Submitted to the National Science Foundation by Dr. Richard Dame, Dr. Dennis Allen, and Dr. Robert Young, this proposal is available to outline in detail the goals and expectations of this three year study.

Introduction and Significance of the Proposed Research

Organisms that actively move between ecosystems and between subsystems and connect components in space and time (mobile link organisms or MLOs) have been often overlooked or only given cursory attention (Lundberg and Moberg 2003). This situation is particularly the case in marsh-estuarine ecosystems where MLOs are prominent providers of services, such as food and recreation, to society. MLOs are also involved in a number of essential marsh-estuarine ecosystem functions, such as grazing, predation, secondary production, nutrient translocation and material cycling. The activities of MLOs or nekton (fishes, shrimps and crabs) are particularly evident during their occupation of intertidal areas in marsh-estuarine ecosystems (Kneib 1997). Many studies have focused on MLOs’ use of tidal channels and marshes as nursery or feeding grounds as well as refuges from predators (Weinstein 1979, Boesch and Turner 1984, Irlandi and Crawford 1997, Peterson et al. 2000, West and Zedler 2000, Beck et al. 2001, Webb and Kneib 2002). In addition, the potential importance of MLOs in the transfer of marsh-estuarine production has often been invoked (Nixon and Oviatt 1973, Valiela et al. 1977, Kneib and Wagner 1994), but has seldom been mentioned or estimated in ecosystem scale studies (Teal 1962, Woodwell et al. 1979, Pomeroy and Wiegert 1981, Dame et al. 1986). In spite of the obvious informational need, few investigations have examined the role of MLOs in the transfer of materials between the shallow waters of salt marshes and coastal waters via migration (Deegan 1993). Some MLO functions such as feeding, growth, and the redistribution of biomass through migrations have been identified, but production of dissolved inorganic materials as byproducts of metabolism is equally essential to understanding the functional role of MLOs in marsh-estuarine systems. MLOs production of dissolved nutrients may be particularly significant in relatively undisturbed coastal systems that are typically nutrient limited (Ryther and Dunstan 1971). The investigation of MLOs in marsh-estuarine ecosystems provides the opportunity to explore a new suite of mechanisms by which high productivity may be achieved in natural systems.

Marsh-estuarine ecosystems are prominent systems marking the transition zone between terrestrial uplands with their freshwater runoff and the sea. These zones have their own unique biota and ecological characteristics. Along the southeastern coast of the US, the broad gently sloping coastal plain allows tides propagated in the adjacent ocean to dominate marsh-estuarine systems with little river input. These systems are multiscalar and typically composed of (1) a tidal inlet that interfaces with the sea, (2) a number of major subtidal channels (partially submerged at low tide) that merge to form the inlet and (3) a multitude of intertidal channels (contain little water at low tide) that connect to the subtidal channels. It is through these small channels that tides flood and drain the ICMBs. Because human use and development of coastal resources continues to increase, the need to more fully understand fundamental ecological processes within the marsh-estuarine system is becoming more acute. Scientific information has played a significant role in the management of estuarine systems and resources, but that knowledge remains insufficient and new approaches are needed (Fisher et al. 2001). For example, efforts to reconstruct marshes and their associated tidal creeks as well as restore their ecological functions have been only marginally successful (Kneib 1997, Zedler 1996). Clearly, the level of understanding necessary to evaluate, manage or restore normal ecosystem functioning is yet to be achieved.

In our recently completed Creek Project, we found that, in spring, summer and fall, the MLO biomass in ICMBs was greater than oyster and resident nekton biomass by as much as an order of magnitude (Dame et al.2002). Furthermore, literature sources and recent work at the (BML) reveal that weight-specific MLO excretion rates are an order of magnitude higher than those of oysters are (Haertel et al. in prep.). Changes in MLO densities coincided with the seasonal pattern of ammonium concentrations in the water column (Fig. 1). Using a spreadsheet model based on Creek Project and literature estimates of ammonium and orthophosphate fluxes in marsh-estuarine systems (Table 1), we computed the flux of these nutrients for a single tidal cycle and for the specific components of an ICMB used in the previous work. These results suggest that MLOs in ICMBs are the largest source of dissolved inorganic nutrients to the primary producers and potentially key feedback components.

