1981.- Physiology of Diving in Marine Mammals

7/29/2019 1981.- Physiology of Diving in Marine Mammals

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Ann -prg Ann n A rg rd

PHYSIOLOGY OF DIVING

IN MARINE MAMMALS

G Kooman 1 A. astn and R W Davs

Phsoogca Research Laboraory, Scrpps Instuton of Oceanograph,Uvesiy o Cafoa, Sa Dego, La Jola, alioa 93093

INTRODUCTION

.314

The rst comprehensive review of diving in vertebrates was publshed in870 by Paul Bert (2) t attempted to correlate the breathhold limits oaquatic birds and mammals with their blood volume In 99 another majorreview detailed th physiological adustments to diving (6) Several surveys

appeared in the mid-toate 960s (,22,) he following eclecticreview emphasizes marine mammals and calls attention to the natural orunorcd dive Expemental rocedures relevant to this subjt boh in thelaboratory and in the eld are discussed

First we brey review (a the response to a forced breathhold (b) therelationship of diving to tissue level biochemistry ( the energetics oetended breathholds with regard to O decit and debt and (d the physiology and behavior of natural dives

GENEL REVIWMarine mammals have considerable breathhold capacities or eample,harpooned sperm whales Physeter atodon, have been reported to remainsubmerged or9 min (26) and Weddell sealsLetonyhotes wedde hvevoluntarily dved for 7 min (7) he true seals Phodae are generalythought to have a greater breathhold capacity than ur seals and sea lions,(Otardae or the small whales Dehndae The latter two groups seldom

lThe writing fhs manuscpt was spportd by NIH Gran #HL 17731 and NSF Gan

# 23424.

34366278/8050$0

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KYMAN CATEINI DAVI

dive longer than 5 min. Sinc most phocids are phlegmatic, and since theirbreathhold abilities are mong the geatest they have been the usual choicefor investigations on diving

Virtually all studies of breathhold responses in maine mammals havebeen conducted on a mly estained animal foced undewate in theaboratory. he invetigator controls the length and the freqency of theexpemental dives uch a procedure has been eective in elicitng cardiovascular neurological and biochemical responses to asphyxia

Oxyge SreIf the oxygen store reects a general breathhold capacity it is not surprsing

that phocids might be the animl of choice fo dive studies Thei oxygencapacity is much lger than that of sea lions o small whes n ses theO2 store provided by the blood alone ranges from ml pe kg of bodymass hereas it is only 5 ml per kg body mass in humans nd onespecies of porpoise; two other porpoise species were intermediate betweenhumans and seals (8 a) However if O2 consumption remained the sameas that measured durng resting peods in air and i aeobic metabolismwere the ony energy source then even a seal's O2 store would be far toosmall for the duation of breathholds observed in both natual dives and

forced submersions

Bradycardia, Cardiac Ouu, Bld Preure VacularRdisribuiDung a beathhold complex vascul esponses occu the most obviousof which is a maed badycardia This slowing of heat vies with species;the most proound response occurs in the phocids, the least in the manatee27 imay cardiac output dops consideably durng bradycrdia as

stroke volume remains nealy constant In seals cardiac output may dopto 1% of the pe-ive esting value (4 4 51) Despite this dopcentral areial blood pressure remains steady ( 4) This nicates aninceased esistance and a deceased distibution of blood within the vascua system is edistbution of bood dung the ve s the ey to extended beathhold ability It promotes the parsimonious use o the limitedoxygen store because much less tissue is perfused during the breathhold ndconsumption of blood and lung oxygen drops greatly

Expements with ow tnsduces have shown that blood ow nealy

stops in some tissues such as the idney (1) Labeled micosphee studiessho th to be true of most perpheral organs (4) his state has cometo be known as the helungbrain system of diving animals: Blood oisdrected to those vital organs that have a sustained enegy euiement

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DVN SO 345

and low anaerobic capacity. t has been demonstrated recently that evencoronary blod ow drops by about% during forced dives(5 5 so thatsuch a diving rspons is mor lik a lung-brain and larg cardiac bypss

system Flow to the brain is maintain or slightly increased(14 1s ow decreases, does th mtabolic function of the organ decreasecommensurately? Renal ltration ceases duing forced dives ( and kidney oxygen consumption is directly related to ltration rate; thereforeduing th dive, th overall nergy consumtion rate of this organ is mostlikely reduced he heart and other organs may also reduce function andmetabolism durng the dive

h idea of a reducd metabolic rate during the div was roosed asearly as 18 (4 n a study of diving birds and mammals the 2 decit

and debt of dives were sldom equal; hn the subject was quie duing thedive the dbt as usually less than the dcit (43).

