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 .
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 THE TROPHIC-DYNAMIC ASPECT OF ECOLOGY
RAYMOND L. LINDEMAN

OsbornZoological Laboratory,Yale University

Recentprogressin thestudyofaquatic 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 enunciatingcertain 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
by bio-ecologists
A chronologicalreview of the major reactionsare considered
to be the dynamic effectors of succession.
viewpointsguidingsynecologicalthought
The trophic-dynamic viewpoint, as
indicates the followingstages: (1) the
paper, emphasizes the
static species-distributionalviewpoint; adopted in this
(2) the dynamic species-distributional relationship of trophic or "energy-avail-
ing" relationships within thecommunity-
viewpoint,withemphasison successional
phenomena;and (3) the trophic-dynamic unit to the process of succession. From
either species-distri- this viewpoint, which is closely allied to
viewpoint. From
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 "oekologische Sicht" 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 cycle (cf.
"climax" (cf. Tutin, '41). The associ- ponentsof the lacustrine
ated animals would be "biotic factors" figure 1) for their very existence. Upon
of the plant environment, tending to further consideration of the trophic cycle,
limit or modifythe developmentof the the discriminationbetweenlivingorgan-
community"
aquatic plant communities. To a strict isms as parts of the "biotic
and dead organisms and inorganic nutri-
zoologist,on theotherhand,a lake would
tives as parts of the "environment"
seem to contain animal communities
The
roughlycoincidentwith the plant com- seems arbitrary and unnatural.
munities,althoughthe "associated vege- difficulty of drawing clear-cut lines be-
tween the living community and the non-
tation" would be consideredmerelyas a
part of the environment'of the animal living environment is illustratedby the
difficulty of determiningthe status of a
' The term habitatis used by certain ecologists slowly dying pondweed covered with
(Clements and Shelford, '39; Haskell, '40; T.
Park, '41) as a synonym for environment in the
periphytes,some of which are also con-
usual sense and as here used, although Park tinually dying. As indicatedin figure1,
points out that most biologistsunderstand" 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

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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 nutritivesub- cept of the ecosystemis believed by the
stance is so completelyintegratedthat 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
morebasic functionalorganization. TROPHIc DYNAMICS
This concept was perhaps first ex-
pressedby Thienemann('18), as a result relationships
Qualitativefood-cycle
of his extensive limnologicalstudies on
thelakes ofNorthGermany. Allee ('34) Althoughcertainaspects of food rela-
expresseda similarview, stating: "The tions have been known for centuries,
picturethan finallyemerges . . . is of a many processes within ecosystems are
sort of superorganismicunity not alone stillveryincompletelyunderstood. The
betweenthe plants and animals to form basic process in trophicdynamicsis the
bioticcommunities,but also betweenthe transferof energy from one part of
biota and the environment." Such a the ecosystemto another. All function,
conceptis inherentin the termecosystem, and indeed all life,withinan 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 thisincidentenergyis 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),includingnot only the introducedby Thienemann ('26), auto-
organism-complex,but also the whole trophic plants are producerorganisms,
complexof physicalfactorsforming what employingtheenergyobtainedby 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 thispotentialenergyin cata-
of the earth.. . . These ecosystems, as bolic processes,a greatsurplusoforganic
we may call them,are of the most vari- substanceis accumulated. Animalsand
ous kinds and sizes. They form one heterotrophicplants,as consumerorgan-
category of the multitudinousphysical isms, feed upon this surplusof potential
systems of the universe, which range energy,oxidizinga considerableportion
fromthe universe as a whole down to of the consumed substance to release
the atom." Tansley goes on to discuss kineticenergyformetabolism,but trans-
the ecosystem as a category of rank formingthe remainderinto the complex
equal to the "biome" (Clements, '16), chemicalsubstancesof 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 energyfor saproph-
"community." The ecosystemmay be agous organisms (feeding directly on
formallydefinedas the systemcomposed dead tissues), which again may act as
of physical-chemical-biological processes energysources for successive categories
active within a space-time unit of any of consumers. Heterotrophic bacteria
2 The ecological system composed of the " bio-
and fungi, representingthe most im-
coenosis + biotop " has been termedthe holocoen
portant saprophagous consumption of
by Friederichs('30) and the biosystemby Thiene- energy,may be convenientlydifferenti-
mann ('39). ated fromanimal consumersas special-

