Metal Accumulation in Intertidal Marshes: Role of Sulphide Precipitation

WETLANDS, Vol. 28, No. 3, September 2008, pp. 735–746 ’ 2008, The Society of Wetland Scientists

METAL ACCUMULATION IN INTERTIDAL MARSHES: ROLE OF SULPHIDE PRECIPITATION

Gijs Du Laing, Benjamin De Meyer, Erik Meers, Els Lesage, Annelies Van de Moortel, Filip M. G. Tack, and Marc G. Verloo Laboratory of Analytical Chemistry and Applied Ecochemistry Ghent University, Faculty of Bioscience Engineering Coupure Links 653 B-9000 Ghent, Belgium E-mail: [email protected]

Abstract: We assessed short-term temporal and spatial variation of metal contents in the upper 100 cm sediment profile of intertidal marshes vegetated by common reed (Phragmites australis) along the Scheldt estuary in Belgium. The upper 0–100 cm sediment profile was sampled in three reedbeds at 56, 94, and 131 km from the river mouth. Sampling was repeated five times, at approximately two month intervals. Sediment properties such as texture and chloride, carbonate and organic matter content differed among locations. Metal accumulation, which is primarily due to association of metals with organic matter and clay in the surface sediment layer, seemed to be supplemented by an accumulation of sulphide precipitates deeper in the sediments. The depth at which sulphide precipitation significantly contributed to metal accumulation depended on the sampling location, and varied from less than 5 cm in clayey, organic sediments to more than 1 m in sandy sediments. Temporal variation of Cu, Cd, Pb, and Zn concentrations could only be linked to newly formed sulphides or sulphide oxidation at the sites with the lowest sulphide content. At sampling sites containing high sulphide amounts, variations should be primarily attributed to metal exchange and the presence of mobile metal complexes. Litter decomposition at the end of the growing season could hereby play a significant role.

Key Words: cadmium, chromium, copper, flooding, inundation, lead, nickel, oxidation, Phragmites australis, redox, reduction, sulfide, trace element, zinc

INTRODUCTION of intertidal flats can therefore contribute to a more sustainable development of wetland ecosystems and The surface area of intertidal marshes in the can help to evaluate whether and under which Scheldt estuary in coastal Belgium has decreased due conditions wetland creation is a safe option. to industrial and urban development. A significant In a previous study (Du Laing et al. 2007a) amount of the remaining intertidal flats is contam- involving observations in 26 intertidal reedbeds inated with heavy metals. The temporarily flooded along the river Scheldt, the superficial intertidal sediments and their associated plant litter constitute sediment layer was found to be contaminated with major metal sinks (Panutrakul and Baeyens 1991, trace metals. Significant correlations were found Vandecasteele et al. 2003, Vandecasteele et al. 2006, among metals, organic matter, and clay concentra- Du Laing et al. 2006, 2007b). Metal accumulation in tions. In this study, short-term temporal and spatial the sediments is determined by inputs from dis- variations of sediment properties and metal contents charge of industrial and urban sewage or atmo- in the upper 100 cm intertidal sediment profile were spheric deposition, but also by the capability of the assessed at three selected locations. Factors affecting substrates to bind and release metals, which is metal accumulation in these deeper sediment layers governed by sediment pH, cation exchange capacity, were identified. organic matter content, redox conditions, and chloride content. These properties determine the type and stability of metal sorption or precipitation, METHODS which are also related to the metal mobility, Sampling Procedure bioavailability, and potential toxicity (Schierup and Larsen 1981, Du Laing et al. 2002, Eggleton and This study was carried out in the part of the Thomas 2004). Revealing the most important Scheldt estuary downstream the city of Ghent. All factors determining the metal contamination levels study sites are tidal marshes vegetated by monospe-

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layer was measured. The sediment accretion rate was ,0.2 cm between October 2003 and April 2004, and thus sediment deposition probably minimally affected metal contents in the upper sediment layer. Callaway et al. (1998) also found low sediment accretion rates at marshes in the Eastern Scheldt (0.68 cm year21 in the low marsh and 0.34 cm year21 in the high marsh).