Our main objective in the proposed work is to quantify the material fluxes between subsystems within ICMBs and examine the under appreciated role of MLOs in a marsh-estuarine system. The data we gather will provide evidence supporting or refuting elementary theories of ecological boundaries as they apply to a pristine marsh-estuarine system. An overarching intent is to build on our approach to training undergraduates in the sciences by providing mentored quality research experiences at the individual and team levels (see RUI Impact Statement). We will accomplish these objectives by using ICMB scale field manipulations to compare systems and subsystems with and without MLOs (excluded), flumes and chambers to make in situ measurements of material fluxes by benthic subsystems and water column biota, and laboratory experiments to determine excretion rates and elucidate other processes. In summary, salt marshes are among the most productive natural ecosystems. Due to their dense biomass content, high surface to volume and edge to area ratios, and pulsating tidal flows linking terrestrial and marine habitats, we argue that ICMBs are the primary functional sites for major biogeochemical processes in the marsh, analogous to the role of capillaries in the circulatory system. We propose that MLOs (nekton) are the most important group of processors and transporters of materials within ICMBs. In short, ICMBs are where the action is, and MLOs are the major players. The traditional paradigm is that MLOs are attracted to salt marsh estuaries because marshes are highly productive. We suggest this can be viewed from the opposite side of a positive feedback loop: a major reason ICMBs are so productive is because MLOs live there.

Background

The earliest concepts of ecological boundaries focused on the change in species composition at the boundary or ecotone between different systems (Clements 1920, Shelford 1963, Valiela et al. 2001). Margalef (1968) first observed that boundaries between ecological systems are often difficult to determine or define and that it would probably be more profitable to focus on the exchanges and interactions between adjacent systems. Recently, Laurance et al. (2001) observed that many ecological boundaries or transition zones act like semi-permeable membranes, admitting some things and inhibiting others, i.e., physical filters. However, other transition zones, particularly wetlands (Mitsch and Gosselink 1993, Levin et al. 2001), are more than filters. They transform both the quantity and quality of material fluxes crossing their interfaces, act as sources and sinks of materials, and have a major MLO component that has both process and resource functions. Laurance et al. (2001) developed a number of general hypotheses of boundary function based on simple first principles. For example, there will be a net flux of energy from the higher to the lower productivity system as asserted by the Mass Effect and 2^nd Law of Thermodynamics. Also, as the degree of contrast increases between adjacent subsystems, the flux of MLOs will decline while the physical flows will increase as predicated by the principles of habitat specialization and diffusion.

Marsh-estuarine systems incorporate some of the characteristics of both aquatic and terrestrial environments, yet they support a unique biota and are generally more functionally diverse (Mitsch and Gosselink 1993). Furthermore, energy subsidies generated by the tides make marsh-estuarine systems some of the most ecologically productive systems in the biosphere (Odum 1963). Roughly 50% to 75% of economically important fish species and over 25% of all US Atlantic coast fish species use estuaries at some stage in their life history (Houde and Rutherford 1993). Also, coastal areas are sites of the most intense economic activity and human population growth (Deegan 2002); world wide, as much as 75% of the human population lives in the coastal zone (Von Bodungen and Turner 2001).

At least, three main ecological subsystems can be distinguished in marsh-estuarine systems: intertidal salt marshes, mudflats and a network of channels (Mitsch and Gosselink 1993, Fagherazzi et al. 1999). Many ICMB systems also have extensive subsystems of benthic suspension feeders and reefs (Dame et al. 2000c, Thompson and Schaffner 2001) and/or beds of macroalgal and subtidal seagrasses (Irlandi and Crawford 1997). The water column subsystem is usually the medium for the active and passive fluxes of materials between different subsystems in the ICMB (Valiela et al. 2001). Tidally driven flooding and ebbing waters serve as expanding and contracting corridors for the active movement of both juvenile and mature MLOs seeking food (prey) and refuge (Boesch and Turner 1984, Fitz and Wiegert 1991, Dame and Allen 1996, Kneib 1997, Irlandi and Crawford 1997, Webb and Kneib 2002, Potthoff and Allen in press) and passive transporters of a dynamic planktonic food web (Lewitus et al. 1998, Wetz et al. 2002). The presence of these subsystems in close proximity to each other provides a unique opportunity to examine the functional role of the ecologically and economically important MLOs in the processing, production, transport and storage of materials within and between subsystems and systems (Fig. 2).

Large animals or macrofauna (>1mm) are thought to influence ecosystems through their processing of matter. Kitchell et al. (1979) first postulated that in addition to feeding on other organisms, macrofauna transform and translocate materials, thus playing both direct and indirect roles in material cycling. Some macrofaunal species may transform or engineer an ecosystem. That is, they directly or indirectly modulate the availability of resources to other species by causing state changes in abiotic or biotic materials (Jones et al. 1994, Lawton and Jones 1995, Coleman and Williams 2002). This engineering concept is consistent with the ecological concept of keystone species that predicts that the removal or exclusion of certain species from the system causes significant change in ecosystem structure and function (Grimm 1995). This notion has been expanded further by Lundberg and Moberg (2003) to include animals that actively move in the landscape and connect habitats in space and time (mobile link organisms). In addition, Huxel and McCann (1998) have explored the idea that MLOs can influence food web stability. That one or a few taxa can exert a major influence on nutrient cycling has been shown or presumed for a variety of ecosystems: beavers (Jones et al. 1994, 1997), oysters and mussels (Dame 1996, Caraco et al. 1997), migratory waterfowl (Post et al. 1998, Kitchell et al. 1999), migrations of fish between estuaries and the coastal ocean (Deegan 1993,Laffaille et al. 1998), the migration of salmon to freshwater systems (Gross et al. 1998, Naiman et al. 2002), fish and reefs (Meyer and Schultz 1985, Geesey et al. 1984), fish within lakes (Brabrand et al. 1990, Schindler 1992, Schaus et al. 1997, Persson 1997, Vanni and Layne 1997), fish in prairie wetlands (Zimmer et al. 2001) and ungulate herbivores (Augustine and McNaughton 1998, Frank 1998). Our recent work in estuaries suggests that MLOs play a similar role. Despite the well-recognized role of estuaries as important feeding grounds, refuges and nurseries for very abundant and diverse nekton assemblages (Boesch and Turner 1984, Beck et al. 2001), the role of nekton in material processing within estuaries remains largely overlooked. Members of the nekton do not just utilize productive marsh-estuarine areas, their activities serve to enhance and sustain them.

