Quantitative Laws in Metabolism and Growth Author(s): Ludwig von Bertalanffy Reviewed work(s): Source: The Quarterly Review

of Biology, Vol. 32, No. 3 (Sep., 1957), pp. 217-231 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/2815257 . Accessed: 26/12/2012 21:20
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VOL. 32., NO.

September, I957

THE QUARTERLY REVIEW

of BIOLOGY
QUANTITATIVE LAWS IN METABOLISM AND GROWTH

beaimed at establishingconnections aspectsofliving tweentwofundamental and growth. their metabolism organisms, of even a simple What we call growth complexphenomenon organism is a tremendously cytological, physiological, fromthe biochemical, viewpoints. Thereare,however, and morphological certainaspects that are amenableto quantitative analysis,and such an approach appears to lead to some insight into the connectionsbetween and growth, and to some answer to metabolism the seemingly trivial,but in fact hardlyexplored question, "Why does an organismgrow at all, and why, after a certain time, does its growth come to a stop?"
QUANTITATIVE RELATIONS BETWEEN BODY SIZE AND METABOLIC RATE

BYLUDWIGVON BERTALANFFY
INTRODUCTION

and University Los Angeles Mt. Sinai Hospital, Biological Research, ofSouthern California, _ HE work reviewed in this paper is
just one example:pulse rate in mammalsclosely to the Y powerof body weightover corresponds seven orders of magnitude,from a dwarf bat weighingsome four grams, to an elephant of 2000 kilograms,in spite of the fact that the animals under comparison belong to different orders,and are adapted to all sorts of climate and ways ofliving(Fig. 1). The relationbetweenmetabolicrate and body size belongsto the classical topicsof physiology. It goes back over more than a hundredyears to the time when Sarrus and Rameaux, Bergmann and Leuckart, and Richet noticed that weightspecificmetabolicrate, that is, the intensity of as measuredby oxygenconsumption metabolism or calorieproduction ofbodyweight, per kilogram decreases with increasingbody size. A classical example is provided by Rubner's experiments size (Table 1). It appears with dogs of different that metabolic rate per kilogramdecreases. If, however,metabolismis calculated per unit of body surface, approximatelyconstant values appear. The comparisonof metabolic rates in mammals led Rubner to the contentionthat warm-blooded animals produce daily about 1000 Cal. per square meterof body surface.This is the originof the famous surfacerule, which was explained ofhomeothermy. byRubnerin terms All warm-blooded animals heat theirbodies to a of ca. 37?C. Heat outputtakesplace temperature thebodysurface. through Hence, thesamenumber of caloriesmust be producedper unit surfacein orderto maintainthe body temperature constant. There are, however, considerable difficulties

it may be In orderto begin this investigation, activities, emphasizedthat,in manyphysiological the absolutesize of the body is a mostimportant Whether the rate of processes. factordetermining heart or respiratory we take total metabolism, of the organism, rate, the chemicalcomposition or the enzymecontentof the cells-we excretion, vary always will findthat theycharacteristically with body size, this being true even thoughthe the organisms comparedin such respectsshow a in their tremendous anatomy, physiologidiversity cal mechanisms, adaptations to certainenvironments,and so forth(cf. Adolph, 1949). To give

217

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218
1000

THE QUARTERLY REVIEW OF BIOLOGY

~~~~80O
IL

co

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BODY WEIGHT
FIG. 1. ALLomETRic DZEPENDENCE OF PULS5E FEREQuENcY ONBODY WEIGHTIN MAMMLS
It rate, pulse basal may be assumed that the volume of blood transported per minute is proportional to the basal metabolic as the oxygen consumed must be transported by the blood. This volume is equal to stroke volume (S) X frequency (F). In a rough first approximation, S may be taken as proportional to body weight (W). The metabolic rate follows interspecifically, in the series of mammals, the W! rule. Hence:

S.F. = CW.', and = = C'W

a =-.28. The constantof pulse frequency, the gross over figmreshows that the allometry Notwithstanding whichneglectsanatomical,physiological, and otherdifferences absolute body size is the ecologicalo simplirication in a rangefromthe dwarfbat (4 g. body weight)to the elefactorin the controlof pulse frequency, dominating (1951a). phant (2000 kg.). ModifiedafterBertalanffy

TABLE 1 Metabolism in dogs AfterRubner (1902).