Laboratory Analyses Metal content was determined in all replicate sediment cores (samples of 0–20, 20–40, 40–60, and 60–100 cm) from August. At other sampling times, sediment in the three cores collected at each location was pooled into a composite sample. Composite samples of both 0–2, 2–5, and 5–10 cm sediment Figure 1. Map of the three sampling locations along the samples taken at each location were also analyzed river Scheldt: Doel, Kijkverdriet, and Konkelschoor. for metal content at all sampling times. Organic matter, carbonate, chloride content, and pH were cific stands of common reed, Phragmites australis determined in samples from May, August, and (Cav.) Trin. ex Steud. Most of these marshes are October. Acid-volatile sulphide (AVS) content was only completely flooded during spring tides. At the determined in the 0–20, 20–40, 40–60, and 60– end of May 2003, sediments were sampled at three 100 cm composite samples from October, Decem- sampling locations, Doel, Kijkverdriet, and Kon- ber, and February. kelschoor (Figure 1), situated at 55.7, 94.4, and All glassware and containers were washed in a 131.4 km from the river mouth, respectively. Sam- laboratory dishwasher, subsequently soaked over- pling was repeated in the beginning of August, night in 5% ultrapure HNO3 (65%) and rinsed with October, December 2003, and February 2004. By deionized water. The pH was measured with a pH means of an auger, three sediment cores (3 cm dia- electrode in a sediment and distilled water suspen- meter) were taken at each location within a distance sion (1:5 ratio) after equilibration for 18 h (Van of approximately two meters from each other. Ranst et al. 1999). Organic matter content was Sediment was sampled from four depths, 0–20 cm, determined by measuring the weight loss after 20–40 cm, 40–60 cm, and 60–100 cm below the incineration (2 h at 450uC) of oven-dried samples. sediment surface. To conduct a more detailed Carbonate content was determined by back-titration sampling of the upper sediment layer, a cylindrical with 0.5 M NaOH of 25 ml of 0.25 M H2SO4 added PVC tube (height 5 15 cm, diameter 5 20 cm) was to 1 g of sediment (Nelson 1982). To determine hammered in the ground, dug up, placed on a PVC chloride content, 10 g of sediment was suspended in plate and transported to the lab. The upper layer of 50 ml of 0.15 M HNO3 and shaken for 30 minutes. these sediment cores was sliced into three sections: The filtrate was titrated with 0.05 M AgNO3 using 0–2 cm, 2–5 cm, and 5–10 cm. This was done in potentiometric end-point detection (Van Ranst et al. duplicate at each sampling site. The major part of 1999). Acid volatile sulphide (AVS) was determined each sediment sample was dried in the laboratory at on fresh sediment samples by conversion of sulphide u 50 C to constant weight, ground using a hammer- to H2S and absorption in a Zn-acetate solution, cross beater mill (Gladiator BO 3567), and stored followed by back titration (Tack et al. 1997). for further analyses. Fresh sediment samples were Therefore, three pyrex gas washing bottles were however used for the determination of acid-volatile connected in series. The first bottle was filled with sulphide (AVS) contents. 100 mL of deionized water, whereas the next two As the sampling sites could bank up during the bottles were filled with 95 mL of deionized water. sampling period due to regular flooding, sediment All flasks were deoxygenated by bubbling N2 accretion rates were also measured. To achieve this, through for 30 minutes. Five mL of 2 M ZnOAc litter was removed from three 30 cm 3 30 cm plots was added to each of the second and third bottles. at each sampling location in October. The sediment Subsequently, 10 g of sediment and 20 mL of 6 M surface was covered with white kaolin clay. At each HCl were added to the first bottle and N2 was re- sampling date, sediment deposition above the white bubbled through it for 30 minutes. The acid induced Du Laing et al., METAL ACCUMULATION IN INTERTIDAL MARSHES 737

Table 1. Results of ANOVA for organic matter (OM), chloride, carbonate content and pH in the sediments.

OM Chloride Carbonate pH df F p df F p df F p df F p site 2 298 0.000 2 5619 0.000 2 0.2 0.855 2 94.0 0.000 time 2 12 0.000 2 181 0.000 2 6.8 0.002 2 2.9 0.065 depth 6 49 0.000 6 578 0.000 6 16.2 0.000 6 7.4 0.000 site * time 4 19 0.000 4 369 0.000 4 2.0 0.106 4 2.2 0.075 site * depth 12 22 0.000 12 794 0.000 12 7.9 0.000 12 5.3 0.000 time * depth 12 4 0.000 12 148 0.000 12 4.8 0.000 12 1.4 0.205 site * time * depth 24 8 0.000 24 107 0.000 24 2.9 0.000 24 1.9 0.020

the conversion of sulphides to H2Sinthefirstbottle, increasing sampling depth. Variation was most which was transported by the N2 carrier gas to the significant in August (Table 2). The decrease with second and third bottle and absorbed in the Zn- increasing sampling depth was particularly pro- acetate solution. The Zn-acetate solution was nounced at Doel, where a clayey sediment layer subsequently acidified, and KI and KIO3 were covers a sandy subsurface layer that is low in added, which induced the formation of I2.Asa organic matter. Salts should leach more easily from 2 result, the collected sulphides (S2 ) were oxidized to sandy subsurface sediments (Qafoku and Sumner elemental sulphur (S0) by an equivalent amount of 2001). Additionally, salty tidal waters primarily 2 I2, which was reduced to I . The excess I2 was come into contact with the upper sediment layer. titrated with Na2S2O3. Pseudo-total metal contents As this clayey upper sediment layer is rather were determined by extraction with aqua regia (Ure impermeable, seepage towards lower sediment layers 1990). A 1:3 mixture of concentrated HNO3:HCl is hampered. was added to one gram of sediment. This suspen- The salinity of the upper layer (0–10 cm) of the sion was left to digest overnight at room tempera- intertidal sediments at Doel was significantly lower ture, and subsequently heated to 150uCfor2h, in the subset May-October compared to August- filtered, and diluted to 100 mL. The metal contents October. This reflects the changes in the salinity of in the extracts were analysed using Inductively the river water. Baeyens et al. (1998) indeed reported Coupled Plasma – Optical Emission Spectrometry that chloride concentration in Scheldt river water is (ICP-OES, Varian Vista MPX, Varian, Palo Alto, higher during periods of low discharge, when the CA). salinity front moves upstream. As a consequence, the Sea Scheldt between Ghent and Antwerp is a tidal Statistical Analysis fresh water river during winter and spring, but it turns brackish during summer and autumn between To detect significant effects of sampling time, Antwerp and the Rupel river mouth (100 km sampling location, sediment profile depth, and upstream) (Du Laing et al. 2008). Salinity variations possible interactions among these factors on mea- decrease with increasing distance from the river sured sediment properties, analysis of variance mouth as the salinity of the river water is not the (ANOVA) was conducted using SPSS 12.0 (2003). only factor determining the salinity of intertidal Tukey post-hoc tests were conducted to determine sediments. In the intertidal marshes, the river water homogenous subsets at 0.05 significance level. mixes in variable proportions with groundwater and rainwater, whereas in the upper sediment layer, salts RESULTS AND DISCUSSION can also be concentrated as a result of evapotranspi- ration. Bear (1964) noted that salinity effects on soils Temporal and Spatial Variation of Physicochemical and plants are determined by the salinity of the pore Sediment Properties water of intertidal sediments rather than by the Sampling location, sampling depth, and sampling salinity of the flooding water. Lau and Chu (1999) time all had a significant effect on chloride observed higher salinities in pore water compared to concentration. Moreover, interactions between all the flooding water. Numerical simulation of the factors were significant (Table 1). Chloride concen- interaction between the groundwater and the surface tration generally decreased with increasing distance water is not a trivial matter as groundwater responds from the river mouth, consistent with a decreasing much slower than the surface water does (Post 2005). influence of salty seawater. It also decreased with This presents a problem of different time scales when 738 WETLANDS, Volume 28, No. 3, 2008

