The Trophic-Dynamic Aspect of Ecology Author(S): Raymond L

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The Trophic-Dynamic Aspect of Ecology Author(s): Raymond L. Lindeman Reviewed work(s): Source: Ecology, Vol. 23, No. 4 (Oct., 1942), pp. 399-417 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/1930126 . Accessed: 30/01/2012 10:50

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http://www.jstor.org THE TROPHIC-DYNAMIC ASPECT OF ECOLOGY

RAYMOND L. LINDEMAN OsbornZoological Laboratory,Yale University

Recent progressin the studyof aquatic community. A more "bio-ecological" food-cycle relationships invites a re- species-distributionalapproach would appraisal of certain ecological tenets. recognize both the plants and animals Quantitative productivitydata provide as co-constituentsof restricted"biotic" a basis for enunciating certain trophic communities,such as "plankton com- principles, which, when applied to a munities," "benthic communities,"etc., series of successional stages, shed new in which membersof the living commu- light on the dynamics of ecological nity "co-act" with each other and "re- succession. act" with the non-livingenvironment (Clementsand Shelford,'39; Carpenter, "COMMUNITY" CONCEPTS '39, '40; T. Park, '41). Coactions and are consideredby bio-ecologists A chronologicalreview of the major reactions effectorsof succession. viewpointsguiding synecological thought to be the dynamic The trophic-dynamicviewpoint, as indicates the followingstages: (1) the paper, emphasizes the static species-distributionalviewpoint; adopted in this (2) the dynamic species-distributional relationshipof trophicor "energy-avail- withinthe community- viewpoint,with emphasis on successional ing" relationships phenomena;and (3) the trophic-dynamic unit to the processof succession. From allied viewpoint. From either species-distri- this viewpoint,which is closely to approach butional viewpoint,a lake, forexample, Vernadsky's"biogeochemical" might be considered by a botanist as (cf. Hutchinson and Wollack, '40) and containingseveral distinct plant aggre- to the "oekologischeSicht" ofFriederichs a primfiary gations, such as marginal emergent, ('30), a lake is consideredas floating-leafed,submerged, benthic, or ecological unit in its own right,since all phytoplankton communities, some of the lesser "communities" mentioned which might even be considered as above are dependent upon other com- food "climax" (cf. Tutin, '41). The associ- ponentsof the lacustrine cycle (cf. ated animals would be "biotic factors" figure1) fortheir very existence. Upon of the plant environment,tending to furtherconsideration of the trophic cycle, limit or modifythe developmentof the the discriminationbetween living organ- community" aquatic plant communities. To a strict isms as parts of the "biotic nutri- zoologist,on the otherhand, a lake would and dead organismsand inorganic "environment" seem to contain animal communities tives as parts of the The roughlycoincident with the plant com- seems arbitrary and unnatural. munities,although the "associated vege- difficultyof drawing clear-cut lines be- non- tation" would be consideredmerely as a tweenthe livingcommunity and the the part of the environment'of the animal living environmentis illustratedby difficultyof determiningthe status of a ' The term habitatis used by certain ecologists slowly dying pondweed covered with (Clements and Shelford, '39; Haskell, '40; T. periphytes,some of which are also con- Park, '41) as a synonym for environmentin the usual sense and as here used, although Park tinuallydying. As indicatedin figure1, points out that most biologists understand " hab- much of the non-livingnascent ooze is itat" to mean "simply the place or niche that rapidly reincorporated through "dis- an animal or plant occupies in nature" in a species-distributionalsense. On the other hand, be hoped that ecologists will shortly be able to Haskell, and apparently also Park, use " environ- reach some sort of agreement on the meanings ment" as synonymouswith the cosmos. It is to of these basic terms. 399 400 RAYMOND L. LINDEMAN Ecology,Vol. 23,No. 4

solved nutrients" back into the living magnitude, i.e., the biotic community "biotic community." This constantor- plus its abiotic environment. The con- ganic-inorganiccycle of nutritive sub- cept of the ecosystemis believed by the stance is so completelyintegrated that writerto be of fundamentalimportance to consider even such a unit as a lake in interpretingthe data of dynamic primarilyas a biotic communityappears ecology. to forcea "biological" emphasis upon a more basic functionalorganization. TROPHIc DYNAMICS This concept was perhaps first ex- pressedby Thienemann('18), as a result Qualitativefood-cycle relationships of his extensive limnologicalstudies on the lakes of NorthGermany. Allee ('34) Althoughcertain aspects of food rela- expresseda similar view, stating: "The tions have been known for centuries, picturethan finallyemerges . . . is of a many processes within ecosystems are sort of superorganismicunity not alone stillvery incompletely understood. The between the plants and animals to form basic process in trophicdynamics is the biotic communities,but also betweenthe transfer of energy from one part of biota and the environment." Such a the ecosystemto another. All function, conceptis inherentin the termecosystem, and indeed all life,within an ecosystem proposedby Tansley ('35) forthe funda- depends upon the utilizationof an exter- mental ecological unit.2 Rejecting the nal source of energy, solar radiation. terms "complex organism" and "biotic A portionof this incidentenergy is trans- community,"Tansley writes, "But the formedby the processof photosynthesis more fundamentalconception is, as it into the structureof living organisms. seems to me, the whole system(in the In the language of communityeconomics sense of physics),including not only the introducedby Thienemann ('26), auto- organism-complex,but also the whole trophic plants are producerorganisms, complexof physicalfactors forming what employingthe energyobtained by photo- we call the environmentof the biome. synthesisto synthesizecomplex organic . . .It is the systemsso formedwhich, substances from simple inorganic sub- fromthe point of view of the ecologist, stances. Although plants again release are the basic units of nature on the face a portionof this potentialenergy in cata- of the earth.. . . These ecosystems,as bolic processes,a greatsurplus of organic we may call them,are of the most vari- substanceis accumulated. Animals and ous kinds and sizes. They form one heterotrophicplants, as consumerorgan- category of the multitudinousphysical isms, feed upon this surplus of potential systems of the universe, which range energy,oxidizing a considerableportion from the universe as a whole down to of the consumed substance to release the atom." Tansley goes on to discuss kineticenergy for metabolism, but trans- the ecosystem as a category of rank formingthe remainderinto the complex equal to the "biome" (Clements, '16), chemicalsubstances of theirown bodies. but points out that the term can also Following death, every organism is a be used in a generalsense, as is the word potential source of energy for saproph- "community." The ecosystemmay be agous organisms (feeding directly on formallydefined as the systemcomposed dead tissues), which again may act as of physical-chemical-biologicalprocesses energysources for successive categories active within a space-time unit of any of consumers. Heterotrophic bacteria im- 2 " and fungi, representingthe most The ecological system composed of the bio- portant saprophagous consumption of coenosis + biotop " has been termed the holocoen by Friederichs ('30) and the biosystemby Thiene- energy,may be convenientlydifferenti- mann ('39). ated fromanimal consumersas special- October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 401

