Biogeochemistry is a field of science that deals with chemical reactions of elements in nature that are mediated by both biological and geological factors. 'Biogeochemistry' is a relatively new term for a field of research that has been in existence for quite some time. A study in biogeochemistry is one that recognizes the importance of both the biology (organic or living component) and the geology (inorganic or non-living component) of a particular environment in controlling chemical transformations. These chemical transformations store or release energy, which, in turn, drives the ordering of the components of an estuarine ecosystem.
Biogeochemical processes in the ACE Basin study area can be considered on a variety of scales. A biogeochemical study on a relatively small scale, such as a mud flat, may focus on the effect of burrowing activity by polychaete worms on nitrogen fluxes (e.g., Kristensen et al. 1985). On the other hand, a study on a much larger scale, like that of the entire Edisto River watershed, may track the transformation of nitrogen through the aquatic food web. For instance, stable isotopes could be used to infer the contribution of nitrogen from wastewater treatment facilities upstream to the nitrogen found in estuarine organisms residing at the mouth of the Edisto River in St. Helena Sound, as has been done by McClelland et al. (1997) in the Waquoit Bay estuarine ecosystem. Both the mud flat and the watershed in these examples represent ecological systems (ecosystems). Depending on the point of reference, one may consider the mud flat a subsystem within the watershed system. In general, however, a system is defined as a group of interacting parts with a collective function or process. One prominent process in ecosystems is the flow of energy that is gained or released during chemical reactions. This flow of energy drives the interactions among the ecosystem parts, including the cycles of elements. The focus of biogeochemical studies is to understand these chemical reactions and the regulatory functions involved as they pertain to specific chemical elements or compounds that are important determinants of ecosystem function.
The geographical boundaries that would define a biogeochemical study in an estuarine ecosystem such as the ACE Basin study area are the river channels to the maximum upstream extent of tidal influence; the surrounding freshwater, brackish, and salt marshes; and the ocean waters affected by the addition of fresh water (see salinity gradient ). Upland habitats such as maritime forests that receive no tidal subsidy may also be considered important to estuarine biogeochemistry especially during periods of precipitation when rain water washes materials into the water column.
Estuarine scientists divide estuaries into zones based on the relative distribution of salts. This points to the importance of salinity in controlling estuarine biological processes. Biogeochemical studies in estuaries also consider the cycling of elements specific to these salinity zones. Because of their complexity, rarely are studies broad enough to encompass the entire estuarine system.
The major elements studied in biogeochemistry include carbon (C), hydrogen (H), nitrogen (N), oxygen (O), phosphorous (P), and sulfur (S),because these make-up the bulk of both plant and animal tissue. Studies tend to focus on the cycling of one or more of these elements between their organic and inorganic states. The biogeochemistry of trace metals such as lead, cadmium, and mercury is also important to consider because their presence in high concentration can be toxic to both fish and humans. (See related section: Hydrochemistry.) Therefore, the reactions that metals undergo may also be a considerable determinant for estuarine health.
In this section, the biogeochemistry of C, N, P, and S and the role these elements play in determining the function of the estuarine ecosystem will be discussed. The concentration of these elements in different abiotic (non-living) and biotic (living) components of the estuary, and the rates at which they undergo chemical transformation during processes like plant production and decomposition regulate environmental quality. Studies in biogeochemistry are important to estuarine management because their goal is to describe the underlying chemical processes that dictate the function of the ecosystem and the response it may have to man-induced changes at the watershed level.
In living tissue most of the bonds between C, H, N, O, P, and S are reduced, or electron rich. It takes a great deal of energy to synthesize the reduced compounds that comprise living tissue. The sun is the ultimate source of this energy. Once created, organisms have to expend energy to maintain the integrity of their tissues because according to the laws of thermodynamics a spontaneous reaction should result in the oxidation of products to a lower energy state. This is why plants photosynthesize, fish eat shrimp, and shrimp eat dead plant material so that energy can be generated to maintain their living tissues at the high-energy state. When living tissue dies and begins to decay the reduced biomolecules are oxidized to their simple inorganic constituents. Bacteria that live in the water column and sediments of estuaries mediate the rate of oxidation of dead tissues. This process of biological oxidation, referred to as decomposition, returns the organic constituents of biogeochemicals back to their inorganic states such as CO2, H20, and NO3. (See related section: Decomposers .)