Table 2. General sediment properties for each sampling site and depth (average 6 standard deviation; each letter denotes a homogenous subset within each column, according to Tukey’s test at a significance level of 0.05; number of samples is indicated in parentheses).

Chloride Organic matter Carbonate 21 % % Sampling site and (mg kg DM) ( ) ( )pH depth All samples a August b All samples a All samples a All samples a Konkelschoor 0–20 cm 99 6 15 a (9) 100 6 16 ab (3) 16.6 6 1.3 cd (9) 6.9 6 0.8 ab (9) 7.39 6 0.16 ab (9) 0–2 cm 78 6 52 a (6) 76 6 0 a (2) 19.1 6 3.5 cd (6) 7.0 6 1.1 ab (6) 7.28 6 0.13 a (6) 2–5 cm 72 6 30 a (6) 85 6 45 ab (2) 19.5 6 6.5 cd (6) 6.2 6 1.5 ab (6) 7.28 6 0.07 a (6) 5–10 cm 104 6 52 a (6) 150 6 27 ab (2) 19.6 6 4.7 cd (6) 6.1 6 0.5 ab (6) 7.31 6 0.11 a (6) 20–40 cm 57 6 31 a (9) 71 6 43 a (3) 17.0 6 2.3 cd (9) 6.8 6 0.6 ab (9) 7.44 6 0.10 ab (9) 40–60 cm 96 6 35 a (9) 96 6 30 ab (3) 17.6 6 1.9 cd (9) 6.6 6 0.7 ab (9) 7.43 6 0.32 ab (9) 60–100 cm 59 6 54 a (9) 102 6 39 ab (3) 17.0 6 1.2 cd (9) 6.4 6 0.8 ab (9) 7.37 6 0.22 ab (9) Kijkverdriet 0–20 cm 386 6 264 a (9) 274 6 76 abc (3) 23.2 6 3.2 d (9) 6.5 6 1.1 ab (9) 7.29 6 0.17 a (9) 0–2 cm 611 6 69 a (6) 671 6 4 cd (2) 23.3 6 8.1 d (6) 7.3 6 0.7 ab (6) 7.41 6 0.07 ab (6) 2–5 cm 504 6 61 a (6) 484 6 72 bc (2) 23.9 6 7.0 d (6) 6.7 6 0.3 ab (6) 7.37 6 0.06 ab (6) 5–10 cm 540 6 144 a (6) 417 6 13 abc (2) 23.1 6 7.0 d (6) 6.2 6 0.8 ab (6) 7.40 6 0.05 ab (6) 20–40 cm 310 6 155 a (9) 281 6 75 abc (3) 20.5 6 1.5 cd (9) 5.4 6 1.4 ab (9) 7.22 6 0.24 a (9) 40–60 cm 215 6 92 a (9) 191 6 110 ab (3) 18.7 6 2.9 cd (9) 6.1 6 1.3 ab (9) 7.27 6 0.26 a (9) 60–100 cm 212 6 108 a (9) 302 6 10 abc (3) 12.9 6 3.8 bc (9) 6.4 6 3.0 ab (9) 7.51 6 0.14 ab (9) Doel 0–20 cm 2722 6 826 bc (9) 2583 6 180 f (3) 5.8 6 2.0 ab (9) 6.3 6 1.1 ab (9) 7.72 6 0.17 bc (9) 0–2 cm 7799 6 2906 d (6) 11446 6 182 h (2) 23.2 6 3.1 d (6) 11.4 6 1.6 c (6) 7.53 6 0.14 ab (6) 2–5 cm 4416 6 2286 c (6) 7009 6 119 g (2) 19.6 6 5.4 cd (6) 7.6 6 1.3 b (6) 7.46 6 0.31 ab (6) 5–10 cm 1768 6 1029 ab (6) 2454 6 60 f (2) 7.4 6 1.4 ab (6) 6.1 6 1.6 ab (6) 7.91 6 0.28 c (6) 20–40 cm 1619 6 545 ab (9) 1269 6 105 e (3) 3.7 6 2.8 a (9) 5.1 6 1.0 ab (9) 8.00 6 0.09 c (9) 40–60 cm 1453 6 598 ab (9) 953 6 152 de (3) 3.2 6 2.3 a (9) 4.7 6 1.1 a (9) 8.05 6 0.10 c (9) 60–100 cm 1540 6 630 ab (9) 990 6 367 de (3) 3.4 6 2.5 a (9) 4.7 6 0.9 a (9) 8.09 6 0.19 c (9) a Average 6 standard deviation for all samples taken in May, August, October, December and February. b Average 6 standard deviation for only the samples taken in August. coupling surface water and groundwater models. expected to be rather low as a result of the anoxic Hydrological models are therefore not yet able to conditions. In contrast, organic matter concentra- adequately predict water fluxes and salinities in tion was lowest in the deeper sediment layers of Doel the transition zone between rivers and upland soils, (Table 2). The sediments are more sandy and which makes it even more difficult to explain seasonal permeable at this site, which results in a lower and temporal salinity variations in intertidal sedi- retention of organic fractions. At Konkelschoor, ments. average concentrations in the 0–10 cm layer were Sampling location, time, and depth, as well as significantly higher in May (October 15.3% , interactions among them, all are significant in August 17.9% , May 26.4%), whereas at Kijkver- explaining the variability in organic matter concen- driet they were highest in August (May 13.1% 5 tration (Table 1). The significance of location effects October 23.6% , August 28.5%). At Doel, the generally increased with increasing sampling depths sampling time did not affect the organic matter (Table 2). The organic matter supply to the upper concentration in samples of the 0–10 cm layer sediment layer, e.g., due to litter accumulation and significantly (May 13.7% 5 October 15.0% 5 belowground biomass production, and the organic August 19.1%). The organic matter concentration matter decomposition rate in this layer thus seem to in this upper sediment layer is probably determined depend only little on the sampling location, whereas by a variety of opposing factors, such as organic different leaching and decomposition rates of matter accumulation just after the growing season of organic fractions at the different sites probably reed plants as a result of reed plant decay and determine organic matter concentration at greater subsequent litter decomposition (Du Laing et al. depths. Indeed, the organic matter concentrations 2006, Du Laing et al. 2007b) and variable below- were highest at Kijkverdriet and Konkelschoor, ground biomass production rates of the reed plants where the organic matter decomposition rate is (Soetaert et al. 2004). Du Laing et al., METAL ACCUMULATION IN INTERTIDAL MARSHES 739

