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FIGURE 6.7 Leaf litter breakdown in a stream ecosystem. (From Cushing, C. E. and J. D. Allan. 2001. Streams: Their Ecology and Life. Academic Press, San Diego, CA. With permission.)

Cummins and Klug, 1979) has developed a classification of functional feeding types of stream invertebrates which illustrates the different roles. His classification includes shredders, collectors, scrapers, and predators, depending on mouthparts and behavior of the animal. The shredder category is particularly important in fragmentation of large pieces of detritus into smaller particles (Anderson and Sedell, 1979; Cummins et al., 1973, 1989; Wallace et al., 1982). Particle size is important in decomposition because it determines the surface area per unit mass exposed to microbial colonization and metabolism. In some commercial-scale composting facilities this kind of fragmentation is carried out with mechanical grinding machines but it is an expensive step that is not always possible. However, in nature it is an inherently important contribution that accelerates the decay process. Figure 6.7 depicts the leaf breakdown process that occurs in freshwater streams. Physical leaching quickly causes an initial weight loss during the first few days. Mineralization by microbes follows after they begin to colonize the leaf surface. Invertebrate animals colonize later and breakdown the main structure of the leaf through their feeding. Complete detritus processing requires approximately 1 year in the temperate zone and follows the exponential decay model described in Chapter 2. A more detailed graphic display of leaf breakdown for a terrestrial forest ecosystem is given by Schaller (1968). Bormann and Likens (1979) identify several fragmentation processes: fenestration, perforation, and deskeletonization and refer to these actions as a kind of "coordinated attack" in the quote given below:

... it would appear that as soon as soft tissues such as leaves or bud scales fall to the forest floor they are subject to a coordinated attack. ... Fungi and bacteria initiate the action but are soon joined by springtails, bark lice, and various larvae which eat or tear holes in the tissue (fenestration), opening it to more rapid microbial attack. Larger larvae and mites bring about further perforation and skeletonization. Large amounts of feces, or frass, are produced, which may be consumed again by other fauna. The activities of the soil fauna and microflora are thus closely linked. Chewing, ingestion, and digestion by fauna not only result in decomposition of the organic matter but simultaneously create surface and moisture conditions more favorable to microbial action both within the faunal gut and in the resultant frass. It seems likely that the detritivores obtain their principal energy supplies from the easily decomposable substances within the litter such as sugars, starches, and simple and crude proteins. Exoenzymes of fungi and bacteria not only attack these easily decomposable substances but are largely responsible for the decomposition of the more resistant compounds, such as hemicellulose, cellulose, and lignins, which compose the bulk of the leafy and wood litter.

Thus, invertebrates are important regulators of the decomposition process in natural ecosystems (Anderson and MacFadyen, 1976; Coleman, 1996; Edwards et al., 1970; Lussenhop, 1992; Seastedt, 1984; Visser, 1985). In addition to the physical breakdown or fragmentation which facilitates microbial colonization, invertebrates

(1) create zones of active microbial growth through mixing and other actions,

(2) select for fast-growing microbial populations through direct grazing, and

(3) fertilize microbes through release of nutrients in their excretion. When highly focused, these kinds of control actions have been referred to as "microbial gardening" (Hylleberg, 1975; Reise, 1985; Rhoads et al., 1978) in that the animals directly channel microbial production into their own growth. An example of this interaction can be seen with the leaf-cutter ants (Attine ants: genera Atta and Acromyrmex) of the tropics that intentionally cultivate fungi for food in their belowground nests with leaves that they cut from the surrounding trees (Lugo et al., 1972; Weber, 1972).

The control of decomposition in soils by earthworms is well known. Charles Darwin (1881) provided some early quantification of the role of earthworms in the last book he wrote before his death in 1882. He felt earthworms were the most important animals on Earth because of their contribution to soil fertility. Earthworms are considered to be keystone species in terrestrial ecosystems because of their (1) physical effects on soils, (2) biogeochemical effects on nutrient cycles, and (3) enhancement of species diversity (Blondel and Aronson, 1995). A huge literature exists on the ecology of earthworms (Edwards, 1998; Satchell, 1983), including popular books with titles such as Worms Eat My Garbage (Appelhof, 1997) and Harnessing the Earthworm (Barrett, 1947). Earthworm biotechnology (Hartenstein, 1986) includes vermicomposting, where earthworms are managed to accelerate composting, and vermistabilization, where they are managed for sewage sludge processing (Reed et al., 1995).

