Freshwater Biology (1995) 33,83-89

OPINION

Death, detritus, and energy flow in aquatic ecosystems

ROBERT G. WETZEL
Department of Biological Sciences, University of Alabama, Tuscaloosa, AL 35487-0344, U,S,A,

SUMMARY
1. Pelagic trophic structure and energy fluxes are evaluated predominantly on the basis of
ingestion of particulate organic matter by living organisms and the effects of consumption
on the population dynamics of trophic levels.
2. Population fluxes are not representative of the material and energy fluxes of either the
composite pelagic region or the lake ecosystem. Metabolism of particulate and especially
dissolved organic detritus from many pelagic and non-pelagic autochthonous and from
allochthonous sources dominates both material and energy fluxes. Because of the very
large magnitudes and relative chemical recalcitrance of these detrital sources, the large but
slow metabolism of detritus provides an inherent ecosystem stability that energetically
dampens the ephemeral, volatile fluctuations of higher trophic levels.
3. The annual time period is the only meaningful interval in comparative quantitative
analyses of material and energy fluxes at population, community, and ecosystem levels.
4. Non-predatory death and metabolism by prokaryotic and protistian heterotrophs
dominate. Continued application of animal-orientated relationships to the integrated,
process-driven couplings of the aquatic ecosystems impedes understanding of
quantitative ecosystem pathways and control mechanisms.

Introduction Trophic structure in the pelagic zone: not only a

The importance of trophic structure in determination of
both the rate of energy fixation by primary producers in
terrestrial and freshwater pelagic communities and the
transfer efficiencies of this energy to higher trophic
levels was argued in a recent review and comparative
synthesis by Hairston & Hairston (1993). This evalua-
tion is among the most lucid and cogent of the plethora
of works on this and related subjects. Several points
must be considered further, however, because of con-
ceptual fallacies associated with extrapolation of their
conclusions on the freshwater pelagic zone to the entire
lake or stream ecosystem. In fresh waters, the relation-
ships presented by Hairston & Hairston (1993) are lim-
ited to the higher trophic levels of the pelagic zone of
certain lakes but are not applicable to the entire coupled
lake ecosystem. Application of principles originating in
animal ecology to the integrated, process-driven cou-
pling of the lake ecosystem is widespread and impedes
acquisition of understanding of ecosystem operations
and control mechanisms.
83
particulate world
Original promulgations of the effects of energy flow on
trophic structure emphasized the restrictions on trophic
complexity by limitations of energy transfers among
trophic levels (Lindeman, 1942; Hutchinson, 1959). As
Hairston & Hairston (1993) illustrate, measurements of
the efficiency of energy transfer among higher trophic
levels are often consistent with the hypothesis that
trophic structure may control the fraction of energy
consumed within each trophic level, rather than ener-
getics controlling trophic structure. Resolution of the
often variable effects of community shifts among four
common dominant trophic levels (phytoplankton -^
grazing zooplankton -> zooplanktivorous fish ->
piscivores) on higher trophic relations in the pelagic
zone is now correctly directed toward variations in the
species involved among different aquatic systems. Effi-
ciency of consumption of primary production by zoop-
lankton is often appreciably greater in the absence of
zooplankton-feeding fish than in their presence. The
84 R.G, Wetzel
community structure of the phytoplankton responds
variably to grazing impacts in concert with their avail-
able resources (light, nutrients, organic constituents)
and may or may not be able to compensate for grazing
losses in overall primary production. Studies of the
effects of pelagic trophic structure on primary produc-
tion have been enormously sophisficated over the past
three decades but largely substanfiate the relationships
described percepfively by HrbaCek et al, (1961,1962).
An important facet of these relafionships of pelagic
trophic structure and energy fluxes, however, is that
they consider almost solely particulate organic carbon.
