ment 380 (2007) 84–92www.elsevier.com/locate/scitotenv

Science of the Total Environ

Mobility of Pb in salt marshes recorded by total content andstable isotopic signature

Miguel Caetano, Nuno Fonseca, Rute Cesário Carlos Vale ⁎

National Institute for Agronomy and Fisheries Research — IPIMAR, Av. Brasília 1449–006, Lisbon, Portugal

Received 14 October 2005; received in revised form 20 November 2006; accepted 21 November 2006Available online 23 February 2007

Abstract

Total lead and its stable isotopes were analysed in sediment cores, leaves, stem and roots of Sacorconia fruticosa and Spartinamaritima sampled from Tagus (contaminated site) and Guadiana (low anthropogenic pressure) salt marshes. Lead concentration invegetated sediments from the Tagus marsh largely exceeded the levels in non-vegetated sediments. Depth profiles of 206Pb/207Pband 206Pb/208Pb showed a decrease towards the surface (206Pb/207Pb=1.160–1.167) as a result of a higher proportion of pollutantPb components. In contrast, sediments from Guadiana marsh exhibited low Pb concentrations and an uniform isotopic signature(206Pb/207Pb=1.172±0.003) with depth. This suggests a homogeneous mixing of mine-derived particles and pre-industrialsediments with minor inputs of anthropogenic Pb. Lead concentrations in roots of plants from the two marshes were higher than inleaves and stems, indicating limited transfer of Pb to aerial parts. A similar Pb isotopic signature was found in roots and invegetated sediments, indicating that Pb uptake by plants reflects the input in sediments as determined by a significantanthropogenic contribution of Pb at Tagus and by mineralogical Pb phases at Guadiana. The accumulation in roots from Tagusmarsh (max. 2870 μg g−1 in S. fruticosa and max. 1755 μg g−1 in S. maritima) clearly points to the dominant role of belowgroundbiomass in the cycling of anthropogenic Pb. The fraction of anthropogenic Pb in belowground biomass was estimated based on thesignature of anthropogenic Pb components in sediments (206Pb/207Pb=1.154). Since no differences exist between Pb signature inroots and upper sediments, the background and anthropogenic levels of Pb in roots were estimated. Interestingly, both backgroundand anthropogenic Pb in roots exhibited a maximum at the same depth, although the proportion of anthropogenic Pb was relativelyconstant with depth (83±4% for S. fruticosa and 74±8% for S. maritima).© 2006 Elsevier B.V. All rights reserved.

Keywords: Lead; Stable lead isotopes; Salt marsh; Roots

1. Introduction

Salt marsh vegetation traps suspended particulatematter and associated metals transported by tidalcurrents. The metal uptake by marsh plants appears to

⁎ Corresponding author. Tel.: +351 2130227070; fax:+351213015948.

E-mail address: cvale@ipimar.pt (R. Cesário Carlos Vale).

0048-9697/$ - see front matter © 2006 Elsevier B.V. All rights reserved.doi:10.1016/j.scitotenv.2006.11.026

be primarily influenced by the capacity of roots tooxidise sediments in their vicinity (Clothier and Green,1997; Sundby et al., 2005). The excess of oxygen that istransported to roots and not consumed during respirationdiffuses into the surrounding sediment and oxidisesreduced components of both solid sediment and porewater (Haines and Duun, 1985). The oxidation of highlyinsoluble sulphides renders the metals soluble andavailable to roots (Caçador et al., 2000; Sundby et al.,

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2003). These modifications may vary in time with theplant activity, changing the Pb partitioning in therizosphere (Sundby et al., 2005). When roots deliveroxygen, lead-bearing solid phases are oxidised andrelease Pb to pore water. This Pb becomes potentiallyavailable for uptake by plants. As oxygen flux tosediment decreases Pb is again immobilised, possibly assulphide or associated with iron sulphide phases.

In the past, most of the understanding of Pb uptake byplants relied on concentration measurements (eg. Zwols-man et al., 1993; Caçador et al., 1996; Weis et al., 2002;Fitzgerald et al., 2003; Velde et al., 2003; Almeida et al.,2004; Deng et al., 2004, 2006). Stable Pb isotopes provideindications of Pb sources. The isotopic composition ofcontaminant Pb and natural Pb generally differs and it isseldom affected by kinetic processes (Gobeil et al., 2001).Lead has four stable isotopes: 204Pb, 206Pb, 207Pb and208Pb. The last three are final end-members of the 238U,

Fig. 1. Location of salt marsh areas in

235U and 232Th decay chains. The Pb isotope ratios varywith the anthropogenic emissions due to the variety oflead ores used to produce lead additives in gasoline, coalburning and industrial activities (Cundy et al., 1997;Alleman et al., 2000; Bollhofer and Rosman, 2001).

