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Ocean & Coastal Management 68 (2012) 102e113 Contents lists available at SciVerse ScienceDirect Ocean & Coastal Management journal homepage: www.elsevier.com/locate/ocecoaman 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 a r t i c l e i n f o a b s t r a c t Article history: Available online 17 June 2012 Tidal flats like the Wadden Sea are areas of high primary production and organic matter remineralization 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 The tidal flats of the Wadden Sea form the largest continuous area of sand- and mudflats worldwide, accounting for 60% of all tidal areas in Europe and North Africa (Marencic, 2009). The region sustains a rich and diverse flora and fauna and is of outstanding international importance as staging and wintering area for migratory birds (Marencic, 2009). Due to its unique nature, the Wadden Sea has been inscribed on the World Heritage List in 2009 and often serves as a worldwide reference for comparisons with other tidal flat systems. This highlights the importance to attain the best possible understanding of biological, chemical and physical processes sustaining this ecosystem. The intense biogeochemical cycling of carbon and nutrients has been identified as crucial for controlling life and ecosystem dynamics in the Wadden Sea. Organisms living in tidal flat ecosystems have to tolerate extreme environmental gradients in salinity, incident light, oxygen availability and temperature. Nevertheless, this type of landscape * Corresponding author. Tel.: þ49 441 7983627; fax: þ49 441 7983404. E-mail address: [email protected] (M. Beck). 0964-5691/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ocecoaman.2012.05.026 exhibits high rates of primary production (Cadée and Hegeman, 2002; Loebl et al., 2007; Poremba et al., 1999). These high rates are not only supported by the presence of well-adapted phytoplankton and microorganism consortia, but also by enhanced nutrient availability due to rapid organic matter (OM) remineralization. In intertidal areas, aerobic and anaerobic OM degradation processes are fuelled by filtration of suspended particles and dissolved OM from the water column within permeable sediments. Continuous supply of organic substrate supports enhanced microbial activity, and ultimately the release of metabolic products such as nutrients and methane (CH4) to the pore waters. Tidal pumping induces advective flushing of permeable sediments and the transport of remineralization products to the open water column, where they can once again support primary production. Furthermore, the Wadden Sea is an open system where water exchange with the North Sea occurs through tidal inlets. Thus, the quality of water, sediment and marine habitats is to a large degree influenced by 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 and CH4. Benthic OM remineralization and the subsequent nutrient recycling are essential mechanisms providing important building M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113 blocks of life. The trace gas CH4, which is produced as metabolic end-member in deeper sediments, may contribute to global warming when released to the atmosphere. However, the assessment of CH4 sources and sinks is still not fully explored in intertidal areas such as the Wadden Sea. Most of the biogeochemical cycles are exemplarily presented using interdisciplinary studies around Spiekeroog Island (Germany). Our paper further addresses open scientific questions and future challenges for the protection of the Wadden Sea. A thorough understanding of biogeochemical processes in the Wadden Sea will be a requirement for its sustainable future management, as biogeochemical cycles form an essential mechanism controlling chemical reactions and biological growth in this ecosystem. Gaps in knowledge, e.g. regarding the effects of climate change on the Wadden Sea, need to be recognized and addressed by future research plans. 103 acceptor in the cascade will occur when the pool of an electron acceptor with a higher energy yield is depleted. Nevertheless, microorganisms may create their niche by using substrates not consumed by the community living in the adjacent zone (van der Maarel and Hansen, 1997; Wilms et al., 2006). Furthermore, pore water exchange may blur the gradients by a continuous resupply of electron acceptors (Beck et al., 2008c; Jansen et al., 2009). Therefore, Fig. 1 does not exhibit the conventional redox sequence in mineralization pathways, but shows that in the highly dynamic intertidal sediments, the classical redox cascade may be disturbed by pore water flow, especially in the strongly irrigated top layer. Finally, processes of OM remineralization lead to the accumulation of dissolved organic carbon (DOC), alkalinity, and nutrients with increasing depth in pore waters (Fig. 1). 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 OM degradation. The depth where oxygen is still available for carbon (C) mineralization depends on sediment permeability. The high permeability of sand facilitates advective pore water transport, in contrast to diffusion-controlled muddy sediments. Furthermore, pore water flow is enhanced in surface sediments with ripple structures due to pressure gradients generated by the interaction of bottom currents with sediment topography (Huettel and Gust, 1992; Huettel et al., 2003). This pore water flow at the sediment surface is an effective mechanism for rapid exchange of oxygen (Precht et al., 2004; Ziebis et al., 1996). Consequently, Bioturbation, bioirrigation, and/or diffusive and advective processes introduce OM into surface sediments of the Wadden Sea (Meysman et al., 2005, 2007; Rusch et al., 2001; Volkenborn et al., 2007; see chapter 3) where it is degraded by a cascade of redox processes. Aerobic respiration is followed by nitrate reduction, reduction of manganese (Mn) and iron (Fe) oxides, sulfate reduction and finally methanogenesis (Froelich et al., 1979; Jørgensen, 2006). Theoretically, the sediments are divided into different zones, each characterized by a microbial community using a specific electron acceptor. In general, a shift to the next electron - Mn [µM] NO [µM] 3 0 0 3 6 9 12 0 8 16 SO Fe [µM] 24 32 0 4 8 12 16 0 8 24 [mM] 16 24 32 Depth [m] 1 2 3 4 5 0 0 1 2 3 + 4 0 12 24 36 3- NH4 [mM] Alkalinity [mM] DOC [mM] 48 0 3 6 9 PO4 [µM] 12 0 300 600 900 1200 Si(OH)4 [µM] 0 300 600 900 1200 Depth [m] 1 2 3 4 5 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 3 produced during OM remineralization. Dissolved organic carbon (DOC), alkalinity, NHþ 4 , 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). M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113 dsrA targets [g-1 sediment] Sulfate [mM] 0 10 20 30 1x106 2x106 0 1 Depth [m] oxygen is depleted within the uppermost millimeters in clay-rich sediments (Böttcher et al., 2000), whereas oxic conditions persist down to some centimeters depth in permeable sediments (Jansen et al., 2009). The oxygen penetration in permeable surface sediments leads to enhanced aerobic mineralization. Highest areal oxygen consumption rates (OCR) reaching up to 190 mmol m2 day1 were measured, for example, in tidal flat margin sediments flushed with seawater each tidal cycle (Billerbeck et al., 2006b; de Beer et al., 2005; Werner et al., 2006). To obtain these areal OCRs, the potential OCRs measured were integrated over the oxygen penetration depths. Aerobic mineralization rates were calculated by subtracting 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 m2 day1 (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., 1993). The importance of denitrification as well as of Mn/Fe oxide reduction for OM remineralization is not as well-constrained as the contribution of aerobic respiration. In general, it was estimated that denitrification accounts only for a small percentage to carbon 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., 1995). A whole ecosystem 15N labeling experiment in a tidal freshwater marsh fringing the nutrient-rich Scheldt River, Belgium, indicated that only 2.4 and 0.02% of the watershed derived 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 m2 h1, one of the highest rates determined in the marine environment so far (Gao 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 remineralization are minor, but gain importance in Mn- or Fe-rich sediment layers (Canfield et al., 1993; Thamdrup et al., 1994). In Wadden Sea sediments, a Fe(III)-reducing bacterial strain accounted for up to 6% of total cell numbers and even exceeded the numbers of sulfate-reducing bacteria in the upper sediment layers (Mussmann et al., 2005). Thus, these bacteria may substantially contribute to carbon degradation via dissimilatory reduction of Fe oxides in surface sediments of tidal flats. 2 3 4 0 50 150 100 Methane [nmol cm-3 ] 10 20 1x105 2x105 mcrA targets [g-1 sediment] dsrA targets [g-1 sediment] Sulfate [mM] 0 30 0 2x106 4x106 6x106 0 5 Depth [m ] 104 10 15 20 0 2x106 4x106 6x106 100 200 300 400 0 Methane [nmol g -1 ] mcrA targets [g-1 sediment] Fig. 2. Sulfate and CH4 show inverse depth profiles, with CH4 maxima in the sulfatedepleted zone. The key-genes for sulfate reduction and methanogenesis, the a-units of the dissimilatory sulfite reductase (dsrA) and the methyl coenzyme-M reductase (mcrA), respectively, correspond well with the vertical sulfateemethane profiles. The grey bars highlight the sulfateemethane interfaces. The figure was modified after Engelen and Cypionka (2009) and Beck et al. (2011). 2.2. Sulfate reduction and methanogenesis Sulfate reduction and methanogenesis are the main terminal pathways of anaerobic OM remineralization in sediments of the Wadden Sea, and have been intensively studied down to 5 m depth in the tidal flats of Spiekeroog Island. Sulfate-reducing bacteria form highly abundant and active populations in anoxic sediments (Gittel et al., 2008; Ishii et al., 2004; Llobet-Brossa et al., 2002). In general, sulfate and CH4 show inverse depth profiles, with a CH4 maximum in the sulfate-depleted zone (Fig. 2; Beck et al., 2009; Wilms et al., 2007). The population sizes of Bacteria, Archaea, sulfate reducers, and methanogens correspond well to the vertical sulfateemethane profiles (Fig. 2; Wilms et al., 2007). Although sulfate reducers and methanogens may compete for the same substrates, methanogens can avoid competition by utilizing noncompetitive substrates such as methylated compounds (Wilms et al., 2006). This may be one reason why methanogens are not restricted to the sulfate-depleted sediment layers. Within tidal flats, large spatial differences in sulfate depth profiles point towards changes in sulfate reduction rates. In central parts of tidal flats, seawater sulfate concentrations persist from the surface down to 5 m depth (Beck et al., 2008c, 2009). In contrast, in creek bank sediments, concentrations decrease strongly with depth and reach values close to zero within a few decimeters (Al-Raei et al., 2009; Beck et al., 2009; Riedel et al., 2011). In these sediments, microbial activity is enhanced by two processes supplying substrate and/or sulfate. First, rapid sedimentation leads to enhanced OM sequestration at prograding tidal flat margins (Beck et al., 2009; Oenema, 1990). Second, surface and deep pore water advection replenishes the dissolved organic matter and sulfate pools (Billerbeck et al., 2006b; Huettel et al., 2007; Huettel and Rusch, 2000; Riedel et al., 2010). The increase in microbial activity across creek bank sediments is not only reflected in sulfate, but also in CH4 profiles as well as in total cell numbers, sulfate reduction rates, and concentrations of remineralization products M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113 (Al-Raei et al., 2009; Beck et al., 2009; Røy et al., 2008; Werner et al., 2006). In contrast to creek bank sediments, low sedimentation rates and pore water flow velocities limit the microbial activity in central parts of the tidal flats despite the high availability of electron acceptors (such as sulfate) for microbial respiration. On average 78 g C m2 year1 are mineralized in surface sediments of the Wadden Sea via sulfate reduction (Al-Raei et al., 2009). This estimate is based on a modeling approach for the 154 km2 large tidal area of Spiekeroog Island using sulfate reduction rates of the top 15 cm sediments, a mapping of surface sediment distribution (mudflats, mussel banks, mixed flats dark, sand flat, and light sand flat), and empirical site-specific temperature relations of sulfate reduction rates. The importance of sulfate reduction for OM remineralization in these surface sediments is, however, constrained by the finding that sulfate reduction contributes only up to 25% to total OM mineralization (Billerbeck et al., 2006b; Werner et al., 2006). In North Sea sediments, the relative contribution of sulfate reduction to total OM remineralization is similar, but rates are a factor 5e10 lower than in Wadden Sea sediments (Upton et al., 1993). Overall, these data can be compared to estimates for pelagic and benthic primary production in the Wadden Sea. A total production between 30 and 950 g C m2 year1 was reported (Billerbeck et al., 2006a; Tillmann et al., 2000). 