This perception is orientated from the standpoint of
ingesfion of particulate organic matter (POM). What-
ever the historical roots of this percepfion,* it is clear that
the flows of energy within the trophic structures and
their variants are specifically orientated along ingestion
of parficles of organic matter. Excellent research and
understanding have been directed toward understand-
ing of the size of POM, the morphological aspects of
ingestion (e.g. gape, filtration) and avoidance of inges-
tion (e.g. transparency/visibility, interference by cellu-
lar or body projecfions), behavioural capabilifies of
organisms for movements within the pelagic zone in
relation to refuges and/or escape from predators, nutri-
tional differences in pardculate food, and others. Al-
though many of these studies reluctantly concede that
many organisms consume variable amounts of particu-
late detritus (= particulate dead organic matter) and
that particulate detritus frequently dominates over liv-
ing POM of the plankton (e.g. Saunders, 1972), quanfi-
tative measures of consumpfion, assimilafion, and re-
sidual egesfion of detrital POM and its associated at-
tached bacteria, particularly among zooplankton, are
practically unknown.
Death and detritus
A further characterisfic of many of these animal-orien-
tated trophic analyses is that energy transfers among
trophic levels use primarily consumpfion efficiencies.
* The premier position that animals have assumed in biological
study, ecological research, and conceptual developments of ecology
cannot be questioned. Historical roots of zoological dominance in
aquatic ecological study and conceptual development are varied and
include the food and economic importance of fishes and aquatic
insects, early relative ease of sampling and examination of
population and community interactions of larger organisms, as well
as in part the religiously founded omnipotence of humans and other
animals over other organisms, particularly plants and microbes.
i.e. the percentage of net production at level n that is
consumed by level n + 1. Assimilation efficiency (the
percentage of energy ingested at level n that is assimi-
lated at level n) is obviously a much more important
facet of the energetics and reproducfive success of the
ingesfing organisms than is ingestion. Ingestion rates
taken alone or coupled with biochenucal parameters are
not reliable predictors of consumer demographic re-
sponses (Chen & Folt, 1993), whereas among zooplank-
ton assimilafion rates are good predictors of food qual-
ity. Assimilation efficiencies vary widely, however, in
relation to food quantity and quality and numerous
other environmental and biotic characteristics, and are
considered and discarded (e.g. Hairston & Hairston,
1993) as less reliable than consumption efficiencies.
Although the physiological importance of assimila-
tion efficiencies is certainly recognized, part of the com-
parative preference for consumpfion efficiencies ema-
nates again from the restricted perspective of the effects
of direct consumer utilization of the prey / food items on
population and community dynamics of prey. The basic
assumpfion is that once the prey organism is ingested, it
is dead, and the populafion and community dynamics
are affected accordingly by the mortality. Although
some organisms not only pass through the intestinal
tract of organisms unharmed and may be enhanced by
enriched nutrient environments of the gut (e.g. Porter,
1975), most planktonic organisms, particularly meta-
zoans, die upon ingesfion.
Death of many individuals of a prey population can
obviously affect appreciably the subsequent ingestion,
growth, reproducfion, and producfivity of size-class or
species-restricted predators. The energefics of material
and energy fiuxes from the prey to the predators are
altered consequently in complex ways. Indeed, no rea-
sonable persons quibble with the relafionships of these
trophic couplings within the higher food web. I argue
strongly, however, that these material and energy fluxes
are not in any way representative of the material and
energyfiuxesof either the composite pelagic region or
certainly not the lake ecosystem. Hairston & Hairston
(1993), in contrast to many ecologists evaluating this
subject, were correctly careful to state that their analysis
was restricted to non-detrital higher trophic levels of the
freshwater pelagic region. Discussion, however, was
not left there, and repeated speculations minimized the
quantitative importance of altemative energy pathways
in pelagic regions and aquatic ecosystems. The clear
assumpfions are that the particulate detrital, as well as

non-particulate components and their metabolism, have
some unknown and therefore minor role in the ob-
served higher trophic level relationships. Nearly all of
their and many other interpretations focus on the use of
particulate organic matter that is ingested into meta-
zoan alimentary tracts and the direct effects of this
ingestion on population and community dynamics of
the prey and predators. The importance of material and
energy fluxes of egested particulate and soluble organic
matter, or of utilization of dissolved organic matter
(DOM), within the pelagic zone and the aquatic ecosys-
tem by non-metazoan heterotrophs is either ignored or
discussed largely in relation to conversion of DOM to
particulate organic matter of sufficient size for ingestion
by metazoans.