Biogeochemistry and Ecosystem Models
Linkages Among Subsystems in Estuaries
As specific aspects about biogeochemicals in the ACE are discussed, keep in mind that the elements of biogeochemistry cycle among primary producers, consumers, and inorganic constituents in estuaries. Primary producers transform inorganic carbon in the atmosphere or seawater to organic biomolecules to make living tissues. During this process other inorganic nutrients (N, P, and S) must be incorporated, and frequently one of these constituents limits the carbon transformation rate. Examples of primary producers in the ACE Basin study area include phytoplankton that reside predominately in the water column (See related sub-section: Phytoplankton: Marine Phytoplankton); macroalgae that adhere to bottom sediments in shallow areas or plant stems, piers, and other semipermanent structures; and marsh macrophytes represented by Spartina alterniflora in salt marshes and numerous other species in the diverse brackish and freshwater marsh communities upstream.
Consumers can not synthesize organic carbon from its inorganic form. They rely on the primary producers to provide the building blocks for their living tissues. Zooplankton, fish, snails, crabs, shrimp, worms, and water column and sedimentary bacteria represent consumers in the estuarine ecosystem of the ACE Basin study area. From a biogeochemical perspective, the consumers that have the greatest influence on elemental transfer rates are the most important to system functioning. In this regard, the heterotrophic bacteria are the most important. As organic matter synthesized by primary producers is degraded by bacteria, the biogeochemical elements cycle back to their inorganic forms, and nutrients are regenerated for new production. The end result of biogeochemistry determines how the estuary functions as a commercial fishery, a contaminant sink, or a recreational waterway.
estuarine food web. Studies in salt marshes have focused on measuring the rates of marsh plant production and decomposition. Much of the information on these processes has been obtained from controlled studies in saltmarsh habitats of North Inlet, SC and Sapelo Island, GA, to the north and south of the ACE Basin study area, respectively. Although there are differences in the zonation patterns of vegetation (see Vegetation zonation ) in salt marshes with latitude, Spartina species (the salt marsh cordgrass) are common to all saltmarsh types. Research has determined the major factors that regulate Spartina growth and decay. Plant growth and decay are tightly coupled to the biogeochemical cycles of sulfur (see Sulfur transformation ) and nitrogen (see Energy flow model ).
The bacterial process of denitrification plays a similar role to sulfate reduction in that it represents a pathway used by microbes to oxidize organic carbon. Denitrification converts NO3 to nitrogen gas (N2). In estuaries, denitrification is now recognized as an important natural attenuation mechanism for nutrient pollution in the form of terrestrial runoff from agricultural land, golf courses, or sewage (Seitzinger 1988). In order for denitrification to be a dominant process in the nitrogen cycle an aerobic / anaerobic interface must be maintained. NO3is produced from NH4 in the presence of oxygen. The NO3 then diffuses downward to the anoxic sediment layers where it is denitrified.
Scientists who study the C cycle are biogeochemists who measure the transfer rate of carbon between its organic and inorganic forms. By determining the rate of transfer and the factors that control that rate, researchers can arrive at residence times for C in its different pools. Then predictions can be made about the effect that changes in residence time will have on different system components if the natural environment was perturbed in some way. When carbon undergoes chemical transformation, energy is stored or released, and this change in energetics drives the system. For instance, scientists have used the current consumption rate of fossil fuels (dead organic C) by humans to predict the rise in global temperature that will result from returning organic carbon from its sedimentary pool to its inorganic pool, represented by CO2, in the atmosphere. This example represents a biospheric response to perturbations to the carbon cycle as the system function changes from a greater source of atmospheric CO2.
At the scale of an estuary, carbon cycle perturbations may result in degraded water quality. This can occur when there is increased algal production as a result of elevated nutrient loading in the form of point sources of wastewater discharge or non-point sources of agricultural runoff or when organic inputs from the surrounding watershed are high. More organic input to the estuarine water column translates to more food for bacteria that are responsible for the decomposition of this material. Oxygen is consumed during decomposition. The concentration of dissolved oxygen in the water column decreases drastically during these periods of high organic carbon input and can become so low that shellfish and other macroorganisms migrate to more favorable areas or die.
If oxygen becomes so low that the system becomes anoxic, which occurs frequently in shallow turbid estuaries in the summer time, anaerobic mechanisms for decomposition become important. Anaerobic C turnover occurs continuously in subtidal and intertidal sediments where oxygen is depleted just a few millimeters below the sediment surface.