Stable Pb isotopes have been studied in severalmarshes (Cundy et al., 1997; Hoven et al., 1999;Marcantónio et al., 1999; Alfonso et al., 2001; Kim etal., 2004). Differences or parallelism between sedimentsand roots have not been examined as yet, despite theevidence that plants play a considerable role on Pbcycling in marshes (Sundby et al., 2005). This paperpresents total Pb concentration and stable Pb isotoperatios in leaves, stem and roots of Sacorconia fruticosaand Spartina maritima and sediments from two saltmarshes with industrial and mining influences. Theeffect of plant activity on the historical record of the totalPb profile and on Pb isotopic signature was examined.

Tagus and Guadiana estuaries.

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2. Materials and methods

2.1. Study areas

The study sites are located in two major estuaries(Tagus and Guadiana) of the southern Iberian Peninsula(Fig. 1). Both estuaries are mesotidal systems, wheretidal water inundates large extensions of salt marshes ona semidiurnal scale. The Tagus marsh (Rosário) iscolonised by S. fruticosa, Halimione portulacoides andS. maritima. Sediments incorporate large quantities ofanthropogenic metals from nearby industries and urbanareas (Caçador et al., 1993, 1996; Sundby et al., 1998).The Guadiana marsh (Castro Marim) is dominated by S.fruticosa, Zostera maritima and S. maritima. Sedimentcomposition appeared not influenced by chemicalindustrial emissions (Fonseca et al., 2001; Caetano etal., 2006). The river crosses the Iberian Pyrite Belt, amassive sulphide deposit that has been mined since theRoman Age (Palanques et al., 1995; Leistel et al., 1998).

2.2. Sampling

Pure stands of S. fruticosa and S. maritima weresampled in 2004 at the Tagus and Guadiana salt marshes(Fig. 1). Aboveground parts were removed at groundlevel and stored in plastic bags. Sediment cores werecollected from vegetated and non-vegetated areas ateach site and sliced in layers of 2–5 cm thickness. At thelaboratory leaves and stems were washed with ultra pureMilli-Q water (18.2 MΩ) to remove dust and sediment,oven dried at 40 °C and ground with an agate mortar.The belowground material of each layer was separatedfrom the sediment carefully under a flux of water using a212 μm mesh size sieve to remove any adheringparticulate matter. Sediments and roots were oven driedat 40 °C, weighed to determine belowground biomass(Gross et al., 1991; Caçador et al., 1999) andhomogenised with an agate mortar for further analysis.

3. Methods

Sediment samples (≈100 mg) were mineralizedcompletely with 6 cm3 of HF (40%) and 1 cm3 of AquaRegia (HCl-36%: HNO3-60%; 3:1) in closed Teflonbombs at 100 °C during 1 h. Subsequently the bombcontents were evaporated to near dryness in Teflonvials (DigiPrep HotBlock— SCP Science) redissolvedwith 1 cm3 of double-distilled HNO3 and 5 cm3 ofMilli-Q water (18.2 MΩ), heated for 20 min at 75 °Cand diluted to 50 cm3 with Milli-Q water. Plant material(≈200 mg) was digested with a mixture of HNO3

(60%) and H2O2 (30%) in open Teflon bombs at 60 °Cfor 12 h and at 100 °C for 1 h with the Teflon bombsclosed. Two procedural blanks were prepared using thesame analytical procedure and reagents, and includedwithin each batch of 20 samples. Total Pb concentrationand stable Pb isotopes (206Pb, 207Pb and 208Pb) weredetermined in the same samples but in separate runsusing a quadropole ICP-MS (Thermo Elemental, X-Series) equipped with a Peltier Impact bead spraychamber and a concentric Meinhard nebulizer. Theexperimental parameters were: forward power=790W;peak jumping mode; 150 sweeps per replicate; dwelltime=10 ms; dead time=30 ns. A 7-points calibrationwithin a range of 1 to 100 μg.L−1 was used to quantifytotal Pb concentration. The precision and accuracy ofthe Pb concentration measurements, determinedthrough repeated analysis of references materials(MESS-2, PACS-2 and MAG-1 for sediments andBCR-60 and BCR-61 for plant material) using In asinternal standard, were 1–4% and 2–5%, respectively.Procedural blanks always accounted for less than 1% ofthe total lead in the samples. For Pb isotopedeterminations, between every two samples, correc-tions for mass fractionation were applied using NISTSRM 981 reference material. The Pb isotopic compo-sition of procedural blanks did not influence signifi-cantly the 206Pb/207Pb and 206Pb/208Pb ratios measuredin both the sediment and plant samples. The coeffi-cients of variation of the NIST SRM 981 referencematerial obtained in between-batch external qualitycontrol were 0.37% for 206Pb/207Pb and 0.22% for206Pb/208Pb ratios.