Sampling time and depth were significant in at the end of the growing season could constitute an explaining the variability in carbonate concentra- additional factor explaining this decrease. tions. Additionally, effects of sampling depth Although the pH varied in narrow ranges (7.16– significantly depended on the sampling location 8.68), there were significant differences in pH among (Table 1). In Doel, the carbonate concentration sampling locations and sampling depths (p , 0.001), decreased from 11.4% in the upper 0–2 cm sediment but not among different sampling times (p 5 0.065) layer to 4.7% in the 60–100 cm sediment layer. At (Table 1). The interaction between sampling loca- the other sampling sites, carbonate concentrations tion and depth was significant (p , 0.001), whereas also decreased with sampling depth, but these interactions of sampling depth and location with variations were not significant (Table 2). Differences time were not (p 5 0.205 and 0.075, respectively). in carbonate concentrations might be due to the Thus, pH change as a function of depth depended operational analysis procedure. Some sediments, on the location. The average pH was higher in Doel, such as those of Kijkverdriet and Konkelschoor compared to Kijkverdriet and Konkelschoor (Doel contain a significant amount of sulphides, whereas 7.85 . Kijkverdriet 7.35 5 Konkelschoor 7.37). those of Doel do not. During drying of the sulphide- Moreover, pH clearly increased with increasing rich samples preceding the analyses, sulphides might depth at Doel, whereas no clear profile was observed be oxidized, simultaneously releasing protons and at Kijkverdriet and Konkelschoor (Table 2). Mea- lowering the carbonate content and pH. For each sured pH changes might also partly be attributed to molecule of FeS oxidized, two protons are produced the operational analysis procedure, as the pH was (van den Berg and Loch 2000). Differences between measured on dry samples and protons are released the highest and lowest average AVS concentrations upon oxidation of sulphides. However, the impact along the sediment profile are below 48 mmol S22 on pH is expected to be very low because the kg21 DM. Upon oxidation of such amount, sediments are still buffered well by the presence of 96 mmol H+ kg21 DM is released, which consumes carbonates and bicarbonates. The calculated maximum pH decrease due to sulphide oxidation was less less than 1% of CaCO3 in the sediment. So this could only partly account for the observed decreases than 0.1 pH-unit. Bicarbonates are probably also of carbonate concentrations with sampling depths, formed by natural processes. A lower permeability which totalled 0.9% to 6.7%. Decreasing carbonate of sediments or a higher organic matter decompo- concentration at greater depths may also result from sition rate can indeed lead to a higher CO2 pressure, an increasing CO pressure. CO is produced during resulting in bicarbonate formation and a small pH 2 2 decrease in the presence of carbonates. Moreover, organic matter decomposition, whereas diffusion to bicarbonates are expected to leach more easily from the atmosphere is expected to be hampered upon sandy sediments during tidal flooding, which may flooding, especially in clayey sediments. Decalcifica- prevent the pH from significantly decreasing upon tion might therefore occur according to the follow- organic matter decomposition. The permeability of ing reaction (van den Berg and Loch 2000): the sediments was indeed lower at Kijkverdriet and z z ? 2z z {: Konkelschoor compared to Doel, whereas the CaCO3 CO2 H2O Ca 2 HCO3 organic matter concentration was also higher. The significantly higher carbonate concentration in Moreover, organic matter and clay concentrations the upper sediment layer of the Doel site is probably decreased with increasing depth at Doel. related to that sampling site being located nearer to the sea. As a result, carbonates can settle during tidal flooding. Moreover, the sediments in Doel are Temporal and Spatial Variation of rather sandy and contain little organic matter. This Metal Concentrations should lead to a lower CO2 and organic acid Short-distance variation in metal concentrations production and a more efficient exchange of CO2 between sampling points situated approximately with the atmosphere. This in turn would limit 2 m from each other was rather low, as illustrated decalcification (van den Bergh and Loch 2000). for Cd and Cu in Figure 2. Short-term temporal Temporal settling fluctuations could explain varia- variations could not be identified due to practical tions in the carbonate concentrations of the upper 0– restrictions as sampling could only be performed at 2 cm sediment layer at Doel. The carbonate low tide. However, they are also expected to be concentration was highest in August (13%), and rather low because sediment accretion rates were lowest in May (9%). Breakdown of settled carbon- found to be very low. Additionally, metals are ates as a result of CO2 and organic acid production expected to migrate rather slowly through the associated with the litter decay and decomposition sediment profile, especially in sediments containing 740 WETLANDS, Volume 28, No. 3, 2008

