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Detritus and Nutrients in Food Webs

Michael J. Vanni and Peter C. de Ruiter

A goal of this book is to integrate various approaches to the study of food webs so that a better understanding of the structure and dynamics of food webs can be gained. In this section we see this call for integration emphasized, and in fact extended. All chap­ters point to the need to integrate two histori­cally separate approaches to ecology-popu­lation interactions and ecosystem processes. Specifically, this set of chapters shows-in a diversity of ways-how explicit incorpora­tion of detritus and nutrients as compartments in species-based food webs can improve our understanding of how food webs are regu­lated. The authors argue that in order to ade­quately understand species interactions we may need to incorporate ecosystem pro­cesses, and vice versa. Such integration can clarify our understanding of several general ecological concepts, including the relative roles of top-down and bottom-up forces; the importance of spatial and temporal scale; the role of individual species in ecosystem pro­ces ses such as nutrient recycling and nu trient budgets; the relative importance of direct and indirect effects; and the roles of organism size and the microbial food web in the regula­tion of energy ftow. Here we first describe key aspects of each chapter and then conclude with some general emergent concepts.

Bengtsson et al. (Chapter 2) point out that soil ecologists have long recognized that the structure of the detrital food web (i.e., spe­cies composition, number of trophic levels, feeding habitats of particular species, etc.) and ecosystem functioning (i.e., decomposi­tion, nu trient recycling, etc.) are linked in

25

soil ecosystems, but that few studies have explicitly studied these linkages. In particu­lar, the recognition that animals higher in the food chain are important for ecosystem processes still needs to be incorporated into research programs on soil food webs.

Bengtsson et al. also emphasize that con­sumers have important indirect effects on re­sources, and that to understand these indirect effects, a more broad-based approach to the study of soil food webs is needed. The broader approach should include incorpora­tion of consumer effects on nutrient recycl­ing, and a longer timescale perspective. For example, grazing of fungal hyphae by inver­tebrates can remineralize nutrients, which then become available to plants. Bengtsson et al. review the results of a model (Bengtsson et al. , 1994) that predicts that rates of decom­position, and hence nutrient remineraliza­tion, may be affected by food web attributes such as consumer mortality and feeding rates, number of trophic levels, and number of food chains. This points out the need to character­ize species-based food webs for a better un­derstanding of ecosystem processes . These authors also point out that considering such indirect effects of consumers and longer timescales casts doubt on the textbook para­digm that soil food webs are donor-con­trolled, that is, the abundance of a resource controls the abundance of its consumer, but not the reverse (Pirnm, 1982). In the short term, consumers in soil food webs may not control the input of detritus, the main re­source in these webs, because this is largely a function of litter input from the aboveground

G. A. Polis et al. (eds.), Food Webs© Springer Science+Business Media Dordrecht 1996

26 / Michael J. Vanni and Peter C. de Ruiter

food web. However, over long timescales, remineralization of nutrients by consumers in soils may increase plant growth rates, alter plant tissue content (e.g., reduce C:N ratios) and modify plant species composition by al­tering competitive relationships. Such effects on plant communities may have strong effects on the production, composition, and refracti­vity of detritus (Vitousek and Walker, 1989; Wedin and Tilman, 1990; Hobbie, 1992), which can then feed back into effects on soil food webs. It is thus evident that the timescale of investigation will affect conclusions re­garding the relative importance of top-down and bottom-up forces because the indirect effects of consumers on detrital supply and nutrient content will occur over longer time­scales than the direct effects of consumers on their prey.