SolarRadiation SolarRadiation

A External DissolvedNutrients N j

Internal A, PhytoplanKters / Pandweids

Bact eria > -* 2 tZooplantkters~z OOZ Brawsers--4-

-N - \/'l X

A3 OmPmdoos Benic PmaWk A3

Betd A3GgQ1 Geerlaized PredatorsnS~~~~~~wimfniiod-yl Predatorsredainhp aftors A3dmanA AIG. na4

ized decomposers3of organic substance. solved nutrientsonce more in resynthe- Waksman ('41) has suggested that cer- sizing complex organic substance, thus tain of these bacteria be furtherdiffer- completingthe food cycle. entiated as transformersof organic and The careful study of food cycles re- inorganic compounds. The combined veals an intricate pattern of trophic action of animal consumersand bacterial predilectionsand substitutionsunderlain decomposerstends to dissipate the po- by certainbasic dependencies;food-cycle tential energy of organic substances, diagrams, such as figure1, attempt to again transformingthem to the inorganic portray these underlyingrelationships. state. From this inorganic state the In general,predators are less specialized autotrophicplants may utilize the dis- in food habits than are theirprey. The 3 Thienemann ('26) proposed the term reducers ecological importanceof this statement forthe heterotrophicbacteria and fungi,but this seems to have been firstrecognized by term suggests that decomposition is produced Elton ('27), who discussed its effecton solely by chemical reduction rather than oxida- the survival of prey species when predation, which is certainly not the case. The term decomposersis suggested as being more appro- tors are numerous and its effect in priate. enablingpredators to survivewhen their 402 RAYMOND L. LINDEMAN Ecology,Vol. 23,No. 4

usual prey are only periodically abun- figure 1) indicates that the terrestrial dant. This abilityon the part of preda- food cycle is essentially "mono-cyclic" tors, which tends to make the higher with macrophyticproducers, while the trophiclevels of a foodcycle less discrete lacustrine cycle, with two "life-forms" than the lower, increasesthe difficulties of producers,may be consideredas "bi- of analyzing the energyrelationships in cyclic." The marine cycle, in which this portionof the food cycle, and may planktersare the only producersof any also tend to "shortenthe food-chain." consequence, may be considered as Fundamental food-cyclevariations in "mono-cyclic" with microphytic pro- differentecosystems may be observed ducers. The relativeabsence of massive by comparinglacustrine and terrestrial supportingtissues in planktersand the cycles. Althoughdissolved nutrientsin very rapid completionof their life cycle the lake water and in the ooze corre- exerta great influenceon the differential spond directlywith those in the soil, the productivitiesof terrestrialand aquatic autotrophicproducers differ considerably systems. The general convexityof ter- in form. Lacustrine producers include restrialsystems as contrastedwith the macrophyticpondweeds, in which mas- concavityof aquatic substrata resultsin sive supportingtissues are at a minimum, strikingtrophic and successional differ- and microphyticphytoplankters, which ences, which will be discussed in a later in larger lakes definitelydominate the section. productionof organic substance. Ter- Productivity restrial producers are predominantly multicellular plants containing much Definitions.-The quantitativeaspects cellulose and lignin in various types of of trophicecology have been commonly supporting tissues. Terrestrial herbi- expressed in terms of the productivity vores, belonging to a great number of of the food groups concerned. Produc- specialized food groups, act as primary tivity has been rather broadly defined consumers(sensu Jacot, '40) of organic as the generalrate of production(Riley, substance; these groups correspond to '40, and others), a term which may be the "browsers" of aquatic ecosystems. applied to any or every food group in a Terrestrial predators may be classified given ecosystem. The problem of pro- as more remote (secondary, tertiary, ductivity as related to biotic dynamics quaternary, etc.) consumers,according has been critically analyzed by G. E. to whetherthey prey upon herbivoresor Hutchinson ('42) in his recent book on upon other predators; these correspond limnologicalprinciples. The two follow- roughly to the benthic predators and ing paragraphsare quoted fromHutchin- swimmingpredators, respectively, of a son's chapter on "The Dynamics of lake. Bacterial and fungaldecomposers Lake Biota": in terrestrialsystems are concentrated The dynamics of lake biota is here treated as in the humus layer of the soil; in lakes, primarilya problem of energy transfer . . . the where the "soil" is overlain by water, biotic utilization of solar energy entering the decomposition takes place both in the lake surface. Some of this energyis transformed water, as organic particlesslowly settle, by photosynthesisinto the structure of phytoplankton organisms,representing an energycon- and in the benthic"soil." Nutrientsalts tent which may be expressed as Al (firstlevel). are thus freed to be reutilized by the Some of the phytoplankters will be eaten by autotrophicplants of both ecosystems. plankton. This concept appears to have a num- The striking absence of terrestrial ber of adherents in this country. The author "life-forms"analogous to plankters4(cf. feels that this analogy is misleading, as the edaphon, which has almost no producers,repre- 4France ('13) developed the concept of the sents only a dependent side-chain of the terres- edaphon, in which the soil microbiota was repre- trial cycle, and is much more comparable to the sented as the terrestrial equivalent of aquatic lacustrine microbenthosthan to the plankton. October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 403

zooplankters (energy content A2), which again Numerous estimates of average respi- will be eaten by plankton predators (energy rationfor photosynthetic producers may content A3). The various successive levels (i.e., stages5) of the food cycle are thus seen to have be obtained from the literature. For successively differentenergy contents (Al, A2, A3, terrestrialplants, estimates range from etc.). 15 per cent (PUtter, re Spoehr, '26) to Considering any food-cyclelevel A., energy is 43 per cent (LundegArdh, '24) under enteringthe level and is leaving it. The rate of change of the energy content A, thereforemay various typesof naturalconditions. For be divided into a positive and a negative part: aquatic producers,Hicks ('34) reported dAn = n + n', a coefficientof about 15 per cent for dt Lemna under certainconditions. Wim- where XAis by definitionpositive and represents penny ('41) has indicated that the respi- the rate of contributionof energy fromA,,- (the ratorycoefficient of marineproducers in previous level) to A,, while Xn' is negative and polar regions(diatoms) is probablymuch represents the sum of the rate of energy dissi- less than that of the more "animal-like" pated from An and the rate of energy content producers (peridinians and coccolitho- handed on to the followinglevel A,,+,. The more interestingquantity is XAwhich is definedas the phorids) of warmerseas, and that tem- true productivityof level An. In practice, it is peraturemay be an importantfactor in necessary to use mean rates over finiteperiods determiningrespiratory coefficients in of time as approximations to the mean rates general. Juday ('40), after conducting XO, Xi, X2. . . . numerous experiments with Manning In the followingpages we shall con- and others on the respirationof phyto- siderthe quantitativerelationships of the plankters in Trout Lake, Wisconsin, followingproductivities: Xo (rate of inci- concludedthat underaverage conditions dent solar radiation), X, (rate of photo- these producersrespire about 13 of the syntheticproduction), X2 (rate ofprimary organic matter which they synthesize. or herbivorousconsumption), X3 (rate of This latter value, 33 per cent, is prob- secondary consumptionor primarypre- ably the best available respiratoryco- dation), and X4 (rate of tertiary con- efficientfor lacustrineproducers. sumption). The total amountof organic Information on the respiration of structureformed per year for any level aquatic primaryconsumers is obtained A', which is commonlyexpressed as the from an illuminating study by Ivlev annual "yield," actually represents a ('39a) on the energy relationships of value uncorrected for dissipation of Tubifex. By means of ingenious tech- energyby (1) respiration,(2) predation, niques, he determined calorific values and (3) post-mortem decomposition. for assimilation and growth in eleven Let us now consider the quantitative series of experiments. Using the aver- aspects of these losses. ages of his calorificvalues, we can make Respiratorycorrections.-The amount the followingsimple calculations: assimi- of energylost fromfood levels by cata- lation (16.77 cal.) - growth(10.33 cal.) bolic processes (respiration)varies con- = respiration(6.44 cal.), so that respira- siderably for the differentstages in the 6.44 life historiesof individuals,for different tion in termsof growth= 1 33= 62.30 levels in the food cycle and for differ- per cent. As a check on the growth ent seasonal temperatures. In termsof stage of these worms, we find that annual production,however, individual growth deviates cancel out and respiratorydif- asmlti .= 61.7 per cent, a value in ferences between food groups may be assimilation observed. good agreement with the classical con- I clusions of Needham ('31, III, p. 1655) The term stage, in some respects preferable with to to the term level,cannot be used in this trophic respect embryos: the efficiency sense because of its long-established usage as a of all developingembryos is numerically successional term (cf. p. 23). similar,between 60 and 70 per cent, and 404 RAYMOND L. LINDEMAN Ecology,Vol. 23,No. 4