The paradigm that emerges from this review is that animals manage microbial work in natural ecosystems (Figure 6.8A). In some cases anaerobic microbes occur within the digestive systems of animals (Figure 6.8B). This is an important type of symbiotic relationship to which both taxa contribute. The animals bring food to the microbes and provide anaerobic microenvironments that are necessary for their survival in otherwise aerobic environments. The microbes break down the food with special enzymes that the animals lack. Although many animals have symbiotic gut microbes, the most highly developed example is the herbivore group of ruminants, including cattle, sheep, and deer. These animals have four stomachs and a symbiotic food web

FIGURE 6.8 Energy circuit diagrams of animal control over microbes in various ecosystems. (A) Conceptual view. (B) Digestive microbes in a ruminant system. (C) Soil microbes in crab burrows. (From Odum, H. T. 1983. Systems Ecology: An Introduction. John Wiley & Sons, New York.)

of bacteria and protozoans with densities of more than 100 million organisms/ml of stomach solution (Hoshino et al., 1990; Hungate, 1966). Ruminant digestion consists of a sequential set of processes: mastication (chewing), pregastric fermentation (breakdown of cellulose in the first stomach), regurgitation of "cud," and acid hydrolysis in the last stomach. This pattern has been suggested as being comparable to the processes in a sewage treatment plant and even has been an inspiration for the design of biore-actors (Beeby, 1993)! Also relevant here is the work of Penry and Jumars (1986, 1987; Jumars, 2000) on modeling animal guts as chemical reactors. Other animals control microbes in external environments (Figure 6.8C). Examples of this kind of control include shredding and gardening mentioned earlier. Burrowing by animals in soils, sediments, and other materials also provides microenvironments that enhance micro-bial activities (Meadows and Meadows, 1991). Various invertebrates have been classed as "ecosystem engineers" because of these kinds of roles in aquatic sediments (Levinton, 1995) and soils (Anderson, 1995).

The question for ecological engineering is whether elements of animal control over microbes can be incorporated into composting systems. Does the tremendous untapped biodiversity of animals from natural ecosystems represent an opportunity for improved composting? The challenge is to design and test new composting ecosystems that have higher biodiversity and more effective decomposition efficiency. Many possible systems can be imagined. Can carrion-based food webs (Payne, 1965) be used to accelerate composting of carcasses at animal farm operations (Murphy and Carr, 1991)? Can burrowing clams (Pholadidae) (Komar, 1998) or the high diversity of bioeroders on coral reefs (Glynn, 1997) be used to break down limestone and concrete construction materials? Can marine boring organisms such as gribbles (isopods of the family Limnoridae) or shipworms (clams of the family Teredinidae) (Ray, 1959) or terrestrial termites (Termitidae) (Lee and Wood, 1971) be used to break down wooden construction materials?

Although some commercial-scale municipal composting facilities do operate in the U.S. and elsewhere, the economics is not very favorable. An exception is composting of sewage sludge which is generated by conventional wastewater treatment plants and by septic tank owners. This is a major industry with well-developed technologies (Clapp et al., 1994; Smith, 1996). Stabilization of sewage sludge requires dewatering, after which composting is often utilized. One fairly common practice is to spread the stabilized sludge on agricultural fields for further decomposition and for use as a soil amendment. This mimics the old practice of manuring, whereby animal wastes from farms are applied to fields (Klausner, no date). This kind of composting can have positive benefits as long as proper application rates are used. The application of excess sludge or animal manure can lead to environmental problems such as nonpoint source pollution. This issue brings to focus the sometimes conflicting motivations of composting. On the one hand, composting is (1) a way of disposing of a waste product while, on the other hand, it is (2) a way of producing a useful product. The potential exists for conflicts to arise between these two motivations. For example, sewage sludge or animal manure may be spread on land with the apparent motivation of improving the soil (motivation [2] above) when actually it is done just to dispose of waste materials (motivation [1] above). In this case, excessive applications can easily occur, creating environmental impacts rather than subsidies. This same phenomenon can occur with the use of dredge material for marsh restoration, as was described in Chapter 5. Composting systems for sewage sludge and animal manures may represent the best opportunities for the incorporation of ecological engineering improvements because these operations are large-scale and common. In this regard reed-based wetland systems are widely used for dewatering sewage sludge at the present time.

The compost toilet is a commercially successful composting system that is particularly relevant for ecological engineering (Del Porto and Steinfeld, 1999; Jenkins, 1994; Stoner, 1977; Van der Ryn, 1995). These are toilets which are meant as a substitute for the flush toilet, requiring little or no water. Human feces are collected and stabilized in the composting toilet and, later, used as a soil amendment. Many designs are available but most take the form of an outhouse with storage chambers, aeration with ducts or venting and the addition of a material such as sawdust that acts as an absorbent (Figure 6.9).

FIGURE 6.9 Energy circuit diagram of a composting toilet.

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