The decomposer community, though not readily visible by virtue of its small size, is an important component of the ACE Basin study area. The term decomposers is used to describe a guild of organisms (e.g., bacteria, fungi, crabs) that process organic constituents (e.g., plant material) to release carbon and other nutrients such as nitrogen (N) and phosphorus (P). This process creates a key link in transfer of energy and cycling of nutrients between various trophic groups in an ecosystem. This transfer of energy from one trophic group to another occurs via the consumption, death and decay of organisms. The breakdown of organic matter and conversion of organically bound nutrients into basic inorganic forms is called mineralization.
Decomposition of organic matter is chiefly regulated by three interacting factors: (1) the decomposer community; (2) the physicochemical environment and; (3) the quality of resource (see organic matter ). In wetland sediments, the soil atmosphere, soil pH, temperature, redox potential and soil structure comprise the physicochemical environment. The redox potential is a measure of the probability of a substance to gain (to be reduced) or lose (to be oxidized) electrons. In addition, the quality of organic matter (estimated by the ratio of its carbon and nitrogen content or C:N ratio) largely determines the rate of carbon turnover and varies with the vegetation type.
The ACE Basin ecosystem comprises various types of sub-ecosystems differing in their biotic and physicochemical properties which control the activity and abundance of decomposers. For instance, the hydro-ecosystem (water columns) and the litho-ecosystem (adjoining marshes) of the ACE Basin study area form the two major environments for decomposition processes. In addition, both the water column and the adjoining wetlands can be further subdivided into fresh, brackish and salt water regions depending on the extent of sea water intrusion due to tidal forcing. Changes in salt concentration and associated parameters such as pH and redox potentials impact the functioning and abundance of decomposers. For example, the abundance of free bacteria decreases exponentially along the salinity gradient, as has been observed for the St. Lawrence estuary (Painchaud et al. 1996). Similarly, estuarine hydrodynamics additionally influence the distribution and function of the microbial community and the type of dominant vegetation that is a source of organic carbon for the decomposers.
In river-dominated tidal estuaries, such as the ACE Basin study area, an important source of carbon is the dissolved organic carbon (DOC) transported from upstream sites to the downstream marshes. This is of particular relevance to the ACE Basin because this ecosystem includes the Edisto River which is laden with dissolved and particulate organic matter; as a result, the Edisto River is often called a blackwater river. Inland waters are dominated by DOC from degradation of terrestrial and aquatic plants. In such waters, DOC can account for about 80% of the total organic carbon pool (DOC + particulate organic carbon attached to clay and sediment particles; Wetzel et al. 1995). The DOC leached from decomposing litter is a mixture of compounds of differing lability. For example, DOC may consist of simple sugars of high lability, organic compounds with intermediate lability and refractory compounds, such as humic acids, with low lability. During transport, more labile compounds of this heterogenous mixture are selectively degraded by microbiota, so that eventually only the refractory fraction of the original DOC reaches the estuaries. This refractory substance is subjected to increased residence time on reaching the estuary. Other abiotic factors such as hydrological conditions and salinity further transform DOC and contribute to the import of organic carbon aggregates and other nutrients to adjoining wetland surfaces.
The organic carbon source in wetlands and soils from other environments is chiefly derived from plant residues, and the quality of the organic substrate is determined by the dominant vegetation. Most plant matter consists of carbohydrates (made up of carbon, hydrogen and oxygen, e.g., sugars, hemicellulose and cellulose), proteins and lignin. Soluble sugars and other simple carbohydrates are energy rich organic compounds composed of carbon, hydrogen and oxygen produced during photosynthesis. Hemicellulose and cellulose are increasingly complex forms of carbohydrates; the former partially soluble and the latter inert. These plant constituents are broken down into less complex forms during decomposition by bacteria and fungi. Proteins are made of subunits called amino acids, which are nitrogen containing compounds. Proteins are degraded very rapidly as they are the most abundant nitrogen containing constituent (see the subsection on organic matter quality). Lignins are organic substances that, with cellulose, form the chief part of a woody tissue in plants. The lignin fraction of plant residue is the slowest to degrade and its decomposition is accomplished primarily by fungi (Paul and Clark 1996). In salt marsh sediments, however, bacterial assemblages are more efficient (relative to fungi) in degrading the lignocellulosic fraction of Spartina alterniflora (Benner et al 1984), which is the dominant vegetation in salt marshes in the southeastern USA and the ACE Basin study area.
