Marine Pollution Bulletin 87 (2014) 104–116

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Marine Pollution Bulletin

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History of bioavailable lead and iron in the Greater North Seaand Iceland during the last millennium – A bivalvesclerochronological reconstruction

http://dx.doi.org/10.1016/j.marpolbul.2014.08.0050025-326X/� 2014 Elsevier Ltd. All rights reserved.

⇑ Corresponding author.

Hilmar A. Holland a,⇑, Bernd R. Schöne a, Soraya Marali a, Klaus P. Jochum b

a Institute of Geosciences, University of Mainz, Johann-Joachim-Becher-Weg 21, 55128 Mainz, Germanyb Max Planck Institute for Chemistry, P.O. Box 3060, 55020 Mainz, Germany

a r t i c l e i n f o a b s t r a c t

Article history:Available online 28 August 2014

Keywords:LeadIronEutrophicationRedox potentialAnthropogenic pollutionRetrospective environmental biomonitoring

We present the first annually resolved record of biologically available Pb and Fe in the Greater North Seaand Iceland during 1040–2004 AD based on shells of the long-lived marine bivalve Arctica islandica. Theiron content in pre-industrial shells from the North Sea largely remained below the detection limit. Onlysince 1830, shell Fe levels rose gradually reflecting the combined effect of increased terrestrial runoff ofiron-bearing sediments and eutrophication. Although the lead gasoline peak of the 20th century was wellrecorded by the shells, bivalves that lived during the medieval heyday of metallurgy showed four-foldhigher shell Pb levels than modern specimens. Presumably, pre-industrial bivalves were offered largerproportions of resuspended (Pb-enriched) organics, whereas modern specimens receive fresh increasedamounts of (Pb-depleted) phytoplankton. As expected, metal loads in the shells from Iceland were muchlower. Our study confirms that bivalve shells provide a powerful tool for retrospective environmentalbiomonitoring.

� 2014 Elsevier Ltd. All rights reserved.

1. Introduction

As a marginal sea bordered by the most densely populated andhighly industrialized countries, the North Sea is severely impactedby human activities (Weichart, 1973). Aside from overfishing, oiland gas exploitation, modification of the sea floor by dredging, bot-tom trawling, and removal of sand and gravel, pollution constitutesa major threat to the biota inhabiting the North Sea. Main sourcesof organic (e.g., PCB, PAH, DDT) and inorganic contaminants (heavymetals, radionuclides, REEs) include rivers, coastal industries,dumping and the atmosphere (Schlünzen et al., 1997). Some ofthese pollutants are water-soluble and can directly deterioratethe water quality (OSPAR, 2000, 2009b), whereas others accumu-late in the sediment. Remobilization of such substances occursduring changes in the biological activity in the water column, inthe sediment or near the sediment surface (e.g., enhanced down-ward transport of organic matter following phytoplankton blooms,increased rates of bioturbation, etc.) and associated changes in pHand DO and can result in secondary pollution effects (Kersten,1988; Kersten et al., 1994).

To determine baseline levels of biologically available contami-nants in the North Sea prior to intensified human perturbation,

distinguish natural from anthropogenic environmental distur-bances, and identify periods of intensified remobilization ofpotentially harmful substances at the sea floor, it is crucial toknow how pollutant levels changed through time. Such informa-tion is indispensable for management purposes and predictingfuture threads of anthropogenic pollution. For this purpose,numerous sediment cores have been retrieved from various local-ities in the North Sea during the last decades (Förstner andReineck, 1974; Behre et al., 1985; Irion and Müller, 1990; Irion,1993). Results clearly indicate rising heavy metal loads towardmore recently deposited strata. The major disadvantage of sedi-mentary deposits, however, is poor temporal resolution and dat-ing control. Bioturbation results in significant time-averagingand obscures short-term cycles. Furthermore, continuous andundisturbed sediment records are absent in large parts of theNorth Sea as a result of repeated sediment reworking and resed-imentation in these shallow-water settings (Kersten et al., 1988;Irion and Müller, 1990; Irion, 1993). Many records only coverthe last one or two centuries or so (Förstner and Reineck, 1974;Behre et al., 1985; Irion, 1993). In addition, sediment recordsalone can barely provide information on levels of biologicallyavailable contaminants close to the sediment water interfacewhere many benthic organisms are dwelling. Such data is partic-ularly relevant from ecotoxicological perspective.

H.A. Holland et al. / Marine Pollution Bulletin 87 (2014) 104–116 105

Skeletal hard parts of animals, in particular bivalve mollusks,serve as powerful archives of pollution. Shells of bivalves grow byperiodic accretion of calcium carbonate and contain distinct annualand daily growth lines and increments (portions between consecu-tive growth lines). These growth patterns can be used to temporallycontextualize each shell portion. If the date of death, and thus thedate of the last shell formation is known, a precise calendar datecan be assigned to each growth increment. Changes in the physico-chemical environment are recorded in the shell in the form of var-iable growth increment widths and chemical properties. Forexample, oxygen isotope values (d18O) can provide informationon ambient water temperature during shell formation. Likewise,increased heavy metal loads in the water are reflected in elevatedlevels of these elements in the shells (e.g., Carriker et al., 1982;Price and Pearce, 1997; Richardson et al., 2001; Gillikin et al.,2005; Liehr et al., 2005; Pearce and Mann, 2006). Respective valuesin fossil shells have previously been used to determine heavy metalloads in the environment prior to major anthropogenic disturbance(e.g., Bourgoin and Risk, 1987; Pitts and Wallace, 1994), but suchstudies only provided snapshots into the climatic past lacking abso-lute temporal alignment of the data. Gillikin et al. (2005) presentedthe first, well-dated, long-term (53-year) record of lead contamina-tion off the coast of North Carolina, USA, based on eleven contem-poraneous shells of Mercenaria mercenaria. Despite differences inPb/Ca ratios among contemporaneous specimens, the increasinguse of leaded gasoline during the 1970s was clearly recorded bythe shells. Krause-Nehring et al. (2012) analyzed the Pb/Ca historyin the North Sea, Iceland and off the coast of Virginia between thelate 18th century and modern times based on LA-ICP-MS (laserablation – inductively coupled plasma – mass spectrometry) analy-sis of three shells of Arctica islandica, a species that can live forseveral hundred years (Schöne et al., 2005a; Butler et al., 2013).While the shells from the North Sea and the US coast confirmedthe findings by Gillikin et al. (2005), the shell from Iceland, a muchless polluted habitat, showed significantly lower Pb/Ca ratios.