Figure 2. Short-distance variation of metal concentrations within the sediment profiles of Konkelschoor, Kijkverdriet, and Doel in August (sampling points 1, 2, and 3 were located approximately 2 m from each other). a significant amount of clay and organic matter, cluded that an accurate chronology of metal input to such as those of Kijkverdriet and Konkelschoor. salt marsh sediments can be difficult to assess because Finally, superficial flooding during only a limited of the potential early-diagenetic mobility of both the period of time is not expected to significantly affect radionuclides used for dating and the contaminants of ground water levels and flows, as the superficial interest. Moreover, some specific characteristics of the sediment layer is rather clayey and impermeable. intertidal marshes, such as the fluctuating water table Some authors (e.g., Giordano et al. 1992, Zwols- levels, the occurrence of emergent vegetation, and man et al. 1993, Monterroso et al. 2003) stated that bioturbation, might facilitate metal redistribution the vertical distribution of metal concentrations in within the upper sediment profile layer. contaminated sediments can generally be attributed We indeed found very low sediment accretion to anthropogenic inputs. Geochronologies or ‘‘con- rates within the experimental time period, although tamination histories’’ of wetlands could thus be we observed a significant effect of the sampling time reconstructed through the collection and analysis of on the metal concentrations, as well as significant profiles of sediment from selected areas (Fox et al. interactions of sampling time with both sampling 1999). As a result, the extent and the history of location and depth (Table 3). Therefore, we did not pollution in estuarine and coastal areas has been attribute fluctuations of the metal distribution estimated from profiles of trace contaminants in within the upper sediment profile primarily to the sediment cores by several authors (e.g., Santschi et pollution history. al. 2001, Bay et al. 2003). They often rely on 137Cs Sampling location, time, depth, and most of their dating (a fallout product of nuclear testing) and interactions all were significant in explaining vari- normalization of metal concentrations to Al or Li ability of the metal concentrations. Sampling time concentrations (e.g., DeLaune et al. 1978, Pardue et was not a significant factor for Fe and Cu al. 1992, Callaway et al. 1998, Spencer 2002, Wang concentrations (p 5 0.932 and 0.307, respectively). et al. 2004). However, according to Spencer et al. However, significant interaction effects of time with (2003), salt marshes in macro-tidal estuaries retain a depth and location were observed also for these time-integrated or ‘‘smoothed’’ signal rather than a elements, which indicates that the occurrence of time record of discrete pollutant inputs, due to extensive effects depended on the sampling depth and location sediment reworking. They found that Fe and Mn (Table 3). Metal concentrations were significantly have been significantly remobilized and that these lowerinDoelcomparedtoKonkelschoorand diagenetic processes have slightly modified the Kijkverdriet (Table 4 and Table 5). This might be vertical distributions of Cu, Pb, and Zn in a dated attributed to the generally lower organic matter and salt-marsh core from the macro-tidal Medway clay concentrations and the higher chloride concen- estuary (southeast England). They therefore con- trations, as observed by Du Laing et al. (2007a). Du Laing et al., METAL ACCUMULATION IN INTERTIDAL MARSHES 741

Table 3. Results of ANOVA for metal concentrations in the sediments.

df F p df F p df F p df F p Cd Cr Cu Fe site 2 537 0.000 2 294 0.000 2 417 0.000 2 108 0.000 time 4 18 0.000 4 8 0.000 4 1 0.307 4 0 0.932 depth 6 57 0.000 6 32 0.000 6 7 0.000 6 4 0.004 site * time 8 64 0.000 8 42 0.000 8 5 0.001 8 8 0.000 site * depth 12 48 0.000 12 27 0.000 12 13 0.000 12 8 0.000 time * depth 21 4 0.001 21 11 0.000 21 5 0.000 21 1 0.942 site * time * depth 42 16 0.000 42 20 0.000 42 2 0.052 42 1 0.478 Mn Ni Pb Zn site 2 112 0.000 2 14 0.000 2 1,573 0.000 2 248 0.000 time 4 12 0.000 4 140 0.000 4 49 0.000 4 10 0.000 depth 6 14 0.000 6 30 0.000 6 39 0.000 6 10 0.000 site * time 8 8 0.000 8 6 0.000 8 66 0.000 8 3 0.022 site * depth 12 12 0.000 12 9 0.000 12 85 0.000 12 8 0.000 time * depth 21 1 0.342 21 28 0.000 21 15 0.000 21 1 0.589 site * time * depth 42 2 0.013 42 9 0.000 42 10 0.000 42 3 0.002

Table 4. Cd, Cr, Cu, and Fe concentrations in the sediments for each sampling site and depth (average 6 standard deviation; each letter denotes a homogenous subset within each column, according to Tukey’s test at a significance level of 0.05).