in kg. Weight

Cal.per production Cal. production per kg. sq. m. body surface 85.8 61.2 1909 1073

11.0 17.7 19.2 23.7 30.4

3.1 6.5

57.3 45.3 44.6 40.2 34.8

1191 1047 1141 1082 984

in measuring the outer surfaces of animals device can be exactly,but a simplemathematical applied. If two bodies are reasonablysimilarin shape, their surfacescan be expressedas a 23 powerofweight, sincethecubicrootofthevolume or weightis a lineardimension, and therefore its square has the dimension of a surface. Hence, the surfaceareas of geometrically similarbodies can be obtained by multiplying the 23 power of the weightby a suitableconstant.This is seen in the ofMeeh: well-known formula
S =bW (1)

The surface rule of metabolism accordingly states that the basal metabolic rate is proportional to the /% powerof the weight.In the case of man, the determination of the basal metabolism is a clinicalroutine,in orderto diagnose disorders and the like.Here thesomewhat thyroid more complicated Dubois formula is applied. Dimensionally, however,the Dubois formulais identical with the surface rule. The Dubois is: S = kW0425 formula X L0 725. As, presupposing geometrical similarity, lengthL = cW', this can 33) = bW be written: S = kWO-420. cW0 725(0 The relationbetweenmetabolicrate and body size can be studiedeitherintraspecifically, i.e., by animalsofthesamespeciesand different comparing body size, or interspecifically, i.e., by comparing adult animals of different species. We are at present mainly concerned with intraspecific comparison. A grave objection can be raised against the surfacerule as foundin textbooks of physiology. In considering the quantitativerelationbetween metabolic rate and body size, homeothermic vertebrates and, in particular, mammals are almost solely taken into account (e.g., Brody, 1945; Kleiber, 1947; Krebs, 1950). However,the case ofmammals is by no meanssimplebut rather

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QUANTITATIVE LAWS IN METABOLISM AND GROWTH

Moreover,as we shall see presently, is intricate. many familiar conclusions and explanatory fall flatif not onlymammalsbut also hypotheses are vertebrates and invertebrates poikilothermic necessary It is therefore takeninto consideration. to considerthe problemon the broaderbasis of A considerablepart of comparativephysiology. in the author's thisworkhas been carriedthrough laboratories. theseresults,one more In orderto understand is necessary.The dependformula mathematical ence of the metabolicrate of an animal on body in the equation: size can be expressed TABLE 2 CO2production pallasii ofArmadillidium (Temperature 21?C.)
MUller (1943b). After

219

in mg. 15 33 50 100 160 Weight 3.0 5.2 7.2 11.2 15.2 Cmm.C02/hr. 200 174 144 112 94 Perg./hr. Perunitsurface (WI)/ 48.5 54.2 53.0 49.8 51.6 hr.

of animals in which the surfacerule does not hold. 3. Thus we come to the statement that several M = bWG, (2) metabolictypesexistwithrespectto the relation rate and body size. metabolic whereM is the metabolic rate per unit time, between In view of what was said previously,three W the body weight,and a and b are constants. types,that is, three different ways of This is a special case of the so-called allometric metabolic fornula (Huxley, 1932) which expresses the dependenceof the metabolicrate on body size this classification applying, amount can be distinguished, on body size foran enormous dependence allometry, and as was emphasized, to intraspecific of morphological, biochemical, physiological, sizes or to be that is, to individuals of different evolutionary data. This formulacan further animalswithin one species. growing in thefollowing way: written metabolicrate is proportional In thefirst type, o? log W (3) log M = log b + or the 23 powerof theweight. to a surface RepreThat is to say, if metabolic rate is plotted sentatives of this type include fishesbut also such as crustaceans, clams, we certaininvertebrates, against body weight double-logarithmically, line the slope of whichindicates and ascaris. Table 2 presentsone example, the obtaina straight a. Ifa = 3, themetabolic ratefollows metabolic rate in the sowbug, Armadillidium. theconstant per unit rule. If a = 1 or the slope is 450, the As can be seen, its oxygenconsumption the surface metabolic rate is proportionalto weight. With weightdecreaseswith increasingbody size, but remainsconstantper unit surface.Subsequently 1 > a > 23, an intermediary case obtains. values are taken, that is, if it will be seen that sowbugand companyreveal If weight-specific metabolicrate per unit weightis plottedinstead quite a bit about human growthas a central ofphysiology. of thatof the total animal,the equationbecomes: problem Here the The second type is quite different. M =bW (4) metabolic rate is proportionalnot to surface so oxygenconsumption area, but to weightitself, metabolic rates, in an animal of double size is simplydoubled,in weight-specific Correspondingly, weight, an animal fourtimesas large is quadrupled,etc. as a generalrule,decreasewithincreasing and the slope of thelogarithmic plot is negative. Direct proportionality of metabolic rate to weight we can summarize is found in growinginsect larvae and hemimeAfter these preliminaries, results in the followingway tabolous insects, as well as interspecifically, the experimental in 1941b,et seq.): (Bertalanffy, related species. comparingimagos of different 1. The surface rulealso holdsforpoikilothermic Table 3 shows metabolic rates in the walking The rule is, stick, Dixippus morosus.Oxygen consumption and certaininvertebrates. vertebrates of a wide application;but the explana- per gramand hour appears to be constantover a therefore, for in wide range,covering tion given by Rubner is too restricted, all body sizes and the entire animals thereis no thermoregula- development.Other groups belonging to this poikilothermic tion, and thus the latter cannot be the basic type are land snails of the familyHelicidae, factor in the relation between body size and intraspecifically as well as interspecifically, and rate. metabolic annelidssuch as the earthworm. 2. On the otherhand, there are many classes Finally, in the thirdtypemetabolicrates are

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220

THIE QUARTERLY REVIEW OF BIOLOGY

TABLE 3 Oxygen consumption ofDixippus morosus (Temperature 20?C.) After Muller (1943a). and larger individuals,in which case it should also be foundin the respiration of tissuestaken out of the organism; or else, it may be regulated by factors present and active onlyin theorganism as a whole. Let us start with the organismic hypotheses. The most familiar one has already been mentioned, namely, thermoregulation. There is no doubt that energyexpense for thermoregulation forms a considerable part of the total metabolism in homeothermic animals.However,this explanation cannot be generalsince the surfacerule also applies,and in factis moreaccurately established, in cold-bloodedvertebrates and even in certain invertebrates wherethereis no thermoregulation. Anotherinterpretation assumes that the surfaceruleis based upon theanatomy and physiology of the circulatory system. The supply of oxygen and nutritive materialsto the tissuesis naturally a function of the intensity of the blood current. The latterdependson factors such as the size and stroke volume of the heart, the frequencyof heart beat, the diameterof the blood vessels,the degree of capillarization, and the like. As has already been indicated, there are rather strict quantitativerelationsbetween body size, metabolic rate, and pulse rate. Thus, in interspecific comparison"fromthe mouse to the elephant", pulse rate decreases approximately proportional to the % power of the weight(Fig. 1). So does basal metabolic ratein theinterspecific comparison of mammals,if adult specimens of corresponding species are plotted (Brody, 1945; Kleiber, 1947). cannot offer However, hemodynamics a general explanation.Remember, for example,the clams, where the circulatory system is completely fromthat foundin vertebrates, different or recall ascaris, which has no blood circulationat allanimalswhosemetabolicrate nevertheless follows the surface rule. Recent investigations of the Ludwiglaboratory (Ludwig, 1956; Kienle and Ludwig, 1956; Sattel, 1956) give some supportto the hypothesis proposed by Ludwig and by Bertalanffy (1951a, p. 252f.) that the "metabolictypes" are connected withtypes of respiratory apparatus.Gill-breathing animalsappearto follow the surface rule;henceits validityin fishand certaininanimateclasses. On the otherhand, the surfaceof tracheasin insect larvae developsproportional to body volume,as was shownby Sattel (1956) in Bombyx mori;hence the proportionality of metabolicrate to weight.