independentof temperaturewithin the have a higher rate of respirationthan range of biological tolerance. We may the more sluggish herbivorousspecies; thereforeconclude that the wormswere the respiratoryrate ofEsox underresting growingat nearlymaximal efficiency,so conditionsat 20? C. was 3' times that that the above respiratorycoefficient is of Cyprinus. The formof piscian growth nearly minimal. In the absence of fur- curves (cf. Hile, '41) suggests that the ther data, we shall tentativelyaccept respiratorycoefficient is much higherfor 62 per cent as the best available respira- fishestowards the end of their normal torycoefficient for aquatic herbivores. life-span. Since the value obtainedfrom The respiratorycoefficient for aquatic Ivlev (above) is based on moreextensive predators can be approximated from data than those of Moore, we shall ten- data of another important study by tatively accept 140 per cent as an aver- Ivlev ('39b), on the energytransforma- age respiratorycoefficient for aquatic tionsin predatoryyearling carp. Treat- predators. ing his calorificvalues as in the preceding Consideringthat predatorsare usually paragraph,we find that ingestion(1829 moreactive than theirherbivorous prey, cal.) - defecation(454 cal.) = assimila- which are in turn more active than the tion(1375 cal.), and assimilation- growth plants upon which they feed, it is not (573 cal.) = respiration (802 cal.), so surprisingto find that respirationwith that respiration in terms of growth respect to growthin producers (33 per 802 cent), in primaryconsumers (62 per cent) = 140 a much - per cent, higher and in secondary consumers(>100 per coefficientthan that found for the pri- cent) increases progressively. These maryconsumer, Tubifex. A roughcheck differencesprobably reflect a trophic on this coefficientwas obtained by cal- principle of wide application: the per- orificanalysis of data on the growthof centage loss of energydue to respiration yearling green sunfishes (Lepomis cy- is progressivelygreater for higherlevels anellus) publishedby W. G. Moore ('41), in the food cycle. which indicate a respiratorycoefficient Predation corrections.-In considering of 120 per cent with respect to growth, the predation losses fromeach level, it suggestingthat thesefishes were growing is most. convenient to begin with the more efficientlythan those studied by highest level, A,. In a mechanically Ivlev. Since Moore's fisheswere fed on perfectfood cycle composed of organ- a highlyconcentrated food (liver), this ically discretelevels, this loss by preda- greater growth efficiencyis not sur- tion obviouslywould be zero. Since no prising. If the maximum growth effi- natural food cycle is so mechanically growth constituted,some "cannibalism" within would occur when ciency assimilationasmlti such an arbitrarylevel can be expected, = 60-70 per cent (AEE of Needham, so that the actual value for predation '31), the AEE of Moore's data (about loss fromAn probably will be somewhat 50 per cent) indicatesthat the minimum above zero. The predation loss from respiratorycoefficient with respect to level A,,- will representthe total amount growthmight be as low as 100 per cent of assimilable energypassed on into the forcertain fishes. Food-conversiondata higherlevel (i.e., the true productivity, from Thompson ('41) indicate a mini- X.), plus a quantity representingthe mum respiratorycoefficient of less than average,content of substance killed but 150 per cent foryoung black bass (Huro not assimilated by the predator,as will salmoides) at 70? F., the exact percent- be discussed in the followingsection. age depending upon how much of the The predation loss fromlevel An-2 will ingestedfood (minnows)was assimilated. likewise representthe total amount of Krogh ('41) showedthat predatoryfishes assimilableenergy passed on to the next October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 405 level (i.e., X,-l) plus a similar factor for saprophages, whose metabolic products unassimilatedmaterial, as illustratedby provide simple inorganic and organic the data of tables II and III. The solutes reavailable to photosynthetic various categoriesof parasites are some- producers. These saprophagesmay also what comparable to those of predators, serve as energy sources for successive but the details of theirenergy relation- levels of consumers,often considerably ships have not yet been clarified,and supplementingthe normal diet of herbi- cannot be included in this preliminary vores (ZoBell and Feltham, '38). Jacot account. ('40) considered saprophage-feedingor Decomposition corrections.- In con- coprophagousanimals as "low" primary formitywith the principleof Le Chate- consumers,but the writerbelieves that lier, the energyof no food level can be in the presentstate of our knowledgea completelyextracted by the organisms quantitativesubdivision of primarycon- which feed upon it. In addition to the sumersis unwarranted. energyrepresented by organismswhich Application.-The value of these the- survive to be included in the "annual oreticalenergy relationships can be illus- yield," much energy is contained in trated by analyzing data of the three "killed" tissues which the predatorsare ecosystemsfor which relativelycompre- unable to digest and assimilate. Aver- hensive productivityvalues have been age coefficientsof indigestible tissues, published (table I). The summaryac- based largelyof the calorificequivalents TABLE I. Productivities of food-groups in of the "crude fiber" fractions in the threeaquatic ecosystems,as g-callcm2Iyear,uncor- chemical analyses of Birge and Juday rectedfor losses due to respiration,predation and decomposition. Data fromBrujewicz ('39), Juday ('22), are as follows: ('40) and Lindeman ('41b). Nannoplankters...... ca. 5 % Algal mesoplankters. . 5-35% Casp ian Lake Cedar 5eapa Men- Bog Mature pondweeds. ca. 20% Sa dota Lake Primary consumers...... ca. 10% Phytoplankters:A...... 59.5 299 25.8 Secondary consumers.... ca. 8% Phytobenthos:Al...... 0.3 22 44.6 Predatory fishes.... ca. 5% Zooplankters:A2...... 20.0 22 6.1 Benthicbrowsers: A2 ...... 1.8* 0.8 Benthicpredators: A3...... 20.6 0.9* 0.2 Corrections for terrestrial producers Planktonpredators: A3. .J.. . .0.8 "Forage" fishes:A3(+A2?) .... . 0.6 ? 0.3 would certainly be much higher. Al- Carp: A3(+A2?)...... 0.0 0.2 0.0 "Game" fishes:A4(+A3?) . 0.... . 0 6 0.1 0.0 though the data are insufficientto war- Seals: As...... 0.01 0.0 0.0 ranta generalization,these values suggest increasingdigestibility of the higherfood * Roughly assuming that 2M of the bottom fauna is herbivorous levels, particularlyfor the benthic com- (cf. Juday, '22). ponentsof aquatic cycles. count of Brujewicz ('39) on "the dy- The loss of energydue to premature namics of living matter in the Caspian death fromnon-predatory causes usually Sea" leaves much to be desired, as must be neglected,since such losses are bottom animals are not differentiated exceedingly difficultto evaluate and into their relative food levels, and the undernormal conditions probably repre- basis for determiningthe annual pro- sent relativelysmall componentsof the duction of phytoplankters(which on annual production. However, consider- theoreticalgrounds appears to be much ing that these losses may assume con- too low) is not clearly explained. Fur- siderable proportionsat any time, the thermore,his values are stated in terms above "decompositioncoefficients" must of thousands of tons of dry weight for be regardedas correspondinglyminimal. the Caspian Sea as a whole, and must Following non-predateddeath, every be roughlytransformed to calories per organismis a potentialsource of energy square centimeterof surfacearea. The for myriads of bacterial and fungal data for Lake Mendota, Wisconsin,are 406 RAYMOND L. LINDEMAN Ecology,Vol. 23,No. 4