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October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 401

j
SolarRadiation SolarRadiation

A
External

Dissolved
Nutrients
N

Internal

A, PhytoplanKters / Pandweids

Bacteria >
2 tZooplantkters~z OOZ Brawsers--4- -*

-N -
\/'l X

A3 OmPmdoos BenicPmaW
k A3

A3G
gQ
1 Geerlaized Predatorsn Betd
od-yl Predators
S~~~~~~wimfnii
redainhp aftors A3dman
A
AIG. na4

ized decomposers3 of organic substance. solved nutrientsonce more in resynthe-

Waksman ('41) has suggested that cer-
tain of these bacteria be furtherdiffer-
entiated as transformers of organic and
inorganic compounds. The combined
action of animal consumersand bacterial
decomposerstends to dissipate the po-
tential energy of organic substances,
again transforming themto the inorganic
state. From this inorganic state the
autotrophicplants may utilize the dis-
3 Thienemann ('26) proposed the termreducers
forthe heterotrophicbacteria and fungi,but this
term suggests that decomposition is produced
solely by chemical reduction rather than oxida-
tion, which is certainlynot the case. The term
decomposersis suggested as being more appro-
priate.
sizing complex organic substance, thus
completingthe food cycle.
The careful study of food cycles re-
veals an intricate pattern of trophic
predilectionsand substitutionsunderlain
by certainbasic dependencies;food-cycle
diagrams, such as figure1, attempt to
portray these underlyingrelationships.
In general,predatorsare less specialized
in food habits than are theirprey. The
ecological importanceof this statement
seems to have been firstrecognizedby
Elton ('27), who discussed its effecton
the survival of preyspecies when preda-
tors are numerous and its effect in
enablingpredatorsto survivewhen their

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 402 RAYMOND L. LINDEMAN Ecology,Vol. 23,No. 4

usual prey are only periodicallyabun- 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 ofa foodcycle less discrete lacustrine cycle, with two "life-forms"
than the lower, increasesthe difficulties of producers,may be consideredas "bi-
of analyzing the energyrelationshipsin 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 comparinglacustrineand terrestrial supportingtissues in planktersand the
cycles. Althoughdissolved nutrientsin very rapid completionof theirlifecycle
the lake water and in the ooze corre- exerta great influenceon the differential
spond directlywith those in the soil, the productivitiesof terrestrialand aquatic
autotrophicproducersdiffer considerably systems. The general convexityof ter-
in form. Lacustrine producersinclude restrialsystems as contrastedwith the
macrophyticpondweeds, in which mas- concavityof aquatic substrataresultsin
sive supportingtissuesare at a minimum, strikingtrophicand 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, belongingto 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 correspondto '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, ductivityas related to biotic dynamics
quaternary, etc.) consumers,according has been critically analyzed by G. E.
to whethertheypreyupon herbivoresor Hutchinson ('42) in his recent book on
upon other predators; these correspond limnologicalprinciples. The two follow-
roughly to the benthic predators and ingparagraphsare 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
decompositiontakes place both in the lake surface. Some of this energyis transformed
water,as organic particlesslowly settle, by photosynthesisinto the structure of phyto-
plankton organisms,representingan energycon-
and in thebenthic"soil." Nutrientsalts tent which may be expressed as Al (first level).
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 terrestrialequivalent of aquatic lacustrine microbenthosthan to the plankton.

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October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 403

zooplankters (energy content A2), which again Numerous estimatesof average respi-
will be eaten by plankton predators (energy rationforphotosyntheticproducersmay
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 differentenergycontents (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
varioustypesofnaturalconditions. 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 undercertainconditions. Wim-
where XAis by definitionpositive and represents penny ('41) has indicated that the respi-
the rate of contributionof energyfromA,,- (the ratorycoefficient of marineproducersin
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
handed on to the followinglevel A,,+,. The more
producers (peridinians and coccolitho-
interestingquantity is XAwhich is definedas the phorids) of warmerseas, and that tem-
true productivityof level An. In practice, it is peraturemay be an importantfactorin
necessary to use mean rates over finiteperiods determiningrespiratorycoefficientsin
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 otherson the respirationof phyto-
siderthequantitativerelationshipsofthe plankters in Trout Lake, Wisconsin,
followingproductivities:Xo(rate of inci- concludedthat underaverage conditions
dent solar radiation), X, (rate of photo- these producersrespireabout 13 of the
syntheticproduction),X2 (rateofprimary organic matter which they synthesize.
or herbivorousconsumption),X3 (rate of This latter value, 33 per cent, is prob-
secondaryconsumptionor primarypre- ably the best available respiratoryco-
dation), and X4 (rate of tertiarycon- efficientforlacustrineproducers.
sumption). The totalamountoforganic Information on the respiration of
structureformedper year for any level aquatic primaryconsumersis obtained
A', which is commonlyexpressedas 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 followingsimplecalculations: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
lifehistoriesof individuals,fordifferent 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
assimilation
ferences between food groups may be
observed. good agreementwith the classical con-
I The term stage, in some respects
clusions of Needham ('31, III, p. 1655)
preferable
to the term level,cannot be used in this trophic with respect to embryos: the efficiency
sense because of its long-established usage as a of all developingembryosis numerically
successional term (cf. p. 23). similar,between60 and 70 per cent, and

