Energy Flow in Ecosystems: A Historical Review

A M . ZOOLOCIST, 8:11-18 (1968).

Energy Flow in Ecosystems: A Historical Review

EUGENE P. ODUM

Institute of Ecology and Department of Zoology, University of Georgia,Athens, Georgia 30601

SYNOPSIS. A generalized model of energy flow applicable both to individual populations andfood chains is discussed. The basic ideas of energy flow and trophic levels are described, and itis emphasized that 'the concept of trophic level is not primarily applicable to individual species.The efficacy of rates of population energy flow as a measure of importance in community func-tion is stressed, and the disadvantages associated with measures of density and biomass arepointed out. Finally, the historical development of energy-oriented thinking in ecology is tracedin a series of ten steps dating from the late 19th century. The growing importance of systemsanalysis and the use of computer models to simulate ecological functions are recognized as majorareas of emphasis during the next decade.

The study, understanding, and intelli-gent manipulation of our environment re-quires systematic investigation of the struc-ture and function of ecological systems atvarious size levels ranging from simplifiedmicrocosms to the biosphere as a whole. Ina recent article (Odum, 1962) I suggestedthat ecology could best be defined as thestudy of the relationships between struc-ture and function in nature, and that thefollowing breakdown might provide a sim-plification of the first order for purposes ofstudy.A. Structure.

1. Composition of the biological com-munity (species, numbers, biomass,life-history, dispersion, etc.).

2. Quantity and distribution of abioticmaterials (nutrients, water, etc.).

3. Range or gradient of conditions ofexistence (temperature, light, etc.).

B. Function1. Range of energy flow through the sys-

tem (eco-energetics).2. Rate of material cycling (eco-cycling).3. Regulation by physical environment

and by organisms (eco-regulation).Thus, we review in this refresher course

one of the several fundamental approachesto ecology—one that lends itself especiallyto the teaching of the subject to student andcitizen alike. My paper is concerned with

a brief history of this approach as an intro-duction to the five papers which follow.Before going into history, I believe it wouldbe well to delimit and define our subject.

The behavior of energy in ecosystemscan be conveniently shorthanded as "en-ergy flow" because energy transformationsare directional in contrast to the cyclic be-havior of materials. The potential andkinetic components of energy flow throughan ecological system are lumped under thedesignations, production (P) and respira-tion (R), respectively. Consequently, en-ergy flow (E) can be very broadly definedas the sum of P and R, or E = P -f- R. Weneed, of course, to further subdivide P andR into their ecologically significant sub-compartments. Since terminologies havenot been standardized and the usage ofequation-symbols varies so widely as to beconfusing, I believe the best way to estab-lish communication, especially in the teach-ing arena, is to fall back on a graphic modelthat shows relationships in the form of aneasily understood picture.

In Figure 1, I present what might becalled a "universal" model of energy flow,one that is applicable to any living compo-nent whether it be plant, animal, micro-organism—or individual, population, troph-ic group. Linked together, such graphicmodels can depict food-chains (as shown in

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12 EUGENE P. ODUM

FIG. 1. Components for a "universal" model of ecological energy flow. See text for explanationof symbols.

the lower right of Fig. 1), or the bioener-getics of an entire ecosystem.

In Figure 1, the shaded box labelled "B"represents the living structure or "biomass"of the component. The designation, "stand-ing crop," is a comparable term often usedwhen we wish to speak of the total mass ofa population or trophic grouping such asphytoplankton in a column of water orphytophagous insects in a grassland. Bio-mass is usually measured and expressed assome kind of weight: either total living(wet) weight, dry weight, or ash-free weight.Varying usages here and the lack of good

conversion factors often pose problems.From the standpoint of energetics it is alsodesirable to express biomass in terms ofcalories so that relationships between therates of energy flow and the instantaneousor average standing-state biomass can beestablished. As will be briefly noted furtheralong in this article, the ratios B/E, B/P,and B/R are of great theoretical interestwith respect to community developmentand ecological succession.

The total energy input or intake is indi-cated by "I" in Figure 1. For strict auto-trophs this is light, and for strict hetero-

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HISTORICAL REVIEW OF ENERGY FLOW 13

trophs organic food. Some species of algaeand bacteria can utilize both energysources, and many may require both in cer-tain proportions. A similar situation holdsfor invertebrate animals and lichens whichcontain mutualistic algae. In such cases theinput flow in the energy flow diagram canbe subdivided accordingly to show the dif-ferent energy sources, or the biomass can besubdivided into separate boxes if one wishesto keep everything in the same box at thesame energy level (i.e., the same trophiclevel).