4. Results and discussion

4.1. Belowground biomass

Plants from the Tagus marsh showed higherbelowground biomass than from Guadiana marsh,particularly S. maritima (Fig. 2). This difference,which usually reflects adaptive responses of plants tothe environment (Groenendijk and Vink-Lieavaart,1987), may indicate intense competition for nutrientsin Tagus marshes. In this marsh belowground biomassof each plant was relatively uniform in the first 20-cmdepth, while in Guadiana it showed a maximum.

4.2. Lead in non-vegetated sediments

Sediments of the two marshes consisted of abundantfine grain material. Aluminium concentration rangedfrom 8.2 to 10.7% while loss on ignition was 5±1.1%.

Fig. 2. Depth profiles of root biomass (g m−2) in sediments colonized by S. fruticosa and S. maritima from Tagus and Guadiana marshes.

Fig. 3. Depth profiles of Pb concentrations (μg g−1) in non-vegetatedsediments from Tagus and Guadiana marshes.

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No macrofauna were found in the collected sediments.Lower and uniform concentrations at Guadiana sedi-ments (Fig. 3) reflect the lack of Pb contamination as aresult of low industrial activities in the drainage basin(Chícharo et al., 2001). The Tagus marsh sedimentpresented a pronounced increase of Pb concentration inthe upper 10-cm (max. 255 μg.g−1) reflecting dis-charges of local industries (Vale, 1990; Caçador et al.,1996).

4.3. Lead in above- and belowground biomass

Partitioning of lead in plants from the two marshesshowed the same pattern: concentrations in below-ground biomass (21–2870 μg g−1 for Tagus and 18–62 μg g−1 for Guadiana) were up to three orders ofmagnitude higher than levels in aboveground parts(1.3–1.7 μg g−1 and 0.09–0.76 μg g−1, respectively).This contrast suggests that either only small amounts ofthe Pb were translocated from roots and accumulated inaerial plant parts, or the translocated metals were notretained in stem and leaves. Levels of Pb werecomparable in leaves and stems of both S. fruticosaand S. maritima, which could be interpreted as no

preferential accumulation in the aboveground tissues.Yet, release from photosynthetic tissues in leaves shouldnot be excluded (Whidham et al., 2003). Similar

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partitioning patterns have been observed for other tracemetals in halophyte plants (Fitzgerald et al., 2003;MacFarlane et al., 2003).

4.4. Lead profiles in vegetated sediment and below-ground biomass

Depth profiles of Pb concentration in sediments andbelowground biomass are presented in Fig. 4. Asobserved in non-vegetated areas, levels and profilesdiffered in vegetated sediments of Tagus and Guadiana.Sediments and roots from Guadiana presented lowlevels and similar intervals, 18–62 μg g−1 and 14–62 μgg−1, respectively. On the contrary, Pb concentrationsvaried within different ranges in sediments and rootsfrom the Tagus marsh. Tagus sediments showed muchhigher concentrations in the rooting zone (max. 463 μgg− 1) than at depths below roots (≈30 μg g− 1)

Fig. 4. Depth profiles of Pb concentrations (μg g−1) in sediments colonized band Guadiana marshes.

confirming previous observations of metal enrichmentin sediment between roots (Caçador et al., 1996;Caçador et al., 2000). Maximum values in rootingsediments (463 μg g−1) were almost twice the levelsregistered in the non-vegetated sediments (max. 255 μgg−1). These additional quantities have been related tothe transport of metals towards the roots, as plantuptakes water and nutrients (Clothier and Green, 1997).Besides the accumulation on roots tissue, higherquantities of metals may become subsequently associ-ated with the solid sediment (Vale et al., 2003). Rootsexhibited concentrations that were 10 times higher thanthe sediments between the roots, with a maximum of2870 μg g−1 in S. fruticosa and 1755 μg g−1 in S.maritima. In addition, concentrations increased withdepth defining vertical profiles with sub-surface max-ima. To our knowledge this is the first report of Pbconcentration profiles in roots of salt marsh plants. The

y S. fruticosa and S. maritima and in belowground biomass from Tagus

Fig. 5. Depth profiles of 206Pb/207Pb ratios in non-vegetated sedimentsfrom Tagus and Guadiana marshes. Error bars indicate standarddeviation of five replicates measurements.