It is easy to recognize that there are potentially complex interactions between the biogeochemistry of C and other elements, such as oxygen in the previous example, that feedback to control the overall response of the estuarine ecosystem to environmental changes. Physical properties of the environment, such as temperature and salt concentration, can regulate the rates of biogeochemical cycling as well. Thus, it is extremely difficult to control all the possible regulatory factors in biogeochemical experiments. This is why studies in estuarine biogeochemistry tend to focus on one component of the ecological system at a time. There is an extensive knowledge on the biogeochemistry of salt marshes, for instance, which makes this subsystem good for explaining the cycling of the remaining elements.
Now that the framework for biogeochemical investigations in estuaries has been described, the next consideration is what makes the ACE Basin study area a unique ecosystem, and how this uniqueness may influence biogeochemical cycles in its estuarine habitat. Because no research on biogeochemical cycles has been conducted in the ACE Basin study area, one must draw on knowledge gained from other estuarine ecosystems in the region like the Cooper River and the Winyah Bay/North Inlet estuaries located near Charleston and Georgetown, SC, respectively, then make educated guesses about how the nature of the ACE Basin study area may cause responses that approximate or differ from these other areas. There are three qualitative observations that can be made about the ACE Basin study area that make it a unique estuarine system compared to others in the region: 1) black water; 2) low urbanization for a river dominated system; and 3) wetlands (freshwater, brackish, and salt marsh) that are a dominant feature of the landscape. The potential effect these characteristics have on biogeochemical cycling will be discussed below.
Phosphorus desorption is a contributing factor to differences in nutrient limitation between upstream and downstream primary producers. Phytoplankton and marsh vegetation are limited by phosphorus in the tidal freshwater regions of estuaries. Here bioavailable phosphorus is intensely removed from the water column by adsorption processes. Thus, phosphorus loading in this region of the estuary would be expected to enhance primary production and the potential for phytoplankton blooms. In the higher salinity regions of the estuary where phosphorus has desorbed and becomes bioavailable, primary production is limited by nitrogen. This shift in the limiting nutrient along the salinity gradient is important to estuarine biogeochemical function. Imagine a point source of nitrogen fertilizer from a golf course. Nitrogen loading in the high salinity estuary will be more important to carbon biogeochemistry than in the low salinity estuary. Results of a physical and ecological characterization of the Cooper River north of the Edisto River support this generalized estuarine model for nutrients. There is a maximum in water column nitrogen and phosphorus in the mid-estuary (McKellar et al. 1990). Pore water in the brackish-water marsh (salinity=4.4 (g/l)) in this region of the estuary also has elevated levels of ammonium compared to the freshwater and saline marshes up and down river (see Ammonia and Phosphorus in marsh pore water ).
The marsh and water column is extremely fertile in the mid-estuary due to geochemical transformations that occur with mixing. Consequently, the biology responds with increased carbon fixation in the form of elevated Chl a. Plant biomass in the mid-estuary marsh is also high compared to the upstream and downstream extremes (data not shown).
One might hypothesize that on an estuarine-wide scale, the black water nature of the waters in the Edisto River supply more bound nutrients to the estuarine system than in a system such as the Cooper River where the headwaters derive from Lake Moultrie. In the case of the Cooper, Lake Moultrie acts as a large settling basin for allochthonous inputs from the upland watershed. The type of river flowing into the estuary may influence the nature of nutrient loading. The Edisto drains the coastal plain. Rivers that drain the Piedmont, like the Congaree River or the Pee Dee which flow into the Cooper River and Winyah bay, respectively, are flashy due to the impermeability of clay sediments. High fluctuations in discharge with storm events are a characteristic of flashy rivers. Water discharge from the storms deliver organic matter to the receiving estuary in pulses whereas in the Edisto the sandy sediments of the coastal plain dampen fluctuations in discharge allowing humic substances to concentrate. Nutrients in marsh pore water along the Edisto River tend to be higher than the concentrations observed in the Cooper River and Winyah Bay/ North Inlet systems. Could the nutrients carried in the black water discharge that dominates the ACE Basin study area impart estuarine wide eutrophication in a relatively pristine estuary? Do the elevated nutrient levels make the system more or less sensitive to nutrient pollution?
Landscape Characteristics and
Differences in water quality and water column community structure are currently being investigated in the North Inlet and Winyah Bay estuarine ecosystem in Georgetown County, SC. North Inlet has no inflow of freshwater from major rivers. This fact alone makes comparison between this system with river dominated estuarine systems like Winyah Bay interesting from a biogeochemical point of view. Another important point about the North Inlet estuarine ecosystem is the absence of urbanization in the watershed.