Decomposers play an important role in formation of soil organic matter by degrading energy rich organic compounds and, in the process, by generating more refractory materials such as humus. In addition, several species of epiphytic fungi are associated with various plant parts of Spartina alterniflora . Some of these species produce humic acid-like substances that could contribute substantial amounts (330 Kg/ha) to the annual input of humic substances in salt marshes (Filip and Alberts 1988, 1989, 1993). Such forms of organic matter are dark colored, complex organic material that are slow to degrade and are depleted in their oxygen and nitrogen content relative to the parent plant and animal organic material. These refractory materials are broadly classified into three main categories (humic acids, fulvic acids and humins) based on their chemical properties. It is rarely possible to separate microorganisms from the decaying plant material and sediments where most of the decomposition occurs. Hence, soil organic matter consists of these partially decayed plant residues, the microorganisms and the small fauna involved in decomposition, and the byproducts of decomposition. (See related section: Soils.)
Soils harbor an extremely high diversity of organisms. The decomposer community consists of four main categories of organisms: microbes, microfauna, mesofauna (litter transformers), and macrofauna (ecosystem engineers) (See Soil biomass ).
Ecological Classification of Bacteria
Linkages between plant litter and groups of decomposers are complex and reciprocal in nature. The overall efficiency of the decomposition process depends on the nature of biotic interactions between soil microbes and soil fauna (see biotic interactions ). Though soil microbes have the enzyme systems most appropriate for breaking down organic matter, their abundance and activity vary with the soil faunal dynamics at a higher trophic level and the variables that regulate them. Interactions can be broadly resolved at three levels: (1) microfood-webs, which involve nematodes, protozoa, and their predators (interaction between microbes and mesofauna ); (2) litter- transforming systems, which involve mesofaunal and some macrofaunal interactions; (3) ecosystem engineering systems, which involve larger organisms that can significantly alter the environment. Altering trophic cascades ultimately influences the cycling of carbon and nutrients. It is important to understand that the role of ecosystem engineers and mesofauna is restricted to fragmentation of large organic material. Bacteria and fungi, on the other hand, represent the primary decomposers because they possess the necessary enzymes to breakdown organic substrates into their constituent inorganic forms. Thus, changes in habitat conditions will dictate the species of bacteria and fungi that in turn, will influence the degradation pathway and the overall rates of carbon turnover. Although the above description of decomposer community is general, the interactions between ecosystem engineers, mesofauna and microbes hold true for various sub-ecosystems that are part of the ACE Basin study area. In the subsequent section, differences in bacterial and fungal community and their role in C, N and S cycling is highlighted for each of the various sub-ecosystems of the ACE Basin study area.
The biological elements C, N, P and sulphur S, are the main building blocks of cellular tissue and are initially absorbed and stored in energy rich organic substances. Plants take up C as atmospheric carbon dioxide (CO2) gas, absorb nutrients and water from soil and use light energy to produce organic compounds which support their growth. The process of converting atmospheric CO2 into more complex forms of organic carbon by using light energy and water is termed photosynthesis. The breakdown of these organic carbon complexes yields energy for growth and is termed respiration. The product of aerobic respiration is CO2 and water. Not all organisms can produce complex organic carbon substances by using light or other sources of energy (organisms that use chemical energy to produce organic carbon substances are called chemoautotrophs ). This means that consumers depend on primary producers for their supply of energy rich organic compounds to respire and grow.
