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NREM/BIOL4464–OrnithologyDr.TimO’ConnellLectures25–2927,29,and31,March;3,5April2017MostMaterialfromthenextseverallectureswillbeassociatedwithinformationinGill,Chapter6.AvianPhysiology–gasexchangeMammalianrespiratorysystem•Nares,trachea,bronchi,bronchioles,alveoli,capillarybeds•Gasexchangetakesplaceincapillariesassociatedwithalveoli•Inrelaxedbreathing,humanshavearesidualvolumeofairinthelungsthatisabout50%ofthevolumeinhaledandexhaledwitheachbreath.•OxygentakeninonlyduringinhalationUnlikemammalianlungs,birdshaveassociatedairsacs.Avianairsacs–generally9ofthem:•Cervical(2)•Interclavicular(1)•Anteriorthoracic(2)•Posteriorthoracic(2)•Abdominal(2)Avianrespiratorysystem•Keyfeature(uniquetobirds):unidirectionalflowthroughlungs;neverany“deadair”•Avianlungsspongybutrigid–theydon’texpandandcontractlikemammalianlungs•Oxygenfrom“freshair”takeninduringbothinhalationandexhalation.•Structure:nares,trachea,1°bronchi,2°bronchi,3°bronchia.k.a.“parabronchi”.Parabronchi–tubeswithintheavianlungthatarethesiteofgasexchange.Parabronchuscrosssection:•Tinytubescarryingairfromtheparabronchus(“aircapillaries”)exchangegaseswithtinytubescarryingblood(capillaries).•Capillariesarrangedperpendiculartotheprimarydirectionofairflowthroughtheparabronchus,resultingin“cross-current”gasexchange.

Inthetissuessurroundingthemaintubeofeachparabronchus,aircapillariesandbloodcapillariesarearrangedwiththeirfluidsmovinginoppositedirections,creatingshortsegmentsofcounter-currentexchange.Becausetheseflowsareorientedperpendiculartotheprimaryflowofair,however,weusetheterm“cross-current”exchangetodescribeit.Here’showdiffusiongradientscanbemoreefficientwithacounter-currentflow:Withcon-currentflow,astronggradientweakenssuchthatonly50%exchangecanoccur,i.e.,equilibriumisreached.

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Withcounter-currentflow,apositivediffusiongradientismaintainedalongtheentirelength.Ifthepathislongenough,near100%exchangecanoccur.Gasexchangeintheavianlungoccursviaacross-currentexchangemechanism.It’snotasefficientascounter-currentexchange,butitisasignificantadvanceoverconcurrentexchange.Hereisthemammaliangasexchangesystem–concurrent.Bloodandairflowtowardeachotheratapointofdiffusion,butoncetheconcentrationofoxygenineithervesselapproaches50%,thegradientsoshallowthatnofurthernetgasexchangetakesplace.•Blue=oxygen(%ofmaximumpartialpressure)•Red=bloodvessel.Oxygencontentisverylowatfirst,butthevesselquicklypicksupoxygen.Asthebloodflowsdownthevesselitpicksupoxygenfromtheairtube,buttheconcentrationofoxygendeclinesandthewidthofgradientbetweenthevesselsdecreases.Oncethatconcentrationapproaches50%,thereisnogradientinoxygenconcentrationandnonetmovementofoxygenintotheblood.

