Functioning of intertidal flats inferred from temporal and spatial dynamics of O2, H2S and pH in their surface sediment
- 1.7k Downloads
In this article, we describe the dynamics of pH, O2 and H2S in the top 5–10 cm of an intertidal flat consisting of permeable sand. These dynamics were measured at the low water line and higher up the flat and during several seasons. Together with pore water nutrient data, the dynamics confirm that two types of transport act as driving forces for the cycling of elements (Billerbeck et al. 2006b): Fast surface dynamics of pore water chemistry occur only during inundation. Thus, they must be driven by hydraulics (tidal and wave action) and are highly dependent on weather conditions. This was demonstrated clearly by quick variation in oxygen penetration depth: Seeps are active at low tide only, indicating that the pore water flow in them is driven by a pressure head developing at low tide. The seeps are fed by slow transport of pore water over long distances in the deeper sediment. In the seeps, high concentrations of degradation products such as nutrients and sulphide were found, showing them to be the outlets of deep-seated degradation processes. The degradation products appear toxic for bioturbating/bioirrigating organisms, as a consequence of which, these were absent in the wider seep areas. These two mechanisms driving advection determine oxygen dynamics in these flats, whereas bioirrigation plays a minor role. The deep circulation causes a characteristic distribution of strongly reduced pore water near the low water line and rather more oxidised sediments in the centre of the flats. The two combined transport phenomena determine the fluxes of solutes and gases from the sediment to the surface water and in this way create specific niches for various types of microorganisms.
KeywordsIntertidal flats Surface sediment Permeable sand Oxygen Sulphide Photosynthesis
Intertidal sediments are important sites of organic matter cycling because large surface areas are combined with high microbial activity, both with respect to biomass production and degradation. It is increasingly recognised that sandy sediments can have a high degradation activity in spite of their low organic matter content and bacterial numbers (e.g. De Beer et al. 2005; D’Andrea et al. 2002). They have a higher permeability than more fine-grained sediments, which facilitates advective pore water transport and thereby promotes a high transport of electron donors and acceptors into and out of the sediments. This can lead to areal reaction rates comparable to essentially diffusion-controlled muddy sediments (e.g. Huettel et al. 1998; Böttcher et al. 2000; Rasheed et al. 2003; Werner et al. 2006).
There are several driving forces for advective pore water transport in these sediments. The currents and waves cause hydrostatic pressures which drive pore water movements through the sediments (Precht et al. 2004). Particularly important is the Bernoulli effect created by currents over ripples which causes water inflow in the ripples troughs and outflow at the crests of the ripples (Huettel et al. 1998; Thibodeaux and Boyle 1987). As the inflow into the sediments must be compensated by an outflow elsewhere, a mosaic of surficial circulation cells develops which influence the pore water chemistry in the top 3–10 cm. Secondly, bioturbation and bioirrigation can also cause efficient mixing of the top layers (e.g. Meysman et al. 2005, 2006; Aller 2001; Wethey et al. 2008). Faunal and pressure-driven transport normally takes place over small spatial and temporal scales in the order of centimetres and minutes. For example, due to this effect, the pore water oxygen concentrations in the top 10 cm can increase from 0 to air-saturated values within minutes (De Beer et al. 2005; Werner et al. 2006). The maximum depth at which ‘surficial’ advective pore water transport takes place varies considerably. Thus, although most of it takes place in the top 10 cm, bioirrigation can also take place at depths up to 30–40 cm.
Besides these small-scale transport mechanisms (skin circulation), the existence of transport processes at much larger temporal and spatial scales was demonstrated for intertidal flats (body circulation; Billerbeck et al. 2006b). This type of transport is driven by a pressure gradient between the pore water level and the low water level during exposure of the flat. The body circulation is characterised by long flow paths (tens of metres) and long residence times (decades) of the pore water (Billerbeck et al. 2006b; Røy et al. 2008). This transport phenomenon drives a pore water flow from the centre of the flat towards the low water line at depths of several metres below the sediment surface.
The two types of transport differ in scale: As stated before, surficial dynamics can range in depth from centimetres to decimetres, whereas horizontal transfers extend for decimetres, and body circulation probably occurs up to 5-m depth over distances exceeding 100 m (Røy et al. 2008). However, the key difference lies in the mechanisms driving the two transport processes.