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comparison between vertical profiles in sediment androots points to the dominant role of the belowgroundbiomass in Pb cycling at Tagus marsh. Changes in thedissolution-precipitation cycle of Pb induced by rootactivity contribute to the enrichment in roots and thehigher retention at sub-surface layers (Sundby et al.,2005). These elevated accumulations were foundalthough S. fruticosa and S. maritima are not consideredto be hyperaccumulator plants (Weis and Weis, 2004).

Fig. 6. Depth profiles of 206Pb/207Pb ratios in sediments colonized by S. frutiError bars are presented as standard deviation of five replicates measuremen

These results are in line with a previous study(Sundby et al., 2005) that pointed to the mobility of Pbafter being buried in salt marsh sediments. A simplecalculation based on seasonal variation of belowgroundbiomass (Caçador et al., 2000) and Pb concentration inroots and sediments indicates that as much as twentypercent of the total mass of Pb in root biomass exchangedannually with the sediment (Sundby et al., 2005). Theelevated accumulation of Pb in roots and the quantityexchanged annually between roots and sediments raisesthe question whether contamination in salt marshes withhigh belowground biomass is effectively stabilised.

4.5. Signature of Pb isotopes in non-vegetated sediments

The 206Pb/207Pb and 206Pb/208Pb ratios along non-vegetated sediments from Tagus decreased towards thesurface (Fig. 5) as typically observed in marine sediments(Gobeil et al., 2001). The upper 13-cm sedimentscontained Pb with lower radiogenic signature (1.163–1.166) increasing gradually until 1.205 at 60-cm depth.The isotopic composition encountered in the upper layersis similar to the anthropogenic signature previously regis-tered in the same Tagus marsh (1.166–1.170) by Sundbyet al. (2005) and falls within the range observed insediments from NW Mediterranean Sea (1.158–1.174)(Ferrand et al., 1999; Alleman et al., 2000). Moreover,ratios are comparable to the isotopic signature for atmos-pheric Pb in aerosols collected in the last decade inWesternEurope (Veron et al., 1999; Bollhofer and Rosman, 2001),suggesting the mixture of high radiogenic background Pb

cosa and S. maritima and in belowground biomass from Tagus marsh.ts.

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and low radiogenic contaminant Pb emissions of alkylleadgasoline (1.06–1.09; Gobeil et al., 2001). Although localgeology may influence the 206Pb/207Pb and 206Pb/208Pbisotopic ratios, signature in deeper sediment layers iscomparable with the pre-pollution Pb signature recorded inthe NW Spain (Kylander et al., 2005) and in severalestuarine systems of France (Elbaz-Poulichet et al., 1986;Alfonso et al., 2001).

The stable isotopic signature at Guadiana marshwas uniformly constant (206Pb/207Pb=1.172±0.003,206Pb/208Pb=0.466±0.001) with depth (Fig. 5) and closeto that of sulphide deposits from the Iberian Pyrite Belt(1.162–1.164; Marcoux, 1998; Pomies et al., 1998). Thefact that the Guadiana River crosses this Belt, which hasbeen mined in the past centuries (Palanques et al., 1995;Leistel et al., 1998), should greatly influence the Pb isotopicsignature of the transported particles and consequently thesalt marsh sediment. Thus, the values found in the sedimentcolumn reflect a homogeneous mixing of mine-derivedparticles and pre-industrial sediments with minor inputs ofanthropogenic Pb.

4.6. Signature of Pb isotopes in vegetated sedimentsand belowground biomass

The depth variation of 206Pb/207Pb ratios in vegetatedsediments fromTagusmarsh (Fig. 6) also presented a lowerradiogenic Pb signature in upper layers followed by amixing zone and higher Pb isotope ratios in deeper sedi-ments. However, the thickness of the sediment layer con-taining lower radiogenic Pb signature (206Pb/207Pb=1.160–1.167) differed between plant species (0–37 cmfor S. fruticosa and 0–16 cm for S. maritima). Thesealterations are presumably attributed to different root-

Fig. 7. Depth profiles of background and anthropogenic Pb concentrationsmarsh.