ung forced breathhold activity, core body temerature of sals dclines even though their insulation increases oing to intense vasoconstiction(18 4 his too must ndicate a reduced metabolic rate duing suchdives

acic Acid large incease in th concntration of lactic acid n the irculation ismeaurable shortly after the conclusion of prolonged breathhold dives (1, 4 his indcates that some areas of the body have been starved ofoygn and have had to function anaerobically he muscles aa to beth maor source of this lactic acid he only muscle biosis of a divr donelong ago,show a stong elationhi between mucle oygen deletionand lactic ad accumulation n youn harbor sealsPho musle deletion during th forced dive occurred within5 min o uote ndrsen(1 "ur best evidence indicates as we have seen that th large muscle

masss not ciculatd in a div sinc thy othis ould tk a hvytoll of th dositsnamely the blood storesWe have outlined above the imlied consensus on how diving mammals

function in the wild f this is their usual modus oerd then it wouldseem logical that these mammals have undergone obvious biochemicaladaptationstowards anaerobic metabolism owever what if anaeobiosisis not the maor energy rsource of most dives: greater exibility invascular redistribution should thn occur some organs may ostpone andredu function until at te surface uch a mhanism would reduce the

general engetic needs of the diving animal. he more exibl vascularresponse would thn make it practical for some of the large blood storesto be shared not only by the heat lung and bran but also by other favordtius or organs as th nd iss duingth animal's daly diving routin

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346 KYMAN CATEN DAV

IING BIOCHEMISRY

otntal Bochmcal Modcatons

Bochemcal schemes nvolved n allowng extended breathholds, must provide energy during periods of low oxygen when standard oxidative pathways for the generation of ATP are inhibited Three main possibilities havebeen studied: (a an increase in activit of the glcoltic enzmes allowingan enhanced ptental for the anaerobic generation of energ durng thedve; (b) possble alteate pathways to standard mammalan glycolsis [ascheme studied only once or twice since these pathways in mammals werefound to be insinicant (24)] and(c) the ability for ecient recovery from

anaerobicmetabolism utiliing the lactic acid poduced duing the dive

Musclecause laborator divng studes had documented that the musculature ofa marne mammal was cut o from blood owassaed the glcoltc enzmes n the epaxal muscles of the acc whitesided porpoise (Lagenorhynchus obquidens) (49) In this study, lactatedehydrogenase activity (LOH is important for lactate metaboism and redox balance) was thought to be higher than the normal mammalian levelruvate kinase was lower than nomal but regulated for more ecienc(PK is important n the control of the entre glycolytic pathway) Severalother enyme activities in the pathway also appeaed elevated hese observations later led to the concluson that marine mammal muscle was able tonction bette durng periods of anaerobc metabolism than was musclefromterrestrial mammals () eparate studies also suggested that harpseal Pa renan muscle was adapted for anaerobic metabolism during a dive because oxdatve enymes appeared to be low n actvty

However PK and OH activities were not quantied n these musclesaples (1) More recently muscle PK levels from harbor sealP vituna)and Weddell seal weddel) were shown to be higher tha that in sealion(Zalopus caloanus). ince PK was thought to corelate well withanaerobic capacit ths ncrease n activit was suggested as a basis for thegrater dving tmes n the phocids (47) In 1977, normal mammalan LOHlevels were found n muscle samples from a sea otter (Enhra /rPacic white-sided porpoise and sea lon (41)

wing to their vaied experimental procedues it is dicult from these

studes to resolve controversies or draw general conclusions about enmeactvty levels n marne mammals he ntal porpose data were based ononmuscle sampl from a sngle animal, and no terrestal mammals wereassayed ther OH and K measurements used onl the whte rat or no

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Rev.Physiol.1981.43:343-356.