Estuaries function as processors and traps for most particulate and dissolved materials including dissolved inorganic nutrients which are often critical limiting factors for primary production in these systems (Ryther and Dunstan 1971, Dame et al. 1991). Internal subsystems and components process the many materials that enter estuaries so that transport of some substances to the adjacent sea is limited (Valiela et al. 1978, Woodwell et al. 1979, Odum et al. 1979, Nixon 1980, Chalmers et al. 1985, Dame et al. 1986, Dame et al. 1991, Dame and Allen 1996). Which materials are processed, retained or transported depends on the extent, configuration and interactions of the specific subsystems. The dynamic water column is another subsystem that expands on flooding tides and contracts on ebbing tides. The water interacts with the other subsystems and serves as the transport medium for materials including the plankton. Thus, these subsystems and components function as processors of materials as well as sources, sinks and transporters of materials. In addition to these functions, MLOs actively transport their functional capabilities and biomass to other areas and systems. A quantitative understanding of how MLOs influence material processing in ICMBs is essential for wise coastal management (Dame et al. 2002).

Many types of estuaries are recognized at the land-sea interface. Along the southeast Atlantic coast, bar–built (barrier island) estuaries that are dominated by extensive intertidal marshes are common (Vernberg et al. 1992). Networks of channels connect the marsh and other intertidal subsystems with the ocean. Such estuaries can be thought of as assemblages of fairly independent intertidal drainage basins that are connected by deeper channels. The drainage basins consist of areas of vegetated marsh and channels perched above the mean low tide level. Intertidal channels meander over shelly, sandy or muddy bottoms that are lined or interspersed with oyster reefs, and they connect to larger channels that hold water throughout the tidal cycle. Tides are the major force controlling circulation and water level and volume in these systems. High edge to area (E: A) and surface to volume (S: V) ratios enhance the passive exchange of materials between the atmosphere, sediments, and tidal water (Dame et al. 2000a). Thus, like headwater streams in freshwater systems (Peterson et al. 2001), intertidal basins may play a disproportionate role in material processing within estuaries. Data from previous work (Vernberg 1977, Dame et al. 1986, Dame et al. 1991) and long-term monitoring of pristine bar-built estuarine systems in the Southeast indicate that ammonium (NH₄) is the dominant form of DIN. DIN concentrations reach maximum levels in the summer, largely following the seasonal changes in NH₄ (Fig. 1). By comparison, nitrate-nitrite (NN)concentrations are relatively low and only increase during periods of excessive rainfall. Potential nutrient sources in these systems include - atmospheric inputs, episodic surface water runoff, groundwater discharge, excretion and remineralization by animals (especially benthos, oysters, and MLOs), and remineralization through decomposition.

Nitrogen can enter estuaries via direct atmospheric deposition in gaseous, dry or wet (water borne) forms, but total input is relatively small (Table 1). The source of most atmospheric nitrogen is thought to be agricultural fertilizers, livestock and human waste, industrial processes, and energy generation by burning fossil fuels (Sutton et al. 1998, Wesely and Hicks 2000). Atmospheric deposition of nitrogen is cited as a contributor to the eutrophication of coastal waters (Lawrence et al. 2000). In the coastal southeastern USA atmospheric deposition of ammonium is low (Poor et al. 2001).

In North Inlet, groundwater movement into the marsh-estuarine ecosystem is very slow (a few meters per year). Because of the almost flat coastal landscape, surface water runoff is mainly confined to a few intermittent blackwater streams with fluxes being orders of magnitude less than tidal flow in the system (Dame et al. 1991).