Since shell growth is governed to a large degree by environmen-tal variables, growth curves (or so-called sclerochronologies) ofcontemporaneous specimens show similar patterns. By stringingtogether increment chronologies based on synchronous changesin interannual shell growth (cross-dating) it is possible to constructa stacked sclerochronology covering centuries to millennia andmany generations of bivalves, a method very similar to dendro-chronology (e.g., Witbaard et al., 1997; Butler et al., 2013; Loh-mann and Schöne, 2013). In combination with heavy metal dataof the shells, cross-dating can open new avenues in retrospectiveenvironmental biomonitoring (Gillikin et al., 2005).

Here, we present the first high-resolution, multi-regional heavymetal record of the North Sea covering the last millennium. Thefocus of this study is on Pb/Ca and Fe/Ca ratios. Specifically, westudied (1) how Pb/Ca and Fe/Ca levels fluctuated through time(focus on interannual and lower time-scales) and space, (2) howthese element levels varied among contemporaneous specimensfrom the same habitat and (3) to what degree diagenesis and bio-logical factors may have obscured the data. Contrary to existingstudies of this kind in which the metal load in discrete shell por-tions was determined (discrete spot analysis), we employed theso-called line-scan method that enabled us to obtain uninterruptedheavy metal chronologies from each shell. We will demonstratethe advantage of this method for shell-based retrospective envi-ronmental monitoring.

1.1. Anthropogenically emitted Pb and Fe in the ocean, transportmechanisms

In modern, industrial times, a significant portion of Pb in theocean is derived from the combustion of leaded gasoline. For

example, in the North Sea, Pb from atmospheric emissionsaccounts for up to ca. 70% of the total lead input (Irion andMüller, 1987; Duce, 1991; Schlünzen et al., 1997; Irion, 1993;Injuk et al., 1998). Among other organic substances, tetraethyl leadhas been added to gasoline as an antiknock agent which reacts tohighly volatile Pb chlorides and Pb bromides during combustionthat are emitted to the atmosphere as aerosols. This resulted in asignificant increase in Pb fluxes to the oceans between 1923 andthe 1980s (e.g., Schaule and Patterson, 1981; Flegal andPatterson, 1983; Nriagu, 1990; Wu and Boyle, 1997; Hoffmanet al., 2003). In preindustrial times, however, lead was mostlyreleased to the environment during mining and smelting (Settleand Patterson, 1980; Nriagu, 1983; Hong et al., 1994; de Calataÿ,2005). As indicated by peat bogs from England, for example, atmo-spheric lead pollution reached an all-time maximum at ca. 1200and was excessively high between 1150 and 1500 (Le Roux et al.,2004). Whereas particulate lead is transported through rivers andaccumulates in the sediment (Balls, 1985; Irion, 1993), lead fromatmospheric emissions becomes soluble in surface waters and isre-adsorbed to biological particles (Wu and Boyle, 1997) whichsink to the sea floor and can be ingested and digested by benthicorganisms (e.g., Kröncke, 1987; Prosi, 1989; Fisher et al., 1996;Darriba and Sánchez-Marín, 2013). Pb is toxic to most organisms(e.g., Eisler, 1988; WHO, 2000; Verma and Dubey, 2003), inter aliabecause it mimics other biologically essential metals (substitutionof Ca2+, Mg2+, Fe2+, Zn2+, and Na+; Lidsky and Schneider, 2003; Floraet al., 2012).

The main iron contributors are hyper-arid terrestrial areas,anthropogenic and volcanic sources (Jickells et al., 2005). Anthro-pogenically released iron largely comes from combustion, (coal)mining and smelting activities (e.g., Tiwary and Dhar, 1994;Vuori, 1995; Rösner, 1997; Chuang et al., 2005; Guieu et al.,2005). The majority of iron reaches coastal and shelf waters inthe form of insoluble iron oxides (detrital iron, e.g., goethite)through riverine input and, to a lesser extent, through the atmo-sphere in the form of aerosols (e.g., mineral dust particles; Duceand Tindale, 1991; Wells et al., 1995; Jickells et al., 2005; Spolaoret al., 2013). The latter react with surface waters and releasewater-soluble FeII which is more bioavailable than FeIII (Shakedet al., 2005; Baker and Croot, 2010; Spolaor et al., 2013). Dissolvediron is an essential and limiting nutrient for marine phytoplanktonthat stimulates primary productivity (e.g., Martin and Fitzwater,1988; Boyd et al., 2007; Smetacek et al., 2012). However, it is read-ily oxidized to FeIII. Residence times for dissolved iron in oxygen-ated water are on the order of several hours (Salomons andFörstner, 1984; Dehairs et al., 1989; Millero and Sotolongo, 1989;González-Dávila et al., 2006; Baker and Croot, 2010) to nearly threeyears (de Jong et al., 2007). Due to their poor solubility, detritaliron (III) oxides sink to the sea floor where they become incorpo-rated into the sediment (Wells et al., 1995; Shaked et al., 2005;Baker and Croot, 2010; Spolaor et al., 2013). When reducing condi-tions prevail in the sediment or near the sediment surface, FeIII canbe converted to the water-soluble, biologically available form.

2. Material and methods

Fourteen shells of A. islandica were collected in the Greater NorthSea (Dogger Bank, German Bight, Norwegian Sea) and NE Iceland(Fig. 1; Table 1). One specimen from the Dogger Bank and GermanBight and the two specimens from Iceland were collected alive, theremaining ten shells were single subfossil valves. One specimen(ICE14-A01L) was collected by scuba diving; all other shells wereobtained by dredging (Table 1). To identify possible effects of waterdepth and substrate type, a broad range of shells from differentsettings were analyzed. Shells from a supposedly pristine habitat

Fig. 1. Map showing sampling regions of Arctica islandica in the North Sea andIceland. (A) Overview map. Open rectangles in (B) and open circle in (C) refer to thespecific localities where shells were collected. In addition, major current systemsare depicted. Maps are based on Turrell (1992) and Turrell et al. (1992) and theIcelandic Marine Research Institute.

106 H.A. Holland et al. / Marine Pollution Bulletin 87 (2014) 104–116

(Iceland) were contrasted to specimens from more pollutedsettings (Greater North Sea). All shells consisted of aragonite(Feigl test) and were largely diagenetically unaltered (CL, SEM).Only the chalky rims of some fossil specimens were enriched insome trace elements (Pb, Fe, Mn, U and S) indicative of diageneticalteration (Sturesson, 1976; Carriker et al., 1991; Kaufman et al.,

Table 1List of specimens of A. islandica used in the present study. Group acronyms stand for NorwD), shallower settings of the Dogger Bank (DOG-S) and Iceland (ICE). Radiocarbon dates (Lcalib/) assuming published marine reservoir correction (DR) values of 20 ± 42 and 14 ± 55 ysee Holland et al. (2014).