Such flexibility in usage can be confusingto the beginner. In teaching, I find that itis important to emphasize that the conceptof trophic level is not primarily intendedfor categorizing species. Energy flowsthrough the community in stepwise fashiondue to the second law of thermodynamics,but a given population of a species may be(and very often is) involved in more thanone step or trophic level. The universalmodel of energy flow illustrated in Figure1 can be used in two ways. The model canrepresent a species-population, in whichcase the appropriate energy inputs andlinks with other species would be shown asa conventional species-oriented food-webdiagram. Or the model can represent a dis-crete energy level, in which case the bio-mass and energy channels represent all orparts of many populations supported bythe same energy source. Foxes, for exam-ple, usually obtain part of their food fromeating plants (fruit, etc.) and part by eat-ing herbivorous animals (rabbits, fieldmice, etc.). A single diagram of energy flowcould be used to represent the species orthe whole population of foxes if our objec-tive is to stress intrapopulation energetics.On the other hand, two or more boxes(such as shown in the lower right of Fig. 1)would be employed should we wish to ap-portion the metabolism of the fox popula-tion into more than one trophic level. Inthis way we can place the fox populationinto the overall pattern of energy flow inthe community. When an entire commu-nity is modeled one cannot mix these twousages unless all species happen to be re-stricted to single trophic levels (e.g., a

highly simplified blue-grass-cow-man eco-system).

So much for the problem of the sourceof the energy input. Not all of the inputinto the biomass is transformed; some of itmay simply pass through the biologicalstructure, as occurs when food is egestedfrom the digestive tract without being me-tabolized, or when light passes throughvegetation without being fixed. This en-ergy component is indicated by "NU" ("notutilized"). That portion which is utilizedor assimilated is indicated by "A" in thediagram. The ratio between these twocomjsonents, i.e., the efficiency of assimila-tion, varies widely. It may be very low, asin light-fixation by plants or food-assimila-tion in detritus-feeding animals, or veryhigh as in the case of animals or bacteriafeeding on high energy food such as sugarsand amino acids.

In autotrophs the assimilated energy("A") is known as "gross production" or"gross photosynthesis." Historically, theterm, "gross production," has been used bysome authors for the analogous componentin heterotrophs. However, since the "A"component in heterotrophs represent foodalready "produced" somewhere else, theterm "gross production" should be re-stricted to primary or autotrophic produc-tion. In higher animals, the term, "me-tabolized energy," is often used for the "A"component.

A key feature of the model is the separa-tion of assimilated energy into the "P" and"R" components as previously described.That part of the fixed energy ("A") whichis burned and lost as heat is designated asrespiration ("R"), while that portionwhich is transformed to new or differentorganic matter is designated as production("P"). This is the "net production" or"net photosynthesis" in green plants andsimply "production" or "secondary produc-tion" in animals. It is important to pointout that the "P" component is energy avail-able to the next trophic level, as opposedto the "NU" component which is still avail-able at the same trophic level.

The ratio between "P" and "R" varieswidely and is of great ecological signifi-

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14 EUGENE P. ODUM

cance. In general, the proportion of en-ergy going into respiration or maintenanceis large in populations of large organisms,such as men and trees, and in mature (i.e.,"climax") communities. Conversely, the"P" component is relatively large in activepopulations of small organisms, such asbacteria or algae, and in the young or"bloom" stages of ecological succession.

Production may take a number of forms.Three subdivisions are shown in Figure 1:"G" refers to additions to the biomass orgrowth. "E" refers to assimilated organicmatter which is excreted or secreted (e.g.,simple sugars, amino acids, urea, mucus,etc.). This "leakage" of organic matter,often in dissolved or gaseous form, may beappreciable but is often ignored because itis hard to measure. Finally, "S" refers to"storage," as in the accumulation of fatwhich may be reassimilated at some latertime. The reverse "S" flow shown in Fig-ure 1 may also be considered a "work loop"in that it depicts that portion of produc-tion which is necessary to insure a futureinput of new energy (e.g., reserve energyused by a predator in the search for prey).

