OMlrsltion Physiology (1980) 44. 25-37liesicr North-Holland Biomedical Press

DESIGN OF THE MAMMALIAN RESPIRATORY SYSTEM.III. SCALING MAXIMUM AEROBIC CAPACITY TO BODY MASS:

WILD AND DOMESTIC MAMMALS*

Kit -HARD TAYLOR, GEOFFREY M.O. MALOIY1, EWALD R. WEIBEL2,VAUGHAN A. LANGMAN, JOHN M.Z. KAMAU1,

HOWARD J. SEEHERMAN and NORMAN C. HEGLUND

\liniiini ni Comparative Zoology, Harvard University, Cambridge, MA 02138. U.S.A.

iisiuii. I he purpose of this study was io determine whether the maximal rate of oxygen consumption, , ,, in scaled proportionally lo Mh' ".as the dilTusingcapaciiy ofthe lung, or proportionally to Mb° '\I ih.- standardized resting rate of oxygen consumption (V(|.„j). Wc measured V„,„ul on a variely ofi-intii.ili.il> species (i4 wild species and 8 domestic or laboratory species ranging in Mh from 7.2 gi '!■■ Lei using ihe same 'treadmill' procedure for all animals, lor the wild species wc found:

\ - I 9 4 M h ' " ' ; r = 0 . 9 9 5

Let' V. „,,, has the units ml sec ' and Mh is in kg. There was a greal variability in V0,nu, among•in, in speciesoflhcsumc size, horse and dog having a V,, ,nu> more than 3 limes that of a cow and sheep,

p.'. mel) Hoih ihe variability in V,,.,„,. wilh body si/e and among animals of lhe same si/e provide.wii.ii tools ti>- investigating the relationship between structure ami funclion at each step in the

;mi ilon system, Iron, the oxygen in environmenlal air lo lhe oxygen sink in lhe mitochondria.

Anaerobic glycolysis

Oxygen consumption

.,/ /..i publication J October I98Q-m.ly «..s supporled by funds from the following sources: NSF grant PCM 75-22684 and

IM s.-tt|.j ui CR. Taylor; NIH grants AM 18140 and AM 18123 lo C. R. Taylor; NRS Trainingr. - I COM (.7117-02; National Geographic Society gram to C. R. Taylor; Guggenheim Foundation

'•• <' R. Taylor: Nuffield Foundation gram lo G.M.O. Maloiy; Wellcome Trusl grant 10i MH Malo iy.■ ib.lraclorparl of this study has been published! Taylor. Scclicrman. Maloiy. licglundand Kam.iu.

II HI address: Department of Animal Physiology, University of Nairobi. Nairobi. Kenya.I "i address: Department of Anoiomy, University of Berne. Hiihlstrasse 26. CH-3000 Bern 9.» l i . u u l

' I nnoo-tioiH. S02.50 ft FIsevicr/Norlh-llolland Biomedical Press

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measured represents .he aerobic capacity available 10 these animals in nature,Bovids were led on a mixture of hay and alfalfa supplemented with salt, calciumand vitamins. Viverrids were fed on fresh meat, supplemented with eggs, vitamins,c a l c i u m a n d c e r e a l . , . . „ , ,

Precedes. As descr ibed in .he preceding paper (Seehenyn «■ a lV„ was measured while animals ran al various speeds on a treadmill. 1 he animalswere exercised on the treadmill for a minimum of one hour each day at moderate-exercise intensities (i.e., V„. = 50 80% V0j ) while being trained. V, lor a particularspeed decreased while animals were trained, until after 2 6 weeks, it reached aconstant value. Once we were able to obtain reproducible values lor V„: at any

speed, we considered the animal •trained". The. we measured V.,: as a function oltread-speed using 15-30-min measurements at any particular speed. Speed wasincreased until V,„ no longer increased with increasing speed. At these high speedsihe small animals'would only run for 3 5 ...in and the larger ones lor 5 15 mmand V was determined for these shorter lime intervals. V,„. was also measuredin a number of experiments, lo determine R values. Blood samples were taken a.the beginning and the end of limed runs and analyzed for lactate. Rates ol ...creasein blood lactate concentration were determined by-dividing the change ut con*cenirat.cn that occurred during the run by the tune lor the run. We consideredthe animal had achieved V„ ,, when V„. no longer increased With mcreasin.speed and the additional energy consumed by the muscles could be accounted loiby anaerobic glycolysis.