Death of organisms occurs in many ways. During
direct ingestion by metazoans, the entire prey organism
can enter the gut. In many cases, however, the prey is
variously injured in capture and inefficiently masti-
cated (e.g. Lampert, 1978; Sierszen & Brooks, 1982), and
much of the POM of the prey is not ingested but enters
the detrital pool as POM and DOM for subsequent
energetic consumption by microbial heterotrophs. A
large literature exists on the assimilation efficiencies of
food types and quantities, particularly among zoop-
lankton and fishes. Under natural conditions, assimila-
tion efficiencies are generally less than 50%, but can vary
greatly with environmental conditions and are certainly
markedly dynamic on both diurnal and seasonal scales.
Regardless of the exact, variable percentage of assimila-
tion, an appreciable portion of food ingested is egested.
The form of egested faeces is not usually packaged into
distinct boluses or pellets, but rather is loosely or not
aggregated, and the material thus readily fragments
and leaches appreciable DOM. Coprophagy is rare
among the plankton. Clearly, most of the egested POM
and DOM enters the detrital pool and is subsequently
utilized by microbial heterotrophs. Although lost in the
short term from the metazoans, this detrital POM and
DOM is not lost from the ecosystem (cf. Wetzel et al,
1972; Rich & Wetzel, 1978).
The common idea that the living net production in
organisms, particularly algae and microbes but also
metazoans, dies largely by ingestive predation is not
only unsubstantiated but intuitively unreasonable. Cer-
tainly numerous herbivores and carnivores are efficient
predators, and reproductive population responses can
be rapid in response to increasing growth of prey popu-
lations (e.g. rapid growth of cladoceran zooplankton
Death, detritus, and energy flow 85
and grazing of larger species in blooms of spring phy-
toplankton which leads to a brief 'clear water phase' in
certain eutrophic waters; Sommer et al, 1989).
Many if not most organisms, particularly bacteria and
fungi but also algae and higher organisms simply ma-
ture physiologically, senesce, and die, and then enter
the combined particulate and dissolved detrital pool for
microbial heterotrophic utilization. Productivity is maxi-
mized within the resources available, and at lower
trophic levels the dynamics change with sufficient ra-
pidity to allow many generation turnovers before preda-
tors with much slower turnover rates can respond re-
productively. The magnitude of mortality of bacteria by
viral senescence is large (>50%) and is now emerging as
a major component of turnover (e.g. Suttle, 1992). Simi-
larly, ingestion of bacteria by protists, which purport-
edly 'short circuit' metabolism in the 'microbial loop'
(see discussion below), is a major diversion of organic
carbon from animal trophic levels. In some groups, such
as higher aquatic plants and their attached periphytic
communities, most (>90%) of the production never en-
ters a metazoan digestive tract, analogous to the situa-
tion in terrestrial ecosystems. The concern being raised
here is that estimates of mortality by ingestion of par-
ticles of certain larger sizes, without measurements of
other types of mortality, do not allow accurate conclu-
sions of impacts of particle ingestion on energy fluxes
within the pelagic region or the lake. For very brief
periods such predation may dominate, but this process
cannot persist or dominate for long periods without
inducing marked ecosystem instability (discussed be-
low).
With the loss of cellular integrity upon senescence,
massive losses of soluble cellular components occur
rapidly, often exceeding 40% of the total organic carbon
within the first 24 h (e.g. Krause, 1962; Otsuki & Wetzel,
1974). The DOM lost at this stage usually consists of the
simplest, non-structural organic compounds of rela-
tively high energy and availability to microbes.
Just because we cannot measure non-predatory mor-
tality well does not mean it does not exist or even
dominate at most times of the year. Many assumptions
that the rate of predation on phytoplankton populations
is occasionally high rest on the accuracy of measure-
ments of the prey populations and of the grazing effi-
ciencies of the predators. Despite purported, strongly
coupled, cause and effect, inverse relationships between
prey and predators, the measurement errors are large
even under the best conditions (e.g. Crumpton & Wetzel,
86 R.G. Wetzel
1982). Grazing efficiencies of greater than 50 per cent of
total phytopiankton community and productivity, for
example, are rare and generally very short lived.
