Size and Shape in Biology Thomas McMahon Science, New Series, Vol. 179, No. 4079. (Mar.

23, 1973), pp. 1201-1204.

Stable URL: http://links.jstor.org/sici?sici=0036-8075%2819730323%293%3A179%3A4079%3C1201%3ASASIB%3E2.0.CO%3B2-8 Science is currently published by American Association for the Advancement of Science.

Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/about/terms.html. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/journals/aaas.html. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission.

The JSTOR Archive is a trusted digital repository providing for long-term preservation and access to leading academic journals and scholarly literature from around the world. The Archive is supported by libraries, scholarly societies, publishers, and foundations. It is an initiative of JSTOR, a not-for-profit organization with a mission to help the scholarly community take advantage of advances in technology. For more information regarding JSTOR, please contact support@jstor.org.

http://www.jstor.org Sat Dec 22 13:41:26 2007

and Society (Wiley-Interscience, New York, (1971); Sci. Amer. 224, 224 (Sept. 1971). 7. A. Coale, Science 170, 132 (1970). 8. I. Taeuber [in Man's Place in the Island E c o s y s t e t ? ~ ~ , . R . Fosberg, E d . (Univ. of F Hawaii Press, Honolulu, 1961). pp. 226-2621 analyzes how absorption into expanding societies affects the age and sex composition of populations in formerly isolated social systems.

9. 0. D . Duncan, Handbook for Modern Sociolo g y , R. E . L. Faris, Ed. (Rand McNally, Chicago, 1964), pp. 36-82. 10. K. Boulding describes the human ecosystem as the "totality of human organizations" [The Organizafional Re~,olution(Quadrangle, Chicago, 1952), p. xxii] and 0. D. Duncan notes that the cycling of information is a unique feature of the human ecosystem (9, pp. 4 M 2 ) . 1 1 . R . Freedman. Pop. Index 31, 417 (1965).

12. S . S. Kuznets, Proc. Amer. Philos. Soc. 111, 170 (1967). 13. M. Abramowitz, A ~ n e r . Econ. Rev. 46, 8 (1965). 14. J. Krebs and J. Spengler, in Technology and the Atnerican Econotny (Report of the National Commission on Technology, Automation, and Economic Progress) (Government Printing Office, Washington, D.C., 1966), vol. 2, pp. 359-360.

Size and Shape in Biology

Elastic criteria impose limits on biological proportions, and consequently on metabolic rates.
Thomas McMahon

material. The mathematician Greenhill ( 1 3 ) showed that when the force due to weight is distributed over the total extent o f the column instead o f being taken as acting at the center o f mass, the critical height becomes:

Observers o f living organisms since well as animals must be built strongly Galileo have recognized that metabolic enough to stand under their own activities must somehow be limited by weight. In the following, a general rule surface areas, rather than body vol- is derived for the changing proportions umes. Rubner ( I ) observed that heat o f idealized trees as a function o f scale, production rate divided by total body and later the results are applied to surface area was nearly constant in animals. dogs o f various sizes, and proposed the explanation that metabolically produced heat was limited by an animal's ability Buckling to lose heat, and thus total body surConsider a tall, slender cylindrical face area. When more precise method? o f measurement became available, column o f length 1 and diameter d Kleiber ( 2 ) noticed that when rate o f loaded by the force P , representing the heat production is plotted against body total weight o f the column, acting at weight on logarithmic scales for ani- the center o f mass. Such a column will mals over a size range from rats to fail in compression i f the applied stress steers, the points fall extremely close P I A , where A = d 2 / 4 , exceeds the to a straight line with slope 0.75 (Fig. maximum compressive stress, u,,,,,. Pro1 ) . The result has since been confirmed vided that the column is slender enough, for animals as different in size as the it may also fail in what is known as mouse and the elephant (3-5),and has elastic buckling, uhereby a small lateral been verified for other metabolically displacement (caused, for example, by related variables, s~lch rate o f oxygen the smallest gust o f wind), allows the as consumption ( 6 ) . Excellent reviews o f weight P to apply a toppling moment the problem are available (7-10). which the elastic forces o f the bent While it is often true that biological column below are not sufficient to relaws are not derivable from physical sist. In this case, "slender enough" laws in any simple sense, Kleiber's r ~ ~ l emeans that l l d is greater than 25, a may be one o f those fort~iitousexcep- range which includes virtually all trees tions which D'Arcy Thompson ( 1 1 ) ( 1 2 ) . The critical length for buckling suggests lie at the basis o f a funda- is related to the diameter b y : mental "science o f form." Plants as
The author is assistant professor of applied mechanics in the division of engineering and applied physics, Harvard University, Cambridge, Massachusetts 02138. 23 M A R C H 1973

