,notsimplyabarrier gas transfer, andthattheyareavery play animportantroleinionaswell transfer infish.Itisnowclearthatgills 2 transfer andnodiscussionofthe 2 and ammonia

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The Journal of Experimental Biology CLASSICS 3192 a comparativeapproachremains conserved throughoutevolutionandthat ancient functionthatwashighly rhythmogenesis isaphylogenetically that ‘currentdataindicaterespiratory agreed withKinkead(Kinkead,2009) centre isstillvaluablereading.They problems ofdefiningacentralrespiratory Hughes andSheltondiscussionof regarding thefishbrain.Ifindthat event butmadenospecialconclusions station inGermany. We recordedthe brain weheardmusicfromaradio as weloweredtheelectrodeinto Perry, 2012). subsequent studies(seeMilsomand and wasaspringboardformany generated agreaterinterestinthesubject than asynthesisofworktodate.It their controlinfishwasmuchmore Shelton ofrespiratorymechanismsand view.’ ThereviewbyHughesand principles andamorecomprehensive important toderivebroaderbiological University ofBritishColumbia [email protected] David Randall The JournalofExperimentalBiology(2014)doi:10.1242/jeb.095513 Weibel, E.R.,Taylor, C.R.andBolisL.(eds) Milsom, W. K.andPerry, S.F. (eds) Kinkead, R. Hughes, G.M.andShelton, Piiper, J.andScheid,P. References University Press. Symmorphosis Debate Principles ofAnimalDesign:TheOptimizationand Academic Press. Hoar andD.J.Randall),pp.229-262.NewYork: vertebrates. rhythmogenesis: insightsfromectothermic Comp. Physiol.Biochem. mechanisms andtheirnervouscontrolinfish. transfer infish.InFishPhysiology 184 Relationships inFishGills Issue: NewInsightsintoStructure/Function , 213-346. (2009). Phylogenetictrendsinrespiratory Resp. Physiol.Neurobiol. . Cambridge,UK:Cambridge (1984). Modelanalysisofgas 1 . , 275-364. Resp. Physiol.Neurobiol. (1962). Respiratory , Vol. XA (ed.W. S. (2012). 168 , 39-48. Special (1998). Adv.

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