sediment interactions, since the two species were collectedclose by (b1 m) and sedimentation rate is unlikely tochange in such a short distance. It is expected that the finersize of S. fruticosa roots, and consequently higher specificarea, promoted intensive exchanges within the rhizosphere.The thicker layer of anthropogenic Pb signature observed invegetated sedimentsmay result fromPbmigration as plantstake up water and solutes (Sundby et al., 2005). Con-sequently Pb isotope ratios might have been modified andthus would provide erroneous information on chronologyof Pb pollution.Onemay therefore conclude that Pb isotopesignature in salt marshes is not a reliable measure for chro-nology records. Depth profiles of Pb isotope ratios in twocolonized sediments at Guadiana's marsh were relativelyconstant in both plants: 206Pb/207Pb=1.179±0.003 forS. maritima and 206Pb/207Pb=1.178±0.002 for S. fruti-cosa. It appears that Pb isotopic ratios mirror mainly themixing of pre-industrial sediments with mining derivedparticles in the sediment column.

Lead Pb isotopic signatures in roots and sedimentswere similar (Fig. 6) suggesting that Pb uptake reflects themixture existent in sediments: contribution of anthropo-genic Pb at Tagus and Pb mineralogical Pb phases atGuadiana. This means that roots extract anthropogenic Pbexisting in the sediments, but most surprisingly roots wereable to remove Pb from mineralogical phases. To ourknowledge these are the first results reporting the ability ofsalt marsh plants to extract geogenic Pb from sediments.

4.7. Estimation of background and anthropogenic Pbaccumulated in roots

Asignificant linear correlation between the 206Pb/207Pband the 206Pb/208Pb ratios in sediment samples fromTagus

in belowground biomass of S. fruticosa and S. maritima from Tagus

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marshwas found (r=0.975;pb0.001). This trend suggeststhat Pb in sediments can be described as a mixture ofbackground Pb and anthropogenic Pb from varioussources (Ferrand et al., 1999; Marcantonio et al., 1999).Such a linear relationshipwas not found forGuadiana onceisotopic ratios were relatively constant. The 206Pb/207Pbratio of the anthropogenic Pb components in Tagussediments can be determined using the mixing modelproposed by Ferrand et al. (1999). This involvesextrapolating the value of the 206Pb/207Pb ratio for 1/Pb=0 (r=0.920; pb0.001). This yielded a 206Pb/207Pbratio of 1.154±0.006 for the bulk anthropogenic compo-nent composed of Pb fromvarious sources. This value wasnot statistically different from the one obtained by Sundbyet al. (2005) in sediments from the Tagus estuary.However, higher Pb concentrations found in our workallowed a better definition of the X-axis intercept. Thefraction x of anthropogenic Pb in each root layer can becalculated by applying the following equation (Sundbyet al, 2005):

206Pb=207PbðsampleÞ ¼ x206Pb=207PbðanthropÞþ ð1−xÞ206Pb=207PbðbkgÞ

where 206Pb/207Pb(anthrop)=1.154 and 206Pb/207Pb(bkg)=1.204. Since no statistical differences exist betweenPb signature in roots and upper sediments (Fig. 6) onemayestimate the background and anthropogenic levels of Pb inroots. In the two analysed plants the anthropogenic con-centrations reached 2443μg g−1 (Fig. 7) greatly exceedingbackground levels (max. 456 μg g−1). Interestingly, bothbackground and anthropogenic Pb in roots exhibited amaximum at the same depth, but the proportion of an-thropogenic Pb is relatively constant with depth (83±4%for S. fruticosa and 74±8% for S. maritima). These depthvariations indicate that salt marsh plants extract back-ground levels of Pb corroborating the conclusions foundfor the Guadiana system.

5. Conclusions

This study pointed out that roots of salt marsh plantsaccumulate higher concentrations of Pb than surroundingsediments. However, roots uptake varied with depth. ThePb isotopic signature in sediment layers and correspondingroots was similar, indicating that uptake reflects themixingof anthropogenic and background Pb in sediments. As aresult of intense root-sediment interactions depth profilesof 206Pb/207Pb in salt marsh sediments are greatlymodified, and thus do not anymore reflect chronology ofPb pollution.

Acknowledgments

This work was funded by the QCAIII Project: MARE22–05–01-FEDER-00005. The authors wish to thankthe colleagues Marta Martins and Hilda de Pablo for thefield work and technical assistance. The manuscript hasbenefited greatly from the reviews of the anonymousreferees and the comments of the editor.

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