A wide range of microbial processes occur in intertidal sediments, from primary production to the whole sequence of organic matter mineralisation with various electron acceptors (oxygen, sulphate, nitrate, iron, etc.) and methanogenesis. Most probably, the primary production, aerobic mineralisation and sulphate reduction are the processes dominating the carbon cycle (Billerbeck et al. 2006a, 2007; Werner et al. 2006), whereas methanogenesis and denitrification maybe important for release of greenhouse gasses (CH4, N2O), but not for element cycling (Røy et al. 2008). Between the islands of Ameland and Spiekeroog, approximately 20 km of potentially seeping low water lines can be mapped out, which could release 130–1,300 mol methane per day. This corresponds to an annual methane release of approximately 0.05–0.5 mmol m−2, a very low value compared to, for example, an estimated yearly primary production of 25 mmol C m−2 and a mineralisation rate of 33 mmol C m−2 in the North Frisian Wadden Sea (Asmus et al. 1998; Van Beusekom et al. 1999). This rough calculation suggests that methane seepage is of limited importance for the carbon cycle in intertidal flats. However, it is probably very significant for the coastal methane budget. The flux of methane from estuarine waters to the atmosphere of 0.13 mmol m−2 day−1 (Middelburg et al. 2002) can be explained by seepage from flats in areas with 1 m of seeping waterline per 50–500 m2 of water surface.
The distribution of the degradation processes is determined by the availability of electron acceptors and donors, whereas photosynthesis is controlled by light and nutrients. Consequently, the main biogeochemical processes are controlled by transport processes. Skin circulation enhances organic matter mineralisation by efficient filtration of fresh organic matter and various electron acceptors into the permeable sediment. Body circulation can cause seepage of highly concentrated reduced compounds that are normally found in deeper sediment layers (Røy et al. 2008), and this can drive the release of considerable amounts of methane (Middelburg et al. 2002), as was shown to occur at many sites throughout the German and Dutch Wadden Sea (Røy et al. 2008). Of course, the efficient mineralisation of organic matter and transport of degradation products will facilitate benthic photosynthesis by a fresh supply of nutrients.
The transport and biogeochemical processes strongly influence both the biological conversions occurring at the surface (such as photosynthesis and sulphide oxidation) and the fluxes of solutes and gases. As the skin circulation efficiently drives infiltration and mineralisation of dissolved organic carbon (DOC) and particulate organic carbon (POC), it promotes high primary productivity. The deep circulation and anaerobic degradation processes produce a sulphate-depleted and methane-enriched plume under the tidal flat surface (Beck et al. 2008), and (the development of) sulfidic and nutrient-rich seeps at the low water line (Billerbeck et al. 2006b; Al-Raei et al. 2009). How the organic material is transported from the sediment surface to a depth of several metres in the tidal flat needs further investigation.
This paper describes the dynamics of some key chemical parameters (mainly oxygen, sulphide and pH) in the surface sediments of a sloping intertidal flat with a maximum height of 1.5 m above the water level at low tide with the aim of giving insights into the importance of local and short timescale processes such as tides and hydrodynamic-pressure-driven transport. To obtain pore water data in a minimally invasive way, autonomous profilers mounted with microsensors were used. These time-resolved fine-scaled results are combined with nutrient analyses from pore waters that were extracted from selected sediment cores.
2 Materials and methods
2.1 Site description
2.2 Sampling strategy
A general difficulty for measurements in permeable sediments is that the pore water composition is influenced by transport, and transport is influenced by the variable hydraulic regime. The hydrodynamics at the sediment–water interface are thus easily disturbed by the observation technique. Obviously, retrieval of sediments and chemical analysis of extracted pore water will not give any information about in situ dynamics. Benthic chambers seal off the sediment surface under investigation and replace the natural flow regime by an artificial one that depends on the rotation speed of the stirrer. In the present study, pore water data for selected dissolved species were measured in situ using autonomous profilers mounted with microsensors, a method which is only minimally invasive and leaves the sediment surface exposed to winds, currents, waves and tides during the measurements. This setup allows for continuous profiling over whole tidal cycles and the evaluation of the corresponding pore water and element flux changes at the sediment–water interface. The time-resolved fine-scaled lander results are combined with nutrient analyses from pore waters that were extracted from selected sediment cores.
Measurements were performed at the upper flat, along the slope and at the low water line. The site was visited repeatedly between 2002 and 2006.