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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 respiratory rate ofEsox underresting
growingat nearlymaximal efficiency, so conditionsat 20? C. was 3' times that
that the above respiratorycoefficientis of Cyprinus. The formofpisciangrowth
nearlyminimal. 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 foraquatic herbivores. life-span. Since thevalue obtainedfrom
The respiratorycoefficient foraquatic 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 tativelyaccept 140 per cent as an aver-
Ivlev ('39b), on the energytransforma- age respiratorycoefficientfor aquatic
tionsin predatoryyearlingcarp. Treat- predators.
ing his calorificvalues as in the preceding Consideringthat predatorsare usually
paragraph,we findthat ingestion(1829 moreactive than theirherbivorousprey,
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 per cent, a much higher and in secondaryconsumers(>100 per
coefficientthan that found for the pri- cent) increases progressively. These
maryconsumer,Tubifex. A roughcheck differencesprobably reflect a trophic
on this coefficient was 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 progressivelygreaterforhigherlevels
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 thesefishesweregrowing is most. convenient to begin with the
more efficiently than those studied by highest level, A,. In a mechanically
Ivlev. Since Moore's fisheswere fed on perfectfood cycle composed of organ-
a highlyconcentratedfood (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
ciency would occur when assimilation
asmlti 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 fromAnprobablywill be somewhat
50 per cent) indicatesthat the minimum above zero. The predation loss from
respiratorycoefficientwith respect to level A,,- will representthe total amount
growthmightbe as low as 100 per cent of assimilable energypassed on into the
forcertainfishes. 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,contentof substance killed but
150 per cent foryoungblack 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 assimilableenergypassed on to the next

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October,1942 TROPHIC-DYNAMIC
level (i.e., X,-l) plus a similar factor for
unassimilatedmaterial,as illustratedby
the data of tables II and III. The
various categoriesof parasitesare some-
what comparable to those of predators,
but the details of theirenergyrelation-
ships have not yet been clarified,and
cannot be included in this preliminary
account.
Decomposition corrections.- In con-
formitywith the principleof Le Chate-
lier, the energyof no food level can be
completelyextracted by the organisms
which feed upon it. In addition to the
energyrepresentedby organismswhich
survive to be included in the "annual
yield," much energy is contained in
"killed" tissues which the predatorsare
unable to digest and assimilate. Aver-
age coefficientsof indigestible tissues,
based largelyof the calorificequivalents
of the "crude fiber" fractions in the
chemical analyses of Birge and Juday
('22), are as follows:
Nannoplankters....................
Algal mesoplankters. .
Mature pondweeds.
Primaryconsumers.......... ...
Secondary consumers....
Predatory fishes....
Corrections for terrestrial producers
would certainly be much higher. Al-
thoughthe data are insufficient to war-
ranta generalization,thesevalues suggest
increasingdigestibilityof the higherfood
levels, particularlyfor the benthiccom-
ponentsof aquatic cycles.
The loss of energydue to premature
death fromnon-predatory causes usually
must be neglected,since such losses are
exceedingly difficultto evaluate and
undernormalconditionsprobablyrepre-
sent relativelysmall componentsof the
annual production. However,consider-
ing that these losses may assume con-
siderable proportionsat any time, the
above "decompositioncoefficients" must
be regardedas correspondingly minimal.
Following non-predateddeath, every
organismis a potentialsource of energy
for myriads of bacterial and fungal
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ASPECT OF ECOLOGY 405
saprophages, whose metabolic products
provide simple inorganic and organic
solutes reavailable to photosynthetic
producers. These saprophagesmay also
serve as energy sources for successive
levels of consumers,often considerably
supplementingthe normal diet of herbi-
vores (ZoBell and Feltham, '38). Jacot
('40) considered saprophage-feedingor
coprophagousanimals as "low" primary
consumers,but the writerbelieves that
in the presentstate of our knowledgea
quantitativesubdivisionof primarycon-
sumersis unwarranted.
Application.-The value of these the-
oreticalenergyrelationshipscan be illus-
trated by analyzing data of the three
ecosystemsforwhich relativelycompre-
hensive productivityvalues have been
published (table I). The summaryac-
TABLE I. Productivities of food-groups in
threeaquatic ecosystems,as g-callcm2Iyear, uncor-
rectedfor losses due to respiration,predationand
decomposition. Data fromBrujewicz ('39), Juday
('40) and Lindeman ('41b).
ca. 5 %
5-35% Casp ian Lake Cedar
ca. 20% Sa Men-
5eapa Bog
dota Lake
ca. 10%
Phytoplankters: A.............59.5 299 25.8
ca. 8% Phytobenthos:Al..............0.3 22 44.6
ca. 5% Zooplankters:A2...............20.0 22 6.1
Benthicbrowsers:A2...........1.8* 0.8
Benthicpredators:A3........... 20.6 0.9* 0.2
Planktonpredators:A3.
"Forage" fishes:A3(+A2?) .... .
.J.. . .0.8
0.6 ? 0.3
Carp: A3(+A2?)............. . 0.0 0.2 0.0
"Game" fishes:A4(+A3?) . 0.... . 06 0.1 0.0
Seals: As......................0.01 0.0 0.0
* Roughly assuming that 2M of the bottom
fauna is herbivorous(cf. Juday, '22).
count of Brujewicz ('39) on "the dy-
namics of living matter in the Caspian
Sea" leaves much to be desired, as
bottom animals are not differentiated
into their relative food levels, and the
basis for determiningthe annual pro-
duction of phytoplankters(which on
theoreticalgroundsappears to be much
too low) is not clearlyexplained. Fur-
thermore,his values are stated in terms
of thousands of tons of dry weight for
the Caspian Sea as a whole, and must
be roughlytransformedto calories per
square centimeterof surfacearea. The
data forLake Mendota, Wisconsin,are
406 RAYMOND L. LINDEMAN Ecology,Vol. 23,No. 4