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DIVIN SIOO 34

erresral orols ad he assas were made a25C hide a realisiierpreaio o meaolism a C

Tale oais vales from a sd i whih osise odiios were

me for measi isse aivi levels of ad PK from a rae oferresrial ad marie mammals (8) he daa ses ha (0) hihaivi, eiher for he rodio or iliaio of laae is o haraerisi of mare mammal msle ad () msle P aiv is o low imaie mammals, or does i parallel dive ime, as sesed ealier Usihese ieia, marie mammal msle does o seem espeial adaped forireased loli eme aivi

phal Ogans

he liver a kie ma also fae hoxi sress ri a ive. Emesdies of hese oras i marie mammas are sare. Tale shows aslh, alhoh f, se i e aivi fr mar mamalliver ad kide This iformaio a e ierreed i several was sho aeroi dives, he liver ad kide ma e slihl vasoosied osave eer ad oxe. The wo oras ma idle a reded meaolilevels "dri sh dives, ad his low level irease i ke aaeroi emes ma e imora for hese eriods Also, seal kides a re

abe ue ezme tvt eve me Da

Kdney KidneyHeart Brin Liver cortex medulla Mucle

LD H (pyrua t to lactat)

Ma 813323 21 29 538 188 382 133 322 99 12 23Trretr 82 243 3 82 32 149 233 93 86 48Rak WSDBHS MO,WS,D HSMWSS WS,B,HS SO,,WS,A WRHS ,WS SA

LDH (lactate to pyruvte)

Marine 189 84 539 5545 16 49 8421 2726 -

rrtl 46 9 9 19 15 1 R WBHM WMD HMW WHD BAW WRWHB

PK

M 8798 1 2 7 47 2 89 48 697 2Terst 225 131 198 45 32 7 24 2 66 61 86 374Rk WSOMD MDWRWS MDSHS HSSW HSSS SAWRW

aActitie are expred as trnatol unt moe of ubtrate corted to product per mnut)per gra wet ma tue at " pH AU tu r from dult nml Mucle acttie repood arage or a te meaure or each anm Mre mamma: Wde ea L weddelli

(WS); habo sal P vitna HS; sa o utrs SO Z calfornian (S) ad popos Stnla attUta SA). ad mmms: mus M mcl M h rbb Orycg cnc (WR) dog, Ca amr (D) dotic pig c (P) ad Bf, B t(B) Ra hows th highet four actte dcreag order gfct dffernce at 95% evel(tudet t-tet) how y underned vaue

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348 MN STINI DVIS

to noal function after a considerably longer anoxic exposure than can dogkdny (17). Prhap low mtaolic rat dung anoxa coupl to sligtlynancd aroic nzym ponil provid t ncsary rsisanc to

anoxia Fuheore the LDH activity for the remova of lactate suggeststhat these organs ar well geared to handle any lactate hat come o themduing or ar a dive Therefore, tese organs may be adapted for both anability to function anaerobically and an ecient rcovry from lactate load

nal OgansLittle biochemic inforation is available for maine mammal hat andbrain Simon al rpotd ta man mammal hart tisu PK incrasdwith diving ability (4) Alo LDH isozme studi on al and al hartdpic pa and kneic tha smd or caracteriic of kleamuscl than of ha (3 4 46) Hocachka Muy mphaiz tat tsisozyme paes imply a trong poential for bot lactae production andutilization in the arine mammal hea (23 4) PK and LDH activitycomparisons beteen Wddell seal and ox hear furher subsantiae thepropoition that anaeroic glycolyi ponal in Wddll sal hat igrar an in trri spcis (3 4). Hovr, owing to ac ofwide-rging samples and control thse ndings ay not be applicable o

most marine mammals Table 1 hows that ovrall enzme activitie forhear tissue ar similar in arine and terrestrial mammals Contray to 4)PK activity appears nol in aine mmal he tissue; aong mainemammals PK activity dos not cal to divig ability except that thWeddll has th ight value a it dos with LDH Ky enzym fornarobic mabolism ar alo claid o hig in in mammal raintissue (23 4)but a more recent repo notes that hese enzmes appearconstant in ll teestial and marine spcies xamined (8 he discrepancy may e xplaind y problm wih ampl iz and trtal con

trols For instanc th compaison of DH activiti betwn th Wddllal and ox may e wa for t lar appa low among trrtamammal 8 23 4) Aps o o ta LDH in t rain of wal andseal has impornt netic propeis ith regard to anaerobic function usedno controls for th cetacens and only showed a 10% diernce beteenrain of oodd sal and hp (4 46) Tu no clar distinctions in brainglycolyic enzym aciviy appar tn mot mmmals, hther testrial or mane

he levaed levl ofPK and LDH in Weddell hea may rct a yem

ang th maolic produc avalal dung t div Th hat lungand rain of the Weddell seal may shuttle lactate produced by the heappral orga or muc to th lung wre ome of it i convtd to