Theoretically,acounter-currentexchange(suchasexistsinthebloodvesselarrangementsofbirds’feettofacilitateheattransfer)coulddomuchbetterthanraisingtheoxygencontentofthebloodto50%.•Red=bloodvessel.Oxygencontentisverylow(0%)atfirst,butalongtheentirelengthofitsarrangementnexttotheairtube,apositivediffusiongradientismaintained.Asthebloodvesselpicksupoxygen,itcontinuallyencountersairwithagreateroxygenconcentration.Birdsactuallydon’tusecounter-currentexchangeintheirlungs,theyusecross-currentexchange.•Red=bloodvessel.Atmultiplepointsalongtheparabronchus,deoxygenatedbloodcomesinclosecontactwiththe“aircapillaries”thatalwayshaveahigheroxygenconcentration.Thisisnotefficientenoughtoincreasetheoxygencontentofthebloodcloseto100%(theoreticalmaximumwithcounter-currentsystem),butitisasignificantimprovementoverthe~50%thatcouldbeachievedwithaconcurrentsystemlikeours.•avianrespiratorysystem–airsacsandunidirectionalflow•Nodiaphragminbirdsasinmammals.•Airbroughtinandoutthroughloweringofthesternum(creatingnegativepressure,justlikedroppingdiaphragm)andinexpansionandcontractionofairsacslikebellows.•Muscleactivitycanassistrespirationinflight;manybirdshaverhythmtoflappingthatfacilitatesrespiration.

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avianrespiratorysystem–airsacsandunidirectionalflow•Inhalation1:“fresh”airmovestoabdominal(posterior)airsacs•Exhalation1:freshairmovesfromabdominalairsacsthroughlungs•Inhalation2:“stale”airnowmovesfromlungstoanteriorairsacs–isreplacedinlungsbynewfreshairwaitinginabdominalairsacs.•Exhalation2:staleair(theoriginalairbroughtinfrominhalation1)nowexpelledfromanteriorairsacsthroughtracheaandnares.Forcoolanimationofunidirectionalflowandairsacinvolvementinrespiration,checkout:http://people.eku.edu/ritchisong/birdrespiration.htmlThermoregulationstrategiesBirdsdealwithextremesoftemperatureinmultipleways.We’vealreadylearnedabitaboutthecounter-currentheatexchangerinlegsofcertainwaterbirds:Counter-CurrentExchanger:Networkofarteriesandveinsarrangedincloseproximitywithoppositedirectionalflowtopromotefavorablegradientfordiffusionoveramaximumdistance.

Left:Cross-sectionofcounter-currentheatexchangetissueinatuna.Thickwalls–arteries,thinwallsareveins.

Notethatsomebirdscanalsoshuntbloodflow(vasoconstriction)awayfromthetoestofurtherreducetheamountthatbloodcoolsattheextremities.

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Generalthermoregulatorychallenges•Forendotherms,thereisazoneofambienttemperaturesatwhichnometabolismincreaseisneededtomaintainhomeostasis.•Abovetheuppercriticaltemperatureandbelowthelowercriticaltemperature,birdsmustexpendenergy,throughevaporativecoolingorshivering,respectively.

Dealingwithcold•Insulation•Counter-currentheatexchangerinlegs•Torpor•Fatdeposition,hyperphagiaBehavioralthermoregulation:•Avoidcold–seekshelterfromwind•Ptarmigan–roostinsnowbanks•Reduceheatgradient(non-torpor)–chickadeeslowerbodytemperatureonreallycoldnights.•Huddlingtoreduceheatloss

Communalroosting,examples:•EmperorPenguin•SpectacledEider•PygmyNuthatch–record179individualsinacommunalroosthole!Dealingwithheat

! Behavioralthermoregulation:•Seekingshade,water,etc.! sleekingfeathers–squeezesoutwarmairclosetotheskin! Counter-currentheatexchangerinhead–allowbodytemptoincreasebutkeepbraincool! Gularfluttering–evaporativecooling.

Evaporativecoolingworksbytakingtheheatenergyofthebodyandusingittoraisetheenergyofwatertothepointofevaporation.Wehumansareunusualinthatweaccomplishthisbysweating.Birdsengageinevaporativecoolingthroughpanting(gularfluttering)likemanymammals.Somebirds(e.g.,storks)alsoachieveevaporativecoolingthroughwettingtheirlegs,eitherbywadingordefecatingdirectlyontheirlegs.Avianphysiologicalextremes:1.Gettinghigh–Bar-headedGoose•ThisspecieswintersinsouthernAsiaandbreedsinthesteppesofcentralAsia.•TheIndianpopulationatleastmigratesalongadirectroute–overtheHimalaya.•ThisspecieshasbeenseenmigratingoverMt.Everest.