taken directlyfroma 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 coefficients
derivedin 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
analysis (Lindeman, '41b) of its food- . S _rected . .s Pre-
_-S Res- r.. D- rected
lcl* cor-
rected
TrophicLevel pro- pira- da- comp~- recte
cycle dynamics. The calorificvalues in duc- tion tion ppi pro- pro-
tivity tion~~~~tiit
table I, representingannual production
of organic matter, are uncorrectedfor Producers: Al. 321*
Primary con-
107 42 10 480 428

energylosses. Secondary
sumers: A2. 24 15 2.3 0.3 41.6 144
consumers:
TABLE II. Productivityvalues for the Cedar A3........ it 1 0.3 0.0 2.3 6
as corrected Tertiary
Bog Lake food cycle,in g-cal/cm2/year, con-
sumers:A4. 0.12 0.2 0.0 0.0 0.3 0.7
derivedin the preceding
by using the coefficients
sections.
* Hutchinson ('42) gives evidence that this
value is probably too high and may actually be
De- Cor- as low as 250.
1es- Pre- co -rected
Rnorctd pi
Trophic level productivity da- corn-pro- t Apparentlysuch organismsas small " forage"
prdciiytion tionPsl duc-
tion tivity fishesare not included in any part of Juday's
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
* This value includes the productivityof the
A3), was about 500 per cent that of lakes
small cyprinoidfishesfound in the lake.
containing mostly "game" fishes (pri-
marily A4), and concluded that "this
Correctingfor the energy losses due differencemust be about one complete
to respiration,predationand 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 differentlighton the produceone pound of fish." While such
relative productivitiesof food levels. high "metabolic losses" may hold for
The calculation of correctionsfor the tertiaryand quaternarypredatorsunder
Cedar Bog Lake values for producers, certain field conditions,the physiologi-
primaryconsumersand secondarycon- cal experimentspreviously cited indi-
sumersare givenin table II. The appli- cate much lowerrespiratorycoefficients.
cationofsimilarcorrectionsto theenergy Even whenpredationand 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- necessarycorrectionsvary 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
blanketcorrectionof 500 per cent of the
annual productionof all consumerlevels The quantitative relationshipsof any
for"metabolism,"whichpresumablyin- 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)

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 October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 407