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DIVI SIOO 4

uose n hen eboze by he brn (22 2 su n osubsres ours he relonshs o ornse enze o

brehhol by y be uh ore oe hn he se ssoons

h he been sulze n he sEsn eene oes no suor he hohess h jor oons o enze y n rne ssues snn sssbrehhold n

METAISM

Reg Seady-Sae MeabThe resn ebos o n rne ls s es reer hnh o erresrl ls o equlen sze (, , 9, 6, Theresrory quoen s usull bou 05 beuse s he rr subsre or ener ebos The ree onenron n he booo hrbor ses (Phoa una s 2 es reer hn h n hunsor os bu s orbe o h n ny r ores (9 5 Crbohyre ulzon suors ess hn 0% o erob enery ebolsn hrbor ses Howeer he uoer res o uose n le llwhn he nor ln rn uose urnoer s roely 0

ol n n e uoer s 60 ol n (9 0More hn 0% o he rbohyre rbon s reye n h oshrouh oon s ree by uoen no s n rbohre n he e The enrl nerous syse ebolzes luose reerenll n ouns or os o he luose oze ( Oherorns n ssues he reonny bse ebos The nero

b hw roes


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35 N SN DS

blood and ss ogn and hgh nrg phospha omponds sh asAP and ran phospha n ss h laad omponn rpresnsnrg rqird o mabolz o glos h la ad prodd anarob

ally drn h dv h hypoha dvsons hav bn dl odisinish prmnlly (6 1 ) Som sdis showin ha h oy

gn db is lss han h smad oygn rqrmn o sppor a resnglvl o mabolsm drn h dv hav ses ha mabolsm wasrdd Howvr no all dv rsd n a small ogn db on hss ina qald h allad rsng onsmpon or h pod oh dv ( 4 45)

I is opraionlly dil o spara araly h oyn db romresng ogn pa Calaion o h ogn db dpnds on h val

sed or resng mabosm Smal hangs n resng oygn onsmpondrin rovy an rsl n sgnn ors n h oyn db alladovr a mn rovry prod Sh hangs ar lil onsidrng hdispion o sadys mbolsm and h addd s o srss andaig

Sn dving mabolism and h rlav onrbons o arob andanarobi pahways anno b drmnd smply rom h posdv oyndb radiosoop ovr hnqs hav bn sd o drmn anaro

b nrgy mabolism drng rsrand dvs in harbor sas Anarobaiviy dn lmin div approimad 1% o rsin mabolismrsling in h prodion o 7 mmol laa Carbohydra sors oranarobosis nld boh blood glos and ss glogn ) Arobmabolism drng dving has no bn drmind Oygn sors n lnblood and iss ar horially sin o ovr only 6% o h rsnmabol rqirmns or lmin dvs I appars ha mabolism drngrsrind divs is rdd a las % blow h rsin rqirmnSbsra or h arob nrgy onrbon may inld no ony arbohy

dra b aso a whh is h mos abndan nrg sbsra Drngrovy mos o h laa prodd dn h div is ryld and lsshan % is oidid ()

hr indir vidn iss or a rdion n mabolism blow hrsing lvl di rsrind or volnay divs involvin lil ronh or mprar o sls oribly sbmrgd (4) and dving volnary rom an i hol () drasd drng or mmdialy arh divs Tis drop dspi nhand hmal inslaion rslin rompriphral vasoonsriion sss a rdion in ha prodion Fr

hrmor nry mabolism old b rdd by as mh as % blowh rsin lvl a rsul o drd ha wor and ssaion o rnrn prodon (). nry savins may also rsl rom a rdion