Group Sample ID Locality Water Depth Ont

(dead (D)/ alive (A)) (m)

WH241-604-BoxL-D8L 58�43.68’N, 2�39.35’E 113

WH241-611-BoxL-D1L 58�28.81’N, 2�18.29’E 113

WH241-615-BoxL-D5R 58�41.54’N, 2�37.57’E 110

WH241-617-BoxL-D6L 58�45.22’N, 2�35.46’E 112

WH241-572-RA6-A1R 54�45.83’N, 7�16,37’E 27

2011-WH-DOGT-7-KU-D1R 54�48.91’N, 1�26.22’E 66-70

2011-WH-DOGT-T4KU-A11L 55�34.21’N, 2�20.10’E 64-69

2011-DOGU-5-RD-D1L 54�37.28’N, 1�41.59’E 24

2011-DOGT-22-KU-D1L 54�46.83’N, 2�33.06’E 21

DOG-K9-KU-D1L 54�59.70’N, 1�40.00’E 26-30

DOG-K36-KU-D1L 55�18.87’N, 3�18.57’E 29

DOG-K39-KU-D1L 55�28.71’N, 3�59.25’E 31-32

ICE14-A01L 66�11.48’N, 15�20.42’W 10-11

M�ller-A9L 66�11.46’N, 15�20.56’W 31-33

NORS

GER

DOG-D

DOG-S

ICE

1996; Jiménez-Berrocoso et al., 2004; Gillikin et al., 2005a; Zhang,2009).

2.1. Temporal alignment

Since the dates of death of live-collected specimens wereknown, it was possible to assign precise calendar dates to each por-tion of these shells. Shells from dead collected specimens weretemporally contextualized by 14CAMS dating of umbonal shell por-tions and the cross-dating technique. For details on the temporalalignment, the reader is referred to Holland et al. (2014) in whichthe construction of a millennial-scale, multi-regional North Seastacked sclerochronology is presented. In the present paper, someof the temporally aligned specimens from that study were used.

2.2. Preparation of shell slabs

Soft tissues of live-collected specimens were removed immedi-ately after collection. One valve of each specimen (‘‘L’’ and ‘‘R’’ inTable 1 denote left and right valve, respectively) was mountedon a plexiglass cube. To protect the fragile shell material duringsawing, a thin layer of epoxy resin (JB KWIK) was applied to theshell surface along the axis of maximum growth. On that axis,two three-mm-thick sections were cut from the shells using alow-speed precision saw (Buehler Isomet 1000) equipped with awafering-thin diamond-coated blade. Subsequently, slabs weremounted on glass slides, rinsed in deionized water and the surfacesground on glass plates (800, 1200 grit SiC powder) and polishedwith 1 lm Al2O3 powder on a Buehler G-cloth. After each prepara-tion step, samples were ultrasonically rinsed with deionized waterto remove adhering particles. One thick-section of each specimenwas used for growth pattern analysis and immersed in Mutvei’ssolution (Schöne et al., 2005b), whereas the remaining slab wasused for geochemical analyses.

2.3. LA-ICP-MS analysis

Trace element concentrations were measured on polished cross-sections with a Thermo-Finnigan Element2 sector-field ICP-MS

egian Sea (NORS), German Bight (GER), deeper settings of the Dogger Bank (Dogger-ibby years) were calibrated with the software tool CALIB 5.0.2 (http://calib.qub.ac.uk/ears (Mangerud and Gulliksen, 1975; Harkness, 1983), respectively. For further details

ogenetic Collected -calibratedLA-ICP-

MS

age dead/ alive calendar year Temporal # samples Date of

(cal yr AD) coverage (AD) measurement

81 (D) 2002 1180-1420 1284-1327 1005 02 Oct 2012

151 (D) 2002 1647-recent 1741-1871 920 02 Oct 2012

152 (D) 2002 1652-recent 1830-1920 926 02 Oct 2012

189 (D) 2002 1325-1588 1376-1522 1215 02 Oct 2012

112 (A) 2002 1894-1996 1326 07 Nov 2011

124 (D) 2011 1400-1519 1362 02 Oct 2012

100 (A) 2011 1936-2004 417 01 Oct 2012

134 (D) 2011 1858-1979 1310 01 Oct 2012

115 (D) 2011 1441-1535 918 02 Oct 2012

115 (D) 2003 1171-1259 1136 02 Oct 2012

172 (D) 2003 1043-1198 1268 02 Oct 2012

102 (D) 2003 1390-1476 944 02 Oct 2012

78 (A) 2012 1847-2010 1400 02 Oct 2012

178 (A) 2003 1925-1999 1268 07 Nov 2011

H.A. Holland et al. / Marine Pollution Bulletin 87 (2014) 104–116 107

coupled to a New Wave UP-213 Nd:YAG laser ablation system(213 nm wavelength, 5 ns pulse length; Jochum et al., 2007, 2012).Laser ablation measurements were conducted in the hinge plate ofthe shells. The crater diameter of individual layer spots measured55 lm. The energy density was 15.8 J/cm2. Helium was used as aninitial carrier gas. Prior to its arrival at the plasma torch, the initialgas was mixed with Argon as a secondary carrier (Jochum et al.,2007, 2012). In order to obtain an uninterrupted chronology, the linescan method (Schöne et al., 2011) was employed instead of measur-ing the element levels at discrete LA spots. Measurements were con-ducted with constant laser propulsion of 5 lm/s. Tracks werepositioned perpendicularly to the growth lines along the axis ofmaximum growth (Fig. 2). The length of the tracks, and thus thenumber of data points per track varied as a function of ontogeneticage of the specimens, curvature of the hinge and the relative rigidityof the laser line segments (Table 1).