Production in the pelagic region and lake ecosystem
continues throughout the year. The annual time period
is the only interval of relevance in comparative analyses
of productivity and utilization of organic matter. Much
of the annual photosynthetic production, even of the
pelagic regions, can occur during cold, low-light pe-
riods when consumption by zooplankton and higher
organisms is reduced or virtually absent (cf. review by
Wetzel, 1983). Although that non-ingested production
may be of little immediate consequence to the metazoan
heterotrophs of the higher trophic levels, this produc-
tivity is of major importance, and usually dominates,
the energy flows within the pelagic region and com-
pletely dominates energy flows of the whole lake eco-
system. The non-ingested particulate and dissolved
organic matter enters the detrital pool for microbial
heterotrophy, and such decomposition is of primary
importance to higher trophic levels in feedback pro-
cesses, both positively (e.g. nutrient recycling and utili-
zation by primary producers) and negatively (e.g. oxy-
gen consumption and production of fermentative meta-
bolic end products).
Sedimentation of living and dead detrital POM is a
dominant feature of lake ecosystems and is occurring
constantly in the pelagic region. Variations in sedimen-
tation rates are large in relation to depth, stratification
and mixing pattems, and to a minor extent depend on
grazing. It is true, as noted by Hairston & Hairston
(1993), that only a small portion of the net phytoplank-
tonic primary production (NPP) reaches the sediment
as particulate organic carbon (POC).t However, much
of the NPP is released as dissolved orgaruc carbon
(DOC) during normal metabolism, and particularly
during senescence and death, whether the latter occurs
'naturally' or during or following ingestion and eges-
tion by predators. Much of the DOC is utilized by
microbes, either directly degraded or cycled intensively,
in the 'microbial loop' of bacteria and proHstians until
mineralized (cf. reviews of Sheer & Sheer, 1988; Caron,
+ This statement is not generally true, however, for the land-water
interface and littoral regions of lake and river ecosystems (cf.
reviews by Wetzel, 1990; Wetzel & Ward, 1993). Rates of deposition
commonly greatly exceed decomposition. Resuspension and
redistribution of these materials occur but transport of particulate
materials to the pelagic region is small; primary export from the
land-water interface regions to the pelagic zone is via dissolved
organic matter.
1991; Sanders, 1991). Although much of the DOC pro-
duced in NPP is not entering higher trophic levels
directly by predation on microbes, and notwithstand-
ing that metabolism of the DOC by microbes is yielding
a 'low return of energy... to the... food chain' (Hairston
& Hairston, 1993, p. 395; but many others as well), does
not mean that this metabolism is a loss or is unimportant
to the energy flows within the pelagic region or the
aquatic ecosystem. Indeed, this metabolism of organic
matter by non-predatory and 'microbial loop' routes
dominates energy flows in both the pelagic region and
the entire lake ecosystem on an annual basis.
Non-predatory carbon and energetic pathways
The distinction between particulate and non-particulate
(dissolved, colloidal) organic matterJ is not trivial. More-
over, the distinction between living and dead organic
matter is not trivial. Obviously, for higher animals that
depend upon ingestion of particles, size is a criterion for
capture and ingestion prior to subsequent enzymatic
hydrolysis of the organic compounds in the gut. Be-
cause of the often higher energetic values of living
particulate organic particles, behavioural evolution may
have favoured selectivity of particle ingestion among
certain animals.§ At any given time, the instantaneous
amounts of dead particulate organic matter equal or
usually exceed that of living particulate organic matter
in the pelagic zone (e.g. Saunders, 1972). The detrital
particulate organic matter is generally heavily colo-
nized by bacteria and fungi, particularly in early stages
of degradation. To ignore or subordinate the nutri-
tional, and ultimately reproductive, value of these detri-
tal particles for ubiquitous omnivorous/detritivorous
planktonic and nektonic animals cannot be justified at
present.