Sample site and depth Cd mg kg21 DM Cr mg kg21 DM Cu mg kg21 DM Fe g kg21 DM Konkelschoor 0–20 cm a 5.6 6 1.4 abcd 171 6 43 abc 88 6 18 cde 36.3 6 2.3 cd 0–2 cm b 5.9 6 0.5 abcd 199 6 93 abc 96 6 21 def 37.4 6 4.1 d 2–5 cm b 6.7 6 0.9 abcd 211 6 101 abc 106 6 24 defg 38.3 6 5.2 d 5–10 cm b 6.2 6 1.6 abcd 183 6 19 abc 109 6 9defg 39.66 1.9 d 20–40 cm a 7.4 6 1.1 bcde 266 6 44 abc 137 6 22 efgh 37.9 6 3.5 d 40–60 cm a 9.9 6 2.3 cde 349 6 94 c 146 6 55 fgh 38.8 6 3.4 d 60–100 cm a 17.3 6 6.3 fg 729 6 408 d 146 6 45 fgh 35.5 6 4.4 cd Kijkverdriet 0–20 cm a 12.1 6 3.3 def 172 612 abc 124 6 18 efg 44.5 6 2.2 de 0–2 cm b 5.5 6 0.7 abcd 156 6 64 abc 89 6 27 cdef 38.8 6 6.8 d 2–5 cm b 6.7 6 0.8 abcd 167 6 71 abc 104 6 25 defg 40.5 6 4.6 d 5–10 cm b 8.9 6 2.4 cde 193 6 86 abc 126 6 35 efg 39.5 6 6.0 d 20–40 cm a 30.5 6 5.2 h 286 6 17 bc 188 6 16 h 54.5 6 1.3 ef 40–60 cm a 23.2 6 8.1 g 345 6 85 c 159 6 23 gh 53.5 6 7.0 f 60–100 cm a 13.9 6 4.5 ef 159 6 42 abc 132 6 36 efg 38.6 6 6.3 d Doel 0–20 cm a 1.3 6 0.5 ab 43 6 3ab 196 4ab 17.56 1.5 ab 0–2 cm b 3.4 6 0.4 abc 122 6 52 abc 64 6 16 bcd 40.1 6 2.5 d 2–5 cm b 3.5 6 0.8 abc 127 6 43 abc 64 6 11 bcd 38.5 6 2.4 d 5–10 cm b 2.0 6 0.8 ab 86 6 37 ab 38 6 14 abc 25.9 6 6.6 bc 20–40 cm a 0.7 6 0.6 a 26 6 6a 66 7 a 11.9 6 2.7 a 40–60 cm a 0.7 6 0.8 a 25 6 7a 567 a 11.3 6 3.2 a 60–100 cm a 1.1 6 1.0 ab 28 6 6a 86 6ab 12.16 3.1 a a n 5 5 for each sampling site and depth, composite samples in May, October, December, February, and average of 3 replicate samples in August. b n 5 5 for each sampling site and depth, composite samples in May, October, December, February, and average of duplicate samples in August. 742 WETLANDS, Volume 28, No. 3, 2008

Table 5. Mn, Ni, Pb, and Zn concentrations in the sediments for each sampling site and depth (average 6 standard deviation; each letter denotes a homogenous subset within each column, according to Tukey’s test at a significance level of 0.05).

Sample site and depth Mn mg kg21 DM Ni mg kg21 DM Pb mg kg21 DM Zn mg kg21 DM Konkelschoor 0–20 cm a 1269 6 218 bcdef 81 6 102 a 134 6 32 de 587 6 120 cde 0–2 cm b 1473 6 270 cdef 32 6 11 a 145 6 27 de 544 6 63 cde 2–5 cm b 1183 6 354 abcdef 35 6 15 a 161 6 30 de 604 6 63 cde 5–10 cm b 1328 6 453 bcdef 43 6 15 a 169 6 19 e 668 6 35 def 20–40 cm a 2049 6 579 ef 143 6 237 a 160 6 35 de 726 6 110 efg 40–60 cm a 2177 6 346 f 45 6 7 a 169 6 62 e 819 6 204 efg 60–100 cm a 997 6 227 abcde 91 6 113 a 275 6 97 fg 1381 6 516 h Kijkverdriet 0–20 cm a 2096 6 679 ef 122 6 154 a 198 6 25 ef 675 6 79 ef 0–2 cm b 2230 6 879 f 33 6 9 a 145 6 42 de 477 6 53 bcde 2–5 cm b 1854 6 1043 def 37 6 11 a 163 6 46 de 544 6 77 cde 5–10 cm b 1936 6 1125 def 43 6 15 a 196 6 58 ef 604 6 103 cd 20–40 cm a 1310 6 285 bcdef 116 6 107 a 311 6 41 g 1070 6 128 gh 40–60 cm a 1025 6 343 abcde 207 6 294 a 288 6 33 fg 985 6 150 fg 60–100 cm a 869 6 146 abcd 230 6 117 a 270 6 72 fg 820 6 176 efg Doel 0–20 cm a 331 6 63 ab 14 6 4a 376 7 abc 110 6 16 a 0–2 cm b 1633 6 185 def 54 6 38 a 115 6 26 bcde 322 6 41 abcd 2–5 cm b 1166 6 194 abcdef 31 6 12 a 117 6 24 cde 299 6 61 abc 5–10 cm b 494 6 169 abc 21 6 9a 716 33 abcd 172 6 67 ab 20–40 cm a 142 6 105 a 10 6 8a 166 7a 566 26 a 40–60 cm a 100 6 62 a 8 6 6a 156 8a 516 27 a 60–100 cm a 125 6 67 a 9 6 6a 196 10 ab 102 6 96 a a n 5 5 for each sampling site and depth, composite samples in May, October, December, February, and average of 3 replicate samples in August. b n 5 5 for each sampling site and depth, composite samples in May, October, December, February, and average of duplicate samples in August.