At the most fundamental level, respiration can be defined as any energy yielding biotic oxidation. This means that there could be several types of respiration in a given environment. This energy yielding oxidation involves transfer of electrons from an oxidized organic substrate to organic or inorganic molecules. These oxidation and reduction reactions are mediated by specific enzymes produced by the decomposers (especially by bacteria and fungi). Depending on the molecular recipient of the transferred electrons, these reactions can be broadly classified into three categories : (1) aerobic respiration- gaseous (molecular) oxygen is the electron acceptor; (2) anaerobic respiration- inorganic compound other than oxygen acts as the electron acceptor; (3) fermentation- an anaerobic process in which an organic compound is the electron acceptor. These three forms of respiration occur in different zones within the soil depending upon the qualitative redox potential decomposition and are mediated by specific microbial groups utilizing the appropriate electron acceptor. Here the product of one microbial group serves as substrate for the subsequent microbial group to convert organic molecules to methane, CO2 and water. Hence, the rate of CO2 and methane evolution from sediments can be used as a proxy for rate of organic matter decomposition.
In the sediment matrix, once oxygen is depleted, a sequential reduction of various electron acceptors follows. The soil redox potential determines the acceptor that will be most energetically favorable at any given time. Similarly, differences in physicochemical characteristics between sub-ecosystems of the ACE Basin study area could alter the activity and speciation of dominant decomposers.
In the following paragraphs, the role of decomposers in C, N and S cycling is described for forests, tidal freshwater and saltwater marshes, which together comprise most of the landscape of the ACE ecosystem. Since, specific information about activity and distribution of decomposer communities in the ACE Basin study area is lacking, insightful parallels are drawn from studies conducted in other similar ecosystems. (See related section: Biogeochemistry.)
The extensive watershed of the ACE ecosystem is represented by bay forests, bottomland hardwood, and upland forests. In the Edisto River Basin, more than 50% of the watershed is forested and is chiefly dominated by pine communities in the uplands (see Upland Community ). A network of streams from these subsystems drains into the major rivers thus forming a continuum. In such ecosystems, the decomposition process begins with the introduction of organic matter (chiefly as plant litter) through mechanical and biotic activity. The soil organic carbon is rich in cellulose, hemicellulose and lignin, which form the main components of woody plant tissue. Typically, there is an initial flush of decomposition as plant residues enter the soil. This is due to decomposition of the most labile fractions of the organic matter. Subsequently, a much slower and steady breakdown of organic matter occurs as stable substances are formed after the initial flush . The breakdown of cellulose is mediated by microbes and the soil animals, which exposes greater surface area for microbial attack through comminution. Earthworms play an important role in this respect. The gut of an earthworm contains high levels of cellulase activity (partially contributed by gut microbes), which facilitates breakdown of this polymeric form of carbon. Depolymerization of cellulose is mainly achieved by specialized saprophytes, e.g., fungi such as brown rot fungi (Basidiomycotina), Fusarium, Aspergillus, Trichoderma and Penicillium species and by bacterial species such as Bacillus, Pseudomonas and Clostridium. Decomposition of cellulose represents the breakdown of high molecular weight compounds into low molecular weight compounds, which are readily utilized by microbes. Once the cellulosic and hemicellulosic components of the soil organic matter are degraded, the lignin fraction is attacked. The decomposition of lignin is carried out by Basidiomycotina fungi, which are collectively called white rots. These include fungi such as Phanaerochaete chrysosporium and Coriolus versicolor. Lignin degradation is inhibited by high levels of nitrogen in some white rot fungi (Killham 1994). This suggests a strong link between carbon and nitrogen cycles , the two elements that are the most important determinants of nutrient cycling in ecosystems.