taken directlyfrom a general summary TABLE III. Productivityvalues for the Lake Mendotafood cycle,in g-cal/cm2/year,as corrected (Juday, '40) of the many productivity by using coefficientsderived in the precedingsec- studies made on that eutrophic lake. tions,and as givenby Juday ('40). The data forCedar Bog Lake, Minnesota, are taken from the author's four-year Uncor- De Cor- Juday's D- cor- . S __-Srected Res-. .s Pre-r.. rectedlcl* rected analysis (Lindeman, '41b) of its food- TrophicLevel pro- pira- da- comp~- recte cycle dynamics. The calorificvalues in duction tion ppi pro- pro- tivity table I, representingannual production tion~~~~tiit Producers: Al. 321* 107 42 10 480 428 of organic matter, are uncorrectedfor Primary consumers: A2. 24 15 2.3 0.3 41.6 144 energylosses. Secondary consumers: TABLE II. Productivityvalues for the Cedar A3...... it 1 0.3 0.0 2.3 6 Tertiarycon- Bog Lake food cycle,in g-cal/cm2/year,as corrected sumers: A4. 0.12 0.2 0.0 0.0 0.3 0.7 by using the coefficientsderived in the preceding sections. * Hutchinson ('42) gives evidence that this value is probably too high and may actually be De- Cor- as low as 250. Rnorctd 1es- Pre- co -rected Trophic level pi da- corn-pro- t Apparentlysuch organismsas small " forage" productivityprdciiytion duc- tionPsltion fishes are not included in any part of Juday's tivity balance sheet. The inclusion of these forms might be expected to increase considerably the Producers:yA 70.4?i 10.14 23.4 14.8 2.8 111.3 productivityof secondary consumption. Primary consumers: A2 7.0 ? 1.07 4.4 3.1 0.3 14.8 Secondary ing-capacity"of lakes containingmostly consumers: A3 1.3?0.43* 1.8 0.0 0.0 3.1 carp and other"coarse" fishes(primarily A3), was about 500 per cent that of lakes * This value includes the productivityof the small cyprinoidfishes found in the lake. containing mostly "game" fishes (primarily A4), and concluded that "this Correctingfor the energy losses due differencemust be about one complete to respiration,predation and decomposi- link in the food chain, since it usually tion, as discussed in the precedingsec- requires about five pounds of food to tions,casts a very differentlight on the produceone pound of fish." While such relative productivities of food levels. high "metabolic losses" may hold for The calculation of correctionsfor the tertiaryand quaternarypredators under Cedar Bog Lake values for producers, certain field conditions,the physiologi- primaryconsumers and secondary con- cal experimentspreviously cited indi- sumersare givenin table II. The appli- cate much lower respiratorycoefficients. cationof similar corrections to theenergy Even when predationand decomposition values for the food levels of the Lake correctionsare included, the resultant Mendota food cycle given by Juday productivityvalues are less than half ('40), as shown in table III, indicates those obtained by using Juday's coeffi- that Lake Mendota is much more pro- cient. Since we have shown that the ductive of producersand primarycon- necessarycorrections vary progressively sumers than is Cedar Bog Lake, while with the differentfood levels, it seems the productionof secondary consumers probable that Juday's "coefficientof is of the same orderof magnitudein the metabolism" is much too high for pri- two lakes. mary and secondaryconsumers. In calculating total productivityfor Lake Mendota, Juday ('40) used a Biological efficiency blanket correctionof 500 per cent of the annual productionof all consumerlevels The quantitative relationshipsof any for"metabolism," which presumablyin- food-cycle level may be expressed in cludes both respirationand predation. terms of its efficiencywith respect to Thompson ('41) found that the "carry- lowerlevels. QuotingHutchinson's ('42) October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 407

definition,"the efficiencyof the produc- of the Lake Mendota productivities,no tivity of any level (An) relative to the definiteconclusions can be drawn from productivityof any previous level (Am) their relative efficiencies. The Cedar Bog Lake ratios, however,indicate that is definedas - 100. If the rate of solar Xm the progressiveefficiencies increase from energyentering the ecosystemis denoted about 0.10 per cent for production,to as Xo,the efficienciesof all levels may be 13.3 per cent for primaryconsumption, referredback to this quantity Xo." In and to 22.3 per cent for secondary con- general, however, the most interesting sumption. An uncorrectedefficiency of efficienciesare those referredto the pre- tertiaryconsumption of 37.5 per cent vious level's productivity(XA1) or those ?t 3.0 per cent (for the weight ratios of "carnivorous" to "forage" fishesin Ala- expressedas 100. These lattermay bama ponds) is indicated in data pub- X~n-1 be termed the progressiveefficiencies of lished by Swingle and Smith ('40). the various food-cyclelevels, indicating These progressivelyincreasing efficiencies for each level the degree of utilization maywell representa fundamentaltrophic of its potential food supply or energy principle,namely, that the consumersat source. All efficienciesdiscussed in the progressivelyhigher levels in the food following pages are progressive effi- cycle are progressivelymore efficientin ciencies, expressed in terms of relative the use of theirfood supply. At firstsight, this generalization of productivities 100). It is impor- increasingefficiency in higherconsumer X~n-1 groups would appear to contradict the tant to remember that efficiencyand previous generalizationthat the loss of productivityare not synonymous. Pro- energydue to respirationis progressively ductivityis a rate (i.e., in the units here greater for higher levels in the food used, cal/cm2/year),while efficiency,be- cycle. These can be reconciled by re- ing a ratio, is a dimensionlessnumber. membering that increased activity of The pointsof referencefor any efficiency predators considerably increases the value should always be clearlystated. chances of encounteringsuitable prey. /Xn The progressiveefficiencies 12 1001 The ultimateeffect of such antagonistic Xn-1 / principleswould present a picture of a forthe trophiclevels of Cedar Bog Lake predator completely wearing itself out and Lake Mendota, as obtained from in the process of completely extermi- the productivitiesderived in tables II natingits prey,a very improbablesitua- and III, are presentedin table IV. In tion. However, Elton ('27) pointedout view ofthe uncertaintiesconcerning some that food-cyclesrarely have more than TABLE IV. Productivities and progressive effi- five trophic levels. Among the several ciencies in the Cedar Bog Lake and Lake factors involved, increasing respiration Mendotafood cycles,as g-cal/cm2/year of successive levels of predators contrastedwith theirsuccessively increasing Cedar Bog Lake Lake Mendota efficiencyof predation appears to be

Produc- Effi- Produc- Effi- importantin restrictingthe number of tivity ciency tivity ciency trophiclevels in a food cycle. Radiation ...... < 118,872 118,872 The effectof increasing temperature Producers: Al...... 111.3 0.10% 480* 0.40% Primary consumers: is alleged by Wimpenny('41) to cause a A2 .14.8 13.3% 41.6 8.7% Secondary decreasingconsumer/producer ratio, pre- consumers: A3.... 3.1 22.3% 2.3t 5.5% Tertiary sumably because he believes that the consumers: A4.... - - 0.3 13.0% "acceleration of vital velocities" of con- * Probably too high; see footnoteof table III. sumers at increasing temperatures is t Probably too low; see footnote of table III. more rapid than that of producers. He 408 RAYMOND L. LINDEMAN Ecology,Vol. 23,No. 4