This result is identical to Eq. 1 , with only a change in the numerical constant. It may be demonstrated that another change in the constant occurs when the solid cylinder is made hollow, provided that the thickness o f the wall is proportional to the diameter. Greenhill further showed that i f the shape o f the column is taken as a cone, or a paraboloid o f revolution, the result is again only to change the numerical constant. Recently, Keller and Niordson ( 1 4 ) have derived that the tallest self-supporting homogeneous tapering column is 2.034 times as tall as a cylindrical column made o f the same volume o f the same material, and that the distance to the top o f such a tapering column above any cross section is proportional to the diameter o f that cross section raised to the 2/3 power. The rule requiring height to go as diameter to the % power is thus independent o f many details o f the model proposed for the elastic stability o f tree trunks.

where p is the weight per unit volume and E is the elastic nlodulus o f the

The limbs o f trees must also be proportioned to endure the bending forces produced by their own weight. I f a branch i s considered to be a cantilever beam built into the trunk, there exists a particular beam length l,, for which the tip o f the branch extends the greatest horizontal distance away from the trunk ( 1 5 ) . Branches longer than I,, droop so much that their tips actually come closer to the trunk. Suppose that the purpose o f branches is to carry their leaves out o f the shadow o f higher branches, and therefore to achieve a maximum lateral displacen~ent from

the trunk. Then the limb should grow n o longer than I,,., where

and C dcpcnds only o n the droop angle O,,, which in turn dcpcnds only o n the angle at which the limb leaves the trunk ( 1 5 ) . The result may be made general for a tapered o r hollow limb exactly as was done for the buckling problem. Comparing Eqs. 1, 2, and 3, it is apparent that elastic criteria set lcngth proportional to the 2/3 power of diameter i n both the trunk and the branches. I t should be possible to check the validity of thcse results by measuring the proportions of trees of different scale. Such a check would be arduoils if it wcre necessary to know E and p for each species; fortunately, the ratio E l p is quite accurately constant in green woods (16, 17). I n Fig. 2, the trunk diameter 1.525 meters from the ground is plotted against the total hcight for 576 individual trees, representing nearly every species found in the United States. T h e data, taken primarily from the American Forestry Association's 'Social register of big trees" ( I s ) , include specimens both very slender and very stout, since trees arc eligible for lhis list according to their bigness, a n index depending o n the sum of thcir circumference and height (19). A solid line representing Eq. 2 is also shown in Fig. 2; it was calci~lated for E = 1.05 x 105 kilograms per square meter and p = 6.18 x 10~ilograms per cubic meter ( 1 6 ) .

T h e broken line, which fits near the center of the data points, has the same slope as the solid line bist rcprcscnts a sequence of trces \\hose hcight in cach case is only one-fourth of the critical buckling hcight. T h e conclusion seems to be that the proportions of trees are limited by elastic criteria. since there arc no data points to the lclt s f the solid line.