A comparison of nitrogen species and chl a between the North Inlet and Winyah Bay estuaries highlights the extreme difference in fertility (see Nutrient concentrations ). North Inlet is dominated by ammonium, whereas nitrate is the dominant nitrogen species in Winyah Bay. Chl a, is inversely related to nitrate concentration suggesting a nitrogen limitation to primary production in Winyah Bay. Water column primary production in North Inlet, however, is limited by zooplankton predation (top down control) (Lewitus et al. 1998). The trend for Winyah Bay is typical of a eutrophic estuary. A similar relationship is found in the Chesapeake Bay, a highly eutrophic system (Magnien et al. 1992).
In relation to the ACE Basin study area, nitrate concentrations in the Edisto River are similar to those found in North Inlet, though slightly higher. Nitrate concentrations in Winyah Bay, for comparison, are on average greater by a factor of 10. The high nitrate concentrations in Winyah Bay may be attributed to the large proportion of industrial activity and high rate of non-point source nutrient run-off from agriculture and other land uses. Ammonium nitrogen in surface and pore water in the Edisto, however, is quite large compared to the other river-dominated estuaries. One hypothesis is that the differences between nitrogen concentrations and the dominant nitrogen species among estuaries is a result of landscape scale differences between watersheds.
The large proportion of forested and emergent wetlands in the ACE Basin study area may act as a sink to nitrates entering the watershed via land surface run-off. Recall that microbial denitrification is an important loss mechanism for nitrate in wetland sediments (see background and Seitzinger 1988). Wetland vegetation also intercepts nitrate converting it to organic nitrogen in plant tissues. Although a potential sink for nitrate nitrogen, the wetlands in the ACE may be a source for the high concentrations of ammonium found in the water column. Ammonium accumulates in wetland sediments as a result of organic matter decomposition. One mechanism of ammonium release to the water column is via diffusion. This process, however, would be slow compared to a second mode of transfer, wetland seepage (see Exchange process ). Marsh pore waters drain when the water table drops below the sediment surface at low tide and slopes toward the low water level in the adjacent river channel. Nutrient rich pore water mixes with surface waters during these events (Whiting and Childers 1989). Since the relative contribution of wetland and forested area is high and the area occupied by non-impervious surfaces (i.e roads, parking lots, etc) is low in the total land use/ land cover pattern for the ACE Basin study area, ammonium dominates the inorganic nitrogen signal. It has been hypothesized that the differences in nutrient profiles between North Inlet and Winyah Bay may regulate the phytoplankton and bacterial communities in the water column due to differences in nutrient uptake physiology among species (Morris pers. comm.). It is likely that the high concentration of ammonium in the ACE, regardless of it source, plays an important part in structuring the biotic community in this ecosystem as well.
The high ammonium concentrations in the Edisto River may be typical of un-urbanized, pristine river dominated estuaries. Unfortunately, there are very few pristine systems like the ACE to which comparisons could be made. As an example of how sensitive biogeochemical processes in the ACE Basin study area may be to anthropogenic disturbance, however, a recent study found that the effect of a timber harvest on the south fork of the Edisto River was to increase rates of organic matter decomposition, possibly due to an increase in soil temperature after clear cutting (Perison et al. 1997). An elevated level of ammonium and dissolved organic carbon in the ground water at the harvest site was attributed to the higher decomposition rates.
Although ammonium levels appear relatively high in the pristine Edisto River, phosphorus levels are also high (see Ammonia and Phosphorus in marsh pore water ). This keeps the ratio of total nitrogen to phosphorus near 12 over the entire basin, as reported by Eidson (1993). This ratio is reflective of a balanced ecosystem based on the ratio in living plant tissue of 10 to 15. Nitrogen limits production of living tissue at ratios below 15 and phosphorus is limiting at ratios above 15. With the extant data it is difficult to make comparisons of the N/P ratio among estuaries, because it is debatable whether to use the inorganic nutrients or the total nutrients, which account for dissolved and particulate organic fractions, to compute N/P ratios. Spatial and temporal patterns in the N/P ratio are likely to be important in regulating production as well.
