Ocean & Coastal Management 68 (2012) 102e113
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Ocean & Coastal Management
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Biogeochemical cycles in sediment and water column of the Wadden Sea: The example Spiekeroog Island in a regional context
Melanie Beck*, Hans-Jürgen Brumsack
Institute for Chemistry and Biology of the Marine Environment (ICBM), Carl von Ossietzky University, Carl-von-Ossietzky-Str. 9-11, D-26129 Oldenburg, Germany article info abstract
Article history: Tidal flats like the Wadden Sea are areas of high primary production and organic matter remineralization Available online 17 June 2012 rates. This paper provides an overview of benthic remineralization pathways and the recycling of various metabolic products, exemplified by interdisciplinary studies around Spiekeroog Island (Germany). Organic matter produced in the Wadden Sea area as well as material imported from the North Sea is remineralized in tidal flat sediments. Wadden Sea sediments may thus be regarded as biogeochemical reactors promoting or accelerating organic matter remineralization. Due to advective flow, which is of special importance in permeable sandy sediments, pore waters enriched in remineralized nutrients and methane are actively released from sediments into the overlying water column. This biogeochemical recycling forms the prerequisite for continuously high primary production in the Wadden Sea, and proves a tight coupling between benthic and pelagic dynamics. Additionally, the export of excess nutrients from the Wadden Sea further offshore may trigger biological activity in coastal waters of the North Sea. In this contribution, we will also summarize open questions which need to be answered for a thorough understanding, management and protection of the unique Wadden Sea ecosystem. In particular, the currently understudied, but potentially significant effects of climate change (e.g., rising sea level and increase in storm surge extremes) on biogeochemical cycles in sediments and open waters of the Wadden Sea are discussed. Ó 2012 Elsevier Ltd. All rights reserved.
1. Introduction exhibits high rates of primary production (Cadée and Hegeman, 2002; Loebl et al., 2007; Poremba et al., 1999). These high rates The tidal flats of the Wadden Sea form the largest continuous are not only supported by the presence of well-adapted phyto- area of sand- and mudflats worldwide, accounting for 60% of all plankton and microorganism consortia, but also by enhanced tidal areas in Europe and North Africa (Marencic, 2009). The region nutrient availability due to rapid organic matter (OM) reminerali- sustains a rich and diverse flora and fauna and is of outstanding zation. In intertidal areas, aerobic and anaerobic OM degradation international importance as staging and wintering area for migra- processes are fuelled by filtration of suspended particles and dis- tory birds (Marencic, 2009). Due to its unique nature, the Wadden solved OM from the water column within permeable sediments. Sea has been inscribed on the World Heritage List in 2009 and often Continuous supply of organic substrate supports enhanced micro- serves as a worldwide reference for comparisons with other tidal bial activity, and ultimately the release of metabolic products such flat systems. This highlights the importance to attain the best as nutrients and methane (CH4) to the pore waters. Tidal pumping possible understanding of biological, chemical and physical induces advective flushing of permeable sediments and the trans- processes sustaining this ecosystem. The intense biogeochemical port of remineralization products to the open water column, where cycling of carbon and nutrients has been identified as crucial for they can once again support primary production. Furthermore, the controlling life and ecosystem dynamics in the Wadden Sea. Wadden Sea is an open system where water exchange with the Organisms living in tidal flat ecosystems have to tolerate North Sea occurs through tidal inlets. Thus, the quality of water, extreme environmental gradients in salinity, incident light, oxygen sediment and marine habitats is to a large degree influenced by availability and temperature. Nevertheless, this type of landscape processes occurring in the North Sea and vice versa. In this paper we will summarize benthic remineralization pathways, with a focus on metabolic products including nutrients * Corresponding author. Tel.: þ49 441 7983627; fax: þ49 441 7983404. and CH4. Benthic OM remineralization and the subsequent nutrient E-mail address: [email protected] (M. Beck). recycling are essential mechanisms providing important building
0964-5691/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ocecoaman.2012.05.026 M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113 103 blocks of life. The trace gas CH4, which is produced as metabolic acceptor in the cascade will occur when the pool of an electron end-member in deeper sediments, may contribute to global acceptor with a higher energy yield is depleted. Nevertheless, warming when released to the atmosphere. However, the assess- microorganisms may create their niche by using substrates not ment of CH4 sources and sinks is still not fully explored in intertidal consumed by the community living in the adjacent zone (van der areas such as the Wadden Sea. Most of the biogeochemical cycles Maarel and Hansen, 1997; Wilms et al., 2006). Furthermore, pore are exemplarily presented using interdisciplinary studies around water exchange may blur the gradients by a continuous resupply of Spiekeroog Island (Germany). Our paper further addresses open electron acceptors (Beck et al., 2008c; Jansen et al., 2009). There- scientific questions and future challenges for the protection of the fore, Fig. 1 does not exhibit the conventional redox sequence in Wadden Sea. A thorough understanding of biogeochemical mineralization pathways, but shows that in the highly dynamic processes in the Wadden Sea will be a requirement for its intertidal sediments, the classical redox cascade may be disturbed sustainable future management, as biogeochemical cycles form an by pore water flow, especially in the strongly irrigated top layer. essential mechanism controlling chemical reactions and biological Finally, processes of OM remineralization lead to the accumulation growth in this ecosystem. Gaps in knowledge, e.g. regarding the of dissolved organic carbon (DOC), alkalinity, and nutrients with effects of climate change on the Wadden Sea, need to be recognized increasing depth in pore waters (Fig. 1). and addressed by future research plans.