3. Benthicepelagic coupling Biogeochemical processes in the sediment are closely coupled to dynamics in the open water and vice versa. Especially in areas dominated by permeable sandy sediments, the exchange of dissolved and particulate compounds between both ecosystems is fast. Billerbeck et al. (2006b) proposed a concept consisting of two pore water circulation processes for permeable sediments, leading to a tight coupling of sediment and water column biogeochemistry. ‘Skin circulation’ forms an effective mechanism for rapid water exchange in surface sediments. It results from pressure gradients generated when bottom currents are deflected by small sediment structures of hydrodynamic or biological origin. This type of circulation exerts a major control on the exchange of dissolved and particulate organic matter across the sedimentewater interface (Ehrenhauss et al., 2004; Huettel and Rusch, 2000; Huettel et al., 1996; Rusch et al., 2001; Rusch and Huettel, 2000), microbial and benthos ecology (de Beer et al., 2005; Evrard et al., 2010; Middelburg et al., 2000), and sediment biogeochemistry (Evrard et al., 2008; Huettel et al., 1998). The close coupling of algal cell concentrations in the boundary layer and those in the uppermost sediment layer even suggest that permeable sediments may act as short-term storage buffer for phytoplankton (Huettel et al., 2007). In contrast, ‘body circulation’ affects pore waters located at greater depth (up to some meters) in creek bank sediments. It is generated by the hydraulic gradient between the seawater level in a tidal channel and the pore water level in the sediment. The hydraulic gradient starts to develop as soon as the tidal flat surface falls dry and is highest during low tide (Riedel et al., 2010; Wilson and Gardner, 2006). The induced deep pore water flow is directed towards the tidal channel, with highest flow velocities in sediments close to the low water line. This deep advective flow supplies permeable sediments with electron acceptors and donors and leads to the discharge of nutrient-rich pore waters into the water column (Beck et al., 2008c; Billerbeck et al., 2006b; Riedel et al., 2011). 3.1. Estimates of pore water flow velocities and discharge Knowledge about pore water flow velocities and the amount of pore water discharged from the sediments to the open water column is essential to budget biogeochemical cycles in the Wadden 105 Sea. Different approaches have been used to estimate exemplarily pore water flow rates in the Janssand tidal flat located in the backbarrier area of Spiekeroog Island. This tidal flat is covered by approximately 1.5e2 m of water during high tide and becomes exposed for about 6e8 h during low tide. It is almost plane, except at the margin where the sediment surface slopes with 1.6 cm m1 over ca. 80 m (Billerbeck et al., 2006a). Pore water flow estimates are still challenging, which is reflected by the different measured or modeled rates. One of the challenges is related to the extrapolation of point measurements to a larger area. The question whether the on-site lithology or topography is representative for the investigated tidal basin or the entire Wadden Sea has to be addressed. By studying eight sites in the West and East Frisian Wadden Sea, Røy et al. (2008) showed that topography and seepage zone of the well-studied Janssand tidal flat are representative on a regional scale. The first estimate for pore water flow velocity and discharge at the Janssand tidal flat was presented by Billerbeck et al. (2006a). The horizontal flux was measured by following the passage of a fluorescent dye through the sediment at depths from 2 to 50 cm, and ranged from 0.5 to 0.9 cm h1. Pore water discharge from the sloping margin was quantified during exposure by measuring the volume of water collected at the end of an open seepage meter. Measured rates of discharge were 2.4 (March) and 4.2 l m2 d1 (July). Finite element modeling was applied by Røy et al. (2008) to predict pathways and ages of pore water. The calculated flow pattern can explain the CH4 and sulfate distributions measured along a transect across the creek bank, and predicts a residence time of the seepage water of about 30 years. This corresponds to a calculated pore water flow ranging from 0.5 to 7 l m2 d1, depending on the permeability used in the model approach. In contrast to the estimate of Billerbeck et al. (2006a), which integrates the rapid shallow flow over the entire slope, Røy et al. (2008) considered only the CH4-rich pore water flowing deeper and slower. Riedel et al. (2010) applied a hydrogeological numerical simulation to investigate groundwater flow in sediment layers down to 5 m depth. Maximum simulated groundwater velocities of up to 7 cm h1 are reached during ebb tide, driving circulation of seawater through the sediment with subsequent discharge. Discharge averages 0.97 m3 per meter of margin length per tide, but may vary significantly, most pronounced with the spring-neap tide cycle. Pore water ages were calculated using the same hydrogeological simulation with some slight modifications (Riedel et al., 2011). For example, sulfate is almost completely depleted after 200 days when it reaches the discharge zone close to the low water line. In a fourth approach, radium isotopes were applied to quantify the flow of pore water entering the tidal channel during low tide. Using a flushing time of four days for the water mass within the backbarrier basin and average activities of 224Ra, 223Ra, and 228Ra measured in the backbarrier surface and pore waters, a balance of these isotopes was constructed, which is sustained by a pore water flow of 2e4 108 l per tidal cycle (Moore et al., 2011). Depending on the applied approach, the total volume of measured or modeled pore water discharge varies. The different estimates are subjected to errors resulting from the necessary approximations. Moore et al. (2011) tried to compare the different fluid flow estimates and concluded that the average flow rate estimated by Riedel et al. (2010) is 20e40 times larger than the flow presented by Billerbeck et al. (2006a), whereas it represents only about 20% of the radium-based fluid flow for the entire area. In contrast to Riedel et al. (2010), who evaluated deep pore water fluxes, Billerbeck et al. (2006a) only considered fluxes in the upper 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 Janssand margin, whereas the radium isotopes include pore water input from other tidal flats as well as groundwater input from terrestrial sources. 