Figure 1 shows only a few of the eco-logically useful subdivisions of the basicpattern of energy flow. In practice, we areoften hampered by the difficulties of meas-urement, especially in field situations. Aprimary purpose of a model, of course, isto define components that we want to meas-ure in order to stimulate research intomethodology. Even if we are not yet ableto chart all the flows, measurements ofgross inputs and outputs alone may be re-vealing. Because energy is the ultimatelimiting factor, the amounts available andactually utilized must be known if we areto evaluate the importance of other poten-tially limiting or regulating factors. Manyof the controversies about food limitation,weather limitation, competition, and bio-logical control could be resolved if we hadaccurate data on energy utilization by thepopulations in question.

Concepts of energy flow provide not onlya means of comparing ecosystems with oneanother, but also a means of evaluating the

TABLE 1. Density, biomass, and energy flow ofdifferent organisms.

ApproximateDensity (m2)

Soil bacteriaMarine copepods

(Acartia)Intertidal snails

(Littorina)Salt marsh

grasshoppers(Orchelimum)

Meadow mice(Microtus)

Deer (Odo-coileus)

Insectivorousbirds

Blue grass{Foa)

1 0 1 2

10°

200

10

io-2

10"°

io-a

40

Biomass(g/m')

0.0012.0

10.0

1.0

0.6

1.1

0.02

200

Energy Flow(Kcal/ma

/day)

1.0

2.5

1.0

0.4

0.7

0.5

0.02

20.0

relative importance of populations of di-verse sizes and rates of metabolism. Table1 lists estimates of density, biomass, andenergy flow rates of eight populations dif-fering widely in size of organism andtrophic position. These estimates are basedon densities and weight-specific metabolicrates (including an estimate for the "P"component) that one might expect to findin a temperate community of moderate nu-trient fertility. For the first six popula-tions listed, the estimated energy require-ments are similar, even though the densi-ties vary over 17 orders of magnitude andthe biomass over five. This indicates thatall six populations are functioning at ap-proximately the same energy level (i.e., asprimary consumers or herbivores). Thehigher rates estimated for blue grass andthe lower rates for insectivorous birds areindicative of their different trophic rolesin the ecosystem. Because numbers over-emphasize the importance of small organ-isms (e.g., bacteria) and weight or biomassoveremphasizes the importance of large or-ganisms, we cannot use either as a reliablecriterion for comparing the functional roleof populations that differ widely in size-metabolism relationships. The rate of en-ergy flow, however, provides a suitable in-dex for comparing the importance, ener-

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getically speaking, of any and all compo-nents of an ecosystem.

The idea of looking at nature as an en-ergy-flow system is deeply rooted in theearly history of science. Interest in the"fires of life" goes back to antiquity. Manyof the concepts that we now apply to thepopulation and community level had theirorigin in the physical sciences and in theearly history of physiology and medicine.For the purposes of this refresher course,I believe we can trace the recent historyof ecological energetics in about ten steps.It should be emphasized that the followingoutline was prepared primarily as a chro-nology of ideas and not as a historical re-view of names and literature. Only a fewsamples of the latter are suggested for theirvalue as background reading.

1. Qualitative description of food webs.The idea that organisms in nature arelinked together in network fashion throughfood was expressed in various ways in thewritings of 19th century naturalists. Ste-phen A. Forbes' classic essay on "The Lakeas a Microcosm" (1887) is a good example,and provides an appropriate beginning forthis historical review.

2. Trophic levels and ecological pyra-mids. In the 1920's, August Thienemann(1926) described trophic levels in terms of"producers" and "consumers," and CharlesElton (1927) wrote about the "ecologicalniche" and the "pyramid of numbers" interms of organization of the food chain.As emphasized earlier in this paper, cri-teria of energy flow should replace num-bers if the "Eltonian pyramid" is to remaina valid concept for all types of ecosystems.

3. Application of thermodynamic prin-ciples. The 1920's also saw the beginningof the influence that the second law ofthermodynamics was to have on ecologicaltheory. A. J. Lotka's book, "The Elementsof Physical Biology" (1925), was a mile-stone. His concepts of the non-equilibriumsteady state and the "law of maximum en-ergy in biological systems" were forerunnersof important ecological generalizations,e.g., the theory of H. T. Odum and Pinker-ton (1955) that nature's low efficiency ofenergy transfer is a consequence of the

tendency for optimum efficiency for maxi-mum power output to be less than maxi-mum efficiency.