cites as evidence Lohmann's ('12) data at the base of a food-chainare relatively for relative numbers (not biomass) of abundant while those towardthe end are Protophyta, Protozoa and Metazoa in progressivelyfewer in number. The re- the centrifugeplankton of "cool" seas sulting arrangementof sizes and num- (741:73:1) as contrasted with tropical bers of animals, termed the pyramidof areas (458:24:1). Since Wimpennyhim- Numbers by Elton, is now commonly self emphasizes that many metazoan known as the Eltonian Pyramid. Wil - planktersare larger in size toward the liams ('41), reporting on the "floor poles, these data do not furnishcon- fauna" of the Panama rain forest,has vincing proof of the allegation. The recently published an interesting ex- data given in table IV, since Cedar Bog ample of such a pyramid, which is Lake has a much higher mean annual reproducedin figure2. water temperaturethan Lake Mendota, The Eltonian Pyramid may also be appear to contradictWimpenny's gener- expressed in terms of biomass. The alization that consumer/producerratios weight of all predatorsmust always be fall as the temperatureincreases. muchlower than that of all food animals, and the total weight of the latter much The Eltonian pyramid lowerthan the plant production(Boden- heimer, '38). To the human ecologist, The general relationships of higher it is noteworthythat the populationden- food-cyclelevels to one another and to sityof theessentially vegetarian Chinese, communitystructure were greatlyclari- for example, is much greater than that fied followingrecognition (Elton, '27) of the more carnivorousEnglish. of the importanceof size and of numbers The principle of the Eltonian Pyra- in the animals of an ecosystem. Begin- mid has been redefinedin termsof pro- ning with primaryconsumers of various ductivity by Hutchinson (unpublished) sizes, there are as a rule a number of in the followingformalized terms: the food-chainsradiating outwards in which rate of production cannot be less and the probabilityis that predatorswill be- will almost certainlybe greaterthan the come successivelylarger, while parasites rate of primaryconsumption, which in and hyper-parasiteswill be progressively turn cannot be less and will almost cer- smaller than their hosts. Since small tainlybe greaterthan the rate of second- primary consumers can increase faster ary consumption,which in turn . . . than largersecondary consumers and are etc. The energy-relationshipsof this so able to supportthe latter,the animals principlemay be epitomized by means

SIZE RANGE IN Mm 1314 12-13.4 11-12' 810-1

7-4

5F7X

3-4

NUMBERor AmI ALs

FIG. 2. Eltonian pyramid of numbers, for floor-faunainvertebrates of the Panama rain forest (fromWilliams, '41). October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 409 of the productivitysymbol X, as follows: fluenceof some combinationof limiting factors,which, until they are overcome Xo > X1 > X2 . . . > Xn. by species-substitution,etc., tend to This rather obvious generalization is decrease the accelerationof productivity confirmedby the data of all ecosystems and maintainit at a moreconstant rate. analyzed to date. This tendencytowards stage-equilibrium of productivitywill be discussed in the followingpages. TROPHIc-DYNAMICS IN SUCCESSION Dynamic processes within an ecosys- Productivityin hydrarchsuccession tem, over a period of time, tend to produce certain obvious changes in its The descriptivedynamics of hydrarch species-composition,soil characteristics succession is well known. Due to the and productivity. Change,according to essentially concave nature of the sub- Cooper ('26), is the essentialcriterion of stratum, lake succession is internally succession. From the trophic-dynamic complicated by a rather considerable viewpoint, succession is the process of influxof nutritivesubstances from the development in an ecosystem,brought drainage basin surrounding the lake. about primarilyby the effectsof the The basins of lakes are gradually filled organismson the environmentand upon withsediments, largely organogenic, upon each other, towards a relativelystable which a series of vascular plant stages conditionof equilibrium. successivelyreplace one another until a It is well known that in the initial more or less stable (climax) stage is phases of hydrarch succession (oligo- attained. We are concernedhere, how- trophy -> eutrophy) productivity in- ever, primarilywith the productivity creases rapidly; it is equally apparent aspects of the successionalprocess. that the colonizationof a bare terrestrial Eutrophication.- Thienemann ('26) area representsa similaracceleration in presented a comprehensivetheoretical productivity. In the later phases of discussion of the relation between lake succession, productivityincreases much succession and productivity,as follows: more slowly. As Hutchinsonand Wol- In oligotrophy,the pioneer phase, pro- lack ('40) pointed out, these generalized ductivity is rather low, limited by the changes in the rate of productionmay amountof dissolvednutrients in the lake be expressedas a sigmoidcurve showing water. Oxygenis abundant at all times, a roughresemblance to the growthcurve almost all of the synthesized organic of an organism or of a homogeneous matteris available foranimal food; bac- population. teria releasedissolved nutrientsfrom the Such smoothlogistic growth, of course, remainder. Oligotrophythus has a very is seldom found in natural succession, "thrifty"food cycle, with a relatively except possibly in such cases as bare high "efficiency"of the consumerpopu- areas developing directlyto the climax lations. With increasinginflux of nutri- vegetationtype in the wake of a retreat- tivesfrom the surrounding drainage basin ingglacier. Most successionalseres con- and increasingprimary productivity (X1), sist of a numberof stages("recognizable, oligotrophyis graduallychanged through clearly-markedsubdivisions of a given mesotrophyto eutrophy,in which con- sere"-W. S. Cooper), so that their dition the productionof organic matter productivitygrowth-curves will contain (X1)exceeds that which can be oxidized undulationscorresponding in distinctness (X1')by respiration,predation and bacte- to the distinctnessof the stages. The rial decomposition. The oxygensupply presenceof stages in a successional sere of the hypolimnionbecomes depleted, apparently representsthe persistentin- withdisastrous effects on the oligotroph- 410 RAYMOND L. LINDEMAN Ecology,Vol. 23,No.4

conditioned bottom fauna. Organisms quantitative value for lakes with com- especially adapted to endure temporary parable edaphic nutrientsupplies being anaerobiosisreplace the oligotrophicspe- dependent on the morphometry(mean cies, accompanied by anaerobic bacteria depth). Since deep lakes have a greater whichduring the stagnationperiod cause depth range for plankton photosynthe- reduction rather than oxidation of the sis, abundant oxygen and more chance organic detritus. As a result of this fordecomposition of the planktondetri- process, semi-reducedorganic ooze, or tus before reaching the bottom, such gyttja,accumulates on the bottom. As deep lakes may be potentially as pro- oxygen supply thus becomes a limiting ductive as shallower lakes, in terms of factorof productivity,relative efficiency unit surface area. Factors tending to of the consumergroups in utilizingthe lessen the comparative productivityof synthesizedorganic substance becomes deep lakes are (1) lower temperaturefor correspondinglylower. the lake as a whole, and (2) greater The validity of Thienemann's inter- dilutionof nutrientsin termsof volume pretation, particularly regarding the of the illuminated"trophogenic zone" of trophic mechanisms,has recentlybeen the lake. During eutrophicationin a challengedby Hutchinson('41, '42), who deep lake, the phosphoruscontent of the states that three distinct factors are sedimentfalls and nitrogenrises, until a involved: (1) the edaphic factor,repre- N/P ratio of about 40/1 is established. senting the potential nutrient supply "The decompositionof organic matter (primarilyphosphorus) in the surround- presumablyis always liberatingsome of ing drainage basin; (2) the age of the this phosphorusand nitrogen. Within lake at any stage, indicatingthe degree limits,the more organic matter present of utilizationof the nutrientsupply; and the easier will be such regeneration. It (3) the morphometriccharacter at any is probable that benthic animals and stage, dependent on both the original anion exchange play a part in such morphometryof the lake basin and the processes" (Hutchinson,'42). The pro- age of the lake, and presumablyinflu- gressive fillingof the lake basin with encing the oxygen concentrationin the sedimentsmakes the lake shallower,so hypolimnion. He holds that true eu- that the oxygen supply of the hypo- trophicationtakes place only in regions limnionis increasingly,and finallycom- well supplied with nutrients,lakes in pletely,exhausted during summerstag- otherregions developing into "ideotrophic nation. Oxidation of the sediments is types." The influx of phosphorus is less complete,but sufficientphosphorus probablyvery great in theearliest phases, is believed to be regeneratedfrom the much greater than the supply of nitro- ooze surface so that productivity in gen, as indicatedby very low N/P ratios termsof surfacearea remainsrelatively in the earliest sediments (Hutchinson constant. The nascent ooze acts as a and Wollack, '40). A large portion of trophic buffer,in the chemical sense, this phosphorus is believed to be in- tendingto maintain the productivityof soluble, as a componentof such mineral a lake in stage-equilibrium(typological particles as apatite, etc., although cer- equilibriumof Hutchinson) during the tainlysome of it is soluble. The supply eutrophicstage of its succession. of available nitrogenincreases somewhat The concept of eutrophicstage-equi- more slowly, being largely dependent librium seems to be partially confused upon the fixationof nitrogenby micro- (cf..Thienemann, '26; Hutchinson and organismseither in the lake or in the Wollack, '40) withthe theoreticallyideal surroundingsoils. The photosynthetic conditionof completetrophic equilibrium, productivity(X1) of lakes thus increases which may be roughly defined as the rather rapidly in the early phases, its dynamic state of continuous, complete October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 411