in mg. 8 130 250 450 630 850 Weight 2.0 30.6 60.7 113.2 154.8206.6 Cmm. 02/hr. Perg./hr. 250 236 243 252 245 242 TABLE 4 Oxygen consumption ofPlanorbis sp. (Temperature 23?C.) After Bertalanffy and Muller(1943). in mg. Weight
Cmm. 02/hr. (WI)/hr.

30-3558-6290-100140 190-200
2.3 3.9 5.4

69 65 56 Perg./hr. Per unit surface 22.9 25.1 26.1

52 48 27.0 28.2

7.3

9.5

between proportionality intermediate to weight to surfacearea. To this type and proportionality belongsuchpond snailsas Planorbisand Lymnaea like Planaria. Table 4 gives data and filatworms fortheramshorn snail,and showsthatitsmetabolic rate decreases with respect to its weight,but withrespectto its surface increases area. mentioned are typicaland characThe relations of the species concerned. Table 5 gives a teristic survey of available observations.A few minor need elucidation, but in generalit discrepancies can be said that the "metabolictype," i.e., the ofmetabolic rate to bodysize,is a physiorelation of the species or group of logical characteristic speciesconcerned.
INTERPRETATIONS OF THE SIZE DEPENDENCE OF METABOLISM

We now come to the question,what is at the basis of the relationbetweenmetabolicrate and of its most familiar body size and, in particular, rule? (Cf. Kleiber, 1947; Bertathe surface form, and Pirozynski, lanffy, 1951a; Bertalanffy 1953; We must admit that we withfurther references). do notknow.What can be shown, is that however, the explanations usuallygivenare insufficient. There seemsto be, first, thealternative whether of metabolicrate on body size is the dependence That is to say, thedecreaseof metabolic rate with increasingbody size may be due to intrinsic in themetabolism ofthecellsofsmaller differences
based upon cellular or upon organismic factors.

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TABLE 5 Relationbetween metabolic rateand bodysize

Species Reference to proportional Respiration W2'8(surface), W (weight) or intermediate

PLATYHELMINTHES Dugesia gonocephala NEMATHELMINTHES Ascaris lumbricoides ANNELIDA Lumbricus sp. Eisenia foetida MOLLUSCA Lamellibranchiata Anodonta cygnaea Dreissensiapolymorpha Prosobranchia Lithoglyphus, Paludina fasciata and P. vivipara Pulmonata Lymnaeastagnalis Lymnaeastagnalis Lymnaeaacuricularia Planorbissp. Planorbiscorneus Planorbiscorneus Isidora proteus Pulmonata and Operculata,15 species intra-andinterspecific Helicidae and Cepaea (interHelix, Chilotrema, specific) Cepaea vindobonensis CRUSTACEA Branchiopoda Daphnia pulex Artemiasalina Isopoda Asellus aquaticus Asellus aquaticus Armadillidium pallasi Porcellioscaber Oniscusasellus Ligia oceanica Decapoda Astacus astacus torrentiuin Potamobius Pugettiaproducta Homarusvulgaris INSECTA Hemimetabola Dixippus morosus Holometabola Various species,intra-and interspecific molitor Tenebrio PISCES Lebistes reticulatus Various species (Scorpaena,Abramis, Cyprinus, etc.) REPTILIA Lacerta

and Muller, 1943 Bertalanffy Kruger,1940 Muller, 1943b Kruger,1952 Weinland,1919 1950 Ludwig and Krywienczyk, 1952a Krywienczyk, and Muller, 1943 Bertalanffy Fusser and Kruger,1951 1952b Krywienczyk, and Maller, 1943 Bertalanffy Fusser and Kruger,1951 1952b Krywienczyk, 1952b Krywienczyk, v. Brand, Nolan and Mann, 1948 Liebsch, 1929 and Muller, 1943 Bertalanffy 1948 Jan6aroik, 1953 and Krywienczyk, Bertalanffy Muller, 1943b Will, 1952 Muller, 1943b Will, 1952 Will, 1952 Ellenby, 1951 Kalmus, 1930 Wolsky,1934 Weymouthet al., 1944 Thomas, 1954 Muller, 1943a Kittel, 1941 and Muller, 1943 Bertalanffy and Muller, 1943 Bertalanffy Jost,1928 Kramer,1934 221

Intermediate Surface Weight Surface? Surface Surface Surface Intermediate Intermediate Weight? Intermediate Intermediate Intermediate Intermediate Surface (high tenperature[30?C.]?) Weight Weight Surface Surface Surface Surface Surface Intermediate Surface Probably surface Surface? Weight? Intermediate Surface Weight Weight Weight Surface Surface Surface

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222

THE QUARTERLY REVIEW OF BIOLOGY