Forperspective-cruisingaltitudes:Smallplanes–10,000’Jetliners–30,000–35,000’Migratingsongbirds–4000’Migratingwaterfowl–7000’Migratingeagles–10,000’

Bar-headedGooseinHimalayanmigration–29,500’•Worldrecordholder–Ruppel’sGriffonVultureseenat37,000’,buttheBar-heaedGooseroutinelycrossesHimalayanpasses>29,000’–andit’sflappingthewholetime.How?OntopofMt.Everest...•ThewindiestplaceonEarth.FromOct.–Mar.,3ofevery4dayswillexperiencehurricaneforcewinds(74mph).Windsroutinelytopoutabove156mph,thethresholdforCategory5hurricane.•“Frikkin’freezingMr.Bigglesworth.”EvenMaytempsaverage-13F.-100Fhasapparentlybeenrecorded.•LowOxygen–about33%partialpressureofOxygencomparedtosealevel.

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HowBar-headsmakeitover(generallyinoneday,andnearthemiddleofa1000-mileflight):•Largerlungsthanotherbirds•Takeingreatervolumeofairwitheachinhalation•RedbloodcellscontainaformofhemoglobinwithextraOxygen-bindingaffinity•Flightmusclesricherinmyoglobinthanotherspecies

2.Goingdown–EmperorPenguin•EmperorPenguinshavebeenrecordedat1,752mdeep.•Confirmedholdingbreathfor15.8minutes.•How?Below–decreaseinO2andincreaseinCO2inbloodafter15minutes.•Aviandivingreflex(verysimilartomammalian,whichisbetterstudied)•(left)OxygenisusedupandCarbonDioxideaccumulatesthelongerthebodyisdeprivedofOxygen.•Thedivingreflexinbirdsandmammalsissimilar,andkicksinwhenthenervoussystemisstimulatedbysubmersionofthefaceincoldwater.•Thegoal?Minimizeoxygenusetothegreatestextentpossible.Howachieved?•StorageofOxygenintissuesotherthanlungs–e.g.,myoglobininmuscles.•PenguinscandosomeairsacstorageComparisonofO2storedintissuesinhumansandselectmarinemammals:

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Howtouselessoxygen?Pumpless!•Bradycardia–slowingheartrate.Right–changeinheartrateinadivingduckduringandafteradive.•Peripheralvasoconstriction–reducingbloodflowtoperipherytokeepvitalorganssuppliedwithOxygenfirst.•Ondeeperdives,bloodflowisfurtherrestrictedfromtheinternalorgansandthebraintakespriorityastheonlythinggettingOxygen.ExampleofreductioninbloodflowtodifferentorgansystemsinWeddellSeal.Onreallydeepdives.Bloodflowisonlymaintained(it’sactuallyslightlyincreased)tothebrain.

Sowhatdopenguinsactuallydo?First,birdsdon’tdothisbradycardiastuff...Ordothey?

Aha!Theydo(left).EmperorPenguins–thedeepestandlongest-divingbirdsknown–actuallydothesamethingthatdivingmammalsdoinslowingtheirheartrateonadive.Theyonlydothislongerdurationdives,however.Penguinsdeviatefrommammals(below)in~3Xtheoxygenstorageinmusclescomparedtohumansand~2Xthatofelephantseals.

Insum,EmperorPenguinsaresuchgreatdiversbecausetheyuse•Bradycardia•PeripheralVasoconstriction•Oxygenstorageinmuscletissue•Tachycardiaonsurfacing!