The synthetic silicate glass NIST SRM 612 was used as externalstandard (Jochum et al., 2011) and 43Ca as internal element stan-dard. The Ca content of the shell carbonate of this species was esti-mated to equal 38 wt% based on previous ICP-OES analyses(Schöne et al., 2011). Up to 46 different elements were measured,but only iron and lead (measured as 57Fe and 208Pb) and some ofthe U, Mn, S, Sr and Mg data (measured as 238U, 55Mn, 34S, 86Srand 26Mg, respectively) are reported in the present study. Calibra-tion of the measurements, subtraction of the blanks and conver-sion of raw data from counts per second (cps) to molar ratios(mmol/mol for Fe/Ca and lmol/mol for Pb/Ca) was conducted withMicrosoft Excel. Limits of detection (LODs) were given as 3 stan-dard deviations of the blank measurements. Since analyses wereperformed on three different days (Table 1), background signalsand detection limits slightly varied during the different measure-ment campaigns (Table 1). LODs ranged from 0.01 to 0.06 mmol/mol in the case of Fe/Ca and 1.04 � 10�2 to 4.42 � 10�3 lmol/mol in the case of Pb/Ca. In Figs. 5 and 6, the maximum LODs areplotted. Discrete element/Ca peaks exceeding four standard devia-tions were considered as outliers. Uncertainties of reproducibility,given as relative standard deviations in percent (RSD%; 2r), werecomputed from repeated measurements of the NIST glass standardand equaled ca. 5% for Pb and ca. 38% for Fe. Average RSD% for U,Mn, S, Sr, and Mg were 5%, 2%, 36%, 5% and 3%, respectively. Thelarge precision error for Fe results from inhomogeneities of thestandard (Eggins and Shelley, 2002; Jochum et al., 2011) and itsextremely low iron concentration.

2.4. LA-ICP-MS data handling

For each specimen and element, several hundred individualdata points were obtained. The precise temporal alignment of

Fig. 2. (A) Mutvei-stained shell slice of Arctica islandica illustrating daily microgrowthreferred to as microgrowth increments. (B) Seaosonal growth curve based on daily microis highlighted by a cubic smoothing spline (smoothing parameter = 0.05; red dashed linreferred to the web version of this article.)

these data was accomplished through comparison with the annualgrowth patterns of Mutvei-stained shell sections (Schöne et al.,2011; Krause-Nehring et al., 2012). Annual growth incrementwidth measurements were completed on digitized images (NikonCoolpix 995 and Canon EOS 550D attached to Wild 3 M binocularmicroscopes) by means of the image processing software Panopea(� Peinl & Schöne).

Annual element/Ca ratios were computed as weighted averages(Table 2, Fig. 2). Since the shell of A. islandica is not growing at theexact same rate throughout the growing season, individual ele-ment/Ca data were weighted so that element levels recordedduring fast growing periods of the year were assigned lowerweights relative to slower growing shell portions. After this math-ematical conversion, it was possible to directly compare annualaverages from different years and different specimens with eachother (e.g., Figs. 3 and 4). To compute these weights (Table 2), dailyincrement widths were determined and a seasonal growth curvewas computed (Fig. 2). For details of this method, the reader isreferred to Schöne et al. (2004).

3. Results

3.1. Spatiotemporal trends of lead and iron

Shell lead-to-calcium and iron-to-calcium ratios of the fourteenspecimens of A. islandica varied through time and between locali-ties (Fig. 4). In shells from the Greater North Sea, the Pb/Ca ratiosattained ca. 0.1 lmol/mol during most studied time intervals ofthe last millennium. Between 1040 and 1180 values remained lar-gely below the detection limit. A strong increase in Pb/Ca wasobserved in specimens from shallow settings of the Dogger Bankand, in particular, the Norwegian Sea between 1180 and ca.1400, with maximum values of 0.42 lmol/mol in 1302 (Fig. 5).Also, Pb/Ca values in the Norwegian Sea were elevated betweenthe mid and late 18th century. Since the middle of the 19th cen-tury, a general Pb/Ca increase from ca. 0.01 lmol/mol (1822) to0.11 lmol/mol (2003) was observed in shells from the North Sea(Fig. 6). In the German Bight (southern North Sea), highest shellPb/Ca values were observed in the 1980s followed by a steadydecline since then (Fig. 5). In deeper settings of the Dogger Bank,however, highest levels were only reached ten years later, i.e. the1990s, and remained at that level at least until 2004 (end of themeasurements). Aside from a few isolated Pb/Ca peaks (largestvalue of ca. 0.19 lmol/mol in 1902), Pb/Ca levels in specimensfrom Iceland barely exceeded the detection limit between 1846and ca. 1900 (Figs. 5 and 6).

Other than Pb/Ca, Fe/Ca ratios remained largely below thedetection limit in all studied shells from the North Sea until ca.

patterns. Portions between consecutive microgrowth lines (black dashed lines) areincrement widths (dog = direction of growth). Long-term signal of the growth curvee). (For interpretation of the references to colour in this figure legend, the reader is

Fig. 3. (A) Pb/Ca and Fe/Ca ratios of the Arctica islandica specimen 2011-WH-DOGT-T4KU-A11L derived from LA-ICP-MS. Annual growth lines are illustrated by vertical blacklines. Note the varying number of samples per year. Precise calendar years are provided for some annual increments. (B) Hinge portion of 2011-specimen WH-DOGT-T4KU-A11L including the LA line scan. (C) Annual Pb/Ca and Fe/Ca curves after applying the weighted annual averaging method (see Table 2).

108 H.A. Holland et al. / Marine Pollution Bulletin 87 (2014) 104–116

1830. Only then, synchronously with Pb/Ca, Fe/Ca showed a strongincrease to values of ca. 0.26 mmol/mol in the mid 20th century(1965). Afterward a slight and gradual decline was observed(Fig. 6). Average Fe/Ca values between 1831 and 2004 equaled0.16 ± 0.06 mmol/mol. During the same time, Fe/Ca levels in shellsfrom the NE Icelandic shelf remained mostly below the detectionlimit. However, some erratic Fe/Ca peaks of up to 2.2 mmol/molwere identified in individual years (e.g., 1904, 1949, 1951, 1970).

Overall, annually resolved Pb/Ca chronologies were noisier thanFe/Ca time-series, i.e., the showed a greater year-to-year variance(Fig. 5). During some time intervals (e.g., the mid 13th century),interannual Pb/Ca values fluctuated by more than 100%. In general,however, Fe/Ca in shells from the North Sea changed moregradually.

Contemporaneous specimens from the same habitat oftenrecorded similar, though not exactly the same, metal-to-calciumratios (Fig. 5). For example, shells of two specimens from shallowsettings of the Dogger Bank that lived during the 15th centuryshowed nearly identical Pb/Ca and Fe/Ca curves. Likewise, two con-temporaneous specimens from the Norwegian Sea (19th century)showed nearly indistinguishable Pb/Ca values. However, Fe/Ca val-ues of the latter differed from each other by more than 1 mmol/mol.