The muddy sediments that compose the flats of intertidal channels and marshes are generally rich in organic materials, bacteria, microbenthic algae, meiofauna and suspension and deposit feeding macrofauna (Dame et al. 2000c). They are also harsh environments that are composed of soft poorly consolidated sediments, and they are exposed to the atmosphere during a large proportion of the tidal cycle. These factors make non-destructive sampling difficult, which may partially explain why muddy tidal flats have been generally overlooked by ecologists (Alongi 1998). Typically, these muddy sediments are strongly reducing, found in zones of high deposition, and support a number of bacterially dominated processes including fermentation, sulfate reduction, denitrification and methanogenesis (Middelburg et al. 1995, Mann 2000).

Salt marshes are usually the most extensive subsystem of temperate bar-built estuarine ecosystems. These systems have often been described as giant sediment traps (Jordan and Valiela 1983, Stevenson et al. 1988), but they are also sinks for inorganic nitrogen (Dame et al. 1991, Childers et al. 1993). The removal of dissolved nutrients by the salt marsh also implies that in addition to marsh grass, epiphytes, benthic microalgae and sediments within the marsh (Jones 1980, Pinckney and Zingmark 1993) are actively taking up these materials.

Oyster reefs are conspicuous components of tidal channels (Bahr & Lanier 1981). Due to their abundance and tremendous filtration capacities, bivalves have been implicated as major controllers of nutrient cycling in estuarine ecosystems (Dame 1996). The rates inorganic nutrient release from intertidal oyster reefs is seasonal with high values in the summer and low values in winter (Dame et al. 1989). Although oysters cover on average 40% of intertidal channel bottoms, our recent experiments comparing intertidal channels with oysters and with oysters removed showed that oysters are not the dominant source of inorganic nutrients (Dame et al. 2002). Instead, much to our surprise, we discovered that seasonal abundances of MLOs can dwarf the biomass of the bivalves by an order of magnitude (Dame et al. 2000b). Summer biomass densities often exceeding 100 g/m³ were composed of numerous transient species (young-of-the-year spot (Leiostomas xanthurus), pinfish (Lagodon rhomboides), mullets (Mugil spp.), and penaeid shrimps) and, to a lesser degree, resident species (e.g. grass shrimps (Palaemonetes spp.), mummichogs (Fundulus heteroclitus)). Using nekton biomass estimates from Creek, some limited literature estimates, and some preliminary data on nekton excretion by (S. Haertel unpublished), we estimate that nutrient production by MLOs may be 5 times higher than that of bivalves and constitute a dominant source of nutrients (Table 1). Thus, the MLOs are an unappreciated source of nutrients in marsh-estuarine ecosystems and as such may be a major force controlling the structure and function of the marsh-estuarine ecosystem, particularly the ICMBs. This information has led us to ask and explore the following core question:

What is the role of mobile link organisms (MLOs) in the processing and flux of materials in intertidal channel-marsh basins (ICMBs)?

Nekton are prominent MLOs of ICMBs (Dame and Allen 1996, Kneib 1997). Although there is a growing amount of information on the role of fish and other MLOs in nutrient cycling in freshwaters (Northcote 1988, Carpenter et al. 1992, Schindler et al. 1993, Brabrand et al 1990, Reinertsen et al. 1990, Attayde and Hansson 2001a, b), relatively little attention has been paid to the potential of MLOs to mediate nutrient fluxes in marine and estuarine systems (Deegan 1993, Gottlieb 1998, Hjerne and Hansson 2002). One exception to this is in regard to aquaculture in fish ponds and pens (Hargreaves 1998). Major early studies in North Inlet, the “Outwelling” (Dame et al. 1986) and “Bly Creek” (Dame et al. 1991) studies, did not consider the role of MLOs (nekton). These animals use tidal channels and marshes as developmental and foraging zones, often modifying the habitat with their activities. Results from our recently completed study on the role of oysters in these habitats indicated that MLOs use of tidal channel habitat could be almost two orders of magnitude greater in summer than winter (Dame et al. in 2002). The seasonal increase of MLOs coincides with the seasonal curve of DIN, and particularly with NH₄ (Fig. 1). This makes sense, especially if one assumes that high rates feeding and inorganic nutrient excretion occur in summer when nekton are most abundant and most metabolically active. We also recognize the potential contributions of other types of MLOs in the system. Wading birds, including egrets, herons, and storks, feed and excrete within the ICMBs. Bottlenose dolphins and sea turtles occur in the ICMBs. We will use field census data and literature reports to estimate feeding and excretion rates for birds, reptiles, and mammals.

Proposed Research

As part of our continuing efforts to understand the structure and function of coastal estuaries, we propose to investigate the role of MLOs in nutrient processing within ICMBs. Our main objective is to ascertain the magnitudes and timing of material fluxes attributable to MLOs in ICMBs as a measure of their importance in the marsh-estuarine ecosystem.

Hypothesis 1: MLOs are major biological sources of dissolved inorganic nutrients in the ICMBs.

Alternatively, MLOs are relatively minor sources of dissolved inorganic nutrients in ICMBs. Other potentially important sources are the mudflats (sediments with associated microbes and benthos), the water column (microbial loop), the oyster reefs (not supported by previous study) and the salt marsh (not supported by previous work).