3.2. Nutrient and methane release from sediments Pore water flux estimates coupled to knowledge of pore water concentrations permit to calculate the release of species such as nutrients and methane from the sediment to the water column. Seepage measurements and pore water nutrient concentrations were used to estimate nutrient effluxes by Billerbeck et al. (2006a). For instance, they reached 7.6 mmol m2 d1 for NHþ 4, 2 1 d for Si(OH)4 in 2.5 mmol m2 d1 for PO34 , and 1.7 mmol m July. Furthermore, the nutrient input by pore water seepage was estimated based on radium isotope measurements. In the entire Spiekeroog tidal flat area, about 2e23 104 mol Si(OH)4 are released from the sediments each tidal cycle (Moore et al., 2011). The release of CH4 from sediments can be reduced by its aerobic and anaerobic oxidation (Krüger et al., 2005; Treude et al., 2005). For example, CH4 diffusing upwards into the sulfate zone is oxidized to CO2 at the expense of sulfate, which amounts to a sulfate loss equivalent to about 10% of the total sulfate reduction in coastal sediments (Jørgensen et al., 2001). In the Wadden Sea area, profiles of the key genes for dissimilatory sulfate reduction and methanogenesis suggest anaerobic oxidation of methane (AOM) at sulfateemethane transition zones (Wilms et al., 2007). First measurements of ex-situ AOM rates show that rates peak in the sulfateemethane transition zones (Beck et al., 2011). At tidal flat margins, pore water exchange occurs on short timescales, supporting the coexistence of sulfate and CH4. Furthermore, the seeps on the slope of the Janssand tidal flat are sulfidic, depleted in sulfate, and saturated with CH4 (Røy et al., 2008). Thus, an oxic surface layer where re-oxidation may prevent the emission of CH4 is partly missing. Røy et al. (2008) tried to assess the importance of CH4 seepage for the carbon cycle in tidal flats. Assuming a pore water flow rate of 0.5 l m2 d1 and CH4 saturation in pore waters, they calculated that 0.65 mmol CH4 are transported to the open water column per square meter per day. They estimated that on the Janssand tidal flat, the anoxic seeps comprise 2% of the surface area, and only leak about 0.013 mmol C m2 d1 averaged over the entire sand flat. The authors conclude that this is at least three orders of magnitude lower than the rates of primary production and mineralization in the Wadden Sea, and thus CH4 seepage is of limited importance for the carbon cycle in tidal flats. Similarly, Middelburg et al. (2002) identified tidal flats and creeks as CH4 sources to estuarine waters, but concluded that estuaries contribute less than 9% to the global marine CH4 emission. 4. Biogeochemical cycles in Wadden Sea waters The release of nutrient-rich pore waters to the overlying water column is an important mechanism triggering biological processes in Wadden Sea waters. Pulses of elevated nutrient concentrations are frequently observed in the water column during low tide (Grunwald et al., 2010), when the discharge of nutrient-rich pore waters from creek bank sediments is highest (Riedel et al., 2010) (Fig. 3). The tight benthicepelagic coupling further prevents extended periods of nutrient depletion that could limit phytoplankton growth. Only shortly after the spring phytoplankton bloom, silicate and phosphate concentrations are close to zero (Fig. 4), but the nutrient pools are quickly replenished by pore water supply (Billerbeck et al., 2006b; Grunwald et al., 2010; Kowalski et al., 2009). In contrast to phosphate, the effect of resupply is less pronounced in seasonal silicate dynamics due to assimilation by diatoms even outside the bloom periods. Only nutrients like nitrate and nitrite, which are not enriched but consumed in pore waters, show a long-lasting depletion in the water column from early spring until autumn (Fig. 4). Similar to nutrients, CH4 exhibits a tidally driven pattern in the water column with highest concentrations during low tide (Grunwald et al., 2009) (Fig. 3). The elevated CH4 levels during low tide may have two major sources: pore water discharge from sediments, and/or freshwater released to the tidal flat area via flood-gates. Pore waters seeping from creek bank sediments during low tide are rich in CH4 (Al-Raei et al., 2009; Røy et al., 2008). These CH4-rich pore waters are the main source transporting CH4 to the 30 20 PO43- [µM] Si(OH)4 [µM] 1.6 10 1.2 0.8 0.4 0 16/Nov 17/Nov 18/Nov 0 11/Jun 19/Nov 12/Jun 13/Jun 14/Jun 21/Nov 22/Nov 23/Nov CH4 [nM] NOx [µM] 22 18 14 300 200 10 18/Nov 19/Nov 20/Nov 21/Nov 100 20/Nov 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 3 Fig. 4. Seasonal variation of the nutrients Si(OH)4, NO in the years x , and PO4 2006e2010 determined in surface Wadden Sea waters at a time series station (Grunwald et al., 2007) close to Spiekeroog Island (East Frisian Wadden Sea). Running average concentrations are displayed. All nutrients strongly decrease during the spring phytoplankton bloom. Nutrients like Si(OH)4 and PO3 4 , which are re-supplied by pore water discharge, do hardly reach concentrations close to zero, whereas NO x exhibits very low concentrations from spring until autumn. PO43 is especially introduced into the water column from surface sediments in summer when anoxic conditions in the uppermost layer lead to reduction of Fe oxides and release of adsorbed PO3 4 . open water column. In contrast, the freshwater contribution to the CH4 budget of the back barrier water column is comparably small. Although the watercourses draining the hinterland may exhibit CH4 concentrations up to 8 mM, which is more than one order of magnitude higher than in Wadden Sea waters, the contribution was estimated to be less than 10% (Grunwald et al., 2009). This phenomenon is explained by the generally low freshwater discharge into the backbarrier area, and the high CH4 concentrations in pore waters. Also, salt marshes may form a CH4 source to the Wadden Sea, but few studies have focused on this topic so far (see 6.3.3). In the water column, CH4 concentrations may diminish due to degassing and oxidation. In the Wadden Sea area, degassing of CH4 probably occurs when waters pass a shoal located off the islands along an extension of the tidal inlets (Grunwald et al., 2009). In general, this zone is characterized by enhanced wave activity and turbulence. Methane oxidation is assumed to be of minor importance in Wadden Sea waters due to the short residence time within the backbarrier area (Grunwald et al., 2009). 