Animal Proportions
Just as trees must assunle thicker proportions with increasing size, so must animals adjust thcir shape with scale. T h e argument has long been offered that animals could not remain geometrically similar from the snlall to the large because thcir limbs, whose cross-sectional area increases as the square of characteristic body dimension L, must then support a weight which increases as L:' ( 7 ) . Thc dillisuity with these arguments bascd on strength criteria is the inevitable concl~tsion that animals may grow no larger than s size which makes the applied stress squal to the yield stress of their materials. Animals larger than this size woilld have to increase supporting areas directly with weight, so that no increases in height could be tolerated, only increases in width. I f yield stress wcre the only criterion, an animal with slender proportions like the bobcat shorlld be capable of attaining the same absolute height as ihe lion. In fact, it is widely found that some animals grow larger than others, and animals of

small scale are relatively more slender than thosc of large scale (scc cover). Perhaps this transformation occurs, as in differently sized trees, for rcasor~s bascd o n elastic rathcr than strength criteria. In the following, M C consider comparisons between animals of the same family, so that thcir shape is grossly similar. 'l'hc only change in shape permitted is I'or lengths to bear a specified relationship to diameters: all lcngths will be proportional to one another, as will be all diameters. Each limb, bone, o r muscle will thus have a length 1 and diameter tl, where length will be taken as it measurement parallel to the direction of tension o r con~prcssionand diameter will be measured perpendicular to this direction. Thus, the lcngth of the trunk is the distance between shoillder and hip whether the animal is bipedal o r yuadrapedal (Fig. 3a, bottom). When a q~ladruped is standing a t rest, the four limbs will be exposed primarily to buckling loads, but the vcrtebra1 colum~nand its nlusculature must withstand bcnding loads. \Vhen the same animal runs, the situation is substantially rcversed in those phases of the motion where the limbs are providing their maximum propulsive cfrort. A t thcse moments, the limbs are supporting bcnding loads, while the vertebral colunln is receiving an end thrust and thus a buckling load. The fact that the loads are dynanlic rather than static is not a consideration: the nlaxinlunl deflection of a structure sliddenly loaded ~ ~ n d e r own weight is its

Body weight (kg)

,.oL-----J-LL .o1

0.1

10 .

I0

Diameter (m)

Fig. 1 (left). bfetabolic heat production plotted against body weight on logarithl-r~ic scales. The solid line has slope %. The broken line, which does not fit the data, has slope % and represents the sray surf;~cenrca increases with weight for geonlelrically similar Fig. 2 (right). Tree height plotted against trunk base diameter on logarithmic scales for record trees shapes [adapted from ( 2 ) ) representing nearly every American species. The trunk proportions are limited by elastic buckling criteria, since no points lie to the left of the solid line. Data from (18, 19).
1202

SCIENCE, VQL. 179

sectional area is A , shortens a length A1 against force oA in time At. T h e power this muscle expends is oAAllAt, where o is the tensile stress developed, and is in general a function of the shortening velocity AllAt. Hill ( 2 3 ) reported that "the inherent strength of a contracting voluntary muscle fiber is roughly constant, being of the order of a few kilograms per square centimeter of cross-section." Me also presented arguments and experimental data to prove that the speed of shortening, AllAt, is a constant in any particular muscle from species to species. If we understand from the work of Hill and others that both u and Allat may be taken as constant, then the power output of a particular muscle and hence all the metabolic variables involved in maintaining the flow of energy to that muscle depend only o n its crosssectional area. But this area is proportional to d', and hence maximal power output a ( W3& = W 0i6 1' (7) This is precisely the statement of Kleiber's law we were looking for, provided we have some confidence that maximal energy metabolism exceeds basal metabolic rate by a factor, the metabolic "scope," which is invariant with respect to scale. Hemmingsen (8) has presented evidence to this effect. According to the model proposed here, if lung volume goes as W (4, 2 1 ) but alveolar ventilation goes as W 0 , i 5 , then respiratory frequency must scale as W-"."? The identical argument may be made for ventricular stroke volume, cardiac output, and heart rate. In fact, Adolph ( 2 4 ) reported that b for respiratory frequency in mammals is - 0.28 [Tenney ( 1 0 ) independently gave the same number]. For heart rate, b has been reported as - 0.27 ( 2 5 ) and - 0.25 ( 2 2 ) . Stahl (9) observed that the ratio of many physiological periods to one another is found to be nearly constant, independent of scale. Thus, the ratio of gut pulsation time to pulse time is nearly the same in all mammals, and each animal lives