3.2. Intra-shell element variations

Pb/Ca and Fe/Ca chronologies of the studied specimens did notexhibit common ontogenetic trends (Fig. 5). Such trends throughlifetime, however, were present in S/Ca, Mg/Ca and Sr/Ca (Fig. 4).

Pb/Ca and Fe/Ca ratios attained in shell portions formed duringyouth were mostly indistinguishable from those formed duringlater stages of life (150 years and older specimens). Only two mod-ern specimens from the Dogger Bank that lived during the mid19th and the 20th century showed significant trends through life-time in Fe/Ca ratios, but in opposing directions. In specimen 2011-DOGU-5-RD-D1R (24 m water depth), Fe/Ca gradually increasedfrom ca. 0.09 mmol/mol in 1858 to 0.31 mmol/mol in 1965(Fig. 5). The opposite trend was observed in specimen 2011-WH-DOGT-T4KU-A11L (64–69 m water depth) in which Fe/Ca gradu-ally decreased from 0.39 mmol/mol in 1937 to ca. 0.21 mmol/molin 2003 (Fig. 5).

Both metal-to-calcium values, in particular Pb/Ca, also fluctu-ated on seasonal time-scales (Fig. 3; seasonal variance of Pb/Ca = ca. 0.18 lmol/mol, Fe/Ca = 0.05 mmol/mol). Occasionally, thePb/Ca peaks exceeded the running mean by more than 100%. Thelarge majority of the highest and lowest metal-to-calcium valuesoccurred between consecutive annual growth lines (Pb/Ca oftenhalf-way between consecutive annual growth lines), but rarely felltogether with the annual growth lines (Fig. 3).

Some of the subfossil shells showed thin (<1 mm), friable andbrightened rims (Fig. 4) that were separated from the harder shellmaterial further inside the hinge plate by a sharp boundary. Theserims were bored by clionid sponges and contained strongly ele-vated concentrations of Pb, Fe, Mn, U and S (Fig. 4). Within theserims, element levels increased toward the shell surface to levelsexceeding average values measured in the remainder of the shellby up to 1000 times (Fig. 4).

Fig. 4. Annual element/Ca ratios of five Arctica islandica specimens of the present study, (A) DOG-K36-KU-D1L, (B) WH241-604-BoxL-D8L, (C) WH241-617-BoxL-D6L, (D)WH241-615-BoxL-D5R, (E) 2011-WH-DOGT-T4KU-A11L. Diagenetically altered rims and their geochemical properties are highlighted red (A–D). (For interpretation of thereferences to colour in this figure legend, the reader is referred to the web version of this article.)

H.A. Holland et al. / Marine Pollution Bulletin 87 (2014) 104–116 109

4. Discussion

According to the data from shells of the bivalve molluskA. islandica presented here, lead and iron concentrations in theGreater North Sea underwent significant changes during the lastmillennium.

4.1. Fe/Ca

A strong and gradual shell Fe/Ca increase in specimens from theGreater North Sea occurred between 1830 and the mid 20th cen-tury. Since then Fe/Ca levels slightly declined (Fig. 6). Fe data fromsediment cores of the southern North Sea show a similar trend dur-ing the last two centuries paralleling the increased processing andmobilization of iron in neighboring countries, in particular sincethe beginning of the industrial revolution (e.g., Förstner andReineck, 1974). A strong and significant correlation also existsbetween land-use changes and the shell Fe/Ca content (Fig. 7;Jickells et al., 2005). Intensified agriculture and animal husbandry(particularly in Germany, Fig. 7) not only resulted in increasedfluxes of fertilizers to the ocean, but also in an expansion of

cropland and, thus, an increased terrestrial runoff of iron oxidesto the ocean. The mid 20th century cropland maximum and subse-quent decline is well reflected in the shell Fe/Ca data (Fig. 7).

Interestingly, Dunca et al. (2009) observed a strong decline of Fein shells of A. islandica from the Swedish coast during the last150 years and hypothesized that the decline of iron foundriesmay have resulted in decreased Fe fluxes to the Skagerrak. Thisinterpretation is further supported by the data in Fig. 7. A signifi-cant reduction of cropland occurred in that region (LUGE 2) sincethe mid 19th century.

Given the rise of metallurgy in medieval times, the extremelylow shell Fe/Ca values prior to 1830 may be surprising at firstglance, but suggest that the increased amounts of Fe in the NorthSea did not result in an increase of biologically available Fe at thattime. A detailed discussion follows in Section 4.3.

The NE Icelandic shelf was apparently much less contaminatedwith heavy metals than the Greater North Sea during the last200 years, because the shells of A. islandica from that region werelargely devoid of lead and iron (Figs. 5 and 6). Based on the presentshell Fe/Ca data we cannot provide interpretations of spatial Fe/Catrends within the North Sea, largely because the precision error is

Fig. 5. Annual metal/Ca chronologies of the studied shells of Arctica islandica. (A) Bars illustrating the life span of each specimens. The temporal coverage of the LA-ICP-MSdata is given in black, the unmeasured and diagenetically altered sections are given in grey and red, respectively. (B–F) Pb/Ca chronologies. (G–K) Fe/Ca chronologies. Shellsfrom different localities are color-coded. GER = German Bight (B&G), DOG-S = shallow settings of the Dogger Bank (C&H), DOG-D = deeper settings of the Dogger Bank (D&I),NORS = Norwegian Sea (E&J), ICE = Iceland (F&K).

110 H.A. Holland et al. / Marine Pollution Bulletin 87 (2014) 104–116

larger than the shell Fe/Ca differences between localities. It shouldbe pointed out, however, that the raised Fe levels in the last twocenturies reflect a true change in biologically available iron inthe water and cannot be attributed to the precision error.

4.2. Pb/Ca

Increasing Pb/Ca values in shells of A. islandica, specificallythose from the Greater North Sea, that grew during the 20th cen-tury compare well to instrumental observations, many sedimen-tary archives (Brännvall et al., 1999, 2001; Renberg et al., 2001),peat bogs (Le Roux et al., 2004) and previous data from bivalveshells (Gillikin et al., 2005; Krause-Nehring et al., 2012; Fig. 6).The increase of lead at the studied localities in the North Sea duringmodern times is mainly associated with the combustion of leadedgasoline and associated atmospheric Pb input; riverine sedimentinput largely affects coastal settings (Irion, 1993; Irion andMüller, 1987; Kersten et al., 1988). In shallower settings of theNorth Sea, shell Pb/Ca values declined since the 1980s, whereas

in deeper settings (Dogger Bank), the decline only began in the1990s (Fig. 5). These findings agree well with instrumental Pbrecordings (OSPAR 2000, 2009a,b; Fuchs et al., 2002; Rüdel et al.,2010).