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DIVING PHYSIOLOGY 1

splanhni oran an msl maolism as of r oo owAlhoh aaroi maolism ma spplmn aroi aivi in hsisss i ma o ompll rsor maboli ra o h rsi lvl in

air Unforal h maboli aivi of ah oran rin ivi haso b rmin

PHYSIOLOGY OF THE NATURAL DIVE

Bradycardiao br rsa som of h ariovaslar rsposs o aral ivshar ras r for ran a fr ivs hav b ompar Mos

of hs sis hav s smirsri nviroms shassnall poolsIn sh a siaion haror sals ma 2mi fr ivs Variaion i harra rlaiv o iv aio ss som assoiaiv lan wih hivs (1) Harbor sals hav also bn rain o iv a srfa ponomma Unr sh oniions animals rahhl for slihl ovrmi an xhibi a lss xrm braaria han rin for ivs (11)

Ur aral ivi oniions wih Wll sals har ras for hiniial phas of h ivs wr rmin for ivs ranin from a fwmins p o min (). Div raio a har ra orrla p oa iv rao of ao 2 mi Th mos inns raaria orrri h lon ivs Similar rsls hav n obai wih ivin irs(

Ths irlaion appars mor opn rin fr or nfor ivs hanri for ivs (or xpioall lo aral ivs) Frhr vinfor his prmis is avalabl from h posiv lai ai oraios ih bloo

Lactc Acdh amlaio of lai ai n msl rn h iv a is bolsprlas io h irlaio afr h iv hav ohr b all hhallmar of ivn in aqai vrbras (2 ) n Wl sals howvr no sh v ors for fr ivs lasi


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KOOYMAN, CASTELLINI & DAVIS

24

6

! 15a

8

TIME (Minut)F The peak arterial lactic acid concentrations obtained durng recovery from a varetyof dve duratons n thr derent adult Weddell seals. he damond at the abscssa zero sthe average restng lactc acd concentraton (n = 9 7

Bod Tempeatue and MetabosmDring long fr iv bo tmratr ro it xtion b thanimal hi ro ma b a mh a2C in or tmratr rng a iv of a g al Althogh it ma b arg that inraontion to th watr ow at th animal nhan hat lo itm that h a ro i not oibl nl mtaboli rate i low 7 him to ort rher th iea that mtaboli rate ring iving evenin frl wimming ll al i not ver grat 6

Dve Behavo arobi iving hele nable an animal to tili mor intl thtime nt iving Aftr a min anaerobi ive a el eal reqire

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00E

wU

0

.

IVING PHYIOLOGY 5

'0 mn.

,

--1324min

-1/.0-0 0 0 0 0 0 0 0

REER ME (m)Figure Arterial lactic acid concentration changes during recovery from a free dive of 43min, pooled samples from three free dives of 13-24 min [moded from (37)] and a 20 minforced dive in Weddell seals [modied from (40)]

abou 0 in o reu o predive lai aid onenraion an pH (Thu ou o a oal o 5 in on 9% i pen ivin I nead h ealake ix 5n ive, eah requirn onl a 4in reover, o 0%o he ie i pen underaer The nora eedin heue o he Weddeea oo hi pae o an hor ive ih hor reoverie (nee, on % o he ive o Weel ea exee heir propoe aerobilii o 5 in ( Suh behavior a be univeral in divin repile

bir, and aal reen evidene on divin pa o u eal lenduppor o hi onep (G L Kooan, unpubihe obervaion Beaueuh varabe a he bood O ore probab diae he uraion o eedinive, ur ea ake horer dive han edde ea an ke rean

aerobi durn he divSUMMARY

Naural dive are uual hor an aerobi, involvin iin eor hai no enereiall ol Preen evidene indiae e i an ajorbioheial enze adapaion ha oud prooe an exended anaerrobi apai in arine aal

We have iue he lak o evidene or unuual bioheial aapa

ion or anaerobioi and he iporane and haraerii o nauraaerobi dive Wha explanaion an e oer or he knon apabili ooe arine aal, uh a Weddell eal and per hae o rnubered or over an hour? ribue ha erve he ell or horer

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354 YMAN ASLLINI DAVIS

dvs pon lso fo long dvs sh s: ( lg ol oxgn lv d si nd () psimonios s of loo oxyn o ow ny imns of vios ons in on ivs

gn dpl h xgn c pdnl dpndnn no ols nd ld p lg qns of l Th sls dg f fg h lvs h nl npl of fh nnsdvng vs f so Consqnl lng n dvs q in n