The nitrogen cycle is tightly coupled to the carbon cycle as most nitrogen transformations in soil depend on the supply of carbon (Paul 1976). Though atmospheric deposition of nitrogen is important (particularly in polluted areas), the largest contribution of nitrogen input in terrestrial environments is from biological nitrogen fixation and nitrogen mineralization. While nitrogen fixation is carried out by various free living and plant associated microbes such as Bacillus, Klebsiella, Rhizobium, Azotobacter, Beijerinkia, Azospirullum and Frankia (actinomycetes), nitrogen mineralization involves participation by soil microbes and animals. The soil animals, in addition to accelerating the mineralization process by comminution, also mineralize nitrogen in their guts. The fecal matter produced is enriched in nitrogen and is a prime site for microbial mediated mineralization. For instance, small mammals such as voles play an important role in C and N mineralization by depositing fecal material, which facilitates dispersal of fungal spore and labile nutrient pools to micro sites of seedling establishment (Pastor et al. 1996). Anderson et al. (1985) show that, in temperate forest soils, mineralization of nitrogen by soil fauna is equal to or greater than that mediated by microbial decomposers. In moorland and acid forests, the faunal contribution to the decomposer community is mainly due to enchytraeid worms, springtails and mites. Earthworms and their interaction with soil microbes is of particular importance in nitrogen mineralization. For instance, in deciduous woodland soils the annual nitrogen flux through earthworms is several times the amount (30 - 70 kg ha-1) contained in the leaf fall (Killham 1994).
The loss of mineralized nitrogen in soils occurs via immobilization, nitrification and denitrification. The balance between mineralization and immobilization is controlled by the C:N ratio of the substrate and the C:N requirements of the decomposers (see relationship between decomposer and C:N ratio ). Although the C:N ratio of decomposing litter determines whether or not nitrogen is mineralized, there are complexities in natural ecosystems that compound this relationship. For example, the soil organic matter is a heterogenous mixture of carbon derived from various plant types that differ in their C:N ratio or litter quality. In the ACE Basin study area Quercus pinus (swamp chestnut oak) and Acer rubrum (red maple), which are important components of swamp forest community, differ in their quality. Maple leaves form medium quality litter, but degrade faster than oak leaves, which contain less available nitrogen (Sinsabaugh and Moorhead 1997). As a result, in such ecosystems the effect of diversity in litter quality on microbial and faunal components of detritus food-web is complex. For instance, in mixed oak and maple litter, assemblages of fungivorous nematodes and mesofaunal were greater and lesser, respectively, than that expected based on litter made up of a single species (Wardle and Lavelle 1997). The mineralized nitrogen (in the form of ammonium) is either taken up by plants and microbes or converted to nitrate (through nitrification process), which is further transformed into nitrous oxide and nitrogen gas by denitrifiers. These two processes are mainly carried out by microbes with no direct participation by larger decomposers. Since the higher trophic assemblages exert a top-down control on the microbial community, natural and anthropogenically induced changes in soil fauna will alter the rates of nitrification and denitrification and that of overall mineralization. For example, Perison et al. (1997), while studying the relative impacts of harvest methods in the blackwater bottomland forests of the Edisto River estuary, found that the decomposition rates were higher in the harvested area. They attributed this to accelerated microbial activities as a result of higher soil temperatures. However, harvesting also resulted in a change in herpetofaunal species composition, though the indices of diversity were similar between the harvested and control plots. Higher ammonium and organic carbon concentrations in groundwater samples were attributed to increased decomposition rates. Similarly, deforestation in such river dominated ecosystems can lead to increased concentrations of ammonium and nitrate in drainage waters that are associated with eutrophication in streams and rivers.