In the upper centimeters, Mn concentration steepest increase was found in the 60–100 cm layer decreased with increasing depth, which was also for Konkelschoor. observed for Fe in Doel. The more elevated Fe and We would attribute the decreases of metal Mn concentrations in the upper layer are likely concentrations with increasing sampling depth at related to more oxic conditions that favor precipi- Doel mainly to the significant decrease of organic tation of Fe and Mn as oxides (Callaway et al. matter and clay content with depth. Metal contents 1998). However, Fe and Mn concentrations also indeed are strongly related to clay and organic showed a peak at greater depths in Kijkverdriet and matter contents in the upper 20 cm sediment layer Konkelschoor, causing a significant depth-location (Du Laing et al. 2007a). The decreasing organic interaction effect for Fe and Mn concentrations. matter contents with increasing sampling depth in These peaks might be attributed to the presence of turn might be related to reed plant rooting and litter sulphides at the greater depths, which in turn induce accumulation in the upper sediment layers. De the formation of insoluble Fe and Mn sulphide Lacerda et al. (1997) accordingly found increased precipitates (Du Laing et al. 2007b,c). Sampling Cd and Zn concentration in the upper sediment depth and location-depth interaction effects were layer of a site vegetated by Spartina alterniflora, also significant for Cd, Cr, Cu, Pb, and Zn compared to adjacent mud flats without plant cover. concentrations. The Cd and Zn concentrations Metal concentrations at 5–15 cm depth were four reached a maximum at 20–40 cm below the sediment times higher at the vegetated site. Similar results surface at Kijkverdriet, whereas they decreased with were found at sites vegetated with Spartina maritima increasing depth at Doel and kept increasing with by Cac¸ador et al. (1996). They concluded that roots increasing depth at Konkelschoor. At Kijkverdriet, influence metal concentrations in marsh sediments the most significant increase was situated between 20 because they produce complex organic compounds and 40 cm below the sediments surface, whereas the and oxidize the rhizosphere. The formation of iron Du Laing et al., METAL ACCUMULATION IN INTERTIDAL MARSHES 743

Figure 3. Correlation between Cd and Zn contents in intertidal sediment samples (0–100 cm below the surface) of Doel, Kijkverdriet, and Konkelschoor. plaque in the oxidized rhizosphere also might rivers or lakes, and accordingly, peak sulphur contribute to increased metal concentration (Sundby concentrations will occur at greater sampling depths. et al. 1998). Moreover, decomposing reed litter was found to cause metal enrichment in the upper layer Role of Sulphide Precipitation (Larsen and Schierup 1981, Du Laing et al. 2006). The higher sulphide content in Kijkverdriet and at Cadmium and Zn usually show similar sorption greatersamplingdepthsinKonkelschoor(Figure4) and mobilization characteristics in upland soils. suggest precipitation of metals as sulphides (Billon et When all sediment samples of Doel (0–100 cm), al. 2001, Du Laing et al. 2007c). This might explain which were the least reduced and contained low the increasing metal concentration with increasing sulphide amounts, are included in a linear regression depths at these locations. In Kijkverdriet, a signif- analysis, the correlation between Cd and Zn icant amount of sulphides was already found in the concentrations is indeed found to be very significant upper 0–20 cm sediment layer, whereas at Kon- (Figure 3). The slope of the regression line is similar kelschoor, significant amounts were found from to the slope calculated for the Cd and Zn about 60 cm below the surface. Metals that leached concentrations in the upper 20 cm sediment layer from the upper sediment layer are thus expected to using the data reported by Du Laing et al. (2007a). be especially concentrated in the higher sediment This indicates that both elements accumulated in the layers at Kijkverdriet and in the lower layers at upper 100 cm sediment layer in the same ratio as in Konkelschoor. White et al. (1989) also observed the upper 20 cm sediment layer. For Kijkverdriet peaks in sulphur content in freshwater lake sedi- and Konkelschoor, which have more elevated AVS ments and attributed these to sulphate reduction and contents, lower slopes were found for the regression Fe sulphide precipitation. However, these peaks lines, and the intercept became more significant, were situated at much lower depths, between 5 and compared to Doel (Figure 3). This effect is most 10 cm below the surface of the sediments. This pronounced at Kijkverdriet, the sampling site with difference might be attributed to the average water the highest AVS content. Cadmium appeared to table level being situated at greater depths in the preferentially accumulate compared to Zn. Sul- intertidal sediments. Moreover, intertidal sediments phides might constitute a pool in which Cd is are subject to alternating hydrological conditions, preferentially accumulated, as the solubility of CdS which do not facilitate sulphide formation in the is much lower compared to ZnS. Moreover, only a upper sediment layers (Du Laing et al. 2007c). As a smallamountofsulphideisneededtoprecipitatea result, sulphate reduction rates are expected to significant portion of all Cd present, whereas more is increase more gradually with depth in the intertidal needed to precipitate all Zn. Accumulation of Cd in sediments, compared to the bottom sediments of this ‘‘sulphide pool’’ might be enhanced by the 744 WETLANDS, Volume 28, No. 3, 2008