the presence and Campbell, 1952), of succinodehydrase and cases wouldresultfrom Intermediate malicodehydrase (Fried and Tipton,1953). apparatus. oftwo typesof respiratory The picture, however, is different in intraStill anotherexplanationof the surfacerule is as betweenrat tissuesfrom comparisons, based upon anatomical or chemicalchanges in specific body size and age. Seven body size. "Metaboli- animals of different withincreasing composition by callyactive" organssuchas theviscera,thebrain, main organsof the rat have been investigated and Pirozynski (1951, 1953), and largerin small as comparedto Bertalanffy etc., are relatively whichis particularly imporlarge animals. So it can be assumed that they skeletalmusculature, a highpercentage of body more oxygenand are respon- tant because it forms consumerelatively and Estwick metabolic mass, was studied by Bertalanffy sible for the higher weight-specific no significant decline rate in smallerorganisms. However,the relative (1953). As Fig. 2 illustrates, one of average Qo2withincreasing from body size is found of innerorgansis verydifferent growth that it in brain, lung, and kidney; a slight decline in and so it is improbable organto the other, can yield the simplerelationof the surfacerule skeletal muscle,liver, and heart; and a marked is no systematic So there 1951a). A quantita- declinein thediaphragm. (cf.Bertalanffy, ofmetabolism and Pirozynski, 1953) decrease of Qo, in the various organs consistent tive estimate(Bertalanffy to account with, and responsiblefor the decrease of the shows that this factoris not sufficient rate. weight-specific metabolic rate with increasing ofbasal metabolic fortheactual variations of body size. These results have been essentially in terms Now we come to the interpretations This amountsto sayingthat confirmedby other workers and with other factors. intracellular metabolic rate materials: in growingchicken by Crandall and the decrease of weight-specific size, as expressedin the surface Smith (1952), in the heart muscle of the guinea with increasing decrease in the pig by Wollenberger and Jehl(1952), in theteleost rule, is due to a corresponding is measured brain by Vernberg and Gray (1953), and in rat Tissuerespiration oftissues. respiration as testes by Homma (1953). Similarly,Fried and as Qo,, that is, ,l 02/mg. dry weight/hr., determinedwith the Warburg apparatus. A Tipton (1953) did not find a decrease in the of respiratory enzymes. considerableamount of work has recentlybeen content From this it would appear that genetic,and done along these lines,partlystimulatedby our in the enzymatic differences just as we may hencespecies-specific, own work now to be presented, in interspecific are found in comparativemetab- activity and Qo, oftissues also say that the interest in animals of however, Differences, olism as classifiedin the metabolictypes men- comparisons. are irregular weight tionedhas been stimulatedby the investigations the same speciesand different The ques- withrespect hereafter. to thevarioustissuesor are absent. lawsto be explained on growth oftissuerespiration is a So we have to assume factorswhich,within tionofthe size dependence of regulate the respiration one, but the statementsto follow the intact organism, controversial of the case. the tissues,the sum total of whichis the metabappear to be a fairpresentation comparison of mammalian olism of the entire animal, but which do not In interspecific fromthe mouse show up in the isolated tissueused forWarburg species of different sizes, ranging and Pirozynski, (Bertalanffy to the horse, a decrease of Qo, with increasing determination 1951, body size is generallyfound, as a number of Schmidt-Nielsen,Bertalanffy,and Pirozynski, have established(Kleiber, 1941; Wey- 1951). We have alreadysaid that the organismic observers mouth, Field, and Kleiber 1942; Krebs, 1950; factors usually contemplateddo not offer a explanation.What one may expect Martin and Fuhrmann, 1955). This decrease, satisfactory is not parallelin the variousorgansand, can be illustrated It is by the action of thyroxin. however, to easy to induce an increase of metabolismby as a generalrule,is less thanwouldcorrespond into the animalin vivo; but ruleor the 3 powerruleofmetabolism. injectionof thyroxin thesurface way,a decreasewithincreasing in spite of many efforts In a corresponding made, nobodyhas been this effect by an body size was found in enzymaticsystemscon- able to reproducesatisfactorily such as in the concentra- administration of thyroxin to a tissue in vitro. nectedwithrespiration, tion of glutathione (Gregoryand Goss, 1933; On the otherhand, chronichormonalconditions c (Rosenthaland are manifestedby significant Patru'sev,1937), of cytochrome changes of the oxidase (Kunkel tissue Qo, as has been shownwith tissuesfrom Drabkin, 1943), of cytochrome

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QUANTITATIVE

LAWS IN METABOLISM

AND GROWTH

223

15

7.~~~~~~~~~~~~~~z
6 t--Y?US

4
31

1o

20

30

40

50

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no

l_

300

400

or VARious ORGANS FIG. 2. TIssuE RESPIRATION OF TIE WHITE RAT IN RELATION TO BODY WEIGHT Qo2 = .dl 02/mg.drywt./hr. lines are shown; for individual data and statisticalevaluation cf. the originalpaper. After Only regression and Pirozynski Bertalanffy (1953).