In the planktonic regime, and in aquatic ecosystems
in general, nearly all of the organic carbon consists of
X The demarcation between particulate and dissolved organic matter
is at 0.5 \xm for an array of analytical reasons (Wetzel & Likens,
1991), a size which is below the ingestive capabilities of most
metazoan animals.
§ Such selectivity in food acquisition, however, probably forces
specialization and greater food chain length with accompanying
increased metabolic costs of food acquisition. Omnivory tends to
truncate food-chain length (Hastings & Conrad, 1979; Hairston &
Hairston, 1993). Habitat complexity and heterogeneity, strongly
coupled to food heterogeneity, also influences food chain length
(Persson et al, 1992).

dissolved organic carbon and dead particulate organic
carbon. The ratio of DCXI to POC is between 6:1 and 10:1
in both lake and running water ecosystems (Wetzel,
1984). Although living POC of the biota constitutes a
very small portion of the total POC, particularly in the
pelagic region, the microbial components are important
in mediating the fluxes of carbon between the dissolved
and particulate phases of detrital organic carbon. Or-
ganic matter originates from photosynthesis within the
lake or river ecosystem per se or from the drainage basin.
Particulate organic carbon loadings from the drainage
basin are relatively small; most orgaruc carbon is trans-
ported and imported in dissolved form. Similarly, much
of very high net primary productivity of the wetlands
and littoral land-water interface regions of lake and
river ecosystems enters the pelagic regions as dissolved
organic matter (Wetzel, 1990; Wetzel & Ward, 1993).
This pool of dissolved organic matter is supplemented
by the low phytoplanktonic primary production to vary-
ing degrees in relation to the size and geomorphology of
the lake and river basins. Clearly, most lakes are small
and shallow, and the ratios of organic carbon loadings
from allochthonous and littoral sources to those of the
pelagic are large (Wetzel, 1990). This pool of organic
matter is variously metabolized, sedimented, or ex-
ported.
A contentious prevailing concept is that the energetic
fluxes of the pelagic zone of lakes are driven by the
photosynthetic productivity of phytoplankton. Again
this view emanates from the particulate consumption
viewpoint of heterotrophic utilization. Very little of
either the particulate or dissolved organic carbon that
makes up the detrital pool in fresh water actually enters
the consumer food chain (Wetzel, 1983,1984). Because
this organic carbon does not enter the consumer food
chain, however, does not mean it is neither metabolized
or important. Not only is this organic carbon the domi-
nant energetic pathway but these fluxes are essential to
the maintenance of metabolic stability to the ecosystem.
Metabolic stability of ecosystems
Most of the detrital organic pool, both in particulate and
dissolved phases, of inland aquatic ecosystems consists
of'residual organic compounds of plant materials. The
more labile organic constituents of complex dissolved
and particulate organic matter are commonly hydrolysed
and metabolized more rapidly than more recalcitrant
organic compounds that are less accessible enzymati-
Death, detritus, and energy flow 87
cally. The greater rates of decomposition of the simpler
compounds results in a general increase in the relative
concentrations of the more recalcitrant compounds
with slower rates of metabolism and turnover. Two
pervading relationships emerge from these general
statements that are critical to the correct evaluations
of energy flow in aquatic ecosystems.
1 The recalcitrant DOC is metabolized, although slowly.
The mechanisms by which these complex compounds
are hydrolysed and metabolized are unclear, but at least
0.5% is decomposed per day. In some cases, for example,
bacterial decomposition of aromatic humic compounds
of decomposing plant structural tissues is markedly
accelerated following exposure to mild UV radiation of
normal sunlight (Wetzel, 1993; Wetzel et al, 1994). Or-
ganic carbon budgets of lake and river ecosystems in-
variably cannot balance without an appreciable compo-
nent of decomposition of IXXI from non-pelagic sources.
Detailed studies of many entire lake ecosystems indi-
cate that a majority of the energy flows are utilizing non-
planktonic organic carbon and that most of the het-
erotrophic metabolism is microbial and benthic rather
than planktonic (Wetzel et al, 1972; Wetzel, 1983; Pace,
1993).