2.3 In situ microsensor measurements
In situ measurements of oxygen penetration depth were performed by microsensors mounted on an autonomous profiler as described in Glud et al. (1999) and Wenzhöfer et al. (2000; Fig. 2b). Clark-type oxygen microelectrodes and amperometric H2S microsensors were made and calibrated as described previously (Revsbech 1989; Jeroschewski 1996). Instead of using normal 5- to 10-μm tips, the sensors were prepared with an approximately 300-μm (200–500 μm) tip diameter to prevent breakage in the relatively firm sediment. Nevertheless, the actual sensing diameter was 2 μm with less than 5-s response time (t 90). Electrodes used for pH measurements were liquid ion-exchange membrane microelectrodes (De Beer 2000) with a 200-μm tip size and an agar reference and a commercial glass electrode (3-mm tip diameter, InLab 423, Mettler Toledo, Switzerland). For temperature measurements, a Pt100 electrode (Umweltsensortechnik, Germany) was used. The position of the sediment surface was monitored with a resistivity microelectrode as described by Glud et al. (2009). To correct for uneven surface topographies, the results of the resistivity measurements were compared to analogous indications inferred from the signals of the other sensors.
The profiler was placed on the flat during low tide with the microsensors initially positioned 1 to 2 cm above the sediment surface (Fig. 2b). Profiles were measured over at least one tidal cycle to a sediment depth of 6 cm at 1-mm intervals. Repeated profiles were measured every 20 to 60 min. The sensors sometimes produced persistent holes in the sediment during low tide; such profiles were discarded from the data set.
2.4 Photopigment analysis
Photopigments in the sediment were collected and analysed as described by Billerbeck et al. (2007). The top 12 cm of the sediment was sectioned at 1-cm intervals down to 2-cm depth and at 2-cm intervals below. The sediment samples were kept frozen and in darkness until analysis. Pigments were extracted in the laboratory by sonification of sediment subsamples in 10 ml 90% acetone and subsequently measured in the supernatant on a Shimadzu UV-160A spectrophotometer. Concentrations of fucoxantine, diadinoxanthine, chlorofyl A and phaeophytine A were determined by comparison to simultaneously measured standards.
2.5 Nutrient profiles
Sediment was sampled at low tide using core liners of 3.6- and 5.4-cm inner diameter for porosity and pore water extraction, respectively. Cores for pore water extraction were immediately sliced inside a glove bag filled with argon gas. The slices, 1-cm steps up to 14-cm depth (March 2004) or 6-cm depth, and 2 cm up to 18-cm depth thereafter, were transferred into closed containers and centrifuged for 20 min at 4,000 rpm. After filtration through 0.2 μm (Millex GP and nylon) syringe filters, aliquots of pore water were kept frozen in plastic centrifuge tubes (Eppendorf) for spectrophotometrical nutrient determination (silicate, phosphate, ammonium, nitrate and nitrite) with a Skalar continuous-flow analyser according to Grasshoff et al. (1999). Samples for dissolved inorganic carbon (DIC) were preserved with saturated mercuric chloride solution and stored in glass vials until analysis. DIC analysis was performed by flow injection (Hall and Aller 1992). Dissolved sulphide was determined from samples fixed with 5% zinc acetate solution and stored frozen for subsequent spectrophotometrical analysis (Shimadzu UV-160A spectrophotometer) with the methylene blue method (Cline 1969).
3 Results and discussion
3.1 Skin circulation
The oxygen dynamics were similar at all locations on the Janssand (Fig. 4a, b). No clear differences were observed in oxygen penetration depths at the low water line, along the slope or on the upper flat (Fig. 4b). At low tide, oxygen penetrated 5 to 10 mm, whereas at high tide, a penetration of several centimetres was usually observed. This indicates that currents can drive water from the water column into the sediments to a depth of at least 5 cm, and probably more, at all three sites. This is a perfect illustration of skin circulation driven by currents over ripples (Huettel et al. 1998; De Beer et al. 2005; Billerbeck et al. 2006a). The permeability near the low water line was a bit lower than at the top of the flat, but this did not result in substantially less advective oxygen penetration; apparently, the hydrodynamic pressure due to tides and water movement is more decisive for the oxygen penetration depth.
3.2 Deep circulation
The seeps are not a constant phenomenon but display dynamics that are much slower than the seasonal time cycle and are certainly not in phase with the seasons. Billerbeck et al. (2006a) found that at one location, nutrient concentration fluctuated with a rhythm of approximately 1.5 years. This is consistent with the notion that seep chemistry is not determined by local processes but by a distant and deep source. The fluctuations in pore water chemistry can be attributed to slow changes in transport which, in turn, are influenced by the surface topography that changes slowly due to erosion and sedimentation or sometimes more dramatically during periods of enhanced hydrodynamics (e.g. storm events).