Energy flow for tidal freshwater marsh ). There are three major sources of energy in such systems. Tidal freshwater marshes are usually well flushed systems with reciprocal relationships with the adjoining river water. This means that the chemistry and biology of the surface water will influence the biogeochemistry in the wetland surface. This is particularly true for the ACE Basin study area where blackwater rivers (e.g., Edisto River, Combahee River) bring terrestrially derived organic carbon to the wetland surface. However, plant detritus and the associated microbial community form the most important sources of energy in freshwater marshes. The decomposer community typically consists of bacteria, fungi, and meiobenthic and macrobenthic communities. The meiobenthic community is primarily dominated by nematodes. Macrobenthos are composed of amphipods, oligochaete worms, freshwater snails and insect larvae. These benthic invertebrates can readily consume plant litter. The vascular plant community in the upper reaches of the Edisto River and the Ashepoo River is dominated by big cordgrass, cattail, sawgrass, wild rice, arrow-arum, and pickerelweed ( See Palustrine Report ). These plant types differ in their litter quality. For instance, the rate of decay of leaves of Zizania aquatica, Pontederia cordata, Sagittaria latifolia and Nuphar luteum varies, with N. luteum decaying the fastest. The broad-leaved perennials (such as Pontederia cordata, Sagittaria latifolia and Numphar luteum) generally have a low C:N ratio in their leaf tissues. Due to the higher nutritional quality of these plants, consumers prefer these over detritus of other low nutrition quality plants such as Spartina. The high marsh grasses, however, have low tissue nitrogen concentration and decay much more slowly.
Temperature and combined availability of oxygen and water in tidal freshwater wetlands provides optimum conditions for decomposition. These conditions also dictate pathway of organic carbon respiration and the type of microbial community that will dominate. Under aerobic conditions, oxygen is the major electron acceptor dominating aerobic respiration. Nitrate and manganese in zone II and Fe3+ in zone III dominate facultative anaerobic respiration. Under strict anaerobic conditions, zone IV and zone V are dominated by sulphate reduction and methane formation, respectively. It is imperative to realize that in any given ecosystem the byproduct of respiration (partially degraded organic matter) from one zone subsidizes the demand for utilizable organic carbon in the subsequent zones. In mineral-rich fresh, brackish and even salt water wetlands, iron reduction is an important pathway for organic matter decomposition (Sorensen 1982; Lovely 1991; Roden and Wetzel 1996). Furthermore, in freshwater wetlands (such as those in the upper reaches of the ACE Basin study area) where sulphate (a major component of sea water) is not present, methane formation is the dominant form of anaerobic respiration. This is consistent with the view that thermodynamic considerations predict that in closed aqueous systems containing living organisms, after O2 is removed during oxidation of organic matter, biological reduction of alternative electron acceptors, NO3-, MnO2, Fe(OH)3 and SO42-, should proceed in that order (Ghiorse 1988).
Tidal salt marshes are unique in that they are characteristic of both terrestrial and aquatic environments. The location of salt marshes in a river dominated continuum, such as those in the ACE Basin study area, makes them susceptible to nutrient and organic matter inputs from upstream marshes and facilitates their important role in subsidizing nutrient and organic carbon requirements of adjacent coastal open waters. In the Southeastern United States and in the ACE Basin study area, salt marshes are dominated by one plant species - Spartina alterniflora (see Estuarine Report ). This dominant food source is of limited nutritional value. Despite the low nutritional value of the dominant organic carbon source and harsh environmental conditions (e.g., salt stress), salt marshes have a high diversity of consumers (see salt marsh food web ). The benthic community in salt marshes is composed of various macrofauna, mesofauna and microbes. The macrofaunal community is dominated by various species of crabs (e.g., fiddler and blue crabs), gastropod molluscs (such as Littorina irrorata), polychaetes and amphipods. These are the primary foragers of marsh vegetation, detritus and mesofauna. The mesofaunal community consists of protozoa, nematodes, copepods, annelids and rotifers. These organisms primarily feed on the microbial population, which chiefly consists of various species of bacteria and fungi. Recall that Spartina alterniflora supports a large number of epiphytic fungi, which not only contribute carbon and nutrients, but also participate in decomposition of standing biomass.