Lterature Cted

Anrsn, . 966 Physiooa aapaions n iving vrbra PhysolRev

46:222 B P 870. D 'a pongr hzs mammirs hz s oisaxrnim on n Le{on sur a Phys-ooe Come de a RespratonPars Bair s. 588 pp

Bx A Brg yhn J 970Laat hyrognas in a ivngmamma h ommon sa (Phatuna tuna) Int Boem292-94

4 Bix A From . 97 Laahyrognas in divng animasa omparaiv sy wth spia rfn o h ir (Somatera mosma Comp ohe Physol 57984

5 Bix A . Kjkshs J K. Eng Bergan, 9 Myoaa owin the ivng sa Acta Pysl an96277-80

6 Brooks O A Branr K. E CassnsR A. 97 Gyogn syhis an mosm of ai ai af isAm Physol 226266

7. Br P J. 979. h s of raio

mry in h sis of iving anying ds n Handbook on Boteeme-t and Rado Trackn . C Am

anr D W aDona pp 56977N: Pramon

8. asi M 980 Enzyme boem-t n te tues of marne mammaPhD hi Uv Caif a Digo LaJoa

9 avis R W 980 Dvn eneetsand ntermeda metabom n teharor sea. Phoa via. PhD hsis in prp Univ an igo

La Joa0 avis R W Kooyman G 979Diving ngis a inmay mosm h ao sa Patuna n Astracts m esentatons

at the 3rd enna Conerene o te

Boo of Marne Mammas O. 7 979. a Washgon

Esnr R. E. 965. art ra rponsin for vrss raind xprimnaiv in pps Haraets Skr 8229

2 Esnr R. E. 99 ariovasar ajusms ing n e oo oMarne Mammas . . Anrsnpp. 75 N: Aami 5 pp

3 Esnr R. E. Frankin D L Van irs R L Knny D W 966 iovasar fns agains asphyxaSene 5949

Esnr R E. Bx A S, Kjkshs J

978. iss prsion an ishmia nving sas Physoost25. Frgson J. . Fak . E 97 Fr

fay ai vs in svra spis of ai aivor Comp ohe PhysolB092

6. Grg J C. Rona K 97. hhap sa Paopus enanduXV Urasu an maboi aaptaion of ska mus. Can 588

7. aasz N A. Esnr R Garvi R. .Gok G . 97 Rna ovyfom ishmia a ompaaiv sy ofharbor sa an og knys Am Physo 2275

8 amm Esnr R W r C. Magg aon R977 morgaoy pons o

aring hypohaami mprar h harbor sa A Physol 22R826

9. as P 99. Lai a a phogson b ao Re 3890

20 aris P. Baman . Bay . JDona K W. Gosr WhhaT 968. Obsrvaions on h os of mai vns aompanyngmi xris Q. p Physo 534

Annu.

Rev.Physiol.1981.43:343-356.



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1. Hason, R. J., Kooyman, L. 1968.eeral physiology o the iiian e ehao andPhysiolog of n-npeds, p. 2119. N: AppletonCetuyCrofs

11 pp. Hhachka, P W., Lgns, C,Qvst J, Sceider, R, Snider, M. YWoders, T R Zal W M. 1977Pulmona meabolsm ug vgotog bloo fo te baene 198831-33

23. Hhacka, P W, Muph, B. 1979Metalic satus duig dig ad reve mae mammas I ntea-tona Reew of hsoo nn-menta hsoo I ol ed. DRotshaw, pp 253-87. Baltimore

University Park Prs2. oaca P. W., O T G, Ale, F, Wtto, G C 195 Multpleend products o anaeoiosis i divingvetebrates. omp ohem hso 5:7

5 ach P W Storey K B195. Meabolc cosuen of vgn amals a ma ene 1863-

6. rig, L. 1939 Rpiratio in divingmammals hso Re 19:1-34

27. Ing, L. 19. Compaave aatoma psolog of gas tas mhansms n Handk of hsooio ' espton W O Fenn, Rahn :177- Wasington DCAm Physo! S.

28 Ivg, L, , I. S. 195. Te meblsm ad insulato o seals as aeski mmals i cold watr a JZl 35497-5

29 Irng L Scholader P F, Grnnell,S W. 191. he rspaton o the poise, Turso tunat e mp

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1981.- Physiology of Diving in Marine Mammals

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