2.1. Aerobic oxidation, reduction of nitrate and Mn/Fe oxides 2. OM remineralization in Wadden Sea sediments In the uppermost sediment layer, aerobic respiration dominates Bioturbation, bioirrigation, and/or diffusive and advective OM degradation. The depth where oxygen is still available for processes introduce OM into surface sediments of the Wadden Sea carbon (C) mineralization depends on sediment permeability. The (Meysman et al., 2005, 2007; Rusch et al., 2001; Volkenborn et al., high permeability of sand facilitates advective pore water trans- 2007; see chapter 3) where it is degraded by a cascade of redox port, in contrast to diffusion-controlled muddy sediments. processes. Aerobic respiration is followed by nitrate reduction, Furthermore, pore water flow is enhanced in surface sediments reduction of manganese (Mn) and iron (Fe) oxides, sulfate reduc- with ripple structures due to pressure gradients generated by the tion and finally methanogenesis (Froelich et al., 1979; Jørgensen, interaction of bottom currents with sediment topography (Huettel 2006). Theoretically, the sediments are divided into different and Gust, 1992; Huettel et al., 2003). This pore water flow at the zones, each characterized by a microbial community using sediment surface is an effective mechanism for rapid exchange of a specific electron acceptor. In general, a shift to the next electron oxygen (Precht et al., 2004; Ziebis et al., 1996). Consequently,
NO - [µM] Mn [µM] Fe [µM] SO 2- [mM] 3 4 0369120 8 16 24 32 0 4 8 12 16 0 8 16 24 32 0
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DOC [mM] Alkalinity [mM] NH + [mM] PO 3- [µM] 4 4 Si(OH)4 [µM] 012340 122436480369120 300 600 900 1200 0 300 600 900 1200 0
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Fig. 1. The redox cascade in Wadden Sea sediments: pore water profiles of nitrate, manganese (Mn), iron (Fe), and sulfate. The compounds are either used as electron acceptors or þ 3 produced during OM remineralization. Dissolved organic carbon (DOC), alkalinity, NH4 ,PO4 , and Si(OH)4 accumulate with depth as they are released when OM or diatom frustules are degraded. The sampling site is located in an intertidal sand flat close to a creek bank in the backbarrier area of Spiekeroog Island. Permanently installed samplers were used to extract pore waters from 20 different depths (Beck et al., 2007). Data are derived from a sampling campaign in April 2006. The figure was modified after Beck et al. (2008a,b). 104 M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113 oxygen is depleted within the uppermost millimeters in clay-rich Sulfate [mM] dsrA targets [g-1 sediment] sediments (Böttcher et al., 2000), whereas oxic conditions persist 0102030 1x106 2x106 down to some centimeters depth in permeable sediments (Jansen 0 et al., 2009). The oxygen penetration in permeable surface sediments leads to enhanced aerobic mineralization. Highest areal oxygen consump- 1 tion rates (OCR) reaching up to 190 mmol m 2 day 1 were measured, for example, in tidal flat margin sediments flushed with ]m[htpeD seawater each tidal cycle (Billerbeck et al., 2006b; de Beer et al., 2 2005; Werner et al., 2006). To obtain these areal OCRs, the poten- tial OCRs measured were integrated over the oxygen penetration depths. Aerobic mineralization rates were calculated by subtracting 3 depth-integrated sulphate reduction rates from OCRs (assuming that sulphate reduction is the most important anaerobic OM degradation process) and reached up to 150 mmol C m 2 day 1 4 (Werner et al., 2006). The OCRs determined in the permeable top layer of Wadden Sea sediments are about 5 times higher than in open North Sea sediments (Osinga et al., 1996; Upton et al., 5 5 0 50 100 150 1x10 2x10 1993). Methane [nmol cm-3] mcrA targets [g-1 sediment] The importance of denitrification as well as of Mn/Fe oxide reduction for OM remineralization is not as well-constrained as the dsrA -1 contribution of aerobic respiration. In general, it was estimated that Sulfate [mM] targets [g sediment] denitrification accounts only for a small percentage to carbon 01020300 2x106 4x106 6x106 0 oxidation in coastal North Sea sediments (Sørensen et al., 1979; Werner et al., 2006). Estuarine intertidal mudflat sediments exhibit decreasing nitrous oxide emissions with increasing salinity, with emissions of almost zero at a salinity of 15 (Middelburg et al., 5 1995). A whole ecosystem 15N labeling experiment in a tidal
freshwater marsh fringing the nutrient-rich Scheldt River, Belgium, ]m[htpeD indicated that only 2.4 and 0.02% of the watershed derived 10 ammonium was transformed to N2,N2O, respectively (Gribsholt et al., 2006). However, permeable Wadden Sea sediments show potential denitrification rates up to 0.19 mmol N m 2 h 1, one of the highest rates determined in the marine environment so far (Gao 15 et al., 2010). The denitrifying bacteria appear well-adapted to tidally induced redox oscillations in these permeable sediments because denitrification is not entirely inhibited even when oxygen is available. The contributions of Mn and Fe reduction to OM 20 remineralization are minor, but gain importance in Mn- or Fe-rich 0 100 200 300 400 0 2x106 4x106 6x106 sediment layers (Canfield et al., 1993; Thamdrup et al., 1994). In Methane [nmol g-1] mcrA targets [g-1 sediment] Wadden Sea sediments, a Fe(III)-reducing bacterial strain accoun- Fig. 2. Sulfate and CH4 show inverse depth profiles, with CH4 maxima in the sulfate- ted for up to 6% of total cell numbers and even exceeded the depleted zone. The key-genes for sulfate reduction and methanogenesis, the a-units of numbers of sulfate-reducing bacteria in the upper sediment layers the dissimilatory sulfite reductase (dsrA) and the methyl coenzyme-M reductase (Mussmann et al., 2005). Thus, these bacteria may substantially (mcrA), respectively, correspond well with the vertical sulfateemethane profiles. The e fi fi contribute to carbon degradation via dissimilatory reduction of Fe grey bars highlight the sulfate methane interfaces. The gure was modi ed after Engelen and Cypionka (2009) and Beck et al. (2011). oxides in surface sediments of tidal flats.