BODY WEi6rT IN G.

animals and in pituitary thegrowth hypophysectomized curvesoftheseveralspecies.It appears dwarf lack somatotrophin mice,which (Bertalanffy that we have been successfulin establishing a and Estwick,1954). definite and strictconnection betweenmetabolic The writer does not feelhappy about thisstate types and growth types, in consequence of a and the situationwould be much more generaltheory of affairs, ofgrowth whichestablishes rational if a straightforward satisfactory relationbetween quantitative laws of growthand indicates the the decrease of the weight-specific metabolic physiologicalmechanismupon which growthis rate and the tissue respiration could be found. based. Indeed, the Ottawa study was startedwith this Let us startwitha ratherobviousdeliberation, was not borne firstindicatedby Putter (1920). Animal growth which,unfortunately, expectation, can be considered out by thefacts. a resultof a counteraction of The explanationof the surfacerule and of the synthesis and destruction, of the anabolismand of metabolismin general thus catabolismof the buildingmaterialsof the body. size-dependence remains rather We have,at present, There will be growth unsatisfactory. so long as building up preto take the metabolictype,in the sense defined, vails over breaking down; the organism reachesa as an empiricaldatum of the species concerned. steady state if and when both processes are However, even this cautious attitude leads to equal. We may expressthisin a generalformula: inferences certainremarkable with respectto the -KWn. dWIdt = nWWm (5) of growth. problem
METABOLIC TYPES AND GROWTH TYPES

It has already been stated that, among the various animal classes, so-calledmetabolictypes can be distinguished by virtue of the relation between the metabolicrate and the body size. Now as thereare different metabolictypes,there are also different growth typeswhich are distinguishedby the course of growthas expressedin

In words: The change of body weight W is given by the difference betweenthe processesof building up and breakingdown; v and K are constants of anabolism and catabolism respecm and n indicatethat tively,and the exponents the latterare proportional to some power of the bodyweight W. Obviously the growthof any organismis of an enormous whether complexity, we considerit

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THE QUARTERLY REVIEW OF BIOLOGY

morphological, physiological physiological, froma biochemical, facts (cf. Bertalanify, 1951a), that of it is directly proportional to weight. On the other or any otheraspect. However,the justification and thesimplemodelit implies hand, mathematicalconsiderations an overallformula (Bertalanffy, Our equationstates that the 1941b) show that our basic equation is rather lies in the following. and degradative processes insensitive to smallerdeviationsof the exponent grossresultofsynthetic the law of allometry, n fromunity.So we may put, withoutany confollows withinthe organism n equal the exponent that is, that the rate of these processescan be siderableloss of generality, ofourbasic equation expressedas a power functionof body mass. to 1. This makesthesolution is justified, because at least mucheasier. But this assumption therateofall physiological The solution approximation in a first ofequation5 (n = 1) is (Bertalanffy, in 1941b): hitherto can be expressed investigated processes allometric or power formulas (Adolph, 1949). W = {87/K - [vq/K- Wo (1-m)]e-(1_-tn)Kt}1-m (6) The intrinsiccomplexityof the phenomenon concerneddoes not preclude it from following withWo = weight at timet = 0. law. Remember, for example, sucha simple, general The case is somewhat different withrespectto what has been found in the dependenceof the anabolism. The synthesisof high-molecular cell of the intact animal. componentsneeds, on the one hand, building metabolism basal or resting Of course,what is called the basal metabolicrate blocks such as amino acids, sugars,phosphates, and to a and so forth, is, in fact,the outcomeof innumerable and on theotherhand energy which, large extentunknownprocessesof intermediary in aerobic animals, is provided by oxidative metabolism. Not only this, but the growing processes. Both can be taken into account as organismundergoeschanges at the biochemical, limiting factors. The experimental results indicate levels. that,so faras higher cellular,and morphological physiological, animalsare concerned, there we can state quite definitely that a is a lawfulconnection Nevertheless, betweenrespiration, anabcertain organismobeys, let us say, the surface olism,and growth which works out in the folof the lowingway. rule; that is, that the rate of metabolism its size or developmental The exponentn in our basic equation denotes entireanimal,whatever age, can be expressedas a functionof the -' the dependenceof anabolismon body weight.If bodyweight. powerofits respective form thatvalue whichis experimentally we insert to define theprocesses foundforthe size dependence We have nowmoreclosely of resting metaboappearing in our basic equation. The catabolic lism,thegrowth laws forthe organism in question loss of follow automatically.Thus we can predict the processesmean, of course,the continuous buildingmaterialas it takes place in any living growth type of an animal from its metabolic thismeans the turnover type,and thisprediction Biochemically, organism. has provedto be correct and particularly materials of proteins, in a largenumber of building of cases, oftenin a quite unexas demonstratedby the isotope techniques. pectedway. it means the renewal of cells, as Cytologically, In a first is proportional type, respiration to the found in many tissues and organs,oftenat an 23 power of weight,according to the surface highrate (cf. Leblond and Stevens, rule. Accordingly, the law of growth unexpectedly assumes the and Leblond,1951; F. D. Bertalanffy following 1948; Storey form: and Leblond, 1953; Leblond and Walker,1956; a dW/dt - W2 -KW. (7) table of the rates of cell