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3.Toocoldandtoosmall–RufousHummingbird•NorthernmostbreedinghummingbirdinNorthAmerica•ManyreallycoldnightseveninsummerinnorthernRockies–upto12,000’•Normalwingbeatfrequency,52–62/sec.•Howdoesthislittledynamokeepfromusingupallitsstoredenergyaccumulatedduringtheday?•Ithibernates!•Severalhummingbirdsthatoccurincoldenvironments(e.g.,theAndes)enterintodailytorportoreduceheatlosstotheexternalenvironment.ThePoorwillalsodoesthisinwesterndeserts.•Heartrateslowsquicklyandbodytemperatureisallowedtodecreaseclosetoambienttemperaturetoreduceheatlossandenergyconsumption.•Torpor–formoffacultativehypothermiainwhichbodytemperatureisloweredtootherwiselethallevels.Cannotregaininstantactivitylevel.AvianEnergyDemandandDigestionBirdsareremarkablyvariedinthefoodstheyeatandhowtheyobtainit.Whathappensafteritsswallowed?Mammalianfoodprocessing:mechanicalbreakdownwithchewingteethfollowedbychemicalbreakdownwithstomachacidsanddigestiveenzymes.Avianfoodprocessing:noteeth!•Chemicalbreakdownfollowedbymechanicalbreakdowninthegizzard.•Billsandtonguescanbegreattoolsforextractingseedsfromhusks,forexample,butnochewinginbirds,perse.

•Esophagus–mucusglandsinlininghelptotransferfooddownthedigestivetract.(Pigeon“milk”producedbytheesophagus.)•Crop–outgrowthoftheesophagus–foodstorage,softening,andregulationofflow.(SiteofforegutfermentationintheHoatzin.)•Stomach=proventriculus+gizzard•Proventriculus–chemicaldigestionhere.Stomachacids(pH0.2–1.2insomebirds)anddigestiveenzymescapableofdissolvingbone.Fishoilsstoredhereincertainspecies.•Gizzard–muscularwalled,crushesfoodintosmallerpieceswiththeaidofswallowedgrit.•Intenstines–absorptionofnutrientsandretentionofwater.Mayincludedevelopmentofceca–outpocketsoflargeintestinethatserveasfermentationchambersforvegetablematter.

•Cropstoragecanbeimportantfortakingfoodbacktoyoungorcollectingfoodtobecachedelsewhere.•CropmilkproductioninColumbiformes•Somebirdsejectpelletsofundigestiblematter.•Gutretentiontimesfast–birdsextractnutrientsquicklyandthenreleaseexcessweight.•Fruit-eatingbirdsprobablythefastest–CedarWaxwingapparentlyholdstherecordat8minutes!•Otherbirds,e.g.,raptors,mightcompletelyprocessamealin6–12hours.

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•Intestines–absorptionofnutrientsandretentionofwater.Mayincludedevelopmentofceca–outpocketsoflargeintestinethatserveasfermentationchambersforvegetablematter.

MaintainingWaterBalance•Birdsusuallycometofreshwateronceortwiceaday.•Thosethateat“wet”foodslikefruitandinsectslesslikelytodependonspecificwatersourcethanthosethateat“dry”foodslikeseeds.•Inhot,dryenvironments,morewaterisneededthanmightbepredicted:heat-stressedCaliforniaTowheesconsumed4XasmuchwaterthanwhenintheirTNZ,butonly2XasmuchOxygen.•Metabolicwater–oxidationoforganiccompoundscanresultinwaterproducedasabyproduct.•Foreverygramoffatmetabolized,1.07gramsof“metabolicwater”isproduced.Birdsalsoconservewaterwiththeirunusualexcretorysystem.•Mammalsexcretenitrogenouswastesintheformofurea,awatersolublecompoundthatrequireslargeamountsofwatertoflushfromtheexcretorysystem.•Birds,likereptiles,excreteuricacid.•Byweight,uricacidcontainstwicethenitrogenandanorderofmagnitudelesswaterthanurea.•Birdscanfurtherconcentrateuricacidincloacato3000timestheacidityoftheblood;kangarooratscanonlygetto20or30Xbloodacidity.Seabirdshavespecialproblems–1%saltcontentinbodyfluidbutforcedtodrink3%saltywater.•Kidneysnotspeciallymodifiedtorestorebalance.•Specializedorgans–saltglands–intheskullsofoceanicbirds.•Counter-currentflowofsaltwaterandbloodflow,andactivetransport,concentratesbrineywaterinsaltglandupto5%!