Pb/Ca levels in our North Sea shells compared well to thosereported by Krause-Nehring et al. (2012) for a shell from Helgo-land, SE North Sea (Fig. 6). For at least three reasons, there is noperfect match between the two datasets. Firstly, Krause-Nehringet al. (2012) applied a different sampling strategy (discrete LAspots) than the present study (line-scan method, weighted annualaverages) which likely explains the greater variance of their Pb/Cachronology. Shell Pb/Ca exhibits considerable seasonal variability(Fig. 3) that is likely exaggerated in a chronology based on discretesampling spots each representing different amounts of time. It maytherefore not be legitimate to directly compare chronologies thatare based on discrete LA spots and with those based on a linescan/weighted annual average method. Secondly, Krause-Nehringet al. (2012) only analyzed the Pb/Ca values of a single shell of A.islandica that did not live at the exact same locality where our

Fig. 6. Annual Pb/Ca (A and C) and Fe/Ca (B + D) chronologies based on Arctica islandica specimens from the Greater North Sea and Iceland during the last millennium (Fig. 5).(C) Enlarged record of the last 200 years depicting the A. islandica Pb/Ca time-series by Krause-Nehring et al. (2012) for comparison. (D) Enlarged Fe/Cashell record of the last200 years. Long-term trends in the North Sea time-series are illustrated by flexible cubic splines with a rigidity of 25 years. Grey shadows denote 95% confidence intervals.

Table 2Weights for isotope samples. Since shell growth rates vary seasonally, each trace element sample (taken at equidistant intervals) represents different amounts of time. Tocompute annual averages from trace element data obtained within each annual increment (column 1), it requires assigning weights (columns 2–11) to the trace element values(see Schöne et al., 2004).

Number of trace elementsamples per annual increment

Weight of nth isotope sample (%) (direction of growth ?)

1st 2nd 3rd 4th 5th 6th 7th 8th 9th 10th

1 1.002 0.58 0.423 0.48 0.20 0.334 0.39 0.19 0.14 0.285 0.33 0.20 0.11 0.12 0.246 0.28 0.19 0.11 0.09 0.11 0.217 0.25 0.18 0.11 0.08 0.08 0.11 0.198 0.22 0.17 0.12 0.08 0.07 0.07 0.11 0.179 0.20 0.16 0.12 0.08 0.06 0.06 0.07 0.10 0.15

10 0.18 0.15 0.12 0.08 0.06 0.05 0.06 0.07 0.10 0.14

H.A. Holland et al. / Marine Pollution Bulletin 87 (2014) 104–116 111

samples have been collected. Thirdly, discrepancies in metal-to-calciumvalues between shells of contemporaneous specimens from thesame site may also be attributed to individual differences in theuptake and incorporation of metals. Gillikin et al. (2005) investi-gated this in detail for M. mercenaria and concluded that such indi-vidual differences do exist. These authors suggested poolingrecords from many specimens to estimate the environmental Pbcontamination. The good agreement of the Pb/Ca series betweenspecimens from different habitats in the Greater North Sea (DoggerBank, Norwegian Sea, German Bight) including the data providedby Krause-Nehring et al. (2012) is still remarkable (Fig. 6).

In comparison to geochemical data from modern specimens ofA. islandica the shell Pb/Ca levels in pre-industrial specimens weresurprisingly high. Several shells from the Norwegian Sea and shal-low settings of the Dogger Bank that lived between the late 12thand the early 15th century contained up to four times higherPb/Ca values than modern shells (Figs. 5 and 6). According to lakesediment and beat bog records atmospheric lead pollution during

medieval times was only as large as today or lower (Brännvallet al., 1999; Le Roux et al., 2004). For example, a peat bog nearManchester deposited during the medieval heyday of metallurgyshowed strongly elevated Pb levels between 1150 and 1500 (LeRoux et al., 2004).

The explanation for this discrepancy is not clear. One couldassume that diagenetic enrichment accounted for the elevated Pblevels in the medieval shells. However, as will be shown in Section4.3, this hypothesis is highly unlikely, and the shells serve as reli-able recorders of elevated Pb levels in their habitat. Perhaps, spatialdifferences in lead availability caused by re-deposition of Pb-bear-ing argillaceous minerals can explain the high Pb/Ca ratios in theshell from that time interval. At many localities in Europe, theexploitation of ores reached a maximum at around 1200 and, asa consequence of the Black Death, experienced a decline afterward(Brännvall et al., 1999). Increased hydrographic activity near thebeginning of the Little Ice Age (LIA) may have resulted in reworkingof older deposits and transporting of fine-grained, metal-bearing

Fig. 7. Land use and shell Fe/Ca data of Arctica islandica. (A) Spatial correlation mapbetween the Fe/Ca data (shells from the Greater North Sea) and the Land Use &Global Environment (LUGE) dataset (Ramankutty and Foley, 1999). Data points withprobabilities above 10% are drawn in pale colors. (B) Shell Fe/Ca chronology fromthe Greater North Sea in direct comparison with the regional average of the LUGEdataset. Cubic smoothing splines (25 year frequency cutoff, red dashed lines) wereused to indicate lower frequency signals of the time-series.

112 H.A. Holland et al. / Marine Pollution Bulletin 87 (2014) 104–116

particles to the habitat of the bivalves. Increased bioturbation ofthe sediment in which the bivalves lived may serve as an alterna-tive hypothesis that increased lead levels near the sediment floor.Also, changes in the prevailing wind directions associated with theclimate cooling of the LIA may have increased spatial differences inlead input, and elevated amounts of Pb aerosols from nearbysmelters reached the site where the shells lived. An alternativeexplanation is that modern shells are no longer capable of faith-fully recording the elevated lead pollution, because ecologicalchanges. This possibility will be discussed in the following section.

4.3. Mechanisms of metal uptake by A. islandica

Understanding how and in which form bivalves acquire metalsfrom their environment and incorporate these in their shell is ofutmost importance for the interpretation of the shell metal con-tents. There are two main mechanisms of metal uptake, passivediffusion of elements over the entire body surface and ingestion/digestion of contaminated particles.