Approximately 90 % of the above ground productivity (from Spartina sp.) dies and decays on the marsh surface where energy is channeled through the detrital pathway. Though decay rates of salt marsh vegetation vary with location, there is evidence that macrofauna may increase the decomposition rates of the plant litter (Hemminga and Buth 1991). Additionally, in a microcosm study, the benthic macrofauna initially increased the release of CO2, primarily by decomposing old and relatively refractory organic matter (Andersen and Kristensen 1992). Mesofauna also stimulate the decomposition of plant litter in salt marshes. For instance, a bacterivorous marine nematode (Diplolaimelloides bruciei) stimulated the decomposition of Spartina anglica leaves (Alkemade et al. 1992). During this study, presence of nematodes increased the CO2 production of green decaying leaves by 20 - 25% while incorporating carbon in their biomass. The microbial community in a salt marsh is primarily responsible for decomposition and cycling of nutrients. As Spartina alterniflora (which has a high C:N ratio) decomposes, the detritus increases in protein content from 10 to 24% of ash free dry weight. This is mediated by the microbial community decomposing the Spartina litter. The increase in nutritional quality of the detritus not only facilitates accelerated decomposition but also enhances the food value for consumers. The microbial production in standing plant litter is strongly dominated by fungi, which can account for virtually all the nitrogen present during certain points in the standing decay period (Newell 1996). Though fungi are generally aerophilic, they play an important role in organic matter decomposition in anaerobic salt marsh sediments (Padgett and Celio 1990). This suggests that the root associated fungi are either microaerophilic or are capable of translocating sufficient oxygen through their hyphae into the oxygen deficient sediments (Padgett et al. 1989). The dominance and adaptations of fungi in salt marshes does not preclude the role of bacteria in these environments. Though fungi participate in the breakdown of the lignocellulosic fraction of salt marsh vegetation, bacterial mediated decomposition of this fraction of Spartina alterniflora litter is more efficient (Benner 1984). Salt marsh sediments support some of the highest rates of heterotrophic bacterial activity (Howarth 1993).
As in the case of freshwater marshes, the physicochemical environment and periodic tidal inundations dictate the dominant pathway for organic matter decomposition in salt marsh sediments. The tidal flushing saturates the marsh surface with sea water (rich in sulfate) and prevents diffusion of oxygen into sediments. In these anaerobic environments, bacterial mediated sulfate reduction is the dominant pathway for organic matter decomposition (See Table-3 ). The links between sulphur, carbon and nitrogen cycles are most obvious in a salt marsh. For instance, Spartina alterniflora, which is the source of organic carbon for sulphate reducers (e.g. various species of genus Desulfovibrio, Desulfotomaculum, and Desulfobacter), is primarily limited by nitrogen. In addition, Spartina alterniflora (and other marine organisms) synthesizes and stores an organic sulfur compound called dimethylsulfonium propionate (DMSP). This DMSP enters the sulfur cycle through microbial action where it is degraded into dimethyl sulfide (DMS) and acrylate. The latter is used as an energy source by bacteria. Acrylate utilizing bacteria support high rates of nitrogen fixation and denitrification in salt marsh sediments and play an insignificant role in brackish and freshwater sediments, as has been observed in the Cooper River estuary in South Carolina (de Souza and Yoch 1996). Furthermore, the products of sulfate reduction are hydrogen sulfide (H2S) gas and other reactive sulfide (S2-) species. These reactive species contribute to the reducing environment and influence the availability of nutrients, particularly phosphorus, by reacting with inorganic minerals such as iron. This phenomenon partially accounts for higher phosphorus availability in salt marshes than in freshwater wetlands.
The structure and function of decomposer communities in these environments have the potential to alter the dynamics of nutrient cycling through various feedback mechanisms between faunal and biogeochemical processes. The interrelatedness of various nutrient cycles means that changes in surface water quality within these ecosystems (with respect to any one nutrient) will impact other components of ecosystem functioning. From the perspective of ecosystem management, the tight coupling between surface water quality and the structure and function of decomposer communities facilitates their use as an efficient management tool for assessing ecosystem changes in response to anthropogenic perturbations. In the ACE Basin study area, sites with varying degrees of anthropogenic impact (e.g. Big Bay vs. St. Pierre) provide an excellent setting for such a study.
P.V. Sundareshwar, University of South Carolina
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