4. Energy budgets and the concept ofprimary productivity. Limnologists wereamong the first to develop these concepts,perhaps because lakes provide such con-venient units for study and because heatand gaseous exchanges are more easilymeasured in standing bodies of water thanin other ecosystems. The work of Birgeand Juday in the 1930's comes to mind inthis connection (see Juday, 1940). As in-strumentation improved, it later becamepossible to deal with energy budgets of ter-restrial environments, and even of thewhole biosphere, as suggested in DavidGates' little book, "Energy Exchange inthe Biosphere" (1962).

To a considerable extent, progress in thestudy of primary productivity depended onthe development of field methods. Thefollowing is a brief chronology of methods(together with one or more pioneer method-ologists):

a. CO2 uptake in terrestrial enclosures.Transeau (1926).

b. Dark and light bottle method (aquat-ic). Gaarder and Gran (1927).

c. The diurnal curve method (aquatic).Sargent and Austin (1949), H. T. Odum(1956).

d. Harvest methods. Penfound (1956),Ovington (1957), E. P. Odum (I960).

e. The pH method (aquatic). Verduin(1956), Beyers, and H. T. Odum (1959).

f. The light-chlorophyll method. Rytherand Yentsch (1957).

g. Infra-red gas analyzer measurement ofCO2 (enclosed terrestrial vegetation). Lem-on (1960), Mooney and Billings (1961).

h. CO2 vertical gradient method (unen-closed terrestrial vegetation). Monteith(1962).

5. Trophic-dynamic concepts and en-ergy flow by trophic levels. RaymondLindeman's classic paper on the "Trophic-dynamic Aspect of Ecology" (1942) usheredin the 1940's and did more than any othersingle contribution to bring concepts ofenergy flow to focus at the level of theecosystem. One should not forget, how-

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16 EUGENE P. ODUM

ever, the contributions to this synthesis byG. E. Hutchinson (1948), George Clarke(1946), Amyan Macfadyen (1949), andothers.

6. The energy-flow diagram and com-munity metabolism. The diagram, of en-ergy flow might be referred to by some as an"Odum" device (H. T. Odum, 1956, 1957;Odum and Odum, 1959; E. P. Odum, 1963),although flow-diagrams are routine inphysics and engineering. The basic unit ofthe ecological energy-flow diagram has beendescribed in this paper. In modified form,flow-diagrams have proved useful in em-phasizing the fundamental partition o£flow into grazing and detritus food-chains(E. P. Odum, 1962; 1963), and as a basisfor models of electrical analogue circuits(H. T. Odum, 1960). The latter approach,which considers the energy channels to bethe "invisible wires of nature," is especiallyappropriate for analogue computer ma-nipulation (see item 10 below).

Studies during the 1950's demonstratedthat important generalizations could be de-rived from measurements of the metabo-lism of whole communities without neces-sarily having detailed information on allcomponent populations (Odum and Odum,1955; H. T. Odum, 1957; Teal, 1957).

7. Secondary production and energy flowin populations. It is only natural that suc-cess in the study of primary productionshould be followed by increased interest inthe energy flow of heterotrophs and con-cern with the utilization of net primaryproduction. Here again, background ex-perience in laboratory physiology was thebasis for the first attempts at field meas-urements. I cite only a few examples ofefforts to combine laboratory respirometrywith field census procedures: Pearson(1954), Phillipson (1962), E. P. Odum andSmalley (1959), E. P. Odum, et al. (1962),Golley (1960). Ecologists are now seekingnew methods which do not require "en-closement" (i.e., confinement in cages orrespirometers). Rates of uptake, elimina-tion, and flux of radionuclide tracers pro-vide the most exciting new tools (Crossleyand Howden, 1961; E. P. Odum and F. B.

Golley, 1963; R. G. Wiegert, E. P. Odum,and J. H. Schnell, 1967; Reichle, 1967).

8. Energetics of laboratory populations.Just as some generalizations are best madefrom the study of "big nature" (such as acoral reef), so other useful generalizationscome from the study of "little nature" inthe laboratory. Ecologists are just begin-ning to take advantage of the precision,control, and experimental design-possibil-ities of the laboratory in studies that rangefrom those focused on the energetics ofpopulations of single species (Richman,1958; Slobodkin, 1959) to those dealingwith the community metabolism of self-sus-taining micro-ecosystems (Beyers, 1963;Cooke, 1967). The latter will be of greatinterest in future attempts o design a re-generative ecosystem for man's space travel.