The mantle epithelia, gills and the digestive gland of bivalvesare cluttered with ion channels through which dissolved elementscan freely exchange between body fluids and the ambient environ-ment (Schöne, 2013). The hemolymph and extrapallial fluids aretherefore largely isosmotic with the ambient environment andcontain – with few exceptions – the same element concentrationand composition as present in the ambient seawater. Active trans-membrane transport by specialized ion pumps (enzymes; Schöne,2013) is only accomplished for a few ions that are either essential

for shell production (Ca2+, HCO3�) or have adverse effects on the

biomineralization process (H+).The second metal uptake mechanism is linked to the ingestion

and possible digestion of nutritive particles. If metals are boundto digested organic substances, they can reach and become partof internal body fluids. Some metals are essential for physiologicalprocesses, whereas others can have detrimental effects on thehealth of the bivalve. Detoxification mechanisms ensure that suchsubstances are quickly removed from body fluids. Specific metal-binding proteins (metallothioneins) play a critical role in capturingnon-essential metals such as Pb or Cd. They can become incorpo-rated into organic-coated vesicles containing amorphous calciumcarbonate (ACC) and, in that form, either be expelled to the envi-ronment or stored for some time in inner organs or epithelial cells.Eventually, some of the ACC-vesicles are remobilized and theircontent being used in the production of new shell material.

Morton (2011) categorizes A. islandica as a ‘‘specialized depositfeeder’’ that lives half-buried (semiendobenthic) in the sediment.His interpretation on feeding habits of this species is largely basedupon anatomical similarities to other deposit-feeding bivalvessuch as mactrids and tellinids and includes the possession of a ‘‘pli-cate ctenidial ciliation’’ and a ‘‘supraaxial extension to the outerdemibranch’’ (Morton, 2011). Since its siphons are unusually short(Morton, 2011), A. islandica merely ‘‘collects the rich surface film’’and suspended particles from the fluffy layer, i.e., a layer nearthe sediment surface which is rich in suspended matter. A. islandicais rather selective of which potential food particles are digestedand which are rejected. Erlenkeuser (1976) noted that ocean qua-hogs are ‘‘real gourmets which feed on the most recent organicmatter only’’, but mostly discards old organic compounds depos-ited at the sea floor. These food preferences are of great relevancefor the recording of Fe and Pb levels.

If reducing conditions prevail in pore waters and/or the fluffylayer, it is likely that detrital iron stored in the sediment becomesremobilized. It can then be absorbed by the bivalve over its entirebody surface and become incorporated into the shell. Reducingconditions can emerge, for example, after phytoplankton bloomswhen excess dead organic material reaches the sea floor. Theamount of detrital iron present near the sediment surface and inthe upper, biodisturbed portion of the sediment is probably posi-tively correlated to the sedimentary (riverine) input of iron-bear-ing particles. In other words, the more detrital iron is depositedin the upper, intensely bioturbated layers of the sediment, themore Fe can be remobilized. Phytoplankton blooms in surfacewaters can be triggered by eutrophication (caused by sewage, fer-tilizers, etc.). In recent decades, the amount of nutrient influxes(nitrite, nitrate, ammonia, phosphate, FeII from aerosols) fromneighboring states to the North Sea has significantly increasedand propelled phytoplankton growth (Hickel et al., 1993; deJonge et al., 1996; Boesch, 2002; Almroth and Skogen, 2010). It istherefore likely that the combined effect of increased terrestrialrunoff of iron-bearing sediments and eutrophication since 1830accounted for a significant increase of dissolved iron in the habitatof A. islandica. Furthermore, as a consequence of these phytoplank-ton blooms, the ratio of fresh-to-old organic matter near sedimentsurface has increased in recent times. This also elevated the rela-tive amount of fresh organics in the food composition of this spe-cies and ultimately resulted in raised concentrations of iron in itsshell (phytoplankton is rich in iron and strongly relies on this ele-ment; e.g., Martin et al., 1994; Coale et al., 1996; Twining et al.,2004; Iwade et al., 2006). Prior to 1830, the influx of iron particlesmay have been high as well (e.g., due to large-scale deforestation,terrestrial runoff and mining activities), but eutrophication wasmost likely not as excessive as in modern times, so that dissolvediron levels in the water column, the fluffy layer and the shellsremained low.

1 Here, we refrain from a detailed interpretation of seasonal Fe/Ca data, because theseasonal variance is smaller than the precision error determined for iron measure-ments based on the NIST standard. It should be pointed out, however, that the largeprecision error for iron results from inhomogeneities of this metal in the NISTstandard (Eggins and Shelley, 2002; Jochum et al., 2011). As indicated by the lowvariability of the seasonal Fe data in Fig. 3, the precision error of Fe measurements oshell carbonate is likely much smaller.

H.A. Holland et al. / Marine Pollution Bulletin 87 (2014) 104–116 113

Iron fertilization may also explain the attenuated Pb levels inmodern shells despite significant increases in Pb fluxes to theocean. Since abundant fresh food is available, modern A. islandicano longer complemented their food with significant amounts ofresuspended, lead enriched organics from the sediment. However,future studies are required to test this hypothesis.

4.4. Factors potentially obscuring shell Pb/Ca and Fe/Ca values

According to a variety of previous studies, bivalves exposed tohigh levels of trace metal contamination not only show elevatedlevels of the respective elements in their soft-parts (e.g., Kröncke,1987; Borchardt et al., 1988; Bourgoin et al., 1991; Jebali et al.,2014), but also in their shells (e.g., Carriker et al., 1982; VanderPutten et al., 2000; Richardson, 2001; Liehr et al., 2005; Krause-Nehring et al., 2012). However, the patterns and trends of Pb/Caand Fe/Ca in hinge portions of A. islandica shells observed in thepresent study could have been obscured by a number of otherenvironmental and biological factors including (1) diagenetic over-print, (2) pre/postmortem transport, (3) ontogenetic age, variablegrowth rates and content of organics in the shell. These potentialinfluences will be scrutinized in the following.

4.4.1. Excellent preservation of the hinge plate: limited diageneticoverprint

To test for possible diagenetic overprint of shell element signa-tures is mandatory if subfossil material is analyzed. Loss andenrichment of elements takes place (Brand and Morrison, 1987),in particular, after the animal has died and shell surfaces areexposed to ambient water and biotic attack. However, early dia-genesis can start even while the bivalve is still alive. Clark andLutz (1980) found pyrite coatings of the outer shell surface of livingM. mercenaria and Geukenisa demissa from low-oxygen environ-ments. Several suitable diagenesis tests should therefore beemployed prior to geochemical analyses irrespective of the age ofthe shell.

