ecology’s big, hot idea

7/25/2019 Ecologys Big, Hot Idea

1/5

PLoS Biology | www.plosbiology.org 2023

Life is complicated. It comes inall sorts of shapes, sizes, places,and combinations, and has

evolved a dizzying variety of solutionsto the problem of carrying on living.

Yet look inside a cell and life takes on,if not simplicity, then at least a certainuniformitya genetic system basedaround nucleic acids, for example, anda common set of chemical reactionsfor turning food into fuel. And lookedat in broad swathes, life shows strikinggeneralities and patterns. Everymammals heart will beat about onebillion times in its lifetime. Both withinand between species, the density of apopulation declines in a regular way

as the size of individuals increases.And the number of species in allenvironments declines as you movefrom the equator towards the poles.

Wouldnt it be good if there were a

simple theory that used lifes sharedfundamentals to explain its large-scale regularities, via its diversity ofindividuals? In the past few years, ateam of ecologists and physicists havecome up with just such a theory. Atits heart is metabolism: the way lifeuses energy is, they claim, a unifyingprinciple for ecology in the same waythat genetics underpins evolutionarybiology. They believe that energy use,in the form of metabolic rate, can be

December 2004 | Volume 2 | Issue 12 | e439 | e440

Open access, freely available online

Feature

Ecologys Big, Hot IdeaJohn Whitfield

Citation: Whitfield J (2004) Ecologys big, hot idea.PLoS Biol 2(12): e440.

Copyright: 2004 John Whitfield. This is an open-ac-cess article distributed under the terms of the Cre-ative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction inany medium, provided the original work is properlycited.

John Whitfield is a freelance science writer basedin London, United Kingdom. He is writing a bookon energy, biology, and the laws of nature. E-mail:[email protected]

DOI: 10.1371/journal.pbio.0020440

If the theory is right, its one

of the most significant in

biology for a long time.


2/5

PLoS Biology | www.plosbiology.org 2024 December 2004 | Volume 2 | Issue 12 | e440

understood from the first principles

of physics, and that metabolic ratecan explain growth, development,population dynamics, molecularevolution, the flux of chemicalsthrough the environment, and patternsof species diversityto name a few.

The work, its originators insist, isnot a theory of everything for biology,or even ecology. But it can often seemthat way. Were making advances ona broad range of questions almost ona weekly basis, says James Gillooly,of the University of New Mexico,Albuquerque. Weve been having an

awful lot of fun.

Beneath the Surface

Metabolic ecology, as it has becomeknown, is still controversial. Somethink its mathematical foundationsare unsound, and that it explainsnonexistent trends. It also dividesresearchers on philosophicallinesthose that see lifes patternsas fundamental versus those whothink that variation is the key, those

who think that simple,general ideas can help usunderstand nature versusthose who think thatcomplicated problemsrequire complicatedanswers. A lot is ridingon the debate: If the

theory is right, its oneof the most significantin biology for a longtime, says ecologistDavid Robinson of theUniversity of Aberdeen.It would provide acommon functional basisfor all biodiversity.

Scientists have knownfor nearly two centuriesthat larger animalshave relatively slowermetabolisms than small

ones. A mouse musteat about half its bodyweight every day notto starve; a human getsby on only 2%. Thefirst theories to explainthis trend, developedin the late nineteenthcentury by the Germannutritionist MaxRubner and the Frenchphysiologist CharlesRichet, were based on

the ratio between an animals surface

area, which changes with the squareof its length, and its volume, which isproportional to its length cubed. Solarge animals have proportionately lesssurface area, lose heat more slowly,and, pound for pound, need less food.The square-versus-cube relationshipmakes the area of a solid proportionalto the two-third power of its mass,so metabolic rate should also beproportional to mass2/3. For many years,most biologists thought that it was.