definition,"the efficiency of the produc- of the Lake Mendota productivities,no

tivity of any level (An) relative to the definiteconclusionscan 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 the progressiveefficiencies increasefrom
Xm
energyenteringthe ecosystemis denoted about 0.10 per cent for production,to
as Xo,the efficiencies of all levels may be 13.3 per cent for primaryconsumption,
referredback to this quantity Xo." In and to 22.3 per cent forsecondarycon-
general, however, the most interesting sumption. An uncorrectedefficiency of
efficiencies are those referredto the pre- tertiary consumption of 37.5 per cent
vious level's productivity(XA1) or those ?t 3.0 per cent (forthe weightratios 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 progressively increasingefficiencies
for each level the degree of utilization maywell representa fundamentaltrophic
of its potential food supply or energy principle,namely,that the consumersat
source. All efficiencies discussed 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 rememberthat 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 reconciledby re-
ing a ratio, is a dimensionlessnumber.
memberingthat increased activity of
The pointsof referenceforany efficiency
predators considerably increases the
value should always be clearlystated.
chances of encounteringsuitable prey.
/Xn
The progressiveefficiencies 12 1001 The ultimateeffectof such antagonistic
Xn-1 / principleswould presenta picture of a
forthe trophiclevels of Cedar Bog Lake predator completelywearing itself out
and Lake Mendota, as obtained from in the process of completely extermi-
the productivitiesderived in tables II natingits prey,a veryimprobablesitua-
and III, are presentedin table IV. In tion. However, Elton ('27) pointedout
viewoftheuncertaintiesconcerningsome that food-cyclesrarely have more than
TABLE IV. Productivitiesand progressiveeffi- five trophic levels. Among the several
cienciesin the Cedar Bog Lake and Lake factors involved, increasing respiration
Mendotafood cycles,as g-cal/cm2/year of successive levels of predators con-
trastedwiththeirsuccessivelyincreasing
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 ..........
Producers: Al......
< 118,872
111.3
118,872
480*
The effectof increasing temperature
0.10% 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% 5.5%
Tertiary
2.3t
sumably because he believes that the
consumers: A4.... 0.3 13.0%
"accelerationof 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. morerapid than that of producers. He

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408
cites as evidence Lohmann's ('12) data
for relative numbers (not biomass) of
Protophyta, Protozoa and Metazoa in
the centrifugeplankton of "cool" seas
(741:73:1) as contrasted with tropical
areas (458:24:1). Since Wimpennyhim-
self emphasizes that many metazoan
planktersare larger in size toward the
poles, these data do not furnishcon-
vincing proof of the allegation. The
data given in table IV, since Cedar Bog
Lake has a much higher mean annual
water temperaturethan Lake Mendota,
appear to contradictWimpenny'sgener-
alization that consumer/producer ratios
fall as the temperatureincreases.
The Eltonian pyramid
The general relationships of higher
food-cyclelevels to one another and to
communitystructurewere greatlyclari-
fied followingrecognition (Elton, '27)
of the importanceof size and of numbers
in the animals of an ecosystem. Begin-
ningwith primaryconsumersof various
sizes, there are as a rule a number of
food-chainsradiatingoutwardsin which
the probabilityis that predatorswill be-
come successivelylarger,while parasites
and hyper-parasites will be progressively
smaller than their hosts. Since small
primaryconsumers can increase faster
than largersecondaryconsumersand are
so able to supportthe latter,the animals
SIZE RANGE
IN Mm
1314
12-13.4
11-12'
810-1
7-4
5F7X
3-4
FIG. 2. Eltonian pyramid of numbers, for floor-faunainvertebratesof the Panama rain forest
(fromWilliams, '41).
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RAYMOND L. LINDEMAN Ecology,Vol. 23,No. 4
at the base of a food-chainare relatively
abundantwhilethose towardthe end are
progressivelyfewerin number. The re-
sulting arrangementof sizes and num-
bers of animals, termedthe pyramidof
Numbers by Elton, is now commonly
known as the Eltonian Pyramid. Wil -
liams ('41), reporting on the "floor
fauna" of the Panama rain forest,has
recently published an interesting ex-
ample of such a pyramid, which is
reproducedin figure2.
The Eltonian Pyramid may also be
expressed in terms of biomass. The
weight of all predatorsmust always be
muchlowerthanthat of all food animals,
and the total weight of the lattermuch
lowerthan the plant production(Boden-
heimer, '38). To the human ecologist,
it is noteworthythat the populationden-
sityoftheessentiallyvegetarianChinese,
for example, is much greaterthan that
of the morecarnivorousEnglish.
The principle of the Eltonian Pyra-
mid has been redefinedin termsof pro-
ductivityby Hutchinson (unpublished)
in the followingformalizedterms: the
rate of production cannot be less and
will almost certainlybe greaterthan the
rate of primaryconsumption,which in
turncannot be less and will almost cer-
tainlybe greaterthan the rate of second-
ary consumption,which in turn . . .
etc. The energy-relationshipsof this
principlemay be epitomized by means
NUMBERorAmI ALs
October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 409

of the productivitysymbolX,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 tendencytowardsstage-equilibrium
of productivitywill be discussed in the
IN SUCCESSION
followingpages.
TROPHIc-DYNAMICS