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 adjacent 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 inorganic Si(OH)4 (128 106 mol a1), PO34 (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 magnitude 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 model approach was used (Grunwald et al., 2009). The model shows that 3.3 106 mol CH4 are exported per year from the tidal basin of Spiekeroog Island to the southern North Sea (Grunwald et al., 2009). Assuming that the study area is representative for the entire East Frisian Wadden Sea, a CH4 export to the North Sea of 7.8 106 mol CH4 per year was calculated, intermediate between 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. To balance the export of species such as dissolved inorganic nutrients and CH4 from the tidal basins, it was hypothesized that OM is imported from the North Sea to the tidal flat system (van Beusekom and de Jonge, 2002). The proposed conceptual model was based on three assumptions: (1) nitrogen limits the primary production in the coastal zone, (2) a proportional part of the primary produced OM is transported into the Wadden Sea and (3) the imported organic matter is remineralized within the Wadden Sea and supports the local productivity by nitrogen turnover. To date, studies further verifying this conceptual model are still missing. However, several studies indicate that nutrients, CH4, dissolved inorganic carbon and metals are exported from the tidal flat area to the adjacent North Sea (Grunwald et al., 2009, 2010; Moore et al., 2011). Further, they present first evidences that the export cannot be balanced by the freshwater discharge to the tidal basins. Therefore, estuaries and North Sea might be of importance to balance the budgets as well. 108 M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113 6. Open questions and future challenges 6.1. Extrapolation of results to the entire Wadden Sea The geographies of the West and East Frisian Wadden Sea are quite similar, whereas North Frisia differs by the lack of closelyspaced barrier islands, and by exhibiting wider tidal inlets. These differences may influence the import/export of OM and metabolic products between the Wadden Sea and the adjacent North Sea as well as biogeochemical processes within the Wadden Sea area. Up to date, few investigations have studied identical processes at the same time in several tidal basins (Kraft et al., 2011), although such studies are essential to differentiate between processes common to the entire Wadden Sea, and dynamics induced by specific local conditions. For example, Kowalski et al. (2011) compared seasonal and tidal dynamics of the trace metal Mn in the East and North Frisian Wadden Seas (Spiekeroog and Sylt-Rømø). The authors observed similarities in seasonal Mn pattern, but significant quantitative differences. Apparently, site-specific properties of the different tidal basins have to be considered when establishing budget calculations for the entire Wadden Sea. Benthic remineralization rates measured in the Spiekeroog and Sylt-Rømø tidal basins show a less converse behavior, e.g., sulfate reduction contributes <20% to total C remineralization in both areas (Billerbeck et al., 2006b; Werner et al., 2006). However, smallscale variations may be large, especially at tidal flat margins (AlRaei et al., 2009; Beck et al., 2009; Billerbeck et al., 2006b; Werner et al., 2006). Therefore, a detailed understanding of sedimentological and hydrodynamic conditions is required before results can be extrapolated to larger areas and finally to different tidal basins. compared to marine settings, and reduction of Fe oxides turns out to be an important electron accepting process for OM remineralization (Jakobsen and Postma, 1999; Larsen et al., 2006). To our knowledge, too few studies have been conducted so far to estimate whether the discharge of groundwater from coastal aquifers into the adjacent Wadden Sea environment is of importance for biogeochemical processes. The influence of large-scale geological structures as well as small-scale sedimentary heterogeneities on groundwater flow, discharge and chemistry complicates an extrapolation of available data sets to larger areas. In the tidal flat area of Spiekeroog Island, two 20 m long sediment cores were retrieved to extend the knowledge on biogeochemistry, microbial abundance, and activity of sulfate reducers/ methanogens beyond the intensively studied 5 m depth interval. One core were drilled through mainly Holocene sediments deposited in a paleo-channel. This core exhibits inverse sulfate and CH4 depth profiles similar to the results described above, however, the maximum CH4 concentrations are found at greater depths (Fig. 2; Beck et al., 2011). The highest CH4 concentrations are located in clay-rich, diffusion-dominated layers. Whether the CH4 trapped in these layers is transported vertically or horizontally, or even released to the atmosphere or the open water column is still unknown. 