renewalas foundby the 1957). Leblond school is given in Bertalanffy, We shall not bother with the mathematical have shownthat elaboration,but show immediatelythe results. The isotopeand othertechniques in a so-called Fig. 3 gives metabolism itself maintains theanimalorganism and growth in the small 1947), aquariumfish, dynamic or steady state (Schoenheimer, Lebistes reticulatus. Metabolicrates, as well as cells being con- measuredas oxygenconsumption, chemicalcomponents are presented tinuallywornout or degraded,and on the other in the log-logor allometric plot. As will be reand membered, hand being replaced by way of resynthesis in the case of the surfacerule the of new cells. So far as the rate of allometricregression the formation line has a slope of 23. So we may assume, as a far as the growth catabolism is concerned, curvesare concerned, the solufirst approximationand based upon various tion of the growth equation gives theoretical

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QUANTITATIVE

LAWS IN METABOLISM

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200 __ _ main characteristics. curves with the following First, growthrates are decreasingand growth eventuallyattains a steady state. Secondly,the a) -0 curves for weightgrowthand linear growthare 4o 0~ The curve of weight characteristically different. growthis sigmoid,with a point of inflexion at - --40 ---about one-third of the finalweight.The curveof -e00 30 lineargrowth is a decayingexponential withouta - 20 60 80 100 200 300 500 800 30 40 turningpoint. This is what we actually find Weight In mg. experimentally. This is themostcommon form ofgrowth curves, in a numberof invertebrate foundin fish, classes and also, with certainrestrictions, in mammals. 160 40 -The validityof these growthequations has been shown in many examples (Putter, 1920; Berta_ 140 5 3 lanffy, 1934, 1951a), and theyhave been adopted 120 6-30 in applied biology. It appears that the "Bertalanffy growth equaE E 00 b) 125----_It tion" is widelyappliedin international fisheries. has been foundto fitthe commercially exploited fish of speciesstudiedby the Fisheries Laboratory 80 4~~~~the Ministry of Agriculture, Fisheries and Food at -0 ?' 2 I 0 Lowestoft (England), withthe possible exception A compreofthehake (Wimpenny, pers.commun.). hensivetheoretical model of the dynamics of exhas beendeveloped, ploitedfish populations where-0 0 in growth of the speciesconcerned is represented 12 10 6 0 4 2 8 by equation 7 (Beverton, 1954; Beverton and Time in weeks Holt, 1957). Discussionof this populationmodel FIG. 3. IHE FIRST METABOLIC AND GROWTH TYPE (which, apartfrom fisheries, maywellbe adaptable curves(b) in the Metabolicrate (a) and growtlh to otherpopulations)is beyondthe scope of the Growth curvesfor, Guppy(Lebistes reticutatus). d: present review.It shouldbe mentioned, however, - - - - weightgrowth; length growth; calculated to equation (7). After Bertalanffy and Millthat examination of the variousgrowth functions according proposed led to the conclusionthat "von Ber- ler (1943). talanify's growth equationis the mostsatisfactory been developed"(Bever- weightis continuallyshiftedin disfavorof the ofanythathave hitherto ton and Holt, l.c.). Ampledata as well as descrip- surface.Consequently, so long as the animal is tionof mathematical analysiscan be foundin this small, surface-proportional anabolism prevails work. over weight-proportional catabolism, and the A relation similarto that stated by Bertalanffy animal grows.The largerit grows,the more the et al. for the surfacedependenceof respiration surplus remaining for growth decreases, and was found by Yoshida (1956) in food intake. eventuallya steady state will be reached where The quantity ofplankton consumed by thesardine anabolism and catabolism balance each other, is proportional to the square of body length, and and growth comesto an end. the same appears to be true for assimilating Now we come to the second type. We have and the gut. organs,such as the gill-rakers said that in certain animals, for example, in This characteristic course of growthis easily insects, respiration does not follow the surface If a body,withnot too muchchange rule but ratheris proportional understood. to weightitself. of shape, increasesin size, its surfacesincrease Let us see whathappensin thiscase (Fig. 4). The approximatelywith the second power of the log-log rate againstbody weight plot of metabolic length,but its volume and mass with the third will give a line witha slope of 45?. On the other power. Hence, the ratio between surface and hand, we have to insert1 for the exponent m in
C',j --

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226
80
60

THE QUARTERLY REVIEW OF BIOLOGY Of course,an insect larva does not grow to any indefinite size. However,growthis stopped here by an altogether different mechanism. It is metamorphosiswhich abruptly intercepts the exponentialincrease,even causing a decrease in body weight as largeamountsof tissueare broken down in order to develop the imago. The same metabolicand growthtype also applies to hemimetabolousinsectslike the walking-stick, where there is no apparent metamorphosis, but the hormonal mechanismsresponsiblefor development appear to be similar.Again,in land snails, whichalso belongto thistype,exponential growth is intercepted by seasonalcycles. Finally, we have described a thirdmetabolic type,one where metabolic rate is intermediate betweensurfaceand weightproportionality, and whichis exemplified by pond snails.Again we can calculate what growth curvesare theoretically to be expected. a value 23 < m < 1 into If we insert the basic equation, it appears that the growth should followa thirdtype. The curve of weight growthdoes not differ very much fromthat in
20

a)~~
0

0-0 10

-j

-A

5--20

30 40

WeightIn mg. (Tenebrio)

60 80 100

200 300

1:
.43

-?-

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b)

2--f a)

0 8jII7
6 =

30 40

20

40

60

80

60 80 100 200 300 Weight in mg.