Eutrophication, however, seems to be the result of a rise in one of the limiting elements relative to the other. In the Chesapeake Bay it is nitrogen. In the Florida Everglades it is phosphorus. Therefore, it makes sense to manage the system under the ratio that promotes the most favorable function. In the case of the Chesapeake, seagrass beds have declined drastically in the face of nitrogen pollution. In the Everglades, the native sawgrass plant community is being replaced by cattails, which are less favorable due to their high rates of transpiration. Hence, it may seem paradoxical to consider the ACE Basin study area pristine when the concentrations of important nutrients are relatively high in the water column and marsh pore water. But the underlying biogeochemical transformations of these nutrients that dictate production and carbon recycling in the system appear to keep the system functioning in a non-eutrophic condition. Landscape characteristics influence biogeochemical processes on a system wide scale, such as the proposed nitrate dissimilation scenario that may take place in the vast mosaic of wetlands that comprise the ACE Basin study area. Increased urbanization or enhanced forest clear-cutting and agricultural activity would likely increase nitrogen levels more than to phosphorus due to the high adsorption capacity of saturated sediments. Elevated nitrogen would increase the N/P ratio, and potentially throw the system out of balance, to a more eutrophic condition.
Wetland Biogeochemistry and the
Source/Sink Potential for Nutrients
Several methods have been used to quantify the source/sink relationship with respect to nutrients all of which have specific advantages and disadvantages (see Nutrient Flux ) (Carpenter 1997). Partly due to the disparity among methods, marsh systems appear to process nutrients in different ways. For example, Nixon (1980) concluded that salt marshes intercept dissolved inorganic nitrogen in runoff from the surrounding land and convert it to organic forms that then exchange with the waters in the tidal channels. Other investigators have shown that intertidal marshes tend to import particulate matter and export dissolved fractions of nutrients and carbon to adjacent estuarine water (Valiella et al. 1978, Jordan et al. 1983, Correl et al. 1991). North Inlet salt marshes, in particular, are nutrient exporters (Whiting et al. 1987), although there appears to be considerable seasonality to this relationship (Whiting et al. 1989). Quantification of the source or sink nature of marshes with respect to nutrients integrates both the biogeochemical processes within the wetland and the geomorphologic characteristics that regulate hydraulic fluxes between the water column and marsh sediments.
Salt marshes are characterized as one of the most productive ecosystem types in the world. In the Southeast, the salt marsh cordgrass, Spartina alterniflora, can have a net primary production up to 1,400 g C/m2/yr according to recent estimates (Dai and Wiegert 1996). Root growth accounts for a large portion of this production. In the short form of Spartina, roots represent 50% of the total plant biomass. The large proportion of roots translates to an abundant reservoir of reactive carbon that fuels the metabolism of microbial communities that live in marsh sediments. Much of the organic matter oxidation undergoes decomposition in an anaerobic environment via sulfate reduction. Therefore, the biogeochemistry of sulfur in salt marshes is tightly linked to energy flow and, hence, carbon and nutrient turnover (see Energy flow model ). Models of wetland carbon cycling highlight the complexity of chemical interactions among components of the marsh ecosystem that ultimately determine the concentration of nutrients in marsh pore waters.
Research is on-going in the ACE to determine relative differences in bulk sediment carbon metabolism in tidal marshes situated along a salinity gradient in the Edisto River. Although much work has been done to understand biogeochemistry of carbon and nutrients in salt marshes, little is known about how these constituents behave in marshes located in lower salinity waters. Chemical constituents in marsh pore water are currently being monitored at sites in the Cooper River, North Inlet, Winyah Bay and the Edisto River (see Ammonia and Phosphorus in marsh pore water ) to gain a better understanding of the variability in pore water carbon and nutrient reservoirs within and between estuarine marshes. In the ACE Basin study area, salt marshes and other lower salinity tidal marshes have long been recognized as important sources of carbon to shellfish and juvenile fish production. Now scientists are beginning to recognize their role in regulating water quality as important determinants for the fertility of open water habitats via nutrient exchanges.
Our understanding of changes currently taking place in estuarine ecosystems and our management of these systems can benefit from a thorough evaluation of the underlying biogeochemical cycles. Physiochemical processes that affect biotic responses drive these cycles. The ultimate goal of studying biogeochemical cycles in estuaries is to understand the chemical processes controlling the underlying function of the estuarine ecosystem. The lack of urbanization and the extensive network of wetlands in the ACE Basin study area make this a unique estuarine system with biogeochemical parameters that are quite different compared to other estuaries along the South Carolina coast. The low levels of nitrate /nitrogen in the estuary and the balanced N/P ratio are indicative of a healthy ecosystem. The lack of symptoms of eutrophication in the face of relatively high concentrations of ammonium and phosphorus in the water column and marshes suggests that future management of the ecosystem should be directed at keeping the existing ratio of these nutrients constant.
C. Nietch, University of South Carolina
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