Of course, some short-term effects can be observed from extreme weather conditions. For example, no accumulation of degradation products was observed in oxic surface sediments at the low water line directly after a storm (Fig. 5). However, this is a very transient phenomenon.
The onset of pore water seepage as soon as the upper flat falls dry is also illustrated in Fig. 5b with the fast reduction of the oxygen penetration depth at the low water line shortly after falling tide.
4 Summary and conclusions
The results presented in this paper clearly demonstrate the high dynamics of oxygen, sulphide and pH in the surface sediments of an intertidal flat.
Due to advective transport, intensive skin circulation occurs which gives rise to strong interaction of solutes in the surface sediments. This leads to rapid exchange between organic matter and oxygen in the surface sediments. The results obtained are in line with other recent findings showing that sandy sediments can be more productive than previously thought because of their functioning as filters (e.g. De Beer et al. 2005; Werner et al. 2006). Values for the oxygen consumption at the surface under the control of these processes were estimated for the site by Billerbeck et al. (2006b). This demonstrated that rates during inundation were significantly higher than under exposure, emphasising the importance of advective transport as compared to diffusive transport.
Next to this filtering in the surface sediments, which occurs more or less over the whole surface, localised seeps were observed with high concentrations of reduced compounds (such as sulphide) and nutrients. It was demonstrated that these too are subject to dynamics, controlled mainly by tides. Together with earlier publications (e.g. Billerbeck et al. 2006b; Røy et al. 2008), these results show the importance of these seeps as sources of reduced compounds.
The data clearly confirm how the two main transport processes shape the chemical and microbial architecture of a permeable sand flat. Skin circulation is an efficient filter for DOC and POC from the water column and transport of oxygen into the sediments. This is the reason for the high areal mineralisation rates of permeable sands. Most of the labile particulate organic matter is degraded aerobically in the surface sediment in the order of days. This is supported by a wave-tank study of Franke et al. (2006) who detected high oxygen consumption downstream of hotspots of buried labile organic matter. Local bacterial decomposition of POM is spatially decoupled from the final degradation of dissolved organic matter by pore water flow. DOM is efficiently distributed over larger sediment volumes, thereby enhancing overall mineralisation processes leading to a mosaic of suboxic and anoxic microniches despite the exposure to oxygenated pore water. Furthermore, fluctuating redox conditions, as observed with the tidally dependent oxygen penetration depth in combination with sediment reworking due to bioturbation and resuspension, have been shown to enhance the overall mineralisation rates as well as extend oxygen exposure times to OM which, under diffusion-controlled conditions, would have been buried in an anoxic environment (Meile and Van Cappellen 2005). Deeper bioirrigation and sediment reworking by Arenicola marina is probably of minor importance at this study site with rather high-energy hydrodynamics. A. marina is relatively rare with approximately four individuals per square metre (determined in summer 2003, Billerbeck et al. 2006b) as compared to other areas with 40–80 individuals of bioturbators per square metre (Kristensen 2001). The importance of bioirrigation for oxygen dynamics can be estimated as follows: For each worm, we can assume a pumping rate of approximately 90 ml h−1 for approximately 10 h day−1 during inundation (Billerbeck et al. 2006b). Using these values, and an oxygen concentration in the water of 240 μM, the rate of oxygen input due to bioirrigation is estimated to be 240 μM × 3.6 individuals per square metre × 90 ml h−1 per individual × 10 h day−1 = 0.8 mmol m−2 day−1, which is small compared to the areal oxygen consumption rates reported for the site by Billerbeck et al. (2006b; in the order of 30–260 mmol m−2 day−1). Even in the case of ten times higher bioirrigation densities, the importance of bioirrigation for overall oxygen dynamics would still be small compared to the overall advective transport. In sites with low-energy hydrodynamics, less permeable sediment and more bioirrigating organisms, bioirrigation will be driving a larger fraction of the total oxygen exchange.