Coleman (Chapter 3) points out that soil food webs seem to be characterized by long food chain lengths and by pronounced spatial heterogeneity. Both of these characteristics can infiuence how nutrients are recycled by the detritus-based web and how this feeds back to the aboveground, grazing-based web. As pointed out above, food chain length can affect the rates of nutrient remineralization (Bengtsson et al., 1994). Spatial heterogene­ity is manifested in hot spots or arenas of interest where consumer activity is high . Ex­amples include rhizospheres, soil particle-mi­crobe aggregates, patches of litter at the soil surface, and earthworm burrows. Each of these areas represents a relatively small per­centage of total soil volume yet may contain disproportionate numbers and activity of soil organisms. Thus, nutrient remineralization rates, and hence their effects on plant com­munities, can be expected to be spatially heterogeneous. Earthworms seem to be par­ticularly important in linking soil and aboveground food webs because their bur­rowing activities encompass larger spatial scales than do activities of smaller soil food web members and because considerable evi­dence exists that earthworms have strong ef­fects on nutrients recycling in soils (James, 1991). Thus Coleman stresses that detritus is not a spatially homogeneous pool, and reiter­ating one theme of Bengtsson et al. , empha­sizes the fact that the composition and supply of detritus is controlled at least partially by

the activities of consumers within soil food webs.

Gaedke et al. (Chapter 5) quantify carbon fiows in a large freshwater pelagic ecosys­tern, Lake Constance. They assess how much C (and hence energy) travels through grazing­based and detritus-based food chains. Detri­tus in this and other large pelagic food webs consists of particulate and dissolved organic materialleaked from the grazing-based food chain, in contrast to smaller aquatic ecosys­terns such as streams and small lakes where detritus is at least partly terrestrial in origin. Thus an important question addressed by the authors is how much of the leaked C makes its way back to the grazing-based food chain by way of the detritus-based food chain. Con­surners such as ciliates, rotifers, and crusta­ceans are important in this role because they prey on detritus-consuming bacteria as weIl as phytoplankton, and are preyed upon by larger animals. Thus they link the two food chains. Gaedke et al. found that although fiux of C through the detritus-based food chain was substantial, little of this energy makes it to animals at the top of the grazer food chain (fish). The loss of C within the detrital chain occurs because there are more steps (trophic transfers) in this food chain compared to the grazer-based chain. Gaedke et al. propose that organism size structure has bearing on this process. Energy transfer in pelagic food webs generally occurs along a gradient of organism size, with each consumer succes­sively larger than its resource. Because mem­bers of the basal trophic level of the detrital food chain (bacteria) are smaller than those of basal level of the grazer-based chain (phy­toplankton), more trophic transfers occur be­tween the basal and top members in the detri­tal chain than in the grazer chain. Thus, food web structure, and in particular size structure, appears to have a large infiuence on energy transfer.

Stemer et al. (Chapter 6) point out that food webs have traditionally been character­ized by population and community ecologists as trophic webs (diagrams of predator-prey interactions) and by ecosystem ecologists as chemical webs (diagrams of fiuxes of matter/ energy among ecosystem pools), with httle attempt to unify the two approaches until re­cently (DeAngelis, 1992). With such unifi-

cation as a goal, they introduce the tropho­chemical diagram, a conceptual scheme combining trophic and chemical webs. This resembles a traditional food web diagram in that there are connections representing preda­tor-prey interactions, but in this case species are positioned upon a chemical coordinate grid. The diagram allows simultaneous as­sessment of trophic relationships, nutrient pools of particular species, nutrient ratios of organisms' bodies, and the quality of food for a given consumer (in terms of nutrient availability). The diagram can thus be used to infer which nutrient is most likely to be limiting for a given species, i.e., information relevant to population and community con­cepts such as demography and competition. Simultaneously, because the nutrient most limiting growth is likely to be recycled at a relatively low rate compared to the nonlim­iting nutrient, the diagram can permit insights into the rates and ratios by which consumers recycle nutrients-i.e., information relevant to ecosystem processes. Trophochemical dia­grams from three northern temperate lakes reveal some consistent patterns. For exam­ple, as nutrients are transferred up the food chain by consumptive interactions, phospho­rus seems to be successively accumulated in organisms relative to nitrogen. As pointed out by Sterner et al. (Chapter 6) and earlier by Paine (1988), the nature in which food webs are pictorially displayed has great bear­ing on conclusions and inferences drawn by ecologists regarding food web pattern and process. Therefore, this diagrammatic at­tempt to wed population and ecosystem ap­proaches to the study of food webs may weil be a big step toward a more holistic food web ecology.

