have beenaprerequisiteforthegigantismseeninpterosaurs. argue thatarespiratoryphysiology similartothatofbirdswould restriction onbatmaximumsizecomparedwithbirds.Secondly, I difference inrespiratoryphysiology iskeytounderstandingthe I extendthisargument intwo ways.Firstly, Isuggest that the explain whythelargest birdsarelarger thanthelargest bats.Here, of wingbeatfrequenciestobodymassinbirdsandbatscanhelp Norberg (Norberg andNorberg, 2012)argued thatdifferent scaling 200–250 estimates forthelargest azhdarchidsareoftheorder the dinosaursanddiedoutatendofCretaceous.Mass azhdarchids, extinctflyingreptilesthatexistedduringtheageof largest knownflyingcreaturesareagroupofpterosaursnamed birds [Argentavis magnificens © 2014.PublishedbyTheCompanyofBiologistsLtd|JournalExperimentalBiology(2014)217,2627-2628doi:10.1242/jeb.104919 Received 3March 2014;Accepted5May2014 *Author ([email protected]) for correspondence Biology, StAndrews, StAndrewsKY169TH,UK. School of University of in batsofthesamesize.They also reportthatdownstrokemuscle in bothbirdsandbats,butwingbeat frequencyishigherinbirdsthan Norberg, 2012)argue thatwingbeatfrequencydeclineswithmass certain type(Alexander, 2006).Norberg andNorberg (Norberg and in theair, sothereisaninevitableupper sizelimitforfliersofa than theforceofgravitythatmustbeovercometokeepanimal With increasingmass,theaerodynamiclift offliersincreasesslower (Dunning, 2007),risingtoperhaps70–80 contrast, thelargest extantflyingbirds(Koribustard flying fox(Neuweiler, 2000;StierandMildenstein,2005)].In few speciesofextinct very different. Thelargest livingorextinctbatisaround 1.6 and pterosaurs.Thelargest bodysizesseeninthesegroupsare Powered flightevolvedinthreelineagesofvertebrates:birds,bats KEY WORDS:Birds,Bats,Scaling,Allometry, Limitstoflight a prerequisiteforthegigantismseeninpterosaurs. argue thatarespiratoryphysiologysimilartobirdswouldhavebeen restriction onbatmaximumsizecomparedwithbirds.Secondly, I different respiratoryphysiologiesarekeytounderstandingthe bats. Here,Iextendthisargumentintwoways.Firstly, Isuggestthat bats canhelpexplainwhythelargestbirdsarelargerthan different scalingofwingbeatfrequenciestobodymassinbirdsand members oftheothertwogroups.Recently, itwasarguedthat known areatleastanorderofmagnitudesmallerthanthelargest birds, thebatsandextinctpterosaurs.Thelargestever Powered flighthasevolvedthreetimesinthevertebrates: Graeme Ruxton* Avian-style respirationallowed gigantisminpterosaurs SHORT COMMUNICATION The findings of Norberg andNorberg Norberg findingsof The INTRODUCTION ABSTRACT olor) arenearlyanorderofmagnitudebiggerat12–14 California condor kg (Witton andHabib,2010).Recently, Norberg and Gymnogyps californianus,muteswan Pteropus (Chatterjee etal.,2007)].The and thegiantgolden-crowned