A further fraction of the filtered organic matter somehow arrives up to several metres depth within the sand flat where it is degraded by a suite of anaerobic processes, mainly sulphate reduction and methanogenesis. Due to the deep body circulation, the degradation products (nutrients, DIC, methane and sulphide) leave the flat at the points where the deep circulation ends, namely in seeps at the low water line. These two transport processes shape the distribution of mineralisation processes. Whereas in the top 3–5 cm of the flat aerobic mineralisation is the main pathway, sulphate reduction leads to depletion of sulphate deep within the flat, as a consequence of which, methanogenesis becomes possible. The products of these processes are partially oxidised by microbial and chemical processes at the seeps. The seeps are probably important sources for methane, a powerful greenhouse gas. Apparently, the methane oxidising capacity does not develop fast enough in this dynamic environment to effectively consume the emitted methane.
This study clearly shows strong differences in local environmental conditions. These are expected to have a huge impact on the biology. One example of this was shown in Fig. 12: Photopigments show a decreased level of algae at a site with high sulphide. Another example is the impact on of seepage on bioirrigation. At the same time, organisms are expected to adapt or even profit from these local conditions. For instance, motile sulphide-oxidising organisms are expected to be present at sites with high sulphide outflow. Also, anaerobic methane oxidation is expected to play a role at these sites with elevated levels of sulphate and methane brought together. Ishii et al. (2004) found aggregates of sulphate-reducing bacteria and archaea in sediment from the study site (September 2002) strongly resembling consortia involved in anaerobic methane oxidation found in sediments near methane hydrate deposits. These occurred in depths >12 cm, but not in black spots, i.e. sulphate-depleted areas where the methane is produced. Total cell counts showed maxima in the upper 2- to 3-cm depth, including Desulfobulbaceae which were found only here. Planctomycetes, presumably aerobic heterotrophic bacteria which are characteristic for permeable sediments with higher O2 penetration depth (Musat et al. 2006), were present in high abundance at all depths but with a maximum in 3–4 cm. This reflects the maximum penetration depth at the site. Black spots were also characterised by high bacterial numbers, except for Desulfosarcinales which showed their lowest abundance there (Ishii et al. 2004).
The data presented in this paper focused on the top layers of the sediments. Next to this, high activity was demonstrated for the same site in deeper sediment layers (upper 5 m), especially in the sulphate–methane transition zone (e.g. Wilms et al. 2006, 2007; Røy et al. 2008). These results demonstrate that microbial communities occur in a stratified manner at the study site and that these are combined with flow patterns which may lead to the transport of reduced compounds to the top layer. Once the compounds have reached the upper layers, the biogeochemical processes discussed in this paper further transform the compounds before their final release into the seawater or atmosphere. As the fluxes are a result of processes at the surface and at greater depth, a complete quantitative evaluation must encompass all of these processes.
We thank Ronald Monas and Iso Speck and the crews of the Twee Gebroeders and Verandering for letting us make use of their ships and their help and Ingrid Dohrmann for microsensor construction and help in the field. We thank Rodrigo da Purificaçăo for photopigment analysis and help in the field. We also gratefully acknowledge the support of others involved in microsensor construction (Gaby Eickert, Ines Schroeder, Anja Eggers, Karin Hohmann), help with sample analysis (Martina Alisch, Daniela Franzke, S. Lilienthal, A. Schipper) and technical assistance of Volker Meyer, Paul Faerber, Harald Osmers, Jens Langreder, Georg Hertz and Alfred Kutsche. We thank Filip Meysman and one anonymous reviewer for their comments. The study was supported by German Science Foundation during DFG research group “Biogeochemistry of Tidal Flats” (JO 307/4, BO 1584/4) and the Max Planck Society. We wish to thank J. Rullkötter for the coordination of the research group and B.B. Jørgensen for his continuous support of the project.