2.2. Sulfate reduction and methanogenesis Within tidal flats, large spatial differences in sulfate depth Sulfate reduction and methanogenesis are the main terminal profiles point towards changes in sulfate reduction rates. In central pathways of anaerobic OM remineralization in sediments of the parts of tidal flats, seawater sulfate concentrations persist from the Wadden Sea, and have been intensively studied down to 5 m depth surface down to 5 m depth (Beck et al., 2008c, 2009). In contrast, in in the tidal flats of Spiekeroog Island. Sulfate-reducing bacteria creek bank sediments, concentrations decrease strongly with depth form highly abundant and active populations in anoxic sediments and reach values close to zero within a few decimeters (Al-Raei (Gittel et al., 2008; Ishii et al., 2004; Llobet-Brossa et al., 2002). In et al., 2009; Beck et al., 2009; Riedel et al., 2011). In these sedi- general, sulfate and CH4 show inverse depth profiles, with a CH4 ments, microbial activity is enhanced by two processes supplying maximum in the sulfate-depleted zone (Fig. 2; Beck et al., 2009; substrate and/or sulfate. First, rapid sedimentation leads to Wilms et al., 2007). The population sizes of Bacteria, Archaea, enhanced OM sequestration at prograding tidal flat margins (Beck sulfate reducers, and methanogens correspond well to the vertical et al., 2009; Oenema, 1990). Second, surface and deep pore water sulfateemethane profiles (Fig. 2; Wilms et al., 2007). Although advection replenishes the dissolved organic matter and sulfate sulfate reducers and methanogens may compete for the same pools (Billerbeck et al., 2006b; Huettel et al., 2007; Huettel and substrates, methanogens can avoid competition by utilizing non- Rusch, 2000; Riedel et al., 2010). The increase in microbial competitive substrates such as methylated compounds (Wilms activity across creek bank sediments is not only reflected in sulfate, et al., 2006). This may be one reason why methanogens are not but also in CH4 profiles as well as in total cell numbers, sulfate restricted to the sulfate-depleted sediment layers. reduction rates, and concentrations of remineralization products M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113 105
(Al-Raei et al., 2009; Beck et al., 2009; Røy et al., 2008; Werner et al., Sea. Different approaches have been used to estimate exemplarily 2006). In contrast to creek bank sediments, low sedimentation pore water flow rates in the Janssand tidal flat located in the rates and pore water flow velocities limit the microbial activity in backbarrier area of Spiekeroog Island. This tidal flat is covered by central parts of the tidal flats despite the high availability of elec- approximately 1.5e2 m of water during high tide and becomes tron acceptors (such as sulfate) for microbial respiration. exposed for about 6e8 h during low tide. It is almost plane, On average 78 g C m 2 year 1 are mineralized in surface sedi- except at the margin where the sediment surface slopes with ments of the Wadden Sea via sulfate reduction (Al-Raei et al., 2009). 1.6 cm m 1 over ca. 80 m (Billerbeck et al., 2006a). Pore water This estimate is based on a modeling approach for the 154 km2 flow estimates are still challenging, which is reflected by the large tidal area of Spiekeroog Island using sulfate reduction rates of different measured or modeled rates. One of the challenges is the top 15 cm sediments, a mapping of surface sediment distribu- related to the extrapolation of point measurements to a larger area. tion (mudflats, mussel banks, mixed flats dark, sand flat, and light The question whether the on-site lithology or topography is sand flat), and empirical site-specific temperature relations of representative for the investigated tidal basin or the entire Wadden sulfate reduction rates. The importance of sulfate reduction for OM Sea has to be addressed. By studying eight sites in the West and East remineralization in these surface sediments is, however, con- Frisian Wadden Sea, Røy et al. (2008) showed that topography and strained by the finding that sulfate reduction contributes only up to seepage zone of the well-studied Janssand tidal flat are represen- 25% to total OM mineralization (Billerbeck et al., 2006b; Werner tative on a regional scale. et al., 2006). In North Sea sediments, the relative contribution of The first estimate for pore water flow velocity and discharge at sulfate reduction to total OM remineralization is similar, but rates the Janssand tidal flat was presented by Billerbeck et al. (2006a). are a factor 5e10 lower than in Wadden Sea sediments (Upton et al., The horizontal flux was measured by following the passage of 1993). Overall, these data can be compared to estimates for pelagic a fluorescent dye through the sediment at depths from 2 to 50 cm, and benthic primary production in the Wadden Sea. A total and ranged from 0.5 to 0.9 cm h 1. Pore water discharge from the production between 30 and 950 g C m 2 year 1 was reported sloping margin was quantified during exposure by measuring the (Billerbeck et al., 2006a; Tillmann et al., 2000). volume of water collected at the end of an open seepage meter. Measured rates of discharge were 2.4 (March) and 4.2 l m 2 d 1 3. Benthicepelagic coupling (July). Finite element modeling was applied by Røy et al. (2008) to Biogeochemical processes in the sediment are closely coupled to predict pathways and ages of pore water. The calculated flow dynamics in the open water and vice versa. Especially in areas pattern can explain the CH4 and sulfate distributions measured dominated by permeable sandy sediments, the exchange of dis- along a transect across the creek bank, and predicts a residence solved and particulate compounds between both ecosystems is fast. time of the seepage water of about 30 years. This corresponds to Billerbeck et al. (2006b) proposed a concept consisting of two pore a calculated pore water flow ranging from 0.5 to 7 l m 2 d 1, water circulation processes for permeable sediments, leading to depending on the permeability used in the model approach. In a tight coupling of sediment and water column biogeochemistry. contrast to the estimate of Billerbeck et al. (2006a), which inte- ‘Skin circulation’ forms an effective mechanism for rapid water grates the rapid shallow flow over the entire slope, Røy et al. (2008) exchange in surface sediments. It results from pressure gradients considered only the CH4-rich pore water flowing deeper and generated when bottom currents are deflected by small sediment slower. structures of hydrodynamic or biological origin. This type of Riedel et al. (2010) applied a hydrogeological numerical simu- circulation exerts a major control on the exchange of dissolved and lation to investigate groundwater flow in sediment layers down to particulate organic matter across the sedimentewater interface 5 m depth. Maximum simulated groundwater