decrease in the Zn over Cd ratio of the total dissolved concentrations. Bi-plots for other combinations of elements showed similar relationships as those represented in Figure 3. Preferential accumulation in the ‘‘sulphide pool’’ at the greater sediment depths, however, seems to be restricted to Cd/Zn, which can probably be explained by their overall higher mobility and rate of leaching from low AVS sampling points. Moreover, plots for other elements were often more scattered, as sorption and mobilization characteristics in the absence of sulphides does not show as much agreement as between Cd and Zn. Temporal variation in sulphide content can thus also be expected and might influence metal accumulation and mobility. In the 40–100 cm layer of Doel, AVS concentrations decreased from low, but detectable concentrations in October and December (2.7–5.3 mmol kg21 DM) to very low concentrations (,0.8 mmol kg21 DM) in February. This coincided with metal concentrations that also decreased from October to February, as illustrated for Cu in Figure 4. Temporal change of low sulphide content may thus indeed be related to variation in metal content, which was already observed in greenhouse experiments (Du Laing et al. 2007c). Sulphide oxidation and subsequent metal release might be caused by oxygen diffusion into the sediment during a period of lower water table levels. Moreover, reed plant decay and litter decomposition in the upper sediment layers during fall, which also seem to result in increased Cu concentrations in the 0–5 cm layer, might result in an increased oxygen consumption and thus lead to more anoxic conditions at greater depths in October-December compared to February. Ongoing leaching of Cu from the litter to the lower layers or increased sulphide precipitation due to increased sulphide formation results in the maximal Cu concentration being reached in February for the 5–10 cm layer and in Figure 4. Temporal fluctuations of Cu and AVS May at the greater depths. At the greatest depths, concentrations in the 0–100 cm intertidal sediment layer similar profiles are observed for Cd, Pb, and Zn. of Doel, Kijkverdriet, and Konkelschoor as a function of sampling depth. However, the increased Cu concentrations in the upper sediment layer in October are not accompa- nied by increased Cd and Zn concentrations. This higher chloride contents at Kijkverdriet, which might be due to a weaker association of Cd and Zn promote leaching of Cd from the upper sediment with the litter as the stability of Cd/Zn-organic layers to the lower layers as soluble Cd chloride matter complexes is lower (Kalbitz and Wennrich complexes (Du Laing et al. 2008). Thus Cd 1998). migration and precipitation at greater depth is At both Kijkverdriet and Konkelschoor, Cu favored. Zinc chloride complexes are indeed less concentrations did not follow fluctuating sulphide stable than Cd chloride complexes. Gerringa et al. concentrations as strongly. The higher sulphide (2001) concluded that the formation of dissolved Cd levels might not be limiting for Cu sulphide chloride complexes when oxidation occurs at high formation anymore at these sites. Conversely, salinities increases the mobility of Cd, causing a oxidation of part of the sulphides will not signifi- Du Laing et al., METAL ACCUMULATION IN INTERTIDAL MARSHES 745 cantly affect Cu sulphide contents. Indeed, total which sulphide precipitation significantly contrib- molar contents of metals with the lowest metal utes to metal accumulation depended on the sulphide solubility products (Cu, Cd, Pb, Ni, Zn) sampling location, and varied from less than 5 cm were lower than the total molar sulphide contents. in clayey, organic sediments to more than 1 m in Thus, Cu sulphide formation should be largely sandy sediments. Temporal variation of Cu, Cd, Pb, determined by Cu availability instead. In October, and Zn concentration can only be linked to newly Cu content was lowest at the greatest depths but formed sulphides or sulphide oxidation at the sites highest in the upper layer. The strong complexation with the lowest sulphide contents. At sampling sites of Cu by organic matter may result in a redistribu- containing high sulphide amounts, variation should tion of Cu within the profile towards lower depths be primarily attributed to metal exchange and the when most reed plant decay and litter accumulation presence of mobile metal complexes. Litter decom- occurs. The increasing Cu concentration from position at the end of the growing season could October to February at greater sampling depths hereby play a significant role. might additionally be linked to gradual leaching of organic Cu-complexes from the litter, which accu- LITERATURE CITED mulate in the upper sediment layer during fall and winter. The decreasing Cu concentration between Baeyens, W., B. Van Eck, C. Lambert, R. Wollast, and L. Goeyens. 1998. General description of het Scheldt estuary. May and October at these greater sampling depths Hydrobiologia 366:1–14. might in turn be related to an increasing organic Bay, S. M., E. Y. Zeng, T. D. Lorenson, K. 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