6.2.1. Subtidal areas Most studies elucidating biogeochemical dynamics in Wadden Sea sediments have focused on eulitoral areas. In contrast, little is known about biogeochemical processes in subtidal sediments, and their importance for OM and nutrient cycles. Böer et al. (2009a,b) studied microbial activities and carbon turnover in subtidal sandy Wadden Sea sediments (Sylt-Rømø Basin, North Frisian Wadden Sea, 0.5e2.5 m water depth). Similar to eulitoral sandy sediments, the rapid input of OM results in a very active bacterial community with a biomass turnover of 2e18 days. Advective pore water transport increases benthic exchange, for example of O2 (Cook et al., 2007). Still, the deposits of the up to 15 m deep channels controlling the water exchange between Wadden Sea and North Sea remain a black box. 6.2.3. Sandy beaches In the Wadden Sea area, most sandy beach ecosystems are located on the North Sea-facing sides of the islands. Additional beach sites are found on the western and eastern tips of the West and East Frisian islands. Therefore, we hypothesize that processes operating in beach ecosystems are not only coupled to the biogeochemistry of coastal North Sea waters, but may influence biogeochemical dynamics in the Wadden Sea as well. In contrast to intertidal or estuarine locations, few studies have focused on these systems, but the awareness is increasing that the impact of beach ecosystems on biogeochemical cycles in coastal oceans is not well constrained, and its importance may be underestimated (Dugan et al., 2010). Beach sediments have been described as “geochemical and microbial deserts” (Boudrau et al., 2001) due to their generally low levels of OM and other reactive substances. This is based on the conception that the biogeochemical importance of sedimentary environments is proportional to their own stocks of OM and reactants. However, recent studies have shown that beach sediments may be regarded as biogeochemical reactors promoting or accelerating OM remineralization (Anschutz et al., 2009). Permeable beach sands permit enhanced seawater infiltration by high wave energy (Robinson et al., 2007), thereby supplying OM and electron acceptors. First studies conducted in beach sands of the western tip of Spiekeroog Island (East Frisian Wadden Sea) show that down to 1.5 m depth, the predominant electron acceptors for OM remineralization are molecular oxygen, nitrate, and Fe/Mn oxides (Schwichtenberg, 2010; Ungermann, 2009). In contrast to intertidal sediments, sulfate is less important for microbial respiration and OM degradation. This implies that OM oxidation in beach sands may lead to the release of nutrient-rich pore waters, but the discharge of CH4-rich waters is rather unlikely, or may only occur below the 1.5 m depth range so far studied. 6.2.2. Coastal aquifers A few studies focused on biogeochemical processes in coastal aquifers hydrologically connected to the Wadden Sea (Andersen et al., 2007; Hansen et al., 2001; Jakobsen and Postma, 1999; Larsen et al., 2006). For instance, rates of sulfate reduction are much lower in a shallow sandy aquifer of Rømø (Denmark) 6.2.4. Salt marshes The importance of salt marshes with respect to their multiple ecological values has been known for a long time. It remains uncertain, however, whether the response of salt marshes to the shifting climate will moderate or exacerbate warming, for example by carbon sequestration or CH4 release (Bromberg Gedan et al., 6.2. Understudied Wadden Sea ecosystems Water column and eulitoral tidal flat sediments are the beststudied compartments of the Wadden Sea. Numerous studies have identified microbial and biogeochemical processes and their seasonal/tidal dynamics in both compartments. In contrast, other Wadden Sea ecosystems have not been subject to extensive research, e.g., subtidal areas, coastal aquifers, sandy beaches, and salt marshes. A better understanding of these ecosystems is essential to unravel OM, nutrient, and CH4 cycling in the Wadden Sea as a whole. M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113 2009). In general, the fresh water- dominated part of the salt marsh system is know to be a relatively large source of CH4 (Chmura et al., 2003). In contrast, the salt water part of the system releases much less CH4 due to the presence of sulfate and AOM (Bridgham et al., 2006). Therefore, Choi and Wang (2004) postulated that due to higher rates of carbon sequestration and lower CH4 emissions, coastal wetlands could be a more valuable carbon sink than other ecosystem in a warmer world with a rising sea level. The Wadden Sea salt marsh system comprises a fresh and a salt water part separated by a transition zone. Biogeochemical studies in the salt marshes of Langeoog Island (East Frisian Wadden Sea) indicate that salt marsh sediments form an important iron source for pore waters due to the presence of a high percentage of reactive sedimentary iron (Kolditz et al., 2009). Only few indications of sulfate reduction were found within this environment. The study further shows the effects of flooding during a storm surge on biogeochemical reactions, which may provide information on possible effects of a rising sea level. Flooding will lead to a shortþ term increase in pore water iron, manganese, PO3 4 , and NH4 concentrations. Nevertheless, it is largely unknown how the Wadden Sea salt marsh system will react to rising seawater levels. A possible consequence might be the introduction of more sulfate into the pore water system that could act as an electron acceptor for OM oxidation. As a result, carbon would be converted into CO2 instead of CH4, which in terms of radiative forcing contributes less to climatic change. Sea level rise may therefore have a negative feedback on the concentration of atmospheric greenhouse gases through the suppression of microbial methanogenesis in salt marsh systems. 6.3. Impact of climate change on biogeochemical cycles Climate change may induce numerous environmental shifts (Pernetta and Elder, 1992), which will probably influence biogeochemical processes. However, we can only describe some future scenarios because few studies have focused on this topic so far. Certain aspects of climate change have already been addressed in recent publications focusing on the Wadden Sea and North Sea, whereas others should be incorporated in future research plans. Although climate change is a gradual process and difficult to study in short-term research projects, scenarios for future changes may be established based on the intensive studies conducted in the Wadden Sea area, and on long-term time series such as Helgoland Roads (Franke et al., 2004; Wiltshire et al., 2008; Wiltshire and Manly, 2004) and Spiekeroog tidal inlet (Grunwald et al., 2010, 2007; Reuter et al., 2009). Furthermore, mild winters or storm surges may serve as ‘proxy conditions’ for global warming and sea level rise, respectively. 