500 700

AND GROWnTYasPE METABOLIC FIG. 4. THE SECOND

Timqe in hours la) (Drosophi

(exponent(b) culrve rate(a) and growth Metabolic and Muller ial) in insectlarvae. AfterBertalanify (1943).

E8

'-

--V4

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get a comthe growthequation, and thereupon cm e 0 _ _ curveand a secondgrowth growth pletelydifferent 4 type,anabolismand to the first type.In contrast 0 run catabolism,both being weight-proportional, at the same pace. The morecatabolismincreases, the more does anabolism. Therefore,growth 4 12 24 8 0 16 20 rates will not decrease but always increase,and Time in weeks it grows. FIG. 5. THE THIRD METABOLIC AND GROWTH TYPE the faster the largertheanimalbecomes, and no Growthis not limitedbut exponential, rate (a) and linear growth (b) (diameter steady state is reached.This seems to be a para- ofMetabolic snail (Planorbis shell)in the ramshorn sp.). After whathappenls. Bertalanffy butis exactly stateofaffairs, doxrical and Muller (1943).

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TABLE 6 Metabolictypesand growth types

Metabolictype Growth type Examples

I. Respirationsurface-proportional (a) Linear growthcurve: attainingwithout Lamellibranchs,fish, mammals inflexion a steady state. (b) Weight growthcurve: sigmoid,attaining,with inflexionat ca. 13 of final weight,a steady state. II. Respiration weight-proportional Linear and weightgrowthcurves exponen- Insect larvae, Orthoptera, Helicidae tial, no steadystate attained,but growth or seasonal by metamorphosis intercepted cycles. curve: attainingwithin- Planorbidae between (a) Linear growth III. Respiration intermediate a steady state. flexion surface- and weight-propor(b) Weight growthcurve: sigmoid,similar tionality to I(b).

of is different, developmentrevisions and the introduction however, type.Lineargrowth, thefirst Again, complicating factorswill be necessary(forrecent as its curveis S-shapedwith an inflexion. discussions of the theory,cf. Duspiva, 1955; (Fig. 5). is verified ourprediction animalclasses thereare different Harms, 1955; Linzbach,1955; Zeuthen,1955; BerSo in different 1957). types of growth, talanffy, metabolic types and different A case in point is growthin mammals.From agreeing with theoreticalexpectation.Table 6 it may be said that, of metabolism, and may the viewpoint givesa surveyof examplesinvestigated, mammals draftfora new chapterin in a firstand crude approximation, as a first be considered of appear to belong to our firsttype, where the physiology namely, a comparative physiology, surfacerule of metabolismapplies. Indeed, the growth. stated by Rubnerformammany surfacerule was first just outlined, of growth From the theory consequences can be derived which have been mals, and it was already mentionedthat the of 1957). Only clinicallyimportantcase, the determination (cf. Bertalanffy verifiedempirically one further examplewill be given. We can com- basal metabolismin man, applies the surface modified form of the Dubois K which rulein the somewhat pare the values of the catabolic constant mammalian curves,withthe standard formula.Correspondingly, werecalculatedfromthe growth pattern followsthe characteristic roughly as directly determined growth values of proteinturnover growth typediscussed. ofcases, theconstants of the first In a number by experiment. witha degreeofcorrespondence In detail, however, there are complications. have been verified there and somewhat paradoxically, model Unfortunately sincethe theoretical whichis quite striking, and, on the other are relativelyfew good data suitable for this is admittedlyoversimplified in thephysiological determinations typeof analysis. hand,theerror If the basal or restingmetabolismin the rat is considerable. For example, of proteinturnover rate of (Fig. 6) is measuredover the entirelife span, it in 1938 the authorcalculatedthe turnover the protein from the growth curve of man. The appears that as a crudeoverallapproximation ruleobtains,thatis, the overallallometric value found was 1.165 g./kg. body weight/day. surface line has a slope of about 23. In more Eleven years later, Sprinson and Rittenberg regression thereis a breakin thisline,such (1949) calculated protein turnoverfrom their detail,however, line is steeper, part of the allometric withN15,and founda value of 1.3g./ that the first experiments could and the second part much flatter,than would Only a sound theory kg. body weight/day. to a slope of 23. The breaktakesplace correspond suchprediction. have permitted at a body weightof about 100 g., that is, preGROWTH IN MAMMALS AND MAN cedingsexual maturation.As we have found in and Pirozynski, (Bertalanify It is, however,obvious that the theoryrepre- otherinvestigations and that withfurther 1952, 1953), similar breaks appear in quite a sentsa first approximation,

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228
1500 _

THE QUARTERLY REVIEW OF BIOLOGY

.