Sub-hypotheses regarding sources and locations of MLO nutrient contributions.

1. MLO contributions of dissolved inorganic nutrients within ICMBs are mostly associated with excretion following periods of feeding.

2. In remobilizing dissolved inorganic nutrients sequestered in the sediments through bioturbation, the foraging activities of MLOs in ICMBs account for a major portion of the overall flux to the water.

3. Maximum nutrient remobilization occurs when MLOs forage in mudflat subsystems.

Hypothesis 2: Transient MLOs (biomass) comprise a major sink for nitrogen and phosphorus in the ICMBs.

An alternative possibility is that the resident MLOs (biomass) comprise a greater sink for nitrogen and phosphorus.

Subhypothesis:

The majority of MLO biomass occupying subtidal channel refuges at low tide moves into the intertidal channels and drainage basins during the flood tide, acquires and stores N and P, and exports it from the ICMBs.

General strategy:

The proposed research combines:

a) seasonal synoptic field sampling to determine nutrient fluxes for all major ICMB subsystems and corresponding patterns of MLOs occurrence in ICMBs;

b) a large-scale manipulative experiment involving exclusion of MLOs from half of the ICMBs after the initial year of field measurements;

c) small-scale field and laboratory-based experiments designed to derive estimates of nutrient excretion by MLOs.

Site

The location of our study is North Inlet Estuary near Georgetown, SC. This pristine system has been the focus of many ecosystem studies that quantified fluxes of materials between the estuary and coastal ocean (Dame et al. 1986) and between large components of a salt marsh basin influenced by freshwater inputs (Dame et al. 1991). Most recently, we have conducted a study on the role of oysters in a group of ICMBs in the North Inlet system (Dame et al. 2002). Our proposed work seeks to expand our understanding of the role of MLOs in these same ICMBs. These ICMBs are ideally suited for the proposed study because we have so much pertinent background information on their geomorphological, hydrological, chemical, and biological features.

Unlike many estuaries, North Inlet and its surrounding forested uplands are undeveloped and in their natural state. Semi-diurnal tides keep the system well mixed and well flushed. Approximately half of the water leaves the estuary with each ebbing tide and is replaced with ocean water on the subsequent flooding tide (Kjerfve et al. 1981). The North Inlet Estuary is comprised of about 15 primary subtidal channels (10-100 m wide, 1000s m long). Hundreds of intertidal channels (1-3 m wide, 100-400 m in length) extend into the surrounding marshes where they function as ICMBs allowing for the exchange of water and materials as the tide floods and ebbs. Our proposed study will focus on a representative subset of these ICMBs.

As a warm temperate system, North Inlet water temperature and light exhibit a typical seasonal pattern of high values in the summer and low values in the winter. Thus, rates of biotic processes that potentially influence nutrient concentrations (photosynthesis, respiration, feeding, excretion, etc.) are higher in the summer. Our recent studies in the ICMBs of North Inlet clearly showed that light, temperature, ammonium concentrations, photosynthesis, metabolic rates, growth, transient nekton biomass, etc., all appear to peak in the summer (Lewitus et al. 1998, Dame et al. 2002). This synchronous seasonal pulsing persisted during strong environmental events such as the ENSO of 1998-99 or hurricane Floyd of 1999 (Fig. 1).

Field Sampling-Year One: surveys, calibrations, and methods development

The configuration of a typical ICMB in the North Inlet Estuary is shown in Figure 2. Each ICMB has a single intertidal channel, which serves as the primary conduit of exchange with the adjacent subtidal channel. Flooding tides extend along the channel axis covering intertidal mudflats and oyster reefs and when the channel is full, water begins to cover the vegetated surface of the marsh. Depending on the astronomical and wind-modified height of the high tide, water depth on the marsh surface at high tide may be from a few to about 100 cm, but the duration of flooding is usually less than 2 h of the typical 12.8 h tidal cycle. Fairly well defined drainage basins can be identified on the marsh, and, for most high tides, all flood waters return (ebb) to the intertidal channel from which they were delivered to the marsh. We will identify the outer boundaries for each ICMB on a high tide that stops short of mixing with an adjacent basin. Sampling will be scheduled only on dates when the predicted high tide levels would be expected to approach but not extend beyond the basin’s boundaries. Thus, during a flood-ebb cycle each ICMB functions independently.

Our three-year research plan will focus on the characterization, monitoring, and partial manipulation of four ICMBs in the North Inlet Estuary. In the first year, the ICMBs will be surveyed to determine elevations, total area, and the locations and sizes of the subsystems. These GIS databases and models of the landscape combined with hydrographic measurements will provide us with information necessary to calculate the flux of water and dissolved constituents between the subtidal channel and the intertidal basin. From these survey and calibration efforts, we will determine the locations of sampling transects and chamber installations, the frequency and number of sample collections, and other related methods as described in the following pages.