6.3.1. Does vertical sediment growth keep pace with sea level rise? How may this influence the biogeochemical cycles in the sediments? The compilation of data from several stations along the Dutch and German coast for the past 150 years indicates a mean sea level rise of 3.6 mm year1 from 1971 to 2008, with higher rates in the eastern part of the German Bight compared to the southern part (Wahl et al., 2011). The threshold up to which sea level rise can be compensated by sedimentation is still under debate, but it is postulated to be lower for large tidal basins than for small ones (Van Goor et al., 2003). The interaction between the rate of relative sea level rise and the rate of sediment supply (from external sources or the existing reservoir) defines the stratigraphic response of the system. Three main types of stratigraphic responses have been proposed: progradational, aggradational and transgressive (Flemming, 2002). 109 If recent sedimentation rates are higher than local sea-level rise evidencing vertical sediment growth, the biogeochemical reactor in Wadden Sea sediments may remain unaffected by climate change. However, if sedimentation cannot balance sea level rise, extended inundation durations would lead to a decrease in pore water discharge from creek bank sediments (Riedel et al., 2010). On the one hand, this may reduce the amount of seawater cycling through the sediment leading to less OM and electron acceptor resupply. On the other hand, less nutrients would be released to the open water column, thereby probably leading to a decrease in primary productivity. 6.3.2. May changes in storm surge frequency/extremes influence biogeochemical cycles? In the Netherlands, an analysis of the number of storms with a magnitude of >7 Bft does not show an increasing trend during the last decades (Oost et al., 2009). In contrast, the yearly highest water levels increased up to 8 mm per year since 1868 in the Northern Wadden Sea (Hofstede, 2007). Apart from artificial causes like dam building, this may be the result of a shift in storm wind directions. Furthermore, storm surge extremes may increase along the North Sea coast towards the end of this century (Woth et al., 2006). A first estimate of the impact of storm surges on nutrient budgets in the Spiekeroog tidal flat area shows that losses in inorganic Si(OH)4 and PO3 4 inventory during storm events account for 3% and 10%, respectively, of the annual export of both species to the North Sea (T. Riedel, unpublished). Autumn and winter storms may therefore be important for exporting nutrients to offshore waters. Consequently, an increase in storm surge frequency or extremes may alter biogeochemical cycles in the Wadden Sea and in coastal waters of the North Sea. 6.3.3. May global warming influence OM remineralization pathways? In the Wadden Sea area, seawater temperature depends on the main wind direction and on global climate development. Longterm observations of the sea surface temperature from the Western Wadden Sea (Marsdiep Inlet) indicate increasing temperatures since 1980 leading to a warming of up to 1.5 C (van Aken, 2008). The Helgoland Roads time series shows a warming trend of 1.1 C since 1962 (Wiltshire and Manly, 2004). Pore water temperatures show highest seasonal variations in surface layers tightly coupled to changes in sea surface temperature (Reuter et al., 2009), but exhibit changes down to 2e3 m depth in permeable sediments (Beck et al., 2008c). Only 5 m below the sediment surface, temperatures remain rather constant throughout the year. Several studies highlight the temperature dependence of OM remineralization steps in Wadden Sea sediments (Al-Raei et al., 2009; Billerbeck et al., 2006b; Jansen et al., 2009; Kristensen et al., 2000; Werner et al., 2006). For instance, depth-integrated sulfate reduction rates of the top 15 cm increase by a factor of about 10 from winter to summer (Al-Raei et al., 2009; Arnosti et al., 1998; Kristensen et al., 2000). Although temperature controls biogeochemical processes, other seasonal factors such as OM availability simultaneously account for increased microbial rates in summer. Overall, global warming may lead to a decrease in oxygen solubility and an increase in sulfate reduction rates, both resulting in lower redox conditions in the sediments. To date, it is still under debate whether this development may have positive or negative effects on biogeochemical cycles and CH4 emissions. One may speculate whether faster OM turnover may lead to less OM availability in sediment layers where methanogenesis occurs thereby 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 biogeochemical cycles? Phytoplankton plays a dominant role in carbon and nutrient cycles of coastal areas by producing the major part of OM. The extent of OM reaching the sea floor and being remineralized in sediments depends on the water depth. In areas with shallow water depth like the Wadden Sea about 50% of the total respiration takes place in the sediment (van Beusekom et al., 1999), whereas the percentage of benthic remineralization is lower in deeper parts of the North Sea (Upton et al., 1993). Some studies addressed how climate change may influence the coupling between the amount of OM produced in the water column and the amount that reaches bottom sediments. It is suggested that the impact of climate change on local biogeochemistry largely depend on the extent of phytoplanktonezooplankton interactions, which are influenced by large-scale atmospheric and oceanographic changes (van Beusekom and Diel-Christiansen, 2009; Wiltshire and Manly, 2004). The interaction between both factors determines how much of the primary production reaches the benthic system. Additional factors possibly influencing future phytoplankton dynamics are global warming, nutrient inventory, alien species, and increased river discharge and turbidity, both induced by an higher precipitation (Philippart and Epping, 2009). 