But in 1932, Max Kleiber, an animalphysiologist working at the University

of Californias agricultural station inDavis, re-examined the question, andfound that, for mammals and birds,metabolic rate was mass0.73closerto three quarters than two thirds.Kleiber looked at animals ranging insize from a rat to a steer. By the mid-1930s, other workers had put togethera mouse to elephant curve thatsupported the three-quarter-power law,and by the 1960s, the plot had beenextended for everything from microbes

to whales, still seeming to show thesame relationship. Quarter-powerscaling also began to stretch beyondmetabolic rate. Biological times, suchas lifespan and heart rate, were foundto be proportional to mass1/4, andfractions related to one-quarter showup in other scaling relationships: the

diameter of the aorta and tree trunks isproportional to mass3/8, for example.It was, however, much harder to

find a theoretical reason for whymetabolic rate should be proportionalto mass3/4and more generally, whyquarter-power scaling laws should beso prevalent in biology. The impassemeant that by the mid-1980s interest inscaling had waned. But it sparked backinto life in 1997, when two ecologistsJames Brown of the University of NewMexico, Albuquerque, and his graduatestudent Brian Enquist, now at the

University of Arizona, Tucsonand aphysicist, Geoffrey West of the Santa FeInstitute, developed a new explanationof why metabolic rate should equal thethree-quarter power of body mass.

West, Brown, and Enquists theoryis based on the structure of biologicaldistribution networks, such as bloodvessels in vertebrates and xylem inplants. The trio assumed that metabolicrate equals the rate at which thesenetworks deliver resources, and thatevolution has minimized the time andenergy needed to get materials from

where they are taken upthe lungs orroots, for exampleto the cells. Theyalso assumed that, although organismsvary greatly in size, the terminal unitsin their distribution networks, such asblood capillaries or leaf stalks, do not.

Bigger plants and animals takelonger to transport materials, and souse them more slowly. In West, Brown,and Enquists model, the maximallyefficient network that serves everypart of a body has a fractal structure,showing the same geometry at differentscales. And the number of uniform

terminal units in such a networkandso the rate at which resources aredelivered to the cellsis proportionalto the three-quarter power of bodymass.

Pattern versus Variation

Whether metabolic rate really varieswith the three-quarter power of bodymass is still debatedsome researchersstill favor two-thirds, others think thatno one exponent fits all the databut

DOI: 10.1371/journal.pbio.0020440.g001

Figure 1.After Correcting for Body Size and Temperature,the Metabolic Rates of a Shark, a Tomato Plant, and a Tree AreRemarkably Similar(Illustration: Sapna Khandwala)


3/5


a majority of biologists favor three-quarters. And whether the fractaltheory really explains the relationshipof metabolic rate to body size is also stillcontentious. In the most wide-rangingcritique so far, published this April,two Polish researchers, Jan Kozlowski,of Jagiellonian University, Krakow, and

Marek Konarzewski of the Universityof Bialystok, claimed that the theorysmaths could not simultaneously containboth uniform terminal units andthree-quarter-power scaling, that largeanimals built along such lines wouldhave more blood than their bodiescould contain, that biological scalinglaws were not built around quarterpowers, and that biological networkswere not generally branching fractals.

I dont believe theres anything toexplaintheres no universal scalingexponent, says Kozlowski. He is also

struck by what is left unexplainedwhen size is accounted for: animalsof the same size can still show morethan an order of magnitude variationin metabolic rate. Whats strikingin nature is the variability, he says.There are regularities that call forexplanation, but that doesnt meanignoring the variability is correct.Kozlowski is the co-author of atheory that relates metabolic rate tocell size and the amount of DNA anorganism has, one of several alternativeexplanations of the scaling of metabolic

rate published since West, Brown, andEnquists model.