Dynamic processes withinan ecosys- Productivity in hydrarchsuccession

tem, over a period of time, tend to
produce certain obvious changes in its The descriptivedynamicsof hydrarch
species-composition,soil characteristics succession is well known. Due to the
and productivity. Change,accordingto essentially concave nature of the sub-
Cooper ('26), is the essentialcriterionof stratum, lake succession is internally
succession. From the trophic-dynamic complicated by a rather considerable
viewpoint,succession is the process of influxof nutritivesubstances fromthe
developmentin 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,largelyorganogenic,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 similaraccelerationin 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) pointedout, these generalized ductivity is rather low, limited by the
changes in the rate of productionmay amountof dissolvednutrientsin the lake
be expressedas a sigmoidcurve showing water. Oxygenis abundant at all times,
a roughresemblanceto the growthcurve almost all of the synthesized organic
of an organism or of a homogeneous matteris available foranimal food; bac-
population. teriareleasedissolvednutrientsfromthe
Such smoothlogisticgrowth, of course, remainder. Oligotrophythushas 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 developingdirectlyto the climax lations. With increasinginfluxof nutri-
vegetationtype in the wake of a retreat- tivesfromthesurrounding drainagebasin
ingglacier. Most successionalserescon- and increasingprimaryproductivity(X1),
sist of a numberof stages("recognizable, oligotrophyis graduallychangedthrough
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,predationand bacte-
to the distinctnessof the stages. The rial decomposition. The oxygensupply
presenceof stages in a successionalsere of the hypolimnionbecomes depleted,
apparentlyrepresentsthe persistentin- withdisastrouseffectson the oligotroph-

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 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
anaerobiosisreplacethe oligotrophicspe- dependent on the morphometry(mean
cies, accompanied by anaerobic bacteria depth). Since deep lakes have a greater
whichduringthe stagnationperiodcause depth range for plankton photosynthe-
reductionrather than oxidation of the sis, abundant oxygen and more chance
organic detritus. As a result of this fordecompositionof 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,relativeefficiency unit surface area. Factors tending to
of the consumergroups in utilizingthe lessen the comparative productivityof
synthesizedorganic substance becomes deep lakes are (1) lowertemperaturefor
correspondingly lower. 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"trophogeniczone" of
trophic mechanisms,has recentlybeen the lake. During eutrophicationin a
challengedby Hutchinson('41, '42), who deep lake, the phosphoruscontentof the
states that three distinct factors are sedimentfallsand nitrogenrises,untila
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 morphometriccharacterat 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 duringsummerstag-
otherregionsdevelopinginto"ideotrophic nation. Oxidation of the sediments is
types." The influx of phosphorus is less complete,but sufficient phosphorus
probablyverygreatin theearliestphases, is believed to be regeneratedfrom the
much greaterthan the supply of nitro- ooze surface so that productivity in
gen, as indicatedby verylow 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 maintainthe 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 nitrogenincreasessomewhat 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 conditionofcompletetrophicequilibrium,
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

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October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 411

utilizationand regenerationof chemical energywhichis lost fromthe food cycle,

nutrientsin an ecosystem,without loss is derivedlargelyfromlevel A1,as plant
or gain fromthe outside, under a peri- structures in general are decomposed
odicallyconstantenergysource-such as less easily than animal structures. The
mightbe 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 occupythoselevels.
ditions, but it is doubtful if any are Several types of animal "microfossils"
sufficientlyautochthonousto 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 existenceof prolongedeutrophic ules and rhizopodshells. Deevey ('42),
stage-equilibriumwas firstsuggestedas after making comprehensivemicrofossil
a resultof a study on the sedimentsof and chemicalanalysesofthesedimentsof
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 estimateof the quantity of zooplankton
chemical analyses (ibid.) and pollen produced" and that "the total organic
analyses (Deevey, '39) of the sediments matter of the sedimentis a reasonable
of Linsley Pond, Connecticut. They estimateof the organicmatterproduced
reporteda gradual transitionfromoligo- by phytoplanktonand littoral vegeta-
trophyto eutrophy(firstattained in the tion." He found a strikingsimilarity
oak-hemlock pollen period), in which in the shape of the curves representing
stage the lake has remainedfor a very Bosmina contentand total organic mat-
long time,perhapsmorethan4000 years. ter plotted against depth, which, when
They reportindicationsof a comparable plotted logarithmically against each
eutrophicstage-equilibriumin 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 preliminaryreporton fororganicmatterwas analogous to that
the sediments of Lake Windermerein forthe 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
ratiooforganicmatterto the silt washed line when a double log plot is made."
into the lake fromthe marginsaffords If we representthe organic matterpro-
an approximationof the photosynthetic duced as Xi and furtherassume that
productivity. This undecomposed or- Bosmina represents the primary con-
ganic matter,representingthe amountof sumers(X2), neglecting benthicbrowsers,