kg forthelargest extinct Ardeotis kori Cygnus

kg [a

kg , masses estimatedforthelargest extinctflyingbirds. lower inbatsthan inbirdsofanequivalentsize. Inbirds,wingbeat (Bernstein, 1987).Thislikelyexplains whywingbeatfrequencyis directly linkedtotheirdifferent respiratoryphysiologies references therein).Thisdifference betweenbirdsandbats canbe movements onpulmonaryair flow orvolume(Maina,2000;and of species;andingeneralthere islittleobservedeffect of wing wingbeat frequencieshasbeen observedonlyinasmallminority frequency. Incontrast,inbirds,matchingofrespiratoryratesand ecology (BullenandMcKenzie,2004). given overtodownstrokeflightmusclescanbelinkedclosely to bats: interspecificcomparisonshowsthatthefractionofbody mass evidence thatdownstrokemusclemassisunderstrongselection in accommodate itsmorevoluminousrespiratorysystem.There is mass maybesubjecttogreaterconstraintallowthebat to lower downstrokemusclemassinbatsthanbirds.Thatis, body cavitybegivenuptoothersystems,andthismayexplain the of themammalianrespiratorysystemrequiresthatlessspace in the and batswithsimilarecologies(Norberg, 1981).Thegreatervolume by strongconvergence inbodyplanandallometricscalingofbirds being constrainedbytheneedfordragreduction).Thisissupported a similarsizeshouldbebroadlyequivalent(withtheircross-section the samesize(Maina,2000).Thebodycavitiesofbirdsandbats have considerablylarger lungs(andassociatedorgans) than birdsof prevalent inmammals.Becauseofthisefficiency difference, bats through thelungs,whereasre-breathingofstaleairismuchmore system thereislittleornorecirculationofairthathasalreadypassed exchange possible(Sherwoodetal.,2005).Secondly, intheavian the lungisnearfullexpansion(andalveoliareopen)effective gas expansion andcontractionarerequiredinmammals,onlywhen essentially fullyexpandedallthetimeinbirds,whereascyclesof a numberoffactors(Maina,2002).Firstly, thelungscanbe system (ProctorandLynch, 1998). Improvedefficiency comesfrom system ismoreefficient atanygivensizethanthemammaliantidal oxygen atsimilarrates.Theavianunidirectional-flowrespiratory aerodynamic andaerobicmuscleefficiencies), theyneedtoconsume organism; thus(forsustainedflight,andassumingsimilar beating theirwingstocounteracttheforceofgravityactingon of thesamesizeneedtogeneratesimilaramountsenergy by Norberg andNorberg (Norberg andNorberg, 2012).A birdandbat be keytothedifferences betweenbirdsandbatsdiscussedby Here, Isuggestthatthehighlyefficient avianrespiratorysystemmay the largest extantspecies,butarelesscompatiblewiththe70–80 1.1–2.3 largest flyingbirdsshouldbeabout12–16 of agivenmass.Norberg andNorberg’s calculationssuggestthatthe that thepoweravailabletobirdsisgreaterthanbats 16% inbirds.Taken together, thesetwosetsofobservationssuggest mass isonly9%ofbodyonaverageinbats,comparedwith extension topterosaurs thesescalingrelationships and Mechanisms underlying In bats,therespirationrateissynchronisedwithwingbeat kg forbats.Theseestimatesarebroadlyinagreementwith