velocities of up to (Ehrenhauss et al., 2004; Huettel and Rusch, 2000; Huettel et al., 7cmh1 are reached during ebb tide, driving circulation of 1996; Rusch et al., 2001; Rusch and Huettel, 2000), microbial and seawater through the sediment with subsequent discharge. benthos ecology (de Beer et al., 2005; Evrard et al., 2010; Discharge averages 0.97 m3 per meter of margin length per tide, but Middelburg et al., 2000), and sediment biogeochemistry (Evrard may vary significantly, most pronounced with the spring-neap tide et al., 2008; Huettel et al., 1998). The close coupling of algal cell cycle. Pore water ages were calculated using the same hydro- concentrations in the boundary layer and those in the uppermost geological simulation with some slight modifications (Riedel et al., sediment layer even suggest that permeable sediments may act as 2011). For example, sulfate is almost completely depleted after 200 short-term storage buffer for phytoplankton (Huettel et al., 2007). days when it reaches the discharge zone close to the low water line. In contrast, ‘body circulation’ affects pore waters located at In a fourth approach, radium isotopes were applied to quantify greater depth (up to some meters) in creek bank sediments. It is the flow of pore water entering the tidal channel during low tide. generated by the hydraulic gradient between the seawater level in Using a flushing time of four days for the water mass within the a tidal channel and the pore water level in the sediment. The backbarrier basin and average activities of 224Ra, 223Ra, and 228Ra hydraulic gradient starts to develop as soon as the tidal flat surface measured in the backbarrier surface and pore waters, a balance of falls dry and is highest during low tide (Riedel et al., 2010; Wilson these isotopes was constructed, which is sustained by a pore water and Gardner, 2006). The induced deep pore water flow is directed flow of 2e4 108 l per tidal cycle (Moore et al., 2011). towards the tidal channel, with highest flow velocities in sediments Depending on the applied approach, the total volume of close to the low water line. This deep advective flow supplies measured or modeled pore water discharge varies. The different permeable sediments with electron acceptors and donors and leads estimates are subjected to errors resulting from the necessary to the discharge of nutrient-rich pore waters into the water column approximations. Moore et al. (2011) tried to compare the different (Beck et al., 2008c; Billerbeck et al., 2006b; Riedel et al., 2011). fluid flow estimates and concluded that the average flow rate estimated by Riedel et al. (2010) is 20e40 times larger than the flow 3.1. Estimates of pore water flow velocities and discharge presented by Billerbeck et al. (2006a), whereas it represents only about 20% of the radium-based fluid flow for the entire area. In Knowledge about pore water flow velocities and the amount of contrast to Riedel et al. (2010), who evaluated deep pore water pore water discharged from the sediments to the open water fluxes, Billerbeck et al. (2006a) only considered fluxes in the upper column is essential to budget biogeochemical cycles in the Wadden sediment layers. However, the Riedel et al. (2010) estimate only 106 M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113 covers pore water input from one distinct transect located at the They estimated that on the Janssand tidal flat, the anoxic seeps Janssand margin, whereas the radium isotopes include pore water comprise 2% of the surface area, and only leak about input from other tidal flats as well as groundwater input from 0.013 mmol C m 2 d 1 averaged over the entire sand flat. The terrestrial sources. authors conclude that this is at least three orders of magnitude lower than the rates of primary production and mineralization in 3.2. Nutrient and methane release from sediments the Wadden Sea, and thus CH4 seepage is of limited importance for the carbon cycle in tidal flats. Similarly, Middelburg et al. (2002) fi fl Pore water flux estimates coupled to knowledge of pore water identi ed tidal ats and creeks as CH4 sources to estuarine concentrations permit to calculate the release of species such as waters, but concluded that estuaries contribute less than 9% to the nutrients and methane from the sediment to the water column. global marine CH4 emission. Seepage measurements and pore water nutrient concentrations were used to estimate nutrient effluxes by Billerbeck et al. (2006a). 4. Biogeochemical cycles in Wadden Sea waters 2 1 þ For instance, they reached 7.6 mmol m d for NH4 , 2 1 3- 2 1 2.5 mmol m d for PO4 , and 1.7 mmol m d for Si(OH)4 in The release of nutrient-rich pore waters to the overlying water July. Furthermore, the nutrient input by pore water seepage was column is an important mechanism triggering biological processes estimated based on radium isotope measurements. In the entire in Wadden Sea waters. Pulses of elevated nutrient concentrations 4 Spiekeroog tidal flat area, about 2e23 10 mol Si(OH)4 are are frequently observed in the water column during low tide released from the sediments each tidal cycle (Moore et al., 2011). (Grunwald et al., 2010), when the discharge of nutrient-rich pore The release of CH4 from sediments can be reduced by its aerobic waters from creek bank sediments is highest (Riedel et al., 2010) and anaerobic oxidation (Krüger et al., 2005; Treude et al., 2005). (Fig. 3). The tight benthicepelagic coupling further prevents For example, CH4 diffusing upwards into the sulfate zone is extended periods of nutrient depletion that could limit phyto- oxidized to CO2 at the expense of sulfate, which amounts to plankton growth. Only shortly after the spring phytoplankton a sulfate loss equivalent to about 10% of the total sulfate reduction bloom, silicate and phosphate concentrations are close to zero in coastal sediments (Jørgensen et al., 2001). In the Wadden Sea (Fig. 4), but the nutrient pools are quickly replenished by pore area, profiles of the key genes for dissimilatory sulfate reduction water supply (Billerbeck et al., 2006b; Grunwald et al., 2010; and methanogenesis suggest anaerobic oxidation of methane Kowalski et al., 2009). In contrast to phosphate, the effect of (AOM) at sulfateemethane transition zones (Wilms et al., 2007). resupply is less pronounced in seasonal silicate dynamics due to First measurements of ex-situ AOM rates show that rates peak in assimilation by diatoms even outside the bloom periods. Only the sulfateemethane transition zones (Beck et al., 2011). nutrients like nitrate and nitrite, which are not enriched but At tidal flat margins, pore water exchange occurs on short consumed in pore waters, show a long-lasting depletion in the timescales, supporting the coexistence of sulfate and CH4. water column from early spring until autumn (Fig. 4). Furthermore, the seeps on the slope of the Janssand tidal flat are Similar to nutrients, CH4 exhibits a tidally driven pattern in the sulfidic, depleted in sulfate, and saturated with CH4 (Røy et al., water column with highest concentrations during low tide 2008). Thus, an oxic surface layer where re-oxidation may (Grunwald et al., 2009)(Fig. 3). The elevated CH4 levels during low prevent the emission of CH4 is partly missing. Røy et al. (2008) tried tide may have two major sources: pore water discharge from to assess the importance of CH4 seepage for the carbon cycle in tidal sediments, and/or freshwater released to the tidal flat area via 2 1 flats. Assuming a pore water flow rate of 0.5 l m d and CH4 flood-gates. Pore waters seeping from creek bank sediments during saturation in pore waters, they calculated that 0.65 mmol CH4 are low tide are rich in CH4 (Al-Raei et al., 2009; Røy et al., 2008). These transported to the open water column per square meter per day. CH4-rich pore waters are the main source transporting CH4 to the