9. The energetics of ecological succes-sion. H. T. Odum and R. C. Pinkerton(1955) were perhaps among the first topoint out that ecological succession in-volves a fundamental change of the pat-tern of basic energy flows. As ecosystemsdevelop toward maturity (i.e., "climax"),the P/R ratio approaches one and the B/E(or B/P or B/R) ratio increases—thestrategy being not to maximize efficiencyof production (as is often desired by man),but to optimize the support of as large andcomplex a biomass structure as possible perunit of available energy flow. Margalef(1963a, 19636) has recently documentedand extended these basic ideas, and hispapers should be required reading for allecologists.

10. Systems ecology. The "input-output,""rate of change," and "flow chart" ways ofthinking lead directly into "systems analy-sis," which is a state of mind as much as itis applied mathematics and computers(Watt, 1966). Because energy flow drivesthe complex cycles of materials that are theform, function, and diversity of life, "eco-energetics" is the core of "ecosystem analy-sis." It is not difficult to predict where theemphasis will be in the next decade!

EPILOGUE

Within our own exploding population,

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there is increasing concern about "foodecology," which is essentially the samething as "energy flow ecology" if we con-sider light as "plant food." The Inter-national Biological Program (IBP) nowbeing planned worldwide around thetheme, "the biological basis for produc-tivity and human welfare," is but one indi-cation of the recognition by scientist andcitizen alike that a better understandingof the biosphere is urgent. The first phaseof IBP, now well underway, involves thescheduling of symposia, planning of pro-grams by national committees, and thepreparation of manuals on methods.1 Thedefinitive phase will involve intensive, mul-tidisciplinary studies of landscapes (suchas forests or croplands), important processes(such as nitrogen fixation), and key prob-lems (such as human adaptation). Toachieve these goals, many more trained andmotivated people than are now availablewill be needed. Hence, training is one ofthe primary concerns of IBP planners. Insome small way we hope that this refreshercourse will prove a useful adjunct to theIBP.

1 Bulletins outlining the U. S. National Programfor IBP may lie obtained by writing: U. S. NationalCommittee for the IBP, National Academy of Sci-ences, 2101 Constitution Avenue, Washington, D. C.20418.

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Beyers, R. J. 1963. The metabolism of 12 laboratoryniicroecosystems. Ecol. Monographs 33:281-306.

Beyers, R. J., and H. T. Odum. 1959. The use ofcarbon dioxide to construct pH curves [or themeasurement of productivity. Limnol. Oceanog.4:499-502.

Clarke, G. L. 1946. Dynamics of production in amarine area. Ecol. Monographs 16:321-335.

Cooke, G. D. 1967. The pattern of autotrophic suc-cession in laboratory microcosms. BioScience 17:717-721.

Crossley, D. A., and H. F. Howden. 1961. Insect-vegetation relationships in an area contaminatedby radioactive wastes. Ecology 42:302-317.

Elton, C. 1927. Animal ecology. The Macmillan Co.,New York.

Forbes, C. A. 1887. The lake as a microcosm. Re-published 1925. Illinois Nat. Hist. Survey Bull.15:537-550.

Gaarder, T., and H. H. Gran. 1927. Investigationsof the production of plankton in the Oslo Fjord.J. Cons. Intern. Explor. Mer 42:1-48.

Gates, D. 1962. Energy exchange in the biosphere.Harper and Row, New York

Golley, F. B. 1960. Energy dynamics of a foodchain of an old-field community. Ecol. Mono-graphs 30:187-206.

Hutchinson, G. E. 1948. Circular causal systems inecology. Ann. New York Acad. Sci. 50:221-246.

Juday, C. 1940. The annual energy budget of aninland lake. Ecology 21:438-450.

Lemon, E. R. 1960. Photosynthesis under field con-ditions. Agron. J. 52:697.

Lindeman, R. L. 1942. The trophic-dynamic aspectof ecology. Ecology 23:399-418.

Lotka, A. J. 1925. Elements of physical biology.Williams and Wilkins, Baltimore.

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Odum, H. T., and E. P. Odum. 1959. Principles andconcepts pertaining to energy in ecosystems, p.43-87. In E. P. Odum, Fundamentals of ecology.W. B. Saunders Co., Philadelphia.

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Energy Flow in Ecosystems: A Historical Review

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