Vanni (Chapter 7) discusses how consum­ers can move nutrients between habitats in lakes and also discusses the implications for the study of food webs and biogeochemical cycles. Consumers in lake food webs (fish, zooplankton, benthic invertebrates) can transport nutrients at a variety of spatial and temporal scales, depending on their mobility, feeding habits, and life history traits. The scale at which nutrients are transported has implications for phytoplankton community structure because phytoplankton species dif­fer in their ability to sequester pulses of nutri-

Detritus and Nutrients in Food Wehs / 27

ents and convert these into new biomass. An example of consumers that may be important in transporting nutrients are fish that feed on benthic or littoral prey. These fish sequester into their growth some of the nutrients in­gested from benthos, but some nutrients are excreted in dissolved inorganic form in open waters (pelagic habitats), where the nutrients are available to phytoplankton. Thus, fish may act as nutrient pumps, transporting nutri­ents from benthic to pelagic habitats. Such effects have largely been ignored in studies of biogeochemical cycles and nutrient budgets. Vanni focuses on gizzard shad, a fish species that feeds on detritus on the lake bottom and which dominates warm-water North Ameri­can lakes and reservoirs. Through the nutrient pump mechanism, excretion of nutrients by these fish probably represents a substantial flux of nutrients (N and P) from benthic to pelagic habitats. Using a mass-balance ap­proach, Vanni shows that the rates and ratios at which nutrients are pumped from sediment detritus to open waters by gizzard shad de­pend heavily on the nutrient composition of detritus. When detritus is relatively enriched in P, fish excrete P at a relatively high rate and also excrete at a low N:P ratio. Fish size is also hypothesized to be an important influence because the N and P contents of fish bodies depend on their size (larger fish have a relatively higher P and lower N content in their tissues than smaller fish). These stoi­chiometric relationships, combined with lower mass-specific ingestion rates of larger fish, should lead to lower P excretion rate and higher N:P ratio excreted by large fish compared to smaller fish. Because phyto­plankton community dynamics are often driven by nutrient supply rates and ratios, the effects of detritivorous fish on phytoplankton communities through the nutrient pump mechanism may depend on food quality (nu­trient content of detritus) and fish population age (size) structure. Thus we see that popula­tion-level (e.g., abundance, age structure) and individual-level (e.g., food selection, al­lometric relationships) traits may play key roles in ecosystem processes.

Schindler et al. (Chapter 8) also discuss how fish can transport nutrients from littoral to pelagic habitats, focusing on northern tem­perate lakes, where many planktivorous fish

28 / Michael J. Vanni and Peter C. de Ruiter

also consume littoral prey such as insects. They provide evidence, through a modeling approach, that this process can represent a substantial ftux of phosphorus from littoral to pelagic habitats. Thus we see here and in the preceding chapter that in both cool, northem temperate lakes and warm-water res­ervoirs, fish may be important in driving bio­geochemical cycles, nutrient budgets, and, hence, the dynamics of primary producers. In addition, Schindler et al. show that the fate of phosphorus transported by fish may depend on pelagic food web structure. When the food web is dominated by planktivorous fish, much of the P transported by fish accu­mulates as phytoplankton biomass. This is because phytoplankton can utilize P excreted by fish and are not limited by grazing herbi­vores (because herbivores are held in check by planktivorous fish). However, when pi­scivorous fish are abundant, much less P is transported by fish, because these larger fish have lower mass-specific feeding and excre­tion rates than smaller fish. Because of this and because herbivorous zooplankton are more abundant, a much greater percentage of the originally littoral P eaten by fish accu­mulates as fish biomass, while much less P accumulates as phytoplankton, as compared to food webs dominated by planktivorous fish. Thus, food web structure affects the strength and fate of littoral pelagic nutrient transport by fish. In addition, much of the trophic cascade effects of fish on phytoplank­ton may be fueled by energy and nutrients derived from littoral habitats and transported to pelagic habitats by fish.