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 412 RAYMOND L. LINDEMAN Ecology,Vol. 23,No. 4

theformulabecomesX2 = 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,remainsto 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- continuallyapproachinga 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 forXiagainst cence is usually characterizedby such
X2, and X2 againstX3, forthe fouryears pond-likeconditionsas (1) tremendous
studied, show no semblance of linear increase in shallow littoral area popu-
relationship,i.e., do not fit any power lated with pondweedsand (2) increased
equation. If Deevey is correct in his marginal invasion of terrestrialstages.
interpretation ofthe LinsleyPond micro- Cedar Bog Lake, which the author has
fossils,allometricgrowthwould appear studiedforseveral years,is in late senes-
to characterizethe phases of pre-equilib- cence,rapidlychangingto 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,togetherwith 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-
withthe trophicprocessesof (1) external houses, absorbing more radiant energy
influxand efflux(partly controlledby per unit volume than deeper areas. At
climate), (2) photosyntheticproductiv- the presenttime the entireaquatic area
ity, (3) sedimentation(partlyby physio- of Cedar Bog Lake is essentiallylittoral
graphic silting) and (4) regenerationof in nature,and its productivityper cubic
nutritivesfrom the sediments. These meterof water is probablygreaterthan
processes apparently maintain a rela- at any time in its history. However,
tivelyconstantratioto each otherduring since radiant energy (Xo) enters a lake
the extended equilibrium period. Yet only fromthe surface,productivitymust
the foodcycleis not in truetrophicequi- 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
whencomparedwith less advanced lakes
6 It should be mentioned in this connection
that Meschkat ('37) found that the relationship
in similaredaphic regions; forinstance,
of population density of tubificids to organic X1 is 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 representsthe population density, x is
the "determining environmentalfactor," and a
('35) generalization 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
to the relationship between populations of ma-
that duringlate lake senescencegeneral
rine plankton and the "controlling factor" of productivity(X,) is increasinglyinflu-
theirenvironment. enced by climaticfactors,actingthrough

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October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 413

water level changes, drainage, duration thussubject to a certainnutrientloss 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 foodgroupsin the lake. nutrientsas can be extracted fromthe
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 productivityrelationshipsin hy-
succession proceeds, both the species- drarch succession, we shall venture to
compositionand the productivityof an diagram (figure3) a hypotheticalhydro-
ecosystemincreasinglyreflectthe effects sere,developingfroma moderatelydeep
of the regional climate. Qualitatively, lake in a fertilecold temperate region
these climaticeffectsare knownforsoil underrelativelyconstantclimaticcondi-
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 productivityrapidlyincreas-
importantcomponentof the food cycle. ing until eutrophicstage-equilibriumis
Quantitatively,these effectshave been attained. The duration of high eu-
so littlestudied 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 growthof phytoplanktonor
productivityis generallygreatestin the regenerationof nutrientsfromthe ooze.
subclimax,except possiblyin the case of As the lake becomesshallowerand more
grasslands. Terrestrial ecosystems are senescent, productivityis increasingly
primarily convex topographically and influencedby climatic fluctuationsand

/ EUTROPHY AE / CLIMA

I- ~~~~~~~~~~~~BO
FOREST

0. MAT

UOGOTROPHY SENESCENCE
TIME ->
FIG. 3. Hypothetical productivity growth-curveof a hydrosere,developing from a deep lake
to climax in a fertile,cold-temperateregion.

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414 RAYMOND L. LINDEMAN Ecology,Vol. 23,No. 4

graduallydeclines to a minimumas the original observations,but are probably

lake is completelyfilledwith sediments. of the correctorderof magnitude. The
The terrestrialaspects of hydrarch mean photosyntheticefficiencyfor 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, oftenpartlyfloating,made up (afterNoddack, '37), forforestsas 0.16
primarilyof sedges and grasses or (in per cent,forcultivatedlands as 0.13 per
more coastal regions) such heaths as cent, for steppes as 0.05 per cent, and
Chamaedaphneand Kalmia with certain fordesertsas 0.004 per cent. The mean
species ofsphagnummoss (cf. Rigg, '40). photosyntheticefficiencyfor the earth
The mat stage is usually followedby a as a whole is given as 0.25 per cent.
bog foreststage, in whichthe 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 biologicalformationsand of theirdevel-
greateror lesser degree by the regional opmentalstages."
climax vegetation. The stage-produc- Almost nothingis 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 cara-
paces withrespectto organicmatterand
Efficiencyrelationships
in succession of Chaoborusfragmentswith respect to
Bosmina carapaces in the sedimentsof
The successionalchangesof 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 concludesfroma comparisonof the P: Z
lake succession,photosynthetic efficiency (phytoplankton:zooplankton) biomass
would be expected to follow the same ratiosofseveraloligotrophicalpine lakes,
course deduced for productivity,rising ca 1: 2 (Ruttner,'37), as comparedwith
to a more or less constantvalue 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
photosynthetic efficiency
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
efficiency forvarious 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,correctedfor eutrophicequilibrium (22-27 per cent).
respiration,do not appear to be very The ratiosforsenescentCedar Bog Lake,
reliable because of imperfectionsin the while not directly comparable because