kg, droppingto 2627

kg

The Journal of Experimental Biology 2628 facilitated gigantismthroughanenhancedabilitytogenerate lift at line ofreasoningsuggeststhatsucharespiratoryphysiology facilitation ofverylarge sizeinsomeflyingpterosaurspecies.This I speculatethatavian-stylerespiratoryphysiologywaskeytothe would haveenhancedtheabilityofpterosaurstogeneratelift.Thus, muscle (allowingmorepowerfulstrokes).Boththesemechanisms respiratory organs allowsmorespaceinthebodycavityforflight respiration (allowingmorerapidflapping),andreducedsizeofthe aerodynamic andmusclefunctioningneedsnottheof respiratory systemallowswingbeatfrequencytobedrivensolelyby mechanisms tothatpreviouslysuggested.Specifically, abird-like allowing gigantisminpterosaursbutthroughentirelydifferent Here, Iargue thataflow-throughrespiratoryanatomywaskeyto are typicalofthelarge long-bonesofbats(Swartzetal.,1992). of terrestrialanimals(Dumont,2010).Further, hollowcross-sections contribute thesamefractionoftotalbodymassasdoskeletons than innon-flyinganimals;andsooveralltheskeletonsofbirds although birdbonesaretypicallyhollow, thebonematerialisdenser compelling asitfirstappears.Recentresearchhasshownthat giant sizeinseveralclades’.However, thisargument maynotbeas increases inbodymass,enablingtheevolutionoflarge andeven critical roleincircumventingthelimitsimposedbyallometric bone marrowbyair-filled pneumaticdiverticulalikelyplayeda they argue that‘densityreductionviathereplacementofboneand adaptation allowedgigantismtooccurinthepterosaurs.Specifically, 2009; Schachneretal.,2014).Claussensal.argued thatthis the tidalsystemofmammals(Claessensetal.,2009;Butler ventilation systemanalogoustothatofbirds,butquitedifferent from of reasoningthatpterosaurshadaflow-throughpulmonary in allowingthemtoreachlarge sizesnotexploitedbybats. unidirectional respiratorysystemofthebirdswasakeyfacilitator respiratory differences; hence,Ispeculatethattheefficient in attributesrelatedtoliftgenerationcanbedirectly 2005). Thus,itseemsthatthedifferences betweenbirdsandbats largest relativelungvolumeofallthemammals(Canalsetal., (Makanya andMortola,2007).Despitethis,batsstillhavethe evidence thatthewingmembranefunctionsingasexchange respiratory gasexchangecanbeseeninrecentlydiscovered exchange tooccurinthelungs.Thatbatsarehighlyselectedfor lungs andpotentiallyinsufficient timeperbreathforeffective gas constraint thatrapidwingbeatswouldmeanventilationofthe driven bylocomotiveselectionpressures.Batswillfacetheadded frequency variesbetweenspecies,andthisvariationislikely SHORT COMMUNICATION There nowseemstobeevidencefromanumberofdifferent lines commercial ornot-for-profitsectors. This researchreceivednospecificgrantfromanyfundingagencyinthepublic, The authordeclaresnocompetingfinancialinterests. I thanktworeviewersforvaluablecommentsonanearlierversion. body mass. least asmuch(andperhapsmorethan)throughareductionin ulr .J,Bret .M n oe,D.J. Gower, and P. M. Barrett, R.J., Butler, uln .D n ceze N.L. McKenzie, and R.D. Bullen, M.H. Bernstein, R.M. Alexander, References Funding Competing interests Acknowledgements itn .P n ai,M.B. Habib, and M.P. Witton, D.R. Carrier, and M.B. Bennett, S.M., Swartz, aas . tl,C,Gos,B n raeDa,J. Iriate-Diaz, and B. Grossi, C., Atala, M., Canals, hrod . lnof .adYne,P. H. Yancey, Stier and H. Klandorf, L., Sherwood, uot E.R. Dumont, D.M. Unwin, and P. M. O’Connor, L.P., Claessens, Jr K.E., Campbell, and R.J. Templin, S., Chatterjee, cahe,E . ir,R . ulr .P n amr C.G. Farmer, and J.P. Butler, R.L., Cieri, E.R., Schachner, J.N. Maina, unn,J . Jr J.B., Dunning, rco,N .adLnh P. J. Lynch, and N.S. Proctor, R.A. Norberg, and U.M. Norberg, J.P. Mortola, and A.N. Makanya, an,J.N. Maina, obr,U.M. Norberg, G. Neuweiler, foraging strategy. Mammal. Philippine flyingfoxes, and air-sacsintheearliestpterosaurs. Seller), pp43-73.BocaRaton,FL:CRCPress. University Press. flightlessness. pterosaurs, theuseofbirdsaspterosauranaloguesandcommentson flying batsandtheevolutionofskeletaldesignforflight. and lungsofsmallbats. facilitated theoriginofpterosaurflightandaerialgigantism. pulmonary airflowpatternsinthesavannahmonitorlizard. Genes toOrganisms Sci. Acad. Sci.USA Argentavis Function. mass inbatsandlimitstomaximumbatsize. comparative perspectives. refinements inbirdsandbats. Raton, FL:CRCPress. wings. and itspossibleroleingasexchange. .adMlesen T. L. Mildenstein, and S. , 277 Philos. Trans. R.Soc.B , 2193-2198. Yale, CN:Yale UniversityPress. 86, 719-728. , theworld’s largestflying bird fromtheMioceneofArgentina. (2000). Whatittakestofly:thestructuralandfunctionalrespiratory (2000). The JournalofExperimentalBiology(2014)doi:10.1242/jeb.104919 (2010). Bonedensityandthelightweightskeletonsofbirds. (2002). Structure,functionandevolutionofthegasexchangers: PLoS ONE (1981). Allometryofbatwingsandlegscomparisonwithbird 104 (1987). Respirationinflyingbirds.In (2006). Aust. J.Zool. (2007). , 12398-12403. The BiologyofBats . Singapore:Brooks/Cole. Acta Chiropterologica Principles ofAnimalLocomotion. Acerodon jubatus 5 CRC HandbookofAvian Body Masses J. Anat. , e13982. J. Exp.Biol. (2005). Dietaryhabitatoftheworld’s largestbats:the 292 52, 605-622. (1998). (2010). Onthesizeandflightdiversityofgiant (2007). Thestructuraldesignofthebatwingweb 201 , 359-398. (2012). Scalingofwingbeatfrequencywithbody (2004). Batflight-musclemass:implicationsfor J. Anat. Biol. Lett. , 281-304. . NewYork, NY: OxfordUniversityPress. Manual ofOrnithology:Avian Structure& 203 (2009). Postcranialskeletalpneumaticity J. Exp.Biol. and , 3045-3064. 211, 687-697. 7 , 65-72. 5 (1992). Wingbonestressesinfree , 557-560. (2005). trpsvmyu lanensis Pteropus vampyrus (2005). Relativesizeofhearts (2009). Respiratoryevolution (2007). Theaerodynamicsof Bird RespirationII Nature 215 Nature Animal Physiology:From PLoS ONE Princeton, NJ:Princeton , 711-722. 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