These six chapters thus illustrate the im­portance of nutrients and detritus in the study of food webs. An important recurring theme is that in order to adequately understand the importance of species interactions (i.e., the inftuence of a given species on other species' dynamics), often we must incorporate how particular species affect the nutrient and detri­tal components of food webs and how this feeds back into effects on other species. Thus species effects on ecosystem processes need to be considered in order to understand spe­cies interactions . Conversely, it is also clear that in order to understand ecosystem aspects such as the processing of detritus, nutrient recycling, and nutrient budgets, the role of individual species must be considered, be-

cause some species have particularly strong andJor unique inftuences on these processes. An emerging example of how population in­teractions and ecosystem processes may be intertwined in food webs is recent theory sug­gesting that nutrient and detritus availability greatly affect the stability of predator-prey interactions (DeAngelis et al. , 1989; DeAngelis, 1992; Moore et al. , 1993).

The chapters in this section also show that it is untenable to characterize food webs as being controlled from either the top-down (i.e., consumers controlling their prey re­sources) or bottom-up (i.e., resources con­trolling consumers). This is because consum­ers have strong impacts on resources such as nu trients and detritus, and this feeds back into effects on members of the food web. The chapters in this section show how nu trient recycling among detritus, decomposer mi­crobes, animals and primary producers links top-down and bottom-up processes in both lake and soil food webs. It is also worth noting that in some cases, the importance of these indirect feedback effects are visible only when food web regulation is viewed at longer temporal scales than are typically considered, and at expanded conceptualiza­tions explicitly incorporating both population interactions and ecosystem processes. This echoes the recognition that population and ecosystem processes can occur at similar spa­ti al and temporal scales, and that a clearer understanding of ecology can emerge from melding population and ecosystem ap­proaches (Allen and Hoekstra, 1992).

The chapters in this section focus on food webs of two ecosystem types-soils and lakes-no doubt in part because detrital and nutrient compartments are relatively weIl characterized in these ecosystems. In addi­tion to the soil and lake food web examples presented in this section, many examples of how animals inftuence ecosystem processes, and how these have feedback effects on plants and other food web members, now exist from a variety of ecosystem types and animals. These include ungulate herbivores in the Ser­engeti (McNaughton et al., 1988), moose in the boreal forest (Pastor et al., 1988), prairie dogs (Whicker and Detling, 1988), and go­phers in old fields (Huntly and Inouye, 1988). While the particular pathways by which ani­mals regulate plants and other food web mem-

bers differ among these ecosystems, the com­mon thread is that effects of animals are often manifested through effects on nutrients, detri­tus, and other abiotic resources.

As is mentioned above and throughout this section, there exists an increasing desire among ecologists to unify the areas of popula­tion interactions and ecosystem processes (Reiners, 1986; Allen and Hoekstra, 1992; DeAngelis, 1992; Jones and Lawton, 1994). Consumer influence on detritus production and nutrient recycling, and how this affects other food web members, provides a clear example of why we need to integrate these areas as weIl as an example of how such integration can be achieved.

Early ecosystem ecologists recognized that certain animal species can have dispropor­tionate effects on ecosystem processes such as biogeochemical cycles (Hagen, 1992). For example, more than three decades ago Kuen­zIer (1961) showed that a particular mussei species had a great influence on phosphorus cycling in a saIt marsh even though it was a minor component of the food web in terms ofbiomass. However, in the last few decades the disciplines of population and ecosystem ecology have diverged. Recent studies (in­cluding chapters in this section and and refer­ences therein) attempt to strengthen the link between these two areas. Furthermore, recent approaches go further toward unifying these areas because they not only quantify the ef­fects of particular species on ecosystem pro­cesses but also assess how these effects are manifested at the population and community levels. Thus these two areas are being inte­grated to a much greater extent than in the past. Clearly then, linkages between popula­tions and ecosystems must be widespread and therefore need to be incorporated more ex­plicitly in future conceptual models and in­vestigations of food webs, as suggested by Reiners (1986) nearly a decade ago. It is our hope that these six chapters and the synthesis that follows will help achieve this goal.

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Detritus and Nutrients in Food Webs / 29

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