7. Comparison with other temperate tidal flat systems In our contribution, we so far focused on biogeochemical cycles in the Wadden Sea. Here we would like to put the described regional environmental dynamics into a broader, more global context. The Wadden Sea represents an outstanding example of a temperate-climate sandy barrier island coast. It differs from all other comparable tidal flat and barrier island depositional systems by its spatial scale and its diversity (Marencic, 2009). However, similar depositional environments are found all around the world in the temperate zone. Examples of tidal flats are found along the Korean coast, the Atlantic coasts of North Africa and North America, and the British channel and North Sea coast. Typically, these environments exhibit high primary production and organic matter remineralization rates. Processes in the water column and the underlying sediments are tightly coupled due to bidirectional exchange of nutrients and organic material. For example, tidal flat systems along the Korean coast exhibit recirculation patterns of seawater into and out of the sediments similar to the Wadden Sea. Nutrients released by submarine groundwater discharge stimulate primary production at the seafloor and in the water column (e.g., Waska and Kim, 2010, 2011). However, the input of terrestrial material is of much greater importance than in the Wadden Sea, as the transport of nutrients to the coastal zone is strongly enhanced during the monsoon season by the huge amounts of rain- and groundwater flushed through the sediments (Waska and Kim, 2011). Furthermore, tidal water level fluctuations reach up to 10 m, compared to a maximum of about 3 m along the southern North Sea coast. Both monsoon and tidal processes may better facilitate pore water recirculation in the Korean tidal flat area compared to the Wadden Sea, however nutrient concentration in seeping pore waters are partly several orders of magnitude lower in the Korean system (e.g., Kim et al., 2005; Moore et al., 2011; Riedel et al., 2011; Waska and Kim, 2011). A system that has been studied in as much detail as the Spiekeroog tidal flat area is Waquoit Bay, located on the southern shoreline of Cape Cod at the East coast of the United States. The bay has served as field site for various oceanographic, hydrological, geological, biological and geochemical studies (e.g., Charette and Sholkovitz, 2002, 2006; Dulaiova et al., 2008; Rouxel et al., 2008; Spiteri et al., 2008; Valiela et al., 1992). In contrast to most sites in the Wadden Sea, Waquoit Bay is a shallow estuary with an average depth of 1 m and a tidal range of about 1 m. Similarly to the Janssand tidal flat, described in our manuscript as a typical permeable sand flat of the Wadden Sea, the coarse-grained sediments/soils in Waquoit Bay permit submarine groundwater discharge (Mulligan and Charette, 2006). In the Wadden Sea, discharge is mainly driven by tides, while in Waquoit Bay saline circulation due to tides and waves is confined to a shallow intertidal zone. Instead, seasonal changes in water table elevation may explain the observed large groundwater discharges (Michael et al., 2005). The saline circulation through the coastal sediments was estimated as 0.56 m3 m1 d1 (Mulligan and Charette, 2006), which is in the same order of magnitude as the respective estimate for the Wadden Sea (considering the relatively large uncertainties induced by different methodologies; Riedel et al., 2010). In the seepage zone, NHþ 4 concentrations are about two orders of magnitude higher on the Janssand tidal flat compared to Waquoit Bay indicating that there discharging pore waters may exert a higher impact on water-column biogeochemistry (Kroeger and Charette, 2008; Riedel et al., 2011). As a conclusion, we can state that despite the global occurrence of temperate tidal flat systems comparable to the Wadden Sea, these environments are strongly influenced by regional climate conditions, tidal amplitudes, coastal currents, local aquifers, weathering in the hinterland, and other environmental factors. It will therefore require additional collaborative research efforts to estimate the influence these tidal flat systems exert on biogeochemical processes and element cycles on a global scale. 8. Summary Wadden Sea sediments function as a coastal filter system. OM captured in this filter is degraded, and recycled nutrients are released. Due to active biota and advective pore water flow, the filter never clogs but is continuously renewed, sustaining the potential for enhanced OM remineralization in this depositional environment. Recirculation of seawater into and out of the sediments leads to a tight coupling between benthic and pelagic dynamics, a prerequisite for continuously high primary production. Numerous studies have already focused on biogeochemical dynamics in the Wadden Sea area. Nevertheless, various processes and ecosystem compartments still need to be studied in more detail to better estimate their contribution to the carbon, nutrient, trace metal and trace gas cycles in the Wadden Sea. Only few studies have addressed the coupling of processes occurring in the Wadden Sea water or sediment column to other adjacent environmental compartments, such as the open North Sea water column or the atmosphere. This knowledge could, for example, help to determine to which extent the Wadden Sea influences biogeochemical cycles in the adjacent North Sea. An understanding of naturally occurring processes, i.e., the environmental baseline, is also necessary to predict whether climate change or other anthropogenic interventions (e.g., dike building, channel dredging) may have negative effects on the ecosystem. Although the Wadden Sea area has been under human influence since the Middle Ages, the rapid changes induced by an increased land use and industrialization may be a particular challenge for a more sustainable management of this ecosystem. All processes described in this contribution may be of importance in temperate tidal flat systems worldwide. However, regional influences like climate conditions, tidal amplitudes or local aquifers have to be taken into account when comparing different systems. M. Beck, H.-J. Brumsack / Ocean & Coastal Management 68 (2012) 102e113 Acknowledgements The authors would like to thank all colleagues involved in the research group “BioGeoChemistry of Tidal Flats” for excellent cooperation and numerous interesting discussions during eight years of Wadden Sea research. Furthermore, we thank the guesteditor Maria A. van Leeuwe, two anonymous reviewers, and Christian März for their comments, which greatly improved the manuscript. 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