Besides defining the spatial and temporal dimensions of the sampling program, we will assess human resource needs, refine sample analysis techniques, and establish data management protocol. Other activities during the first year will include the construction of boardwalks and other access/collection infrastructure that will be necessary to minimize short-and long-term impacts (primarily trampling) on the basins. We will also design and test the in situ chambers to determine nutrient changes in the subsystems (described below).

Seasonal synoptic samplings and weekly water collections

Formal sampling to test our hypothesis that MLOs are the primary source of dissolved inorganic nutrients in the ICMBs will begin in the second year and continue through the third year. Based on our experience over more than twenty years of monitoring and recent collections during the Creek Project, we have identified five periods within the annual cycle during which environmental conditions and nekton composition (species, life stages, relative and actual abundance) are distinctive. Our proposed target dates are mid- February, mid-May, mid-July, early September, and mid-October (Ogburn, et al. 1988).

During each period, we will sample all four ICMBs on each of two dates separated by about two weeks. This timing will allow us to sample a similar 13-hour period from morning low tide to evening low tide. Because of the lunar-regulated progression of tides, predicted high tide levels will guide our choice of dates that can be treated as replicates in the analysis. Logistical constraints, disturbance impacts, and the probability of adverse weather conditions limit the frequency and number of times each basin can be sampled per period. However, because sudden rainfall events associated with typical summer thunderstorms resuspend sediments and likely cause changes in dissolved and particulate fluxes, we will be prepared to collect data on a third date for comparison. Logistic and safety limitations associated with sampling at night will force us to confine the regular seasonal synoptic samplings to the daylight hours. We will sample at least one complete nocturnal tidal cycle on another summer date.

Synoptic collections of water and physical data will form the basis of our spatial comparison of nutrient concentrations and other conditions at various locations within each ICMB. Current velocity will be measured in the intertidal channel cross-sections. Since we will also need to understand the relationship between the intertidal basin and the subtidal channel that serves as the source of water during the flooding tide and recipient during the ebb tide, we will make a simultaneous set of velocity measurements in the subtidal channel cross-section. Determination of material fluxes in marsh-estuarine tidal channels requires the estimation of material concentrations and the concurrent observation of water discharge. The cross multiplication of water discharge and material concentration values yields material flux estimates. Early studies (Boon 1978, Kjerfve and Proehl 1979, Kjerfve et al. 1981, Roman 1984) showed that lateral cross sectional variations in both material concentrations and water velocities must be accounted for in any determination of material exchanges in marsh-estuarine tidal channels. They also noted that the numerical value for water volume per unit time was much larger than the corresponding material concentration terms. Thus, small errors in measuring water velocity and calculating water discharge could potentially lead to large errors in material flux estimates (Kjerfve and Proehl 1979, Valiela et al. 1980, Roman 1984, Kremer et al. 2000). Further, stochastic climatic events, i.e., storms, may overwhelm day-to-day flux estimates (Kremer et al. 2000). This problem is particularly evident in macro-tidal (range >4 m) systems with high water velocities and large discharges (Lane et al. 1997). In order to minimize errors in estimating material exchanges in our meso-tidal (avg. tidal range 1.8 m and water velocities usually less than 30 cm/s) channels, we will comprehensively assess lateral and vertical water velocity and material concentrations over a typical tidal cycle in each of our intertidal and subtidal channel cross-sections with a calibration study using a dense spatial and temporal sampling array. This method was suggested by Kjerfve and Proehl (1979) and Roman (1984), and extensively used by our team in the past (Kjerfve et al. 1981, Dame et al. 1986, 1991). It is important to note that former measuring devices were accurate to 1-4 cm/s. We will measure water velocities with mini ADV (Acoustic Doppler Velocity) meters that have an accuracy of 0.1 cm/s at a water velocity of 10 cm/s, an order of magnitude more accurate than the previous devices. Thus, by using much more accurate ADV meters, working in low flow tidal channels and calibrating each cross-section as described above, we are confident that we will observe significant differences in material fluxes for ICMBs with MLOs and with MLOs excluded.

Water samples will be collected at the same time the physical measurements are made at each cross-section during the 13-hour series. The samples will be iced and immediately taken to the nearby BML. Water samples will be processed and analyzed using standard techniques for the following measurements: suspended organic and inorganic material by filtering through glass fiber filters and weighing; ammonium concentrations using a Technicon AutoAnalyzer technique (Glibert and Loder 1977); nitrate + nitrite by cadmium reduction with autoanalysis of nitrite (Glibert and Loder 1977); orthophosphate will be analyzed using the Murphy and Riley (1962) method as applied to autoanalysis by Glibert and Loder (1977); urea will be measured by the urease method (Parson et al. 1984); C, N, P proportions of MLO biomass will be determined by standard techniques; and chlorophyll a using the freeze-thaw acetone procedure of Glover and Morris (1979), In addition to the chemical analyses of water samples collected during the replicated, intensive, 13 hour (seasonal) sampling series within the ICMBs in Year 2, we will collect and process samples once each week during both Years 2 and 3. Samples will be collected from the same intertidal cross-sections at mid ebb tide to track changes in nutrient concentrations that may be associated with short-term (storms) and long-term stochastic events (ENSO).