30 1.6 ]Mµ[
20 ]Mµ[ 1.2 4 )HO(iS -3
4 0.8 10 OP 0.4
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22 ] ]Mn[
Mµ[ 18 x 4 ON HC 300 14 200
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Fig. 3. Tidal dynamics of nutrients and CH4 at a time series station (Grunwald et al., 2007) close to Spiekeroog Island (East Frisian Wadden Sea) in 2007 and 2005, respectively. Figures slightly modified after Grunwald et al. (2009, 2010). Grey lines indicate the tidal state. M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113 107
5. Transport of nutrients and CH4 between Wadden Sea and North Sea
Along the East and West Frisian coastline, the boundary between the North Sea and the Wadden Sea is formed by a chain of barrier islands separated by tidal inlets. These tidal inlets control the water exchange between the tidal flat area and the North Sea. In contrast, the North Frisian Wadden Sea islands located several kilometres off the coastline are separated by much wider channel systems. The tidally induced water exchange leads to import/export of biological and chemical compounds between the Wadden Sea and coastal waters of the North Sea. Metabolic end-members like nutrients and CH4, enriched in Wadden Sea waters compared to the North Sea during most of the year, are exported and influence the biogeochemistry of coastal North Sea waters. Nutrient export from the Spiekeroog tidal flat area to the adja- cent North Sea was estimated using a coupled EulereLangrangian model as part of the ecological tidal model EcoTIM (Kohlmeier and Ebenhöh, 2007, 2009). The model indicates that dissolved 6 1 3- 6 1 inorganic Si(OH)4 (128 10 mol a ), PO4 (3 10 mol a ), and 6 1 NOx (29 10 mol a ) are exported from the tidal flat system to the North Sea (Grunwald et al., 2010). A comparison of nutrient levels and patterns of the Spiekeroog tidal flat area with data from the North Frisian Wadden Sea shows similarities (Grunwald et al., 2010; van Beusekom et al., 2009). Therefore, the model results of the Spiekeroog area were extrapolated to the entire German Wadden Sea. This extrapolation highlights an export of dissolved nutrients from the Wadden Sea area in the same order of magni- tude as the total nutrient input of the three German rivers Elbe, Weser and Ems discharging into the North Sea (Grunwald et al., 2010; Lenhart and Pätsch, 2001). The nutrient export by tidal currents and a decreased turbidity in the open North Sea can lead to high primary production in a belt of coastal waters seaward of the barrier islands (Colijn and Cadee, 2003). To estimate the net CH4 export from the Spiekeroog tidal flat area to coastal waters of the North Sea, a similar EulereLangrangian 3 Fig. 4. Seasonal variation of the nutrients Si(OH)4,NOx , and PO4 in the years e model approach was used (Grunwald et al., 2009). The model 2006 2010 determined in surface Wadden Sea waters at a time series station 6 (Grunwald et al., 2007) close to Spiekeroog Island (East Frisian Wadden Sea). Running shows that 3.3 10 mol CH4 are exported per year from the tidal average concentrations are displayed. All nutrients strongly decrease during the spring basin of Spiekeroog Island to the southern North Sea (Grunwald 3 phytoplankton bloom. Nutrients like Si(OH)4 and PO4 , which are re-supplied by pore et al., 2009). Assuming that the study area is representative for water discharge, do hardly reach concentrations close to zero, whereas NOx exhibits 3 the entire East Frisian Wadden Sea, a CH4 export to the North Sea of very low concentrations from spring until autumn. PO4 is especially introduced into 6 the water column from surface sediments in summer when anoxic conditions in the 7.8 10 mol CH4 per year was calculated, intermediate between 3 uppermost layer lead to reduction of Fe oxides and release of adsorbed PO4 . the methane exported by the rivers Rhine and Weser (Grunwald et al., 2009; Upstill-Goddard et al., 2000). Overall, the estimates highlight the importance of the tidal flat system for the nutrient and CH4 budgets of the southern North Sea. open water column. In contrast, the freshwater contribution to the To balance the export of species such as dissolved inorganic CH4 budget of the back barrier water column is comparably small. nutrients and CH4 from the tidal basins, it was hypothesized that Although the watercourses draining the hinterland may exhibit CH4 OM is imported from the North Sea to the tidal flat system (van concentrations up to 8 mM, which is more than one order of Beusekom and de Jonge, 2002). The proposed conceptual model magnitude higher than in Wadden Sea waters, the contribution was was based on three assumptions: (1) nitrogen limits the primary estimated to be less than 10% (Grunwald et al., 2009). This production in the coastal zone, (2) a proportional part of the phenomenon is explained by the generally low freshwater primary produced OM is transported into the Wadden Sea and discharge into the backbarrier area, and the high CH4 concentra- (3) the imported organic matter is remineralized within the tions in pore waters. Also, salt marshes may form a CH4 source to Wadden Sea and supports the local productivity by nitrogen the Wadden Sea, but few studies have focused on this topic so far turnover. To date, studies further verifying this conceptual (see 6.3.3). In the water column, CH4 concentrations may diminish model are still missing. However, several studies indicate that due to degassing and oxidation. In the Wadden Sea area, degassing nutrients, CH4, dissolved inorganic carbon and metals are of CH4 probably occurs when waters pass a shoal located off the exported from the tidal flat area to the adjacent North Sea islands along an extension of the tidal inlets (Grunwald et al., 2009). (Grunwald et al., 2009, 2010; Moore et al., 2011). Further, they In general, this zone is characterized by enhanced wave activity and present first evidences that the export cannot be balanced by turbulence. Methane oxidation is assumed to be of minor impor- the freshwater discharge to the tidal basins. Therefore, estuaries tance in Wadden Sea waters due to the short residence time within and North Sea might be of importance to balance the budgets the backbarrier area (Grunwald et al., 2009). as well. 108 M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113