utilizationand regenerationof chemical energywhich is lost fromthe food cycle, nutrientsin an ecosystem,without loss is derivedlargely from level A1,as plant or gain fromthe outside, under a peri- structures in general are decomposed odically constantenergy source-such as less easily than animal structures. The might be found in a perfectlybalanced quantity of energypassed on into con- aquarium or terrarium. Natural eco- sumer levels can only be surmisedfrom systemsmay tend to approach a state of undecomposed fragmentsof organisms trophic equilibrium under certain con- whichare believedto occupy thoselevels. ditions, but it is doubtful if any are Several types of animal "microfossils" sufficientlyautochthonous to attain, or occur rather consistentlyin lake sedi- maintain, true trophic equilibrium for ments,such as the carapaces and post- any lengthof time. The biosphereas a abdomensof certaincladocerans, chiron- whole, however,as Vernadsky ('29, '39) omid head-capsules, fragmentsof the so vigorouslyasserts, may exhibita high phantom-midgelarva Chaoborus, snail degreeof true trophicequilibrium. shells,polyzoan statoblasts,sponge spic- The existence of prolongedeutrophic ules and rhizopodshells. Deevey ('42), stage-equilibriumwas firstsuggested as after making comprehensivemicrofossil a result of a study on the sedimentsof and chemicalanalyses of thesediments of Grosser Pl6ner See in Germany (Gro- Linsley Pond, suggested that the abun- schopf,'36). Its significancewas recog- dant half-carapaces of the planktonic nized by Hutchinsonand Wollack ('40), browser Bosmina afford "a reasonable who based their critical discussion on estimate of the quantity of zooplankton chemical analyses (ibid.) and pollen produced" and that "the total organic analyses (Deevey, '39) of the sediments matter of the sediment is a reasonable of Linsley Pond, Connecticut. They estimateof the organicmatter produced reporteda gradual transitionfrom oligo- by phytoplanktonand littoral vegeta- trophyto eutrophy(first attained in the tion." He found a strikingsimilarity oak-hemlock pollen period), in which in the shape of the curves representing stage the lake has remained for a very Bosmina contentand total organic mat- long time,perhaps more than 4000 years. ter plotted against depth, which, when They reportindications of a comparable plotted logarithmically against each eutrophicstage-equilibrium in the sedi- other, showed a linear relationshipex- ments of nearby Upper Linsley Pond pressedby an empiricalpower equation. (Hutchinsonand Wollack, unpublished). Citing Hutchinsonand Wollack ('40) to Similar attainmentof stage-equilibrium the effectthat the developmentalcurve is indicated in a preliminaryreport on fororganic matter was analogous to that the sediments of Lake Windermerein for the developmentof an organism,he England (Jenkin, Mortimer and Pen- pressed the analogy furtherby suggest- nington, '41). Every stage of a sere ing that the increase of zooplankton is believed to possess a similar stage- (Bosmina) with referenceto the increase equilibrium of variable duration, al- of organicmatter (Xi) fittedthe formula though terrestrialstages have not yet y = bxkfor allometricgrowth (Huxley, been definedin termsof productivity. '32), "where y = Bosmina, x = total The trophicaspects of eutrophication organic matter, b = a constant giving cannot be determinedeasily from the the value of y when x = 1, and k = the sediments. In general, however, the 'allometryconstant,' or the slope of the ratio of organicmatter to the silt washed line when a double log plot is made." into the lake from the margins affords If we representthe organic matter pro- an approximationof the photosynthetic duced as Xi and furtherassume that productivity. This undecomposed or- Bosmina represents the primary con- ganic matter,representing the amountof sumers(X2), neglectingbenthic browsers, 412 RAYMOND L. LINDEMAN Ecology,Vol. 23,No. 4

the formulabecomes X2 = bXlk. Whether continuing,at a rate correspondingto this formulawould expressthe relation- the rate of sedimentaccumulation. In ship found in other levels of the food the words of Hutchinson and Wollack cycle, the developmentof other stages, ('40), "this means that duringthe equi- or otherecosystems, remains to be dem- librium period the lake, through the onstrated.6 Stratigraphic analyses in internal activities of its biocoenosis, is Cedar Bog Lake (Lindeman and Linde- continuallyapproaching a conditionwhen man, unpublished) suggest a roughly it ceases to be a lake." similar increase of both organic matter Senescence.-As a result of long-con- and Bosmina carapaces in the earliest tinued sedimentation, eutrophic lakes sediments. In the modern senescent attain senescence, first manifested in lake, however,double logarithmicplot- bays and wind-protectedareas. Senes- tingsof the calorificvalues forXi against cence is usually characterizedby such X2, and X2 againstX3, forthe fouryears pond-like conditionsas (1) tremendous studied, show no semblance of linear increase in shallow littoral area popu- relationship,i.e., do not fit any power lated with pondweeds and (2) increased equation. If Deevey is correct in his marginal invasion of terrestrialstages. interpretationof the LinsleyPond micro- Cedar Bog Lake, which the author has fossils,allometric growth would appear studied forseveral years,is in late senes- to characterizethe phases of pre-equilib- cence, rapidlychanging to the terrestrial rium succession as the term "growth" stages of its succession. On casual indeed implies. inspection,the massed verdureof pond- The relative duration of eutrophic weeds and epiphytes,together with spo- stage-equilibriumis not yet completely radic algal blooms, appears to indicate understood. As exemplifiedby Linsley great photosyntheticproductivity. As Pond, the relation of stage-equilibrium pointed out by Wesenberg-Lund ('12), to succession is intimately concerned littoral areas of lakes are virtual hot- with the trophicprocesses of (1) external houses, absorbing more radiant energy influxand efflux(partly controlled by per unit volume than deeper areas. At climate), (2) photosyntheticproductiv- the presenttime the entireaquatic area ity, (3) sedimentation(partly by physio- of Cedar Bog Lake is essentiallylittoral graphic silting) and (4) regenerationof in nature,and its productivityper cubic nutritives from the sediments. These meterof water is probably greaterthan processes apparently maintain a rela- at any time in its history. However, tivelyconstant ratio to each otherduring since radiant energy (Xo) enters a lake the extended equilibrium period. Yet only fromthe surface,productivity must the foodcycle is not in truetrophic equi- be definedin termsof surfacearea. In librium, and continues to fill the lake these terms,the presentphotosynthetic with organic sediments. Succession is productivity pales into insignificance when comparedwith less advanced lakes 6 It should be mentioned in this connection in that Meschkat ('37) found that the relationship similar edaphic regions; for instance, of population density of tubificids to organic X1is less than 13 that of Lake Mendota, matter in the bottom of a polluted "Buhnen- Wisconsin (cf. table IV). These facts feld" could be expressed by the formulay = a-, attest the essential accuracy of Welch's where y represents the population density, x is ('35) generalization the "determining environmentalfactor," and a that productivity is a constant. He pointed out that for such an declines greatly duringsenescence. An expression to hold the population density must interesting principle demonstrated in be maximal. Hentschel ('36), on less secure Cedar Bog Lake (Lindeman, '41b) is grounds,suggested applying a similar expression that late to the relationship between populations of ma- during lake senescencegeneral rine plankton and the "controlling factor" of productivity (X,) is increasinglyinflu- their environment. enced by climaticfactors, acting through October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 413