These sampling programs will provide an understanding of nutrient dynamics at the ICMB system scale. Since we are also interested in the relative roles of the subsystems (Fig. 2) as processors of materials within the intertidal areas, we will conduct another series of measurements. During each seasonal sampling (13 hour series), we will conduct short-term experiments to determine changes in material concentrations within each subsystem type. We propose to install in situ chambers in three benthic subsystems. A fourth type of chamber will be installed in each ICMB to measure nutrient generation by zooplankton and other water column biota smaller than 5 mm. Each subsystem type will be replicated among creeks. We believe that this approach will yield more representative results than land-based mesocosms. The proposed chambers will consist of two long, parallel walls permanently fixed in the sediment and two removable watertight end plates. The water column chamber will have a solid Plexiglas bottom instead of a sediment interface. At one to two hour intervals, the end plates of these flume-like chambers will be closed trapping a parcel of tidal water for a short incubation period. Chamber size will be determined by the average size of the mudflat and oyster patches in the intertidal channel beds, but we will strive for the largest practical size to reduce artifacts that are associated with small containment devices (Asmus et al. 1998, Gardner, et al. 2001). Water collections at the beginning and end of each incubation period will allow us to estimate the extent to which the different bottom types and associated microbial and macro-biota (mud, mud with marsh vegetation, mud with oysters) alter materials in the overlying water column. We have chosen to keep the incubation periods short (probably on the order of 10 minutes, to be determined in year one) in order to reduce unforeseen feedbacks associated with a closed system. We will screen the ends of all chambers to exclude MLOs from the parcels of water captured. This procedure will allow us to assess nutrient changes in the water column that are only associated with the benthic subsystem of interest. However, we will address the contributions of MLOs associated with these different bottom types in another set of experiments described in the section on nekton excretion and bioturbation below.

During each 13-hour sampling period, synoptic measurements and water samples will be collected at these intertidal subsystem chambers as well as at the intertidal and subtidal cross-sections. A team of participants stationed along each ICMB will respond to horn signals to ensure synoptic collections. As the actual number of locations and frequency of collections within each ICMB will not be determined until the Year 1 calibration studies are complete, we anticipate between 60-80 water samples per ICMB per date. About 2800 samples would be produced during the ten proposed 13 hr studies in Years 2 & 3.

MLO Sampling

MLO occupation of the ICMB and subtidal channels will be quantified during all of the 13-hour studies in Years 2 and 3. In the intertidal area, we will use non-destructive methods to determine characteristics of the fishes, shrimps, and crabs as they depart the creek during the ebbing tide. At slack high tide, a funnel net will be set near the intertidal channel cross-section and MLOs moving toward the subtidal channel with the ebbing tide will be quantified (Cain and Dean 1976, Bozeman and Dean 1980, Rozas et al. 1988, Hettler 1989). Motile animals larger than 15 mm will be retained by the mesh and shunted through the open down-tide end of the net and across a long chute into the subtidal channel refuge with minimal disturbance. We will use video recordings from cameras mounted above the chutes to acquire abundance information. A pair of observers will verify species composition, and remove sub-samples to determine size distributions, weights and chemical composition. At low tide, seines will be used to collect MLOs remaining in low tide refuges (pools) within the intertidal basin (Allen et al. 1992). To test of Hypothesis 2, we will sub-sample nekton remaining, entering and leaving the ICMBs as well as conduct tissue (C-N-P) analyses. In order to quantify MLOs prey consumption within the ICMBs relative to the subtidal channel refuges, we will conduct quantitative analyses of the gut contents of a subset of fishes on each sampling date. These efforts will provide very complete information on feeding and estimates of material exported from the ICMBs.

MLOs associated fluxes in the specific intertidal subsystems will be on days other than routine samplings. By closing the open-ended subsystem chambers and quantifying the MLO present, we will be able to estimate MLO use of the different bottom types at different stages of the tide. These kinds of chambers or flumes have been used to quantify MLO in a variety of estuarine habitats (McIvor and Odum 1986, Peterson and Turner 1994, Rozas and Minello 1997). These data, combined with MLO density data from the proposed whole basin chute sampling, historic data from these sites, results from the MLO-excluded subsystem chamber experiments, and results of the excretion experiments (below), will enable us to estimate MLO material processing for each of the subsystems.

In order to quantify our current understanding that most of the small MLOs leave the subtidal areas and occupy intertidal areas when they are flooded, we will also quantify the species composition and biomass of MLO in the subtidal channel using a flume technique that has been designed and tested in intertidal systems (Bretsch and Allen ongoing). We are confident that this new and highly efficient method can be adapted to areas. These data combined with the synoptic water samples will allow us to examine the relationship between MLOs and nutrient levels in the subtidal channel at different stages of the tide.