6. Open questions and future challenges compared to marine settings, and reduction of Fe oxides turns out to be an important electron accepting process for OM reminerali- 6.1. Extrapolation of results to the entire Wadden Sea zation (Jakobsen and Postma, 1999; Larsen et al., 2006). To our knowledge, too few studies have been conducted so far to estimate The geographies of the West and East Frisian Wadden Sea are whether the discharge of groundwater from coastal aquifers into quite similar, whereas North Frisia differs by the lack of closely- the adjacent Wadden Sea environment is of importance for spaced barrier islands, and by exhibiting wider tidal inlets. These biogeochemical processes. The influence of large-scale geological differences may influence the import/export of OM and metabolic structures as well as small-scale sedimentary heterogeneities on products between the Wadden Sea and the adjacent North Sea as groundwater flow, discharge and chemistry complicates an well as biogeochemical processes within the Wadden Sea area. Up extrapolation of available data sets to larger areas. to date, few investigations have studied identical processes at the In the tidal flat area of Spiekeroog Island, two 20 m long sedi- same time in several tidal basins (Kraft et al., 2011), although such ment cores were retrieved to extend the knowledge on biogeo- studies are essential to differentiate between processes common to chemistry, microbial abundance, and activity of sulfate reducers/ the entire Wadden Sea, and dynamics induced by specific local methanogens beyond the intensively studied 5 m depth interval. conditions. For example, Kowalski et al. (2011) compared seasonal One core were drilled through mainly Holocene sediments depos- and tidal dynamics of the trace metal Mn in the East and North ited in a paleo-channel. This core exhibits inverse sulfate and CH4 Frisian Wadden Seas (Spiekeroog and Sylt-Rømø). The authors depth profiles similar to the results described above, however, the observed similarities in seasonal Mn pattern, but significant maximum CH4 concentrations are found at greater depths (Fig. 2; quantitative differences. Apparently, site-specific properties of the Beck et al., 2011). The highest CH4 concentrations are located in different tidal basins have to be considered when establishing clay-rich, diffusion-dominated layers. Whether the CH4 trapped in budget calculations for the entire Wadden Sea. these layers is transported vertically or horizontally, or even Benthic remineralization rates measured in the Spiekeroog and released to the atmosphere or the open water column is still Sylt-Rømø tidal basins show a less converse behavior, e.g., sulfate unknown. reduction contributes <20% to total C remineralization in both areas (Billerbeck et al., 2006b; Werner et al., 2006). However, small- 6.2.3. Sandy beaches scale variations may be large, especially at tidal flat margins (Al- In the Wadden Sea area, most sandy beach ecosystems are Raei et al., 2009; Beck et al., 2009; Billerbeck et al., 2006b; located on the North Sea-facing sides of the islands. Additional Werner et al., 2006). Therefore, a detailed understanding of sedi- beach sites are found on the western and eastern tips of the West mentological and hydrodynamic conditions is required before and East Frisian islands. Therefore, we hypothesize that processes results can be extrapolated to larger areas and finally to different operating in beach ecosystems are not only coupled to the tidal basins. biogeochemistry of coastal North Sea waters, but may influence biogeochemical dynamics in the Wadden Sea as well. In contrast to 6.2. Understudied Wadden Sea ecosystems intertidal or estuarine locations, few studies have focused on these systems, but the awareness is increasing that the impact of beach Water column and eulitoral tidal flat sediments are the best- ecosystems on biogeochemical cycles in coastal oceans is not well studied compartments of the Wadden Sea. Numerous studies constrained, and its importance may be underestimated (Dugan have identified microbial and biogeochemical processes and their et al., 2010). seasonal/tidal dynamics in both compartments. In contrast, other Beach sediments have been described as “geochemical and Wadden Sea ecosystems have not been subject to extensive microbial deserts” (Boudrau et al., 2001) due to their generally low research, e.g., subtidal areas, coastal aquifers, sandy beaches, and levels of OM and other reactive substances. This is based on the salt marshes. A better understanding of these ecosystems is conception that the biogeochemical importance of sedimentary essential to unravel OM, nutrient, and CH4 cycling in the Wadden environments is proportional to their own stocks of OM and reac- Sea as a whole. tants. However, recent studies have shown that beach sediments may be regarded as biogeochemical reactors promoting or accel- 6.2.1. Subtidal areas erating OM remineralization (Anschutz et al., 2009). Permeable Most studies elucidating biogeochemical dynamics in Wadden beach sands permit enhanced seawater infiltration by high wave Sea sediments have focused on eulitoral areas. In contrast, little is energy (Robinson et al., 2007), thereby supplying OM and electron known about biogeochemical processes in subtidal sediments, and acceptors. their importance for OM and nutrient cycles. Böer et al. (2009a,b) First studies conducted in beach sands of the western tip of studied microbial activities and carbon turnover in subtidal sandy Spiekeroog Island (East Frisian Wadden Sea) show that down to Wadden Sea sediments (Sylt-Rømø Basin, North Frisian Wadden 1.5 m depth, the predominant electron acceptors for OM reminer- Sea, 0.5e2.5 m water depth). Similar to eulitoral sandy sediments, alization are molecular oxygen, nitrate, and Fe/Mn oxides the rapid input of OM results in a very active bacterial community (Schwichtenberg, 2010; Ungermann, 2009). In contrast to intertidal with a biomass turnover of 2e18 days. Advective pore water sediments, sulfate is less important for microbial respiration and transport increases benthic exchange, for example of O2 (Cook et al., OM degradation. This implies that OM oxidation in beach sands 2007). Still, the deposits of the up to 15 m deep channels controlling may lead to the release of nutrient-rich pore waters, but the the water exchange between Wadden Sea and North Sea remain discharge of CH4-rich waters is rather unlikely, or may only occur a black box. below the 1.5 m depth range so far studied.