\h-lhods Rates of oxygen consumption and carbon dioxide production weremeasured simultaneously using an open-circuit system as described ... the previou,

paper (Seeherman el al.. I98l>. The animals wore light-weight masks lor measuremenlS of gas exchange. Air was metered through lhe masks a. rates between Iand 5 I sec ' (STI>) for the small animals and 5 and 40 I sec (SI I') lor tinlarger animals. V„ and V,„. were calculated using the equations derived by I uekc(|%8) for a similar system. Flow meters were calibrated daily by metering N.. ml.the box or mask al a known rale and measuring the resulting changes in conceniration as described in the previous paper, lhe masks were checked lor leakof exhaled air by decreasing the How rate by 30",, as the O, consumption wa.monitored. Thi, procedure should increase the magnitude ol any loss ol exhale,air No difference was found between lhe two measurements ol Vtl. indicating n-leaksexisted. Two paramagnetic oxygen analyzers were used: a Beck.nan Model G-lfor the viverrids; and a Taylor Servomex Model OA 272 lor the bovids. Bothwere connected lo poie.uiometric recorders lhat were spanned to give a lull seal.deflection as oxygen concentration changed from 20 lo 21 "„. Both oxygen analyze. -were calibrated by changing the total pressure of the air (lowing through the sensocell and calculating the change in concentration of oxygen using Boyle s lawThe oxygen concentration ol a lank ofcomprcsscd oxygen and nitrogen was lhe,measured and Ihe oxygen analyzer was calibrated on a daily basis using th-analyzed gas mixture. The CO.. analyzer (Beck.nan Model 15-A) was calibrate I

SCALING OP V,,.,,,,, TO BODY MASS

daily by metering CO- at known rates into the face mask while room air wasbang drawn through lhe mask at lhe same rate as il was in the experiments.Accuracy ofthe entire system for measuring V„. and V,„. was better than ±3%.

Net rales of anaerobic glycolysis of the animal were determined from rates of

change in lactate concentration in the blood during the runs. Blood samples wereobtained through catheters that had been chronically implanted in the external

■tigular vein. The laclale concentrations of blood samples were analyzed usingU.K-luinger Mannheim Lactate Test Combinations and a Beckman UV Spectrophotometer (model 24). 0.5 nil-samples of blood were used for the analyses.

\., increased with increasing tread-speed up lo a maximal rate. Vllmj%, and thenu-inained constant wilh further increases in speed in each of the twenty-sevenniimals lhat we used in this study. Values for V„.,„, for each individual and the

i.uige of speeds over which il was observed are given in table I. V„;mj> was achievedluring level treadmill running in all of lhe animals except the elands. It wascvvssary IO incline the treadmill slighily i2.83") and measure V„. while the elandshi up the incline in order to obtain their V,, All of the animals would continue

.. run at speeds faster than that where V,,.,,,,, was first reached. Al these speeds.elate accumulated during the run unti l blood lactate concentration reached' 29 mmolkg ' . At (h is point the animals would s top running and i t was

accessary to terminate the experiments, lhe maximum concentrations of bloodLiciate measured al the end of a run are given in table I. The maximum rales ofurease in blood laclale concentration (Le. the increase in lactate concentrationluting lhe run divided by the duration of lhe run) increased with increasingpeed after V„.,„,,, had been reached. Ihese maximal rales varied from 2.8 to'i tijinol -kg•min"1 (table I).

Vii.hu. is plotted on logarithmic co-ordinates as a funclion of M,, for wild (circles)ml domestic (triangles) mammals in fig. 2. The slope of lhe relationship for thelid mammals is 0.79. for lhe domestic mammals it is 0.76. and for the two groupsnil).ned il is 0.77. None of these slopes is significantly different from the oilier

i lhe 95",, level of confidence (table 2). The coefficients ol" the allometric equations'ciliated by least squares regression loi these three relationships are given inhie 2. The proportionality of V,,.,,,,, to M,,"" resulted in a decrease in V,,:nu,/Mh

.'• 4-fold with increasing M,, over the size range of animals that were used in.se experiments (table I). Because of lime constraints during our experimentsVfrica. we were not able lo make the morphological and physiological mcasure-•ois on the same individuals in every case. In fig. 2, those individuals on which

were able to make both measurements are denoted by closed symbols andindividuals on which only V,,.,,,,, was measured, by open symbols.

