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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

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.

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Trophic structure in the pelagic zone: not only a 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

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,

Death, detritus, and energy flow

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

& 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.

to the

food chain' (Hairston

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

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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.

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 Vereingungfiir 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.

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.

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 ofProtozoology, 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. Sherr E. & Sherr B. (1988) Role of microbes in pelagic food webs: A revised concept. Limnology and Oceanography, 33,

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(Manuscript accepted 6 September 1994)