The criticisms are serious, saysRobinson. The jury is outquestionsabout the fundamental maths areworrying a few people. On the otherhand, he says, West, Brown, and

Enquists model seems a plausibletemplate for designing an organism,and its predictions fit real-world dataremarkably well. Whether this fit trulycaptures the physical and chemicalmechanisms underlying the patternsremains to be seen; Robinson hopesthat criticism can strengthen West,

Brown, and Enquists model, perhapsleading to a new, improved theory.The metabolic theorys authors

are not budging. Weve yet to see acriticism we feel we cant answer prettyreadily, says Brown. Kozlowski andKonarzewskis arguments are basedon a misreading of the work, he says,and criticisms that focus on one aspect,such as the structure of mammalianvascular systems, miss the key point,which is generality: If were wrongon quarter powers, why do they keepshowing up in everything from life-

history processes to evolutionary rates?

From Sharks to Tomatoes

After accounting for size, Brownsgroup turned its attention to thesecond most important influence on

metabolism: temperature. The effectis exponential, and a 5 C rise in bodytemperature equals a roughly 150%rise in metabolic rate. The team builtan equation for metabolic rate thatcombined the mass3/4term with theBoltzmann factor. The latter is anexpression of the probability that twomolecules bumping into each otherwill spark a chemical reaction. Thehigher the temperature, the greater theprobability, and the faster the reaction.

Adding temperature explainedmuch of the variation in metabolic

rate that remained after adjustingfor size. It also explained some of themetabolic differences between groups.For example, a reptile has a slowermetabolic rate than a mammal of thesame size. But adjusting for its lowerbody temperature removes much ofthe difference, suggesting that the twogroups share fundamental metabolicprocesses. The same even goes forplants and animals. When you correctfor size and temperature, the metabolic

rates of a shark, a tomato plant and atree are remarkably similar, (Figure1) says Gillooly, who joined Brownsgroup as a grad student to work onthe temperature question. Its notyet clear what the activation energyrepresents, says Gillooly. It could be akind of average for all the hundreds of

chemical reactions in metabolism, ormaybe the energy needed to get overone crucial hump in the path.

The metabolic theorys thirdcomponent, resources, is alsosomething of a black box at this stage.Nutrient supply, the team reasons, isthe next most important determinantof metabolic rate, and will account forsome of the remaining unexplainedvariation. As with temperature, theoverall effect could be a balance ofmany processes, or it could be due toone limiting elementthe growth of

lake phytoplankton is often limited byphosphorus, for example, while formarine phytoplankton iron is usuallythe crucial nutrient. Its a workin progress, says Brown. But ourvision for a metabolic theory of life isultimately going to include materialresource limitation.

These three things still do notaccount for all the variation inmetabolic rate, but more detailedknowledge of species can yieldmore precise predictions. Usingbody size, altitude, and diet, Brian

McNab, of the University of Florida,Gainesville, has explained 99.0% ofthe variation in metabolic rate forbirds of paradise (Figure 2), and99.4% of the rate variation in leaf-nosed bats. Nevertheless, when McNabsees attempts to explain variation inmetabolism using a few parametersapplied across a wide range of sizes andtaxonomic groups, what isnt explainedstrikes him as forcefully as what is.

I have serious reservations as towhether there is a single relationshipfor body size and metabolic rate, he

says. I think we will be able to findgeneralizations in ecology, but theyrenot going to be simplethere will be abunch of clauses and restrictions, andanimals have a lot of ways to bend therules.

No theory matches data exactly,Brown points out; having a baselineprediction for metabolism lets youidentify exceptional cases worthy offurther investigation. Viewed from thisangle, the metabolic theory is a kind


Figure 2.Adult Male Raggiana Bird of Paradise(Paradisaea raggiana)Body size, altitude, and diet account for99.0% of the variation in the metabolicrates of birds of paradise.(Photo: Brian McNab)

Temperature could also

explain why biodiversity

peaks at the equator.

December 2004 | Volume 2 | Issue 12 | e440


4/5


of null hypothesis of how organismswork. Until you have a theory thatmakes a prediction, you dont knowhow to interpret any of the variation,says Brown. And, he adds, despite thisvariation, the underlying trends arealso meaningful. There are themesof life that are deep-seated and

fundamental.All the business of life needs energy.So if you know the rate at which anorganism burns fuelor if you knowhow big and hot it is, and apply themetabolic theoryyou can make asuite of predictions about its biology,such as how fast it will grow andreproduce, and how long it will live.