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 October,1942 TROPHIC-DYNAMIC ASPECT OF ECOLOGY 415

of its essentiallylittoralnature,are even sumers,secondaryconsumers,etc., each

higher. These meagerdata suggestthat successivelydependentupon the preced-
the efficiencies of 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 successivestagesapproach- 4. The progressive energy relation-
ing the regionalclimax. Since the pho- ships of the food levels of an "Eltonian
tosyntheticproductivityof the stages Pyramid" may be epitomizedin termsof
probablyalso increased,it is impossible the productivitysymbolX, as follows:
to determineprogressiveefficiency rela-
tionships. The problems of biological XO > Xl > X2. . . > Xn.
efficienciespresent a practically virgin
5. The percentageloss of energydue
field,which appears to offerabundant
to respirationis progressively greaterfor
rewardsforstudiesguided by a trophic-
higherlevels in the foodcycle. Respira-
dynamicviewpoint.
tion with respectto growthis about 33
In conclusion,it should be emphasized per cent for producers,62 per cent for
that the trophic-dynamic primary consumers,and more than 100
principlesindi-
cated in the followingsummarycannot per cent forsecondaryconsumers.
be expectedto hold foreverysinglecase, 6. The consumers at progressively
in accord with the known facts of bio- higher levels in the food cycle appear to
logical variability. a priori, however, be progressively moreefficient in the use
of their food supply. This generaliza-
these principlesappear to be valid for
the vast majorityof cases, and may be tioncan be reconciledwiththe preceding
one by rememberingthat increased ac-
expectedto possess a statisticallysignifi-
cant probabilityof validityforany case tivityof predatorsconsiderablyincreases
selectedat random. Since the available the chances of encountering suitable
data summarizedin this paper are far prey.
too meager to establish such generaliza- 7. Productivityand efficiency increase
tions on a statistical basis, it is highly during the early phases of successional
In lake succession, pro-
importantthat furtherstudies be initi- development.
ated to test the validity of these and ductivity and photosynthetic efficiency
othertrophic-dynamic increase from oligotrophy to a prolonged
principles.
eutrophicstage-equilibriumand decline
SUMMARY
with lake senescence,risingagain in the
terrestrialstages of hydrarchsuccession.
1. Analysesof food-cyclerelationships 8. The progressiveefficiencies of con-
indicatethat a biotic communitycannot sumerlevels,on the basis of verymeager
be clearly differentiated fromits abiotic data, apparentlytendto increasethrough-
environment;the ecosystemis hence re- out the aquatic phases of succession.
garded as the more fundamentaleco-
logical unit. ACKNOWLEDGMENTS
2. The organismswithinan ecosystem
may be grouped into a seriesof moreor The author is deeply indebted to Professor
G. E. Hutchinson of Yale University,who has
less discrete trophic levels (Al, A2, A3, stimulated
many of the trophic concepts devel-
An) as producers, primary con- oped here, generously placed at the author's

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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
of this paper in every way possible. Many of
the concepts embodied in the successional sec-
tions of this paper were developed independently
by Professor Hutchinson at Yale and by the
author as a graduate student at the University
of Minnesota. Subsequent to an exchange of
notes, a joint preliminaryabstract was published
(Hutchinson and Lindeman, '41). The author
wishes to express gratitude to the mentors and
friends at the University of Minnesota who
encouraged and helpfully criticized the initial
development of these concepts, particularlyDrs.
W. S. Cooper, Samuel Eddy, A. C. Hodson,
D. B. Lawrence and J. B. Moyle, as well as
other membersof the local Ecological Discussion
Group. The author is also indebted to Drs.
J. R. Carpenter, E. S. Deevey, H. J. Lutz,
A. E. Parr, G. A. Riley and V. E. Shelford,as
well as the persons mentionedabove, forcritical
reading of preliminary manuscripts. Grateful
acknowledgmentis made to the Graduate School,
Yale University, for the award of a Sterling
Fellowship in Biology during 1941-1942.
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ADDENDUM
While this, his sixth completed paper, was in
the press, Raymond Lindeman died after a long
illness on 29 June, 1942, in his twenty-seventh
year. While his loss is grievous to all who knew
him, it is more fitting here to dwell on the
achievements of his brief working life. The
present paper represents a synthesis of Linde-
man's work on the modern ecology and past
history of a small senescent lake in Minnesota.
In studying this locality he came to realize, as
othersbeforehim had done, that the most profit-
able method of analysis lay in reduction of all
the interrelated biological events to energetic
terms. The attempt to do this led him far