This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
- Aller RC (2001) Transport and reactions in the bioirrigated zone. In: Boudreau BP, Jørgensen BB (eds) The benthic boundary layer. Oxford University Press, OxfordGoogle Scholar
- Aloisi G, Drews M, Wallmann K, Bohrmann G (2004) Fluid expulsion from the Dvurechenskii mud volcano (Black Sea). Part I. Fluid sources and the relevance to Li, B, Sr, I and dissolved inorganic nitrogen cycles. Earth Plan Sci Lett 225:347–363Google Scholar
- Al-Raei AM, Bosselmann K, Böttcher ME, Hespenheide B Tauber F (2009) Seasonal dynamics of microbial sulfate reduction in temperate intertidal surface sediments: controls by temperature, sedimentology, and organic matter load. Ocean Dynamics (in press)Google Scholar
- Asmus R, Jensen MH, Mruphy D, Doerffer R (1998) Primary production of microphytobenthos, phytoplankton and the annual yield of macrophytic bomass in the Sylt-Rømø Wadden Sea. In: Gätje C, Reise K (eds) The Wadden sea ecosystem—exchange, transport and transformation processes. Springer, Berlin, pp 367–391Google Scholar
- Berg P, Risgaard-Petersen N, Rysgaard S (1998) Interpretation of measured profiles in sediment pore water. Limnol Oceanogr 43(7):1500–1510Google Scholar
- Böttcher ME, Al-Raei AM, Hilker Y, Heuer V, Hinrichs KU, Segl M (2007) Methane and organic matter as sources for excess carbon dioxide in intertidal surface sands: Biogeochemical and stable isotope evidence. Geochim Cosmochim Acta 71:A111Google Scholar
- Böttcher ME, Oelschläger B, Höpner T, Brumsack HJ, Rullkötter J (1998) Sulfate reduction related to the early diagenetic degradation of organic matter and “black spot” formation in tidal sandflats of the German Wadden sea: stable isotope (13C, 34S, 18O) and other geochemical results. Org Geochem 29:1517–1530CrossRefGoogle Scholar
- Böttcher ME, Hespenheide B, Llobet-Brossa E, Beardsley C, Larsen O, Schramm A, Wieland A, Böttcher G, Berninger UG, Amann R (2000) The biogeochemistry, stable isotope geochemistry, and microbial community structure of a temperate intertidal mudflat: an integrated study. Cont Shelf Res 20:1749–1769CrossRefGoogle Scholar
- Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14(3):454–458Google Scholar
- D’Andrea AF, Aller RC, Lopez GR (2002) Organic matter flux and reactivity on a South Carolina sandflat: the impacts of pore water advection and macrobiological structures. Limnol Oceanogr 47:1056–1070Google Scholar
- De Beer D (2000) Potentiometric microsensors for in situ measurements in aquatic environments. In: Buffle J, Horvai G (eds) In situ monitoring of aquatic systems: chemical analysis and speciation. Wiley, Chichester, pp 161–194Google Scholar
- De Beer D, Sauter E, Niemann H, Kaul N, Foucher JP, Witte U, Schlüter M, Boetius A (2006) In situ fluxes and zonation of microbial activity in surface sediments of the Håkon Mosby Mud Volcano. Limnol Oceanogr 51:1315–1331Google Scholar
- De Beer D, Wenzhöfer F, Ferdelman TG, Boehme SE, Huettel M, Van Beusekom J, Böttcher ME, Musat N, Dubilier N (2005) Transport and mineralization rates in north sea sandy intertidal sediments, Sylt-Rømø basin, Wadden sea. Limnol Oceanogr 50:113–127Google Scholar
- Franke U, Polerecky L, Precht E, Huettel M (2006) Wave tank study of particulate organic matter degradation in permeable sediments. Limnol Oceanogr 51:1084–1095Google Scholar
- Glud RN, Stahl H, Berg P, Wenzhofer F, Oguri K, Kitazato H (2009) In situ microscale variation in distribution and consumption of O2: a case study from a deep ocean margin sediment (Sagami Bay, Japan). Limnol Oceanogr 54:1–12Google Scholar
- Hall POJ, Aller RC (1992) Rapid, small-volume, flow injection analysis for ΣCO2 and NH4+ in marine and freshwaters. Limnol Oceanogr 37:1113–1119Google Scholar
- Meysman FJR, Galaktionov OS, Gribsholt B, Middelburg JJ (2006) Bioirrigation in permeable sediments: advective pore-water transport induced by burrow ventilation. Limnol Oceanogr 51:142–156Google Scholar
- Precht E, Franke U, Polerecky L, Huettel M (2004) Oxygen dynamics in permeable sediments with wave-driven pore water exchange. Limnol Oceanogr 49:693–705Google Scholar
- Røy H, Lee JS, Jansen S, De Beer D (2008) Tide-driven deep pore-water flow in intertidal sand flats. Limnol Oceanogr 53:1521–1530Google Scholar
- Werner U, Billerbeck M, Polerecky L, Franke U, Huettel M, Van Beusekom JEE, De Beer D (2006) Spatial and temporal pattern of mineralization rates and oxygen distribution in a permeable intertidal sandflat (Sylt, Germany). Limnol Oceanogr 51:2549–2563Google Scholar