curveis different from all others.Since our growth formulas to a apply large number of species, 1000 _ the shapes of theirgrowthcurves are the same, 800 _ and the same curve can be used to represent the 600 growthof various species, simplyby takingdifE 400 YmuS Wt1n *th r g. scales fortimeand body size. Fig. 8 shows ferent the growthcurves of a fish and a mouse. The latter, similar to that of the rat, also shows a 300 growth cycle in detailedanalysis,whichdoes not CP 100 much alter the picture.If, however,the growth it appears to be unique. curve of man is entered, 8e0 ib. verQor2 n0 with The second part of the curve, beginning is t fn 5 50 The first puberty, follows the general pattern. 4 40 In infancyand part, however,is very different. I I I 11II 1II1II1 30 400~ 10 15 20 30 40 60 100 200 childhood,the curve is enormously protracted. Body weighti'n g. A new growthcycle is added, as it were,to the or RELATivE GRowTHI typicalpatternof growth.Althoughthis change FIG. 6. DISCONTINUITIES IN THlE ALBiNo RAT is heralded in thegrowth cyclesoflowermammals, of ap- onlyin man does it lead to a singular discontinuities shape of the !FAII appearat a bodyweight 100g.,i.e.,before A correspond-growth puberty. proximately curve.This growth curveofman,abnormal in thegrowth of theentire is found ingdiscontinuity withchangesin animal(see Fig. 7). Onlyregression linesareshown in as it were,is of courseconnected data and statistical individual thefigure; analysis are the hormonalbalance. This is demonstrated by and pathological cases, such as pubertaspraecox in givenin the original papers.After Bertalanffy Racine and Piozynski 1953) (1953). (1952, pituitarydysfunction, when pubertytakes place an at in othermammalsand early age, as it does at the number of physiologicalcharacteristics, in still apes. The singular growth curveofman is a same age and body size: in the allometric growth of the liver, the involutionof the thymus,the quantitative expression of the retardation of ofliverand thymus, and certainly human developmentwhich, according to Bolk tissuerespiration (1926), is one of the basic factors in the evolution thereare others(Fig. 6). There is small wonder of man. is At the same time, it an important that these breaks and shiftsare found,as the factorforhis uniquenessin nature.Animalsrun cominginto play of the sex hormonesentails a theirdevelopmental through periodspeedily,and deep-reachingchange in the entire metabolic pattern. _ _ _ _ _ __ _300 300 On the other hand, the growthcurve of the rat was analyzed long before the physiological E __E studiesjust mentioned 1938, 1951a; c200 (Bertalanify, - _ -200 _ _ _ _ on rat growth is a discussionof recentliterature given in Bertalanffy, 1957). The result was of the rat followsthe first foundthat the growth too R100 _______ change,howgrowthtype, with a characteristic again at the ever,in the values of the constants, criticalpoint of around 100 g. body weight.If these growthcycles are taken into account, an 200 300 400 0 100 Time in days excellentfit of the empiricalgrowthcurves by can be obtained(Fig. 7). FIG. 7. GROWTH OF THE ALBINO RAT meansof our formulas So it wouldappear thatmammalsbelongto the Donaldson'sdata (d1). Length growth calculated according to equafirsttype, with the qualification, however,that weight growth----, shows twogrowth cycles, with the tion(7). The calculation two growth cycles must be distinguished, a breakat approximately 100g. body weight. Donaldfrom thefirst to thesecondcycletaking son'sdataaretoday transition notconsidered tobe optimal, since laboratory dietshave increased thegrowth in This is to modern place at the timeof sexual maturation. the rat.The figure shows, however, the excellent nuno morethan a first be considered approximation. merical fitthatcan be obtained withthe theoretical whose growth formulas. However,thereis one organism After Bertalanffy (1941b).
\P

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100

LAWS IN METABOLISM

AND GROWTH

229

_80

80~~~~~~~~~~
-______ ________x

z-

0
<

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c

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and the theNational Cancer search Institute, Council, of of Canada.A survey Council Research Humanities is givenin in general of animalgrowth the problem 1951a,and 1957. Bertalanffy,
Man* Mouse x
5 5 lo

SUMMARY years

40

37
5

40

_
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_____

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FIG.8. CO1PARISON THE GROWTH CURVES O0F OF A FISH,MOUSE, AND MAN After Bertalanffy (1951a). soon they reach puberty and the adult stage. Man, on the otherhand,is givena longperiodof youth,and is thusenabled to learnand to collect experience. Thus the characteristic humangrowth curve is a prerequisite for that mental development and civilizationwhich so sharply distinall otherbeings. guishesman from
ACKNOWLEDGMENT

Time in days

Thisessayis baseduponwork carried through in the author's laboratories at theUniversity ofViennaand theUniversity ofOttawa(Canada).Partofthiswork was aided by research grants from the NationalRe-

between connections Workaimedat establishing In thevarious is reviewed. and growth metabolism animal classes, three "metabolic types," i.e., formsof dependenceof metabolicrate on body of size can be distinguished:proportionality metabolicrate to surfacearea, or to weight,or one intermediatebetween surface and weight The various theoriesregarding proportionality. are discussed, of metabolism the size dependence of the relation of with particularconsideration to to body size. Corresponding tissue respiration the "metabolic types" mentioned, there are growth by different "growthtypes" distinguished A generaltheory curvesof the speciesconcerned. permits advancedby theauthor, ofanimalgrowth, betweenmetabolic explanationof the connection is illustrated types.The theory typesand growth and verteby examplestaken frominvertebrate brate classes. Mammalian and human growth, type," growth the "first following whilegenerally with curve connected show breaksin the growth herald The data and conceptspresented puberty. a new chapter of physiology,the comparative ofgrowth. physiology

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THE QUARTERLY REVIEW OF BIOLOGY

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