water level changes, drainage, duration thus subject to a certainnutrient loss by of winterice, snow cover, etc., to affect erosion,which may or may not be made the presence and abundance of practi- up by increased availability of such cally all food groups in the lake. nutrientsas can be extracted from the Terrestrialstages.-As an aquatic eco- "C" soil horizon. system passes into terrestrialphases, Successional productivitycurves.-In fluctuationsin atmospheric factors in- recapitulating the probable photosyn- creasingly affect its productivity. As thetic productivityrelationships in hy- succession proceeds, both the species- drarch succession, we shall venture to compositionand the productivityof an diagram (figure3) a hypotheticalhydro- ecosystemincreasingly reflect the effects sere,developing from a moderatelydeep of the regional climate. Qualitatively, lake in a fertilecold temperate region these climatic effectsare known for soil underrelatively constant climatic condi- morphology(Joffe, '36), autotrophicvege- tions. The initial period of oligotrophy tation (Clements, '16), fauna (Clements is believed to be relativelyshort (Hutch- and Shelford, '39) and soil microbiota inson and Wollack, '40; Lindeman (Braun-Blanquet, '32), in fact forevery '41a), with productivityrapidly increas- importantcomponent of the food cycle. ing until eutrophicstage-equilibrium is Quantitatively,these effectshave been attained. The duration of high eu- so little studied that generalizationsare trophic productivitydepends upon the most hazardous. It seems probable, mean depth of the basin and upon the however, that productivity tends to rate of sedimentation,and productivity increase until the system approaches fluctuatesabout a high eutrophicmean maturity. Clements and Shelford ('39, until the lake becomes too shallow for p. 116) assertthat both plant and animal maximum growth of phytoplanktonor productivityis generallygreatest in the regenerationof nutrientsfrom the ooze. subclimax,except possiblyin the case of As the lake becomes shallowerand more grasslands. Terrestrial ecosystems are senescent, productivity is increasingly primarily convex topographically and influencedby climatic fluctuationsand

/ EUTROPHY AE / CLIMA

I- ~~~~~~~~~~~~BOFOREST

0. MAT

UOGOTROPHY SENESCENCE TIME -> FIG. 3. Hypothetical productivity growth-curveof a hydrosere,developing from a deep lake to climax in a fertile,cold-temperate region. 414 RAYMOND L. LINDEMAN Ecology,Vol. 23,No. 4

gradually declines to a minimumas the original observations,but are probably lake is completelyfilled with sediments. of the correctorder of magnitude. The The terrestrialaspects of hydrarch mean photosyntheticefficiency for the succession in cold temperate regions sea is given as 0.31 per cent (afterRiley, usually follow sharply defined,distinc- '41). The mean photosynthetic effi- tive stages. In lake basins which are ciency for terrestrialareas of the earth poorly drained, the firststage consists is given as 0.09 per cent ? 0.02 per cent of a mat, oftenpartly floating, made up (afterNoddack, '37), for forestsas 0.16 primarilyof sedges and grasses or (in per cent, forcultivated lands as 0.13 per more coastal regions) such heaths as cent, for steppes as 0.05 per cent, and Chamaedaphneand Kalmia with certain fordeserts as 0.004 per cent. The mean species of sphagnummoss (cf. Rigg, '40). photosyntheticefficiency for the earth The mat stage is usually followedby a as a whole is given as 0.25 per cent. bog foreststage, in which the dominant Hutchinsonhas suggested (cf. Hutchin- species is Larix laricina, Picea mariana son and Lindeman, '41) that numerical or Thuja occidentalis. The bog forest efficiencyvalues may provide "the most stage may be relatively permanent fundamental possible classification of ("edaphic" climax) or succeeded to a biological formationsand of theirdevel- greater or lesser degree by the regional opmentalstages." climax vegetation. The stage-produc- Almost nothing is known concerning tivities indicated in figure3 represent the efficienciesof consumer groups in only crude relative estimates,as practi- succession. The general chronological cally no quantitativedata are available. increase in numbers of Bosmina carapaces with respectto organicmatter and Efficiencyrelationships in succession of Chaoborusfragments with respect to Bosmina carapaces in the sedimentsof The successionalchanges of photosyn- Linsley Pond (Deevey, '42) suggests thetic efficiencyin natural areas (with progressivelyincreasing efficienciesof respect to solar radiation, i.e., Xi 100 zooplankters and plankton predators. On the other hand, Hutchinson ('42) have not been intensivelystudied. In concludesfrom a comparisonof the P: Z lake succession,photosynthetic efficiency (phytoplankton: zooplankton) biomass would be expected to follow the same ratiosof several oligotrophic alpine lakes, course deduced for productivity,rising ca 1: 2 (Ruttner,'37), as comparedwith to a more or less constant value during the ratios for Linsley Pond, 1: 0.22 eutrophicstage-equilibrium, and declin- (Riley, '40) and three eutrophic Bava- ing duringsenescence, as suggestedby a rian lakes, 1: 0.25 (Heinrich, '34), that photosyntheticefficiency of at least 0.27 "as the phytoplanktoncrop is increased per cent for eutrophic Lake Mendota the zooplanktonby no means keeps pace (Juday, '40) and of 0.10 per cent for with the increase." Data compiled by senescent Cedar Bog Lake. For the Deevey ('41) for lakes in both meso- terrestrialhydrosere, efficiencywould trophic (Connecticut) and eutrophic likewise follow a curve similar to that regions (southern Wisconsin), indicate postulated forproductivity. that the deeper or morphometrically Rough estimates of photosynthetic "younger" lakes have a lower ratio of efficiencyfor various climatic regionsof bottom fauna to the standing crop of the earth have been summarized from plankton (10-15 per cent) than the the literature by Hutchinson (unpub- shallower lakes which have attained lished). These estimates,corrected for eutrophicequilibrium (22-27 per cent). respiration,do not appear to be very The ratiosfor senescent Cedar Bog Lake, reliable because of imperfectionsin the while not directly comparable because October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 415