6.2.2. Coastal aquifers 6.2.4. Salt marshes A few studies focused on biogeochemical processes in coastal The importance of salt marshes with respect to their multiple aquifers hydrologically connected to the Wadden Sea (Andersen ecological values has been known for a long time. It remains et al., 2007; Hansen et al., 2001; Jakobsen and Postma, 1999; uncertain, however, whether the response of salt marshes to the Larsen et al., 2006). For instance, rates of sulfate reduction are shifting climate will moderate or exacerbate warming, for example much lower in a shallow sandy aquifer of Rømø (Denmark) by carbon sequestration or CH4 release (Bromberg Gedan et al., M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113 109
2009). In general, the fresh water- dominated part of the salt marsh If recent sedimentation rates are higher than local sea-level rise system is know to be a relatively large source of CH4 (Chmura et al., evidencing vertical sediment growth, the biogeochemical reactor in 2003). In contrast, the salt water part of the system releases much Wadden Sea sediments may remain unaffected by climate change. less CH4 due to the presence of sulfate and AOM (Bridgham et al., However, if sedimentation cannot balance sea level rise, extended 2006). Therefore, Choi and Wang (2004) postulated that due to inundation durations would lead to a decrease in pore water higher rates of carbon sequestration and lower CH4 emissions, discharge from creek bank sediments (Riedel et al., 2010). On the coastal wetlands could be a more valuable carbon sink than other one hand, this may reduce the amount of seawater cycling through ecosystem in a warmer world with a rising sea level. the sediment leading to less OM and electron acceptor resupply. On The Wadden Sea salt marsh system comprises a fresh and a salt the other hand, less nutrients would be released to the open water water part separated by a transition zone. Biogeochemical studies column, thereby probably leading to a decrease in primary in the salt marshes of Langeoog Island (East Frisian Wadden Sea) productivity. indicate that salt marsh sediments form an important iron source for pore waters due to the presence of a high percentage of reactive 6.3.2. May changes in storm surge frequency/extremes influence sedimentary iron (Kolditz et al., 2009). Only few indications of biogeochemical cycles? sulfate reduction were found within this environment. The study In the Netherlands, an analysis of the number of storms with further shows the effects of flooding during a storm surge on a magnitude of >7 Bft does not show an increasing trend during biogeochemical reactions, which may provide information on the last decades (Oost et al., 2009). In contrast, the yearly highest possible effects of a rising sea level. Flooding will lead to a short- water levels increased up to 8 mm per year since 1868 in the 3 þ term increase in pore water iron, manganese, PO4 , and NH4 Northern Wadden Sea (Hofstede, 2007). Apart from artificial concentrations. causes like dam building, this may be the result of a shift in storm Nevertheless, it is largely unknown how the Wadden Sea salt wind directions. Furthermore, storm surge extremes may increase marsh system will react to rising seawater levels. A possible along the North Sea coast towards the end of this century (Woth consequence might be the introduction of more sulfate into the et al., 2006). pore water system that could act as an electron acceptor for OM A first estimate of the impact of storm surges on nutrient oxidation. As a result, carbon would be converted into CO2 instead budgets in the Spiekeroog tidal flat area shows that losses in 3 of CH4, which in terms of radiative forcing contributes less to inorganic Si(OH)4 and PO4 inventory during storm events account climatic change. Sea level rise may therefore have a negative for 3% and 10%, respectively, of the annual export of both species to feedback on the concentration of atmospheric greenhouse gases the North Sea (T. Riedel, unpublished). Autumn and winter storms through the suppression of microbial methanogenesis in salt marsh may therefore be important for exporting nutrients to offshore systems. waters. Consequently, an increase in storm surge frequency or extremes may alter biogeochemical cycles in the Wadden Sea and 6.3. Impact of climate change on biogeochemical cycles in coastal waters of the North Sea.
Climate change may induce numerous environmental shifts 6.3.3. May global warming influence OM remineralization (Pernetta and Elder, 1992), which will probably influence biogeo- pathways? chemical processes. However, we can only describe some future In the Wadden Sea area, seawater temperature depends on the scenarios because few studies have focused on this topic so far. main wind direction and on global climate development. Long- Certain aspects of climate change have already been addressed in term observations of the sea surface temperature from the recent publications focusing on the Wadden Sea and North Sea, Western Wadden Sea (Marsdiep Inlet) indicate increasing whereas others should be incorporated in future research plans. temperatures since 1980 leading to a warming of up to 1.5 C(van Although climate change is a gradual process and difficult to study Aken, 2008). The Helgoland Roads time series shows a warming in short-term research projects, scenarios for future changes may trend of 1.1 C since 1962 (Wiltshire and Manly, 2004). be established based on the intensive studies conducted in the Pore water temperatures show highest seasonal variations in Wadden Sea area, and on long-term time series such as Helgoland surface layers tightly coupled to changes in sea surface tempera- Roads (Franke et al., 2004; Wiltshire et al., 2008; Wiltshire and ture (Reuter et al., 2009), but exhibit changes down to 2e3m Manly, 2004) and Spiekeroog tidal inlet (Grunwald et al., 2010, depth in permeable sediments (Beck et al., 2008c). Only 5 m 2007; Reuter et al., 2009). Furthermore, mild winters or storm below the sediment surface, temperatures remain rather constant surges may serve as ‘proxy conditions’ for global warming and sea throughout the year. Several studies highlight the temperature level rise, respectively. dependence of OM remineralization steps in Wadden Sea sedi- ments (Al-Raei et al., 2009; Billerbeck et al., 2006b; Jansen et al., 6.3.1. Does vertical sediment growth keep pace with sea level rise? 2009; Kristensen et al., 2000; Werner et al., 2006). For instance, How may this influence the biogeochemical cycles in the sediments? depth-integrated sulfate reduction rates of the top 15 cm increase The compilation of data from several stations along the Dutch by a factor of about 10 from winter to summer (Al-Raei et al., and German coast for the past 150 years indicates a mean sea level 2009; Arnosti et al., 1998; Kristensen et al., 2000). Although rise of 3.6 mm year 1 from 1971 to 2008, with higher rates in the temperature controls biogeochemical processes, other seasonal eastern part of the German Bight compared to the southern part factors such as OM availability simultaneously account for (Wahl et al., 2011). The threshold up to which sea level rise can be increased microbial rates in summer. compensated by sedimentation is still under debate, but it is Overall, global warming may lead to a decrease in oxygen postulated to be lower for large tidal basins than for small ones solubility and an increase in sulfate reduction rates, both resulting (Van Goor et al., 2003). The interaction between the rate of relative in lower redox conditions in the sediments. To date, it is still under sea level rise and the rate of sediment supply (from external debate whether this development may have positive or negative sources or the existing reservoir) defines the stratigraphic response effects on biogeochemical cycles and CH4 emissions. One may of the system. Three main types of stratigraphic responses have speculate whether faster OM turnover may lead to less OM avail- been proposed: progradational, aggradational and transgressive ability in sediment layers where methanogenesis occurs thereby (Flemming, 2002). reducing CH4 emissions to the water column. 110 M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113