for approximately the same number of heartbeats o r breath cycles. Other authors have discussed the importance of this conclusion in arriving at the "physiological age" of living organisms.

Summary and Corrclusions

Arguments based on elastic stability and flexure, as opposed to the more conventional ones based on yield strength, require that living organisms adopt forms whereby lengths increase as the % power of diameter. The somatic dimensions of several species of animals and of a wide variety of trees fit this rule well. It is a simple matter to show that energy metabolism during maximal sustained work depends on body crosssectional area, not total body surface area as proposed by Rubner (1) and many after him. This result and the result requiring animal proportions to change with size amount to a derivation of Kleiber's law, a statement only empirical until now, correlating the metabolically related variables with body weight raised to the % power. I n the pr~ssent model, biological frequencies are predicted to go inversely as body weight to the % power, and total body surface areas should correlate with body weight to the 96 power. All predictions of the proposed model are tested by comparison with existing data, and the fit is considered satisfactory. In T h e Fire o f Life, Kleiber ( 5 ) wrote "When the concepts concerned with the relation of body size and metabolic rate are clarified, . . . then compartive physiology of metabolism will be of great help in solving one of the most intricate and interesting problems in biology, namely the regulation of the rate of cell metabolism." Although Will ( 2 3 ) realized that "the essential point about a large animal is that its structure should be capable of bearing its own weight and this lcaves less play for other factors," he Mas forced to use an oversimplified "geo-

metric similarity" hypothesis in his important work on animal locomotion and muscular dynamics. It is my hope that the model proposed here promises useful answers in comparisons of living things on both the microscopic and the gross scale, as part of the growing science of form, which asks precisely how organisms are diverse and yet again how they are alike.
References and Notes 1. M . Rubner, Z. Biol. Munich 19. 535 (1883). 2. M. Kleiber, Hilgardia 6, 315 (1932). 3. F. G. Benedict, Vital Energetics: A Studj, in Conzparative Basal Melabolisnl (Carnegie Institution of Washington, Washington, D.C., 1938). 4. S. Brody, Bioenergetics and Growth (Reinhold, New York, 1945). 5. M. Kleiber. The Fire o f Life (Wiley, New York, 1961). 6. S. M. Tenney and J. E. Remners, N a t ~ l r e 197, 54 (1963); A. C. Guyton, Anzer. I . Phvsiol. 150. 70 (1947): E. Zeuthen, Quart. ~ e ; .BioL 2'8 (NO: I), 'I (1953). 7. K. Schmidt-Nielsen, Proc. Amer. Physiol. Soc. 29, 1524 (1970); A. M. Hemmingsen, R e p . Steno M e m . Hosp. N o r d . Insulin Lab. 4, 1 (1950); S. J. Gould, Anler. Natur. 105, 113 (1971): W. R. Stahl, Science 137, 205 (1962). '. 8 . A. M. Hemmingsen, Rep. Steno Menl. Hosp. Nord. Insulin Lab. 9, 1 (1960). 9. W. R. Stahl. Advan. Biol. Med. Phys. 9, 355 (1963). 10. S. M. Tenney, Circ. Res. 20-21 (Suppl. I), 1-7 (1967). 11. D . W. Thompson, On Growth and Form (Cambridge Univ. Press, London, 1917). 12. S. Timoshenko, Elements o f Strengtil o f Materials (Van Nostrand, Princeton, N.J., 1962). 13. G. Greenhill, Proc. Canzbrirlge Phil. Soc. 4. 65 (1881). 14. J. B. Keller and F. I. Niordson, I. Matlz. Mech. 16 (No. 5), 433 (1966). 15. T . A. McMahon, in preparation. 16. T. A. McElhanney and R. S. Perry, Forest Service Bulletin N o . 78 (Forest Products Laboratories of Canada, Ottawa, 1927). 17. G. A. Garratt, The Mechanical Properties o f W o o d (Wiley, New York, 1931). 18. "Social register of big trees," Anler. Forests 72, 16 (May 1966); ibid. 77, 25 (January 1971). 19. Other data used in Fig. 2 are from the following books: Royal Horticultural Society, Conifers in Cultivation (Royal Horticultural Society, London, 1932), p. 316; W. Fry and J . R. White, Big Trees (,Stanford Univ. Press, Stanford, Calif., 1930). Mathenlatical Bioph~jsicr 20. N. Rashevsky, (Dover, New York, 1960), vol. 2. 21. W. R. Stahl and J. Y. Gummerson, Growth 37. 21 (1967). 22. W: R. ~ t a h l ;I . Appl. Physiol. 22, 453 (1967). 23. A. V. Hill, Sci. Progr. London 38 (No. 150), 209 (1950). 24. E. F. Adolph, Science 109, 579 (1949). 25. A. J. Clark, Comparative Physiology o f the Heart (Cambridge Univ. Press, Cambridge, 1927). 26. The author is grateful to B. Budiansky, K. E. Kronauer, S. J. Gould, C. R. Taylor, and G. P. DeWolf for assistance through helpful discussions.