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D E S I G N O F T H E M A M M A L I A N R E S P I R ATO RY S Y S T E M SCALING OF V,)jniJ< TO BODY MASS

TABLE 3

Coefficients of ihe. illometric functions relating v0.mj< and body muss (Mb) in l4speciesof wild mammals,8 species of domestic/laboratory animals and ihe 22 wild and domestic species combined (determined

using our treadmill exercise procedure); and in 55 wild and domestic species obtained by combiningour dala with 23 values taken from ihe literature (where a variety of procedure's were used to obtain

vo.m..v>- V0 m,-aMbk and the units for V"o.m-« and M,, are ml sec'1 linTJ k^; r - Correlationcoefficient between log(V„ ,,,,.„) and log (Mb)

I VS*,; loitjideiuiniei \,il I

l - 0 . 2 2 . 3 A l i U K 5 5D o m e s t i c m a m m a l s ' I < > ' ^

Wild und domestic mammals' 1.92

Wild .nul domestic mammals, 1.67

including 23 sallies fromlilcc.ilurc' and our

' Wilh cu'llc divided inio two Size classes of M,, because M,, of our ...lull animals varied by 2-fold.• V„.llu, values for shrews (Morrison el <■/.. 1959); P)fc-iii> mice, kespcl mice, while mice, feral house

mice, tundra voles, white rais. Al'g.in pika (Roscnmunn und Morrison. 1974); wild nils (Hart andHcrouJt. 1963): musknit (Han. I%2); rahhiis. lemming (Hurl and Heroux, 1955): vole (Roscnmunn• l ,il.. I'J75|; while-fooled mouse (Scgrcin and Hurl. 1967): chipmunk (Wunder. 1970); snow-shoe hare(Feist and Roscnmunn. 1975); while mice, hamsters, while ruts, guinea pigs (Pascjuis .■/ .;/. 1970);dog (Clulounel and Minaire. 1966): dog (Young el .//.. 1959); dog (Ccneiclli el ,il. 1964): h.imslcr(Pohl, 1965); horses (Urody. 1945); humans (As. rand. 1952; Murgariti etal., 1933; lloppeler etal., 1973).

O u r d a t a c o n fi r m t h e a s s u m p t i o n m a d e b y m a n y a u t h o r s ( W i l k i e , 1 9 5 9 ;Hemmingsen. 1960; McMahon. 1975) and the general finding of previous studies(see Pasquis et al., 1970; Lechncr, 1978) thai maximum rate of oxygen consumption

Vcnui is nearly a constant multiple of ID limes resting metabolism V,,.,,,,, andscales approximately proportionally lo M,," .

Despite lhe fact that we did not find a "new" allomelric function between V„.„U1and M,,, we have obtained a more accurate and reliable relationship than was

previously available. There was remarkably little variability in the data we obtainedfrom the wild animals (table 3) and this probably best reflects the optimization ol

design of respiratory structures as demands for oxygen change with si/e. Foiihese reasons, we prefer to use the regression calculated for wild animals as the

general allometric relationship for V,,.,,,,,. i.e.

V „ . = 1 . 9 4 - M , . " " ' ( I i

I'■■ | or comparison, Kleiber's equation for standardized resting oxygen consumption

j;w:V , , , , , . , = 0 . 1 8 8 • M b ° " « ( 2 )

1 : in both cases V0j has Ihe units ml 02 sec"1, and l\ib is in kg. Among domestic

j j .uiimals the variability in the relationship between V„!11U, and Mb was very large.Ihe 95% confidence limits of the scaling factor ranged from 0.61 to 1.10. For

j ' nimals of similar body size we find V„./Mh for horses or dogs to be 3.5 times; ; ieater than that for cattle or sheep and goats, respectively. Thus, domestic animals