of its essentiallylittoral nature, are even sumers,secondary consumers, etc., each higher. These meagerdata suggestthat successivelydependent upon the preced- the efficienciesof consumergroups may ing level as a source of energy,with the increase throughoutthe aquatic phases producers (A1) directlydependent upon of succession. the rate of incidentsolar radiation (pro- For terrestrialstages, no consumer ductivityX0) as a source of energy. efficiencydata are available. A sug- 3. The more remote an organism is gestive series of species-frequenciesin fromthe initial source of energy (solar mesarch succession was published by radiation), the less probable that it will Vera Smith-Davidson ('32), which in- be dependentsolely upon the preceding dicated greatly increasing numbers of trophiclevel as a source of energy. arthropodsin successivestages approach- 4. The progressive energy relation- ing the regionalclimax. Since the pho- ships of the food levels of an "Eltonian tosyntheticproductivity of the stages Pyramid" may be epitomizedin termsof probably also increased,it is impossible the productivitysymbol X, as follows: to determineprogressive efficiency relationships. The problems of biological XO > Xl > X2. . . > Xn. efficienciespresent a practically virgin 5. The loss of field,which appears to offerabundant percentage energydue to respirationis progressively rewardsfor studies guided by a trophic- greaterfor higherlevels in dynamicviewpoint. the foodcycle. Respira- tion with respect to growthis about 33 per cent for producers,62 In conclusion,it should be emphasized per cent for primaryconsumers, and more that the trophic-dynamicprinciples indi- than 100 per cent for secondaryconsumers. cated in the followingsummary cannot 6. The consumers at be expectedto hold forevery single case, progressively higherlevels in the food cycle in accord with the known facts of bio- appear to be progressivelymore efficient in logical variability. a priori, however, the use of their food supply. This these principlesappear to be valid for generalization can be reconciledwith the the vast majorityof cases, and may be preceding one by rememberingthat expectedto possess a statisticallysignifi- increased ac- tivityof predators cant probabilityof validityfor any case considerablyincreases the chances of selectedat random. Since the available encountering suitable prey. data summarized in this paper are far 7. Productivityand efficiencyincrease too meager to establish such generaliza- during the early phases of successional tions on a statistical basis, it is highly development. In lake importantthat furtherstudies be initi- succession, productivity and photosynthetic ated to test the validity of these and efficiency increasefrom to a othertrophic-dynamic principles. oligotrophy prolonged eutrophicstage-equilibrium and decline with lake SUMMARY senescence,rising again in the terrestrialstages of hydrarchsuccession. 1. Analysesof food-cyclerelationships 8. The progressiveefficiencies of con- indicate that a biotic communitycannot sumerlevels, on the basis of very meager be clearly differentiatedfrom its abiotic data, apparentlytend to increasethrough- environment;the ecosystemis hence re- out the aquatic phases of succession. garded as the more fundamentaleco- logical unit. ACKNOWLEDGMENTS 2. The organismswithin an ecosystem may be grouped into a series of more or The author is deeply indebted to Professor G. less discrete trophic levels A2, E. Hutchinson of Yale University,who has (Al, A3, stimulated many of the trophic concepts devel- An) as producers, primary con- oped here, generously placed at the author's 416 RAYMOND L. LINDEMAN Ecology,Vol. 23,No. 4

disposal several unpublished manuscripts,given * 1941. Limnological studies in Connecti- valuable counsel, and aided the finaldevelopment cut: VI. The quantity and compositionof the of this paper in every way possible. Many of bottom fauna. Ecol. Monogr., 11: 413-455. the concepts embodied in the successional sec- * 1942. Studies on Connecticut lake sedi- tions of this paper were developed independently ments: III. The biostratonomy of Linsley by Professor Hutchinson at Yale and by the Pond. Amer. Jour. Sci., 240: 233-264, 313- author as a graduate student at the University 338. of Minnesota. Subsequent to an exchange of Elton, C. 1927. Animal Ecology. N. Y. notes, a joint preliminaryabstract was published Macmillan Co. (Hutchinson and Lindeman, '41). The author France, R. H. 1913. Das Edaphon, Unter- wishes to express gratitude to the mentors and suchungenzur Oekologie der bodenbewohnen- friends at the University of Minnesota who den Mikroorganismen. Deutsch. Mikrolog. encouraged and helpfully criticized the initial Gesellsch., Arbeit. aus d. Biol. Inst., No. 2. development of these concepts, particularlyDrs. Munich. W. S. Cooper, Samuel Eddy, A. C. Hodson, Friederichs, K. 1930. Die Grundfragen und D. B. Lawrence and J. B. Moyle, as well as Gesetzmassigkeiten der land- und forstwirt- other membersof the local Ecological Discussion schaftlichenZoologie. 2 vols. Berlin. Ver- Group. The author is also indebted to Drs. schlag. Paul Parey. J. R. Carpenter, E. S. Deevey, H. J. Lutz, Groschopf, P. 1936. Die postglaziale Ent- A. E. Parr, G. A. Riley and V. E. Shelford,as wicklung des Grosser Pl6ner Sees in Ost- well as the persons mentionedabove, for critical holstein auf Grund pollenanalytischerSedi- reading of preliminary manuscripts. Grateful mentuntersuchungen. Arch. Hydrobiol., 30: acknowledgmentis made to the Graduate School, 1-84. Yale University, for the award of a Sterling Heinrich, K. 1934. Atmung und Assimilation Fellowship in Biology during 1941-1942. im freien Wasser. Internat. Rev. ges. Hy- drobiol. u. Hydrogr., 30: 387-410. LITERATURE CITED Hentschel, E. 1933-1936. AllgemeineBiologie des SuidatlantischenOzeans. Wiss. Ergebn. Allee, W. C. 1934. Concerning the organiza- Deutsch. Atlant. Exped. a. d. Forschungs-u. tion of marine coastal communities. Ecol. Vermessungsschiff"Meteor" 1925-1927. Bd. Monogr., 4: 541-554. XI. Birge, E. A., and C. Juday. 1922. The inland Hicks, P. A. 1934. Interaction of factors in lakes of Wisconsin. The plankton. Part I. the growth of Lemna: V. Some preliminary Its quantity and chemical composition. Bull. observations upon the interaction of tem- Wisconsin Geol. Nat. Hist. Surv., 64: 1-222. perature and light on the growth of Lemna. Bodenheimer, F. S. 1938. Problems of Animal Ann. Bot., 48: 515-523. Ecology. London. OxfordUniversity Press. Hile, R. 1941. Age and growth of the rock Braun-Blanquet, J. 1932. Plant Sociology. bass A mbloplites rupestris (Rafinesque) in N. Y. McGraw-HillCo. Nebish Lake, Wisconsin. Trans. Wisconsin Brujewicz, S. W. 1939. Distribution and dy- Acad. Sci., Arts, Lett., 33: 189-337. namics of living matter in the Caspian Sea. Hutchinson, G. E. 1941. Limnological studies Compt. Rend. Acad. Sci. URSS, 25: 138-141. in Connecticut: IV. Mechanism of interme- Carpenter, J. R. 1939. The biome. Amer. diary metabolism in stratifiedlakes. Ecol. Midl. Nat., 21: 75-91. Monogr., 11: 21-60. 1940. The grassland biome. Ecol. . 1942. Recent Advances in Limnology Monogr., 10: 617-687. (in manuscript). Clements, F. E. 1916. Plant Succession. Car- and R. L. Lindeman. 1941. Biological negie Inst. Washington Publ., No. 242. efficiency in succession (Abstract). Bull. and V. E. Shelford. 1939. Bio-Ecology. Ecol. Soc. Amer., 22: 44. N. Y. John Wiley & Co. Cooper, W. S. 1926. The fundamentals of and Anne Wollack. 1940. Studies on vegetational change. Ecology, 7: 391-413.. Connecticut lake sediments: II. Chemical Cowles, H. C. 1899. The ecological relations analyses of a core fromLinsley Pond, North of the vegetation of the sand dunes of Lake Branford. Amer. Jour. Sci., 238: 493-517. Michigan. Bot. Gaz., 27: 95-391. Huxley, J. S. 1932. Problems of Relative Davidson, V. S. 1932. The effectof seasonal Growth. N. Y. Dial Press. variability upon animal species in a decidu- Ivlev, V. S. 1939a. Transformationof energy ous forest succession. Ecol. Monogr., 2: by aquatic animals. Internat. Rev. ges. 305-334. Hydrobiol. u. Hydrogr., 38: 449-458. Deevey, E. S. 1939. Studies on Connecticut . 1939b. Balance of energy in carps. lake sediments: I. A postglacial climatic chro- Zool. Zhurn. Moscow, 18: 303-316. nology for southern New England. Amer. Jacot, A. P. 1940. The fauna of the soil. Jour. Sci., 237: 691-724. Quart. Rev. Biol., 15: 28-58. October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 417

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