By correcting for mass andtemperature, Brown, Gillooly, and theircolleagues believe they have revealedunderlying similarities in all the ratesof life. The hatching times for egg-laying animals, including birds, fish,amphibians, insects, and plankton, turnout to follow the same relationshipifa fish egg were the same size andtemperature as a bird egg, it would

take equally long to hatch (Figure 3).The same goes for growth: a tree and amammal of equal size and temperaturewould gain mass at the same speed.And size and temperature even explainmuch of the variation in mortality ratesbetween specieswhich one mighthave thought to be strongly dependenton external factors such as predatorsperhaps through metabolismsinfluence on aging processes, such asfree-radical damage to the genome.

One Rule for All?

If all organisms work in the same way,understanding individual biology offersan obvious route to explaining naturespatternsecological processes becomea kind of meta-metabolism. Indeed, theteam has used their theory to predictthe flux of carbon dioxide throughforestsa measure more usually usedto determine individual metabolic rate.They have also found that body sizeand temperature predict the densitiesand growth rates of populations. So

hotter environmentsshould support lowerpopulation densities, aseach individual consumesresources more quickly,leaving less to go round.One thing that does notscale with a quarter power

of body size is the area ofanimals home ranges;this increases more or lesslinearly with body size. Butin October, Brown, alongwith researchers fromPrinceton University andthe Institute of Zoologyin London, published amodel that brought this,too, into the metabolictheory. They borrowedanother trick from physics,using an equation that describes

colliding gas molecules to model theinteractions between neighboringanimals.

Temperature could also explain whybiodiversity peaks at the equator, theteam believes. Organisms with fastermetabolisms have faster mutationrates. So the genomes of smaller,hotter animals change more quickly,and they will also get through theirgenerations more rapidly. One wouldtherefore expect to see more newspecies created in small organisms andwarm environments. The large-scale

trend in all these rateshatchingtime, individual and populationgrowth, ecosystem metabolism, DNAsubstitutionis closely proportional toa quarter power of body mass.

In the future, Browns group plansto examine the dynamics of colonialorganisms and societies through thelens of metabolic ecology; insteadof capillaries, the terminal units ofthe networks would become ants, orpeople. There are also many appliedproblems within the theorys scope,including some of the most significant

human impacts on the biosphere.Carbon emissions and the consequentglobal warming are increasing boththe temperature and nutrient supply.And exploited populations, such asfisheries often show a decrease inindividual size, as larger animals arepreferentially killed. Both these wouldtend to speed up biological processes.Another team of United States andItalian researchers has found thatthe same model that describes the

growth of individuals can also predict

the growth of tumors, hinting thatmetabolic ecology may have medicalapplications.

Brown hopes that metabolic ecologywill one day become an uncontroversialpart of researchers toolkits, like thetheories population geneticists useto predict changes in the frequenciesof genes. Before that happens, boththe theorys proponents and itsopponents have years of work aheadof them. Adopting the theory may alsorequire a shift in ecologists worldview.Most ecologists work by carrying out

experimental manipulations on smallgroups of similar organisms: thewarblers in a woodland, for example,or the grasses of a meadow. Whenthey build models, they do so fromempirical data, not from physical firstprinciples. The philosophy behindmetabolic ecology disconcerts manyresearchers, says Robinson. A lot oftraditional biologists are uncomfortablewith thinking about data in theseterms.

Kozlowski doubts that simpletheories can make precise predictions

about the behavior of biologicalsystems on large scales. He believesthat metabolic ecology risks leading thediscipline up a blind alley: If Im right,and the basic model contains an error,correcting the results will be a very longprocess. If theyre not right, theyll havedone a disservice to ecology.