;' provide the extremes of adaptation for oxygen demand within a size class, and iti interesting lo note that the wild animals generally fall midway between thesei ciremes, as witnessed by the group of large species shown in fig. 3. For this reason.: eluding Ihe domestic animals in the allometric relationship between V-,,^, and\| of wild animals changes the scaling factor little, but does increase the range ofi ic 95",, confidence interval for the coefficienl and the exponent of the equation.un lhe other hand, different design strategies might conceivably be used to meet; ,e different demands for V„. between animals of Ihe same size than between

iinials of different size. For this reason, comparisons of the structure-function

l.tlionships of animals ol" the same size should provide another powerful tooli helping us to understand how lhe respiratory system is designed.

Including the values obtained for V,,;in.„ from the literature in the allometricnions changes the scaling factor from 0.79 to 0.85, although these values arei significantly different at the 95% level of confidence. This increase in the

ponenl is due to a systematic error. Most of the values for V,,.,„„ in the literature. from small animals exposed to the cold and are about 20% lower than the

.,. that would be obtained using our exercise procedure which was applied to•si of ihe large animals (Seeherman el <//., 1981). For this reason, we prefer not

j include data obtained using other procedures in our allometric relationship.; i 11 can be seen by looking at table I of the previous paper (Seeherman el al.. 1981)I (able I of this paper that animals reach their V,,.,,,.,, at very different running

| -c . ls I f one ca lcu lates the re la t ionship between the min imum speed where| '• ., is reached and M,,, the following equation is obtained:

Speed ai which V„.IIU, is reached:

j | 2 . 3 - 1 M „ " ' ' - ' ; r = 0 . 4 5 ( 3 ).•re sp^.J is in msec ' and M„ in kg. lhe low r value reflecls the great

j iwhiliiy in this relationship. For example the horse had not reached its V0.mJ,

j \ ■ speed of 10 m • sec ' (the top speed of our treadmill) while a cow of the"•' Mb reached V„.inj, at a speed of about 4 m sec '. Comparing the speeds

] l"l"h V„.„u> is reached with the speeds at which animals travel in nature, one findsj ' 'i some animals move back and forth across that speed as they move about innv. while other animals probably never reach Vl)jm4l, even when being chased

. predator. This has two practical consequences: (1) the speed at which V,,.,,,,,

I \

J 0 D E S I G N O F T H E M A M M A L I A N R E S P I R AT O R Y S Y S T E M

is reached is not an equivalent speed in terms of the mechanics of the locomotory ['system of animals with different Mb; and (2) it is relatively easy to obtain V0jm,, |on animals that normally exceed it (rats, humans, sheep, goats, cattle, wildebeest, |eland etc.) and very difficult to obtain V0inul for animals that normally never |r e a c h i t ( d o g s a n d h o r s e s ) . _ ' « • '

In conclusion, we have ruled out the possibility that both V0inu, and Dl0, are ggscaled proportionally to Mb10, its it appeared possible al the start of this study. |On the other hand, estimating Dl0i by morphometry on the same individual panimals for which V0|m„ had been obtained in this study, Gehr el al. (1981) |confirmed the previous finding that Dl0j is scaled approximately proportionalh |to Mb10. Thus, our measuremenls of V()jmJ, and Dl()j on the same individual- |confirm, rather than resolve the intriguing findings that maximal rate of oxyger. Aflow across the lung per unit diffusing capacity decreases witfc increasing body mas-. M(i.e. V„ „u,/DL0l ocMb"°"). This results in approximately a 10-fold difference in f jthis parameter relating function and structure of the respiratory system as th-: ;-.jlevel of the lung over the size range of mammals we have considered. Possibl • i Jexplanations for this paradox arc outlined in the concluding paper of this serie. •>( W e i b e l e l a l . , 1 9 8 1 ) . j

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Gehr. P.. D.K. Mwangi. A. Ammaii.i. Ci. MO. Maloiy. C. R. Taylor and E. R. Weibcl (1981), Desi aof the mammalian respiratory system. V. Scaling morphometric pulmonary diffusing capaclo body mass: wild and domestic mammals. Respir. Physiol. 44: 61 86.

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