2 Predominance of a dissolved organic detrital carbon
pool that is very much larger than the total carbon in
planktonic particles, and is dominated by relatively
recalcitrant organic matter, results in a collectively large
but slow rate of microbial heterotrophy. Similarly, in the
benthic component of the ecosystems, particulate or-
ganic matter is dominated by detrital organic matter
that is often metabolized much more slowly, because of
both residual organic matter of relatively large particle
sizes and environmental conditions (e.g. reducing con-
ditions) that slow rates of heterotrophic microbial me-
tabolism. Similarly, in the benthic environment, the
organic matter is concentrated, and although specific
metabolism per unit organic matter is less, the cumula-
tive decomposition usually far exceeds that of the inte-
grated water column overlying the sediments.
In planktonic systems, extreme fluctuations in popu-
lation sizes of both producers and consumers are quite
typical (Wetzel, 1983, p. 702; 1984; Hairston & Hairston,
1993). The living components generally exhibit rapid
oscillations of productivity and of heterotrophy by con-
sumers in an opportunistic series of competitive re-
sponses to rapid changes in availability of constraining
factors governing growth and mortality. In contrast, the
dominant pool of organic carbon in the dissolved form.
88 R.G. Wetzel
as well as particulate organic carbon, is both large and
relatively recalcitrant to rapid microbial heterotrophy.
From the standpoint of the composite energy flow of the
ecosystem, it is irrelevant whether the organic carbon is
in particulate or dissolved form. From the standpoint of
metabolic stability, however, it is particularly important
that most of the organic carbon is dissolved and rela-
tively recalcitrant, which ameliorates the violent oscilla-
tions so characteristic of the particulate components of
the ecosystem. Herein resides ecosystem stability: a
large pool of slowly degrading organic matter is main-
tained because of the combined complex chemical struc-
ture of the dissolved organic substrates and because
much of the particulate organic matter is displaced to
reducing, anoxic environments of the littoral and
profundal sediments. Animal trophic couplings and
energy flows are one component of but do not control
ecosystem energy fluxes and stability. Rather, the large
pool of organic carbon, and particularly of dissolved
organic carbon largely of higher plant origins, provides
this stability and is the currency for the quantitatively
more important detrital pathways in aquatic ecosys-
tems.
Acknowledgments
I particularly acknowledge the stimulating interactions
with Peter H. Rich, Gene E. Likens, Karen G. Porter,
Amelia K. Ward, and Nelson G. Hairston Jr. on this
subject. The editorial critique of A. G. Hildrew is greatly
appreciated. Portions of this research were supported
by subventions of the National Science Foundation and
the Department of Energy.
References
Caron D.A. (1991) Evolving role of protozoa in aquatic
nutrient cycles. Protozoa and Their Role in Marine Processes
(eds P.C. Reid, CM. Turley and P.H. Burkill), pp. 387-
415. Springer-Verlag, Berlin.
Chen C.Y. c& Folt C.L. (1993) Measures of food quality as Sherr E. & Sherr B. (1988) Role of microbes in pelagic food
demographic predictors in freshwater copepods. fournal
of Plankton Research, 15,1247-1261.
Crumpton W.G. & Wetzel R.G. (1982) Effects of differential Sierszen M.E. & Brooks A.S. (1982) The release of dissolved
growth and mortality in the seasonal succession of phy-
toplankton populations in Lawrence Lake, Michigan.
y, 63,1729-1739.
Hairston N.G. Jr. & Hairston N.G. Sr (1993) Cause-effect
relationships in energy flow, trophic structure, and inter-
specific interactions. American Naturalist, 142, 379-411.
Hastings H.M. & Conrad M. (1979) Length and evolution-
ary stability of food chains. Nature (London), 282, 838-
839.
Hrba&k J. (1962) Species composition and the amount of
the zooplankton in relation to the fish stock. Rozpravy
Ceskoslovenske Akademie Vid, Rada Matematickych a
PfirodnichV id 72(10), 1-114.
Hrbac! ek J., Dvof akova M., Kof lnek V. & Prochazkova L.