SCIENCE, VOL. I f 9

http://www.jstor.org

LINKED CITATIONS
- Page 1 of 1 -

You have printed the following article: Size and Shape in Biology Thomas McMahon Science, New Series, Vol. 179, No. 4079. (Mar. 23, 1973), pp. 1201-1204.
Stable URL:
http://links.jstor.org/sici?sici=0036-8075%2819730323%293%3A179%3A4079%3C1201%3ASASIB%3E2.0.CO%3B2-8

This article references the following linked citations. If you are trying to access articles from an off-campus location, you may be required to first logon via your library web site to access JSTOR. Please visit your library's website or contact a librarian to learn about options for remote access to JSTOR.

References and Notes

6

Oxygen Uptake as Related to Body Size in Organisms Erik Zeuthen The Quarterly Review of Biology, Vol. 28, No. 1. (Mar., 1953), pp. 1-12.
Stable URL: http://links.jstor.org/sici?sici=0033-5770%28195303%2928%3A1%3C1%3AOUARTB%3E2.0.CO%3B2-A
7

Geometric Similarity in Allometric Growth: A Contribution to the Problem of Scaling in the Evolution of Size Stephen Jay Gould The American Naturalist, Vol. 105, No. 942. (Mar. - Apr., 1971), pp. 113-136.
Stable URL:
http://links.jstor.org/sici?sici=0003-0147%28197103%2F04%29105%3A942%3C113%3AGSIAGA%3E2.0.CO%3B2-I
7

Similarity and Dimensional Methods in Biology Walter R. Stahl Science, New Series, Vol. 137, No. 3525. (Jul. 20, 1962), pp. 205-212.
Stable URL:
http://links.jstor.org/sici?sici=0036-8075%2819620720%293%3A137%3A3525%3C205%3ASADMIB%3E2.0.CO%3B2-8
24

Quantitative Relations in the Physiological Constitutions of Mammals E. F. Adolph Science, New Series, Vol. 109, No. 2841. (Jun. 10, 1949), pp. 579-585.
Stable URL:
http://links.jstor.org/sici?sici=0036-8075%2819490610%293%3A109%3A2841%3C579%3AQRITPC%3E2.0.CO%3B2-N

NOTE: The reference numbering from the original has been maintained in this citation list.