6.3.4. May climate change influence primary production and finally Spiteri et al., 2008; Valiela et al., 1992). In contrast to most sites biogeochemical cycles? in the Wadden Sea, Waquoit Bay is a shallow estuary with an Phytoplankton plays a dominant role in carbon and nutrient average depth of 1 m and a tidal range of about 1 m. Similarly to the cycles of coastal areas by producing the major part of OM. The Janssand tidal flat, described in our manuscript as a typical extent of OM reaching the sea floor and being remineralized in permeable sand flat of the Wadden Sea, the coarse-grained sedi- sediments depends on the water depth. In areas with shallow water ments/soils in Waquoit Bay permit submarine groundwater depth like the Wadden Sea about 50% of the total respiration takes discharge (Mulligan and Charette, 2006). In the Wadden Sea, place in the sediment (van Beusekom et al., 1999), whereas the discharge is mainly driven by tides, while in Waquoit Bay saline percentage of benthic remineralization is lower in deeper parts of circulation due to tides and waves is confined to a shallow intertidal the North Sea (Upton et al., 1993). Some studies addressed how zone. Instead, seasonal changes in water table elevation may climate change may influence the coupling between the amount of explain the observed large groundwater discharges (Michael et al., OM produced in the water column and the amount that reaches 2005). The saline circulation through the coastal sediments was bottom sediments. It is suggested that the impact of climate change estimated as 0.56 m3 m 1 d 1 (Mulligan and Charette, 2006), which on local biogeochemistry largely depend on the extent of is in the same order of magnitude as the respective estimate for the phytoplanktonezooplankton interactions, which are influenced by Wadden Sea (considering the relatively large uncertainties induced large-scale atmospheric and oceanographic changes (van by different methodologies; Riedel et al., 2010). In the seepage þ Beusekom and Diel-Christiansen, 2009; Wiltshire and Manly, zone, NH4 concentrations are about two orders of magnitude 2004). The interaction between both factors determines how much higher on the Janssand tidal flat compared to Waquoit Bay indi- of the primary production reaches the benthic system. Additional cating that there discharging pore waters may exert a higher factors possibly influencing future phytoplankton dynamics are impact on water-column biogeochemistry (Kroeger and Charette, global warming, nutrient inventory, alien species, and increased 2008; Riedel et al., 2011). river discharge and turbidity, both induced by an higher precipi- As a conclusion, we can state that despite the global occur- tation (Philippart and Epping, 2009). rence of temperate tidal flat systems comparable to the Wadden Sea, these environments are strongly influenced by regional 7. Comparison with other temperate tidal flat systems climate conditions, tidal amplitudes, coastal currents, local aquifers, weathering in the hinterland, and other environmental In our contribution, we so far focused on biogeochemical cycles factors. It will therefore require additional collaborative in the Wadden Sea. Here we would like to put the described research efforts to estimate the influence these tidal flat systems regional environmental dynamics into a broader, more global exert on biogeochemical processes and element cycles on context. The Wadden Sea represents an outstanding example of a global scale. a temperate-climate sandy barrier island coast. It differs from all other comparable tidal flat and barrier island depositional systems 8. Summary by its spatial scale and its diversity (Marencic, 2009). However, similar depositional environments are found all around the world Wadden Sea sediments function as a coastal filter system. OM in the temperate zone. captured in this filter is degraded, and recycled nutrients are Examples of tidal flats are found along the Korean coast, the released. Due to active biota and advective pore water flow, the Atlantic coasts of North Africa and North America, and the British filter never clogs but is continuously renewed, sustaining the channel and North Sea coast. Typically, these environments exhibit potential for enhanced OM remineralization in this depositional high primary production and organic matter remineralization rates. environment. Recirculation of seawater into and out of the Processes in the water column and the underlying sediments are sediments leads to a tight coupling between benthic and pela- tightly coupled due to bidirectional exchange of nutrients and gic dynamics, a prerequisite for continuously high primary organic material. For example, tidal flat systems along the Korean production. coast exhibit recirculation patterns of seawater into and out of the Numerous studies have already focused on biogeochemical sediments similar to the Wadden Sea. Nutrients released by dynamics in the Wadden Sea area. Nevertheless, various processes submarine groundwater discharge stimulate primary production at and ecosystem compartments still need to be studied in more detail the seafloor and in the water column (e.g., Waska and Kim, 2010, to better estimate their contribution to the carbon, nutrient, trace 2011). However, the input of terrestrial material is of much metal and trace gas cycles in the Wadden Sea. Only few studies greater importance than in the Wadden Sea, as the transport of have addressed the coupling of processes occurring in the Wadden nutrients to the coastal zone is strongly enhanced during the Sea water or sediment column to other adjacent environmental monsoon season by the huge amounts of rain- and groundwater compartments, such as the open North Sea water column or the flushed through the sediments (Waska and Kim, 2011). Further- atmosphere. This knowledge could, for example, help to determine more, tidal water level fluctuations reach up to 10 m, compared to to which extent the Wadden Sea influences biogeochemical cycles a maximum of about 3 m along the southern North Sea coast. Both in the adjacent North Sea. An understanding of naturally occurring monsoon and tidal processes may better facilitate pore water processes, i.e., the environmental baseline, is also necessary to recirculation in the Korean tidal flat area compared to the Wadden predict whether climate change or other anthropogenic interven- Sea, however nutrient concentration in seeping pore waters are tions (e.g., dike building, channel dredging) may have negative partly several orders of magnitude lower in the Korean system (e.g., effects on the ecosystem. Although the Wadden Sea area has been Kim et al., 2005; Moore et al., 2011; Riedel et al., 2011; Waska and under human influence since the Middle Ages, the rapid changes Kim, 2011). induced by an increased land use and industrialization may be A system that has been studied in as much detail as the Spie- a particular challenge for a more sustainable management of this keroog tidal flat area is Waquoit Bay, located on the southern ecosystem. shoreline of Cape Cod at the East coast of the United States. The bay All processes described in this contribution may be of impor- has served as field site for various oceanographic, hydrological, tance in temperate tidal flat systems worldwide. However, regional geological, biological and geochemical studies (e.g., Charette and influences like climate conditions, tidal amplitudes or local aquifers Sholkovitz, 2002, 2006; Dulaiova et al., 2008; Rouxel et al., 2008; have to be taken into account when comparing different systems. M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113 111
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