MLO exclusion experiments.

A replicated BACI (Before-After Control-Impact) design (Stewart-Oaten ET al.1986, Dame et al. 2000b) will be used to evaluate the contribution of MLO to nutrients with the ICMBs. Due to many limitations including small numbers of experimental systems, time, logistics, and expenses, adequate replication is often difficult to achieve in ecosystem experiments (Carpenter 1989). In such cases, paired-system experiments (one reference and one experimental system) are often preferable, even though classical statistics cannot be used to detect manipulation effects (Carpenter 1989). BACI is a method to identify non-random changes in manipulated systems. In an expanded version with replicated controls (Underwood 1994, Dame et al. 2000b). Based on our past work (Dame et al. 2002), we propose to use BACI to test the effect of MLOs in this study as well.

In the third (final) year, we will randomly select two of the four ICMBs and construct plastic mesh fences around their perimeters to exclude MLOs (>10 mm). The basin will be fenced at low tide and any MLOs remaining in pools or stranded during subsequent ebb tides will be removed. After three days (six consecutive low tides), the basin should be almost devoid of MLOs. The 13-hour sampling will begin on the fourth day. A preliminary trial to exclude MLOs from several intertidal basins was successful, and we are confident that we can accomplish this large-scale manipulation.

          Water chemistry and physical measurements identical to those made in Year 2 will be made in the

ICMBs with and without MLOs. In this experimental design, both the ‘impacted’ and ‘control’ ICMBs will be

sampled before and after the impact. This approach will allow us to test whether MLOs contribute

significantly to material fluxes in the ICMBs.

Laboratory and field based excretion experiments

During each period in Years 2 and 3, nutrient production by MLOs and the relative importance of excretion versus bioturbation for MLO-mediated nutrient regeneration will be measured in a set of field experiments using common species held in closed systems. Since excretion rates depend on many ecological and physiological conditions including body size, condition, diet, and temperature (Mather et al. 1995), we will measure them in situ. MLOs that have fed in the intertidal basin during the high tide will be collected during the ebbing tide. Individuals will be transferred to bags with 1 µm-filtered ICMB water and incubated in the field. Nutrient release will be measured after 2 -3 h (Schaus et al.1997). Ten replicates (plus MLOs-less controls) will be run for each major species and size class. Preliminary experiments were run in summer 2001 with spot, pinfish, and penaeid shrimp. Using a range of biomass densities (0.6 – 4.5 g l^-1) resulted in ammonia excretion rates of 1.6 – 6.9 µM g^-1 wet weight h^-1. These changes are easily detected above background concentrations and suggest that the signal related to nekton activity in the ICMBs will be detectable in the field studies.

The relative importance of nutrient regeneration through bioturbation compared to excretion by feeding MLOs will be assessed in a set of laboratory-based tank experiments in which MLOs are provided with natural foods in sediments or deprived of access to sediments (through a mesh screen) but provided the same source of food above the sediments (Havens 1991, Schaus & Vanni 2000). These experiments will test differences in the extent of bioturbation and associated nutrient releases as a function of species assemblage, bottom type (e.g. vegetated mud, oyster shell/reef), and time of exposure. During preliminary experiments in March 2002, bioturbation was found to be negligible. The nekton community at this time of the year is, however, dominated by small spot and grass shrimp, and we expect different results when we repeat this experiment with the more diverse summer assemblage dominated by larger young-of-the-year nekton in August.

Together these independent measurements of excretion rates and the relative importance of bioturbation will enable us to estimate the amount of nutrients contributed by the MLOs, and give insight into the mechanisms involved. The nutrient production rates coupled with estimates of MLOs composition and biomass from the field studies will be used to estimate the total nutrient production potential of the MLOs for each basin on each date, and can be compared to the field estimates during the exclusion and the intertidal subsystem chamber experiments.

Summary

We have proposed to: (1) determine the seasonal fluxes of materials (including MLOs) and water

simultaneously in four ICMBs, (2) perform a set of small and intermediate scale laboratory and field

experiments to quantify material fluxes by the major subsystems of the ICMBs, (3) establish material

flux relationships between the major subsystems of the ICMBs, and (4) conduct an ICMB scale

exclusion experiment to determine the relative contribution of MLOs to the pool of dissolved inorganic

nutrients. Together, these independent but coordinated field and laboratory studies will allow us to

test our hypotheses and subhypotheses and provide quantitative information on the adequacy of

several general ecological boundary theories. These observations and experiments will lead us to a

greater understanding of these highly productive and threatened ecosystems. More specifically,

results will provide the first comprehensive and quantitative data on the role of MLOs in processing

and transporting materials within the ICMBs and between the intertidal and subtidal channels.

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