But many ecologists are moreoptimistic that some unifyingprinciples of nature can be found,and that metabolic ecology, and the

If theyre not right, theyll

have done a disservice to

ecology.

December 2004 | Volume 2 | Issue 12 | e440


Figure 3.Apple Snail EggsThe hatching times for egg-laying animals, includingbirds, fish, amphibians, insects, and planktonor eventhese Apple Snail eggsturn out to follow the samerelationship. (Photo: Gary M. Stolz, U. S. Fish and WildlifeService)


5/5


debate around it, is a step in the rightdirection. Some think the theorymay be part of an even grander idea.Stephen Hubbell, of the Universityof Georgia, is one of the architectsof another idea causing a stir amongecologists. Called neutral ecology, itproposes a general explanation of

how competition between individualsproduces the dynamics of birth, death,and migration seen in ecosystems,and its predictions match closely theabundance and diversity of species inthe wild. He believes that metabolicand neutral ecology can becomeelements of some larger theoreticalframework.

Ive never been more excited inmy life, says Hubbell. Ecology nowis like quantum mechanics in the1930swere on the cusp of somemajor rearrangements and syntheses.

Im having a lot of fun.

Further Reading

Allen AP, Brown JH, Gillooly JF (2002) Globalbiodiversity, biochemical kinetics and theenergy equivalence rule. Science 297: 15451548.

Brown JH, Gillooly JF, Allen AP, Savage VM,West GB (2004) Towards a metabolic theoryof ecology. Ecology 85: 17711789. (Part of aforum on metabolic ecology in the August 2004issue ofEcology.)

Enquist BJ, Economo EP, Huxman TE, Allen AP,

Ignace DD, et al. (2003) Scaling metabolismfrom organisms to ecosystems. Nature 423:639642.

Gillooly JF, Brown JH, West GB, Savage VM,Charnov EL (2001) Effects of size andtemperature on metabolic rate. Science 293:22482251.

Gillooly JF, Charnov EL, West GB, SavageVM, Brown JH (2002) Effects of size andtemperature on developmental time. Nature417: 7073.

Gillooly JF, Allen AP, West GB, Brown JH (2004)Metabolic rate calibrates the molecular clock:Reconciling molecular and fossil estimates ofevolutionary divergence. Proc Natl Acad Sci US A. In press.

Guiot C, Degiorgis PG, Delsanto PP, Gabriele P,Deisboeck TS (2003) Does tumor growth follow

a universal law? J Theor Biol 225: 147151.

Hubbell SP (2001) The unified neutral theory ofbiodiversity and biogeography. Princeton (NewJersey): Princeton University Press. 448 p.

Jetz W, Carbone C, Fulford J, Brown JH (2004)The scaling of animal space use. Science 306:266268.

Kozlowski J, Konarzewski M (2004) Is West,Brown and Enquists model of allometricscaling mathematically correct and biologicallyrelevant? Funct Ecol 18: 283289. (The April2004 issue ofFunctional Ecologycontains several

more papers on scaling and metabolism.)Kozlowski J, Konarzewski M, Gawelczyk AT (2003)

Cell size as a link between noncoding DNA andmetabolic rate scaling. Proc Natl Acad Sci U S A100: 1408014085.

McNab BK (2003) Ecology shapes birdbioenergetics. Nature 426: 620621.

McNab BK (2003) Standard energetics ofphyllostomid bats: The inadequacies ofphylogenetic-contrast analysis. Comp BiochemPhysiol A 135: 357368.

West G B, Brown JH, Enquist BJ (1997) A generalmodel for the origin of allometric scalingmodels in biology. Science 276: 122126.

West GB, Brown JH, Enquist BJ (2001) A generalmodel for ontogenetic growth. Nature 413:628631.

Whitfield J (2001) All creatures great and small.

Nature 413: 342344.

December 2004 | Volume 2 | Issue 12 | e440 | e430

Open access, freely available online

ecology’s big, hot idea

Documents