(1961) Demonstration of the effect of the fish stock on the
species composition of zooplankton and the intensity
of metabolism of the whole plankton association. Ver-
handlungen der Internationale Vereingung fiir theoretische
und angewandte Limnologie, 14,192-195.
Krause H.R. (1962) Investigation of the decomposition of
organic matter in natural waters. FAO Fisheries Biology
Report 34(FB/R34), 1-19.
Lampert W. (1978) Release of dissolved organic carbon by
grazing zooplankton. Limnology and Oceanography, 23,
831-834.
Otsuki A. & Wetzel R.G. (1974) Release of dissolved or-
ganic matter by autolysis of a submersed macrophyte,
Scirpus subterminalis. Limnology and Oceanography, 19,
842-845.
Pace M.L. (1993) Heterotrophic microbial processes. The
Trophic Cascade in Lakes, (eds S.R. Carpenter and J.F.
Kitchell), pp. 252-277. Cambridge University Press, New
York.
Persson L., Diehl S., Johansson L., Andersson G. & Hamrin
S.F. (1992) Trophic interactions in temperate lake ecosys-
tems: A test of food chain theory. American Naturalist,
140,59-84.
Porter K.G. (1975) Viable gut passage of gelatinous green
algae ingestedhy Daphnia, Verhandlungen der Internationale
Vereinigungfiir theoretische und angewandte Limnologie, 19,
2840-2850.
Rich P.H. & Wetzel R.G. (1978) Detritus in lake ecosystems.
American Naturalist, 112, 57-71.
Sanders R.W. (1991) Mixotrophic protists in marine and
freshwater ecosystems, fournal of Protozoology, 38,76-81.
Saunders G.W. (1972) The transformation of artificial detri-
tus in lake water. Memorie deU'Istituto Italiano di Idrobiohgia
29 (Suppl.), 261-288.
webs: A revised concept. Limnology and Oceanography, 33,
1225-1227.
organic carbon as a result of diatom fragmentation dur-
ing feeding by Mysis relicta, Hydrobiologia, 93,155-161.
Sommer U., Gliwicz G.M., Lampert W. & Duncan W. (1986)
 Death, detritus, and energy flow 89
The PEG-model of seasonal succession of planktonic on humic compounds and total dissolved organic
events in fresh waters. Archiv fiir Hydrobiologie, 106,433- carbon. Abstracts American Society ofLimnology and Ocean-
471. ography, p. 136. Edmonton, Alberta.
Suttle C.A. (1992) Inhibition of photosynthesis in phy- Wetzel R.G., Rich P.H., Miller M.C. & Allen H.L. (1972)
toplankton by the submicron size fraction concentrated Metabolism of dissolved and particulate detrital carbon
from seawater. Marine Ecology Progress Series, 87, 105- in a temperate hard-water lake. Memorie deU'Istituto
112. Italiano di Idrobiohgia 29(Suppl.), 185-245.
Wetzel R.G. (1983) Limnology, 2nd edn. Saunders, Philadel- Wetzel R.G. & Likens G.E. (1991) Limnological Analyses, 2nd
phia. 860 pp. edn. Springer-Verlag, New York. 394 pp.
Wetzel R.G. (1984) Detrital dissolved and particulate Wetzel R.G. & Ward A.K. (1992) Primary production. Riv-
organic carbon functions in aquatic ecosystems. Bulletin ers Handbook (eds P. Calow and G.E. Petts), pp. 354-369.
of Marine Science, 35, 503-509. Blackwell Scientific Publications, Oxford.
Wetzel R.G. (1990) Land-water interfaces: Metabolic and Wetzel R.G., Bianchi T.S. & Hatcher P.G. (1994) Ultraviolet-
limnological regulators. Verhandlungen der Internationale B photolysis of dissolved organic matter and enhanced
Vereinigung fiir theoretische und angewandte Limnologie, bacterial productivity in aquatic ecosystems. Applied and
24, 6-24. Environmental Microbiology (in review).
Wetzel R.G. (1993) Ultraviolet photolysis of dissolved
organic compounds: Enhanced bacterial productivity (Manuscript accepted 6 September 1994)