Yet, findings of the present study suggest that diagenetic alter-ation is limited to the outermost (<1 mm), chalky margin of somesubfossil shells which likely started to disintegrate in response todecaying organic matrices and increased porosity. After immersionin Mutvei’s solution, these rims remained largely unstained,whereas the remainder of the shell was stained deeply blue. Inter-estingly, the deep blue stain of the subfossil shells was indistin-guishable from that of the modern shells. Since the Alcian Bluedye of the Mutvei’s solution binds to sugar which can easily disap-pear during diagenetic alteration, the subfossil shells were verylikely preserved in pristine condition.

Another indication for limited diagenesis comes from trace ele-ment analysis. The chalky rims contained strongly elevated con-centrations of a variety of elements that are known toaccumulate in shells during diagenesis (e.g., Pb, Fe, Mn, U and S;Brand and Morrison, 1987; Carriker et al., 1991; Labonne andHillaire-Marcel, 2000; Gillikin et al., 2005). In supposedly unal-tered shell portions, however, enrichment of Pb occurred indepen-dently from increases in Fe, and concentrations of Pb and Fe neverreached values as high as those in the visibly altered rims (Fig. 4).Furthermore, concentrations of other diagenetically sensitive traceelements such as Mn and U remained at very low levels in pris-tinely preserved shell portions. We also did not observe elementgradients toward the better protected core of the hinge portionsand, therefore, conclude that Pb/Ca and Fe/Ca levels measured inthe (unaltered) hinge resemble the values that originally existedin the shells when the bivalves were alive.

In this study, the hinge portion was deliberately chosen for geo-chemical analyses. (1) In contrast to the ventral margin, the hingeis microstructurally uniform and should, hence, also be chemically

less heterogeneous than the outer shell layer of the ventral margin(element-microstructure-coupling: Carriker et al., 1991; Schöneet al., 2013). (2) The hinge contains a condensed record, in chrono-logical order, of the life history of the animal (Butler et al., 2009;Schöne et al., 2011). (3) The growing edge of the hinge plate isdirected toward the inside of the bivalve, and is hence better pro-tected against microbial attack, boring sponges or other adverseenvironmental conditions during lifetime than the outer shell layerof the ventral margin. Diagenesis can only start modifying thehinge portion of the shell after the animal has died. The outer sur-face of the shell at the ventral margin, however, is just protectedagainst the ambient environment by a thin organic layer, the peri-ostracum. If this protective layer is damaged locally, the outer sur-face of the shell (outer shell layer) can be affected by earlydiagenesis while the animal is still alive. It should be noted thatthe studied portion of the hinge plate of A. islandica was formedin the same outer extrapallial space as the outer shell layer ofthe ventral margin and recorded the same history of the animal.Therefore, our data can be directly compared to those of otherstudies in which the ventral margin was sampled (Dunca et al.,2009; Krause-Nehring et al., 2012).

4.4.2. Par/autochthonous depositionAs demonstrated by the above cited study of Clark and Lutz

(1980) on early pyritization, the embedding sediment and localmicrohabitat can significantly influence diagenetic processes.Some elements can be enriched in shells deposited in coarsegrained sediment, whereas others are elevated in shells frommuddy, organic substrates. It is therefore also crucial to analyzeif the studied shells were dislocated while the animal was stillalive, after its death or after the initial burial in the sediment. Noneof the shells used in this study showed any signs for displacementfrom their habitat during lifetime. This would have resulted in adisruption of shell growth, retreat of the mantle, damage of theshell and the formation of a distinct disturbance line (Owen andRichardson, 1996; Richardson, 2001; Butler et al., 2009). None ofthe specimens showed signs of abrasion or shell damage that couldhave occurred during postmortem transport over longer distances.It is therefore assumed that the studied shells lived close to the sitewhere they were recovered. Specifically, the high Pb/Ca ratios inthe shell from the Norwegian Sea that lived at around 1300 likelyreflect temporally elevated concentrations of biologically availablePb at that particular site and is not attributed to an earlier deposi-tion in a Pb-rich sediment and subsequent transport.

4.4.3. Pb/Ca and Fe/Ca: ontogenetic age, variable growth rates,organics

As reported in previous studies (Gillikin et al., 2005; Duncaet al., 2009), Pb/Ca and Fe/Ca ratios did not show consistent trendsto lower or higher values through lifetime (but see Westermarket al., 1996). This finding implies that Pb/Ca and Fe/Ca ratios areuncoupled to shell growth rates and metabolic rates which, in turn,are both tightly linked to ontogenetic age. Similar conclusions canbe drawn from intra-annual Pb/Ca values. In different years, high-est and lowest values of Pb/Ca occurred at different times of thegrowing season (Fig. 3). Thus, no correlation exists between sea-sonal shell growth rates and Pb/Ca (Fig. 3).1 Notably, the highestand lowest Pb/Ca values were never measured directly at the

f

114 H.A. Holland et al. / Marine Pollution Bulletin 87 (2014) 104–116

organic-rich annual growth lines. This suggests that lead is bound tothe organic matrix of the biomineral (see also Gillikin et al., 2005),but substitutes Ca in the crystal lattice or is adhesively bound tocrystal surfaces. Furthermore, similar Pb/Ca and Fe/Ca values in con-temporaneously deposited shell portions (representing several yearsto decades) of different specimens from the same locality (Fig. 4)strongly suggest an environmental rather than a biological controlon shell Pb/Ca and Fe/Ca.

5. Summary and conclusions

According to geochemical data from shells of A. islandica, dis-tinct fluctuations of bioavailable iron and lead occurred in theGreater North Sea during the last millennium. These changes wereassociated with variable fluxes of these heavy metals to the oceanthrough time, but most likely also depended on changes of theredox potential near the sediment surface. As expected, Fe andPb levels in the shells increased, since the beginning of the indus-trial revolution due to the expansion of cropland, intensification ofanimal husbandry, processing of iron, use of leaded gasoline andfossil combustible material. Four-fold higher Pb/Ca values in shellsfrom medieval times than today were probably linked to the risingmetal industry atmospheric lead emitted from smelters. However,shell Fe/Ca values remained low to non-detectable until 1830. Wehypothesize that eutrophication and subsequent phytoplanktonblooms in modern times potentiated the bioavailable iron levelsfor benthic organisms.

The next logical step is to study at which proportion elementlevels in the water are reflected in the shell carbonate of A. islandic-a. This will enable quantifiable reconstructions of contaminants inseawater. In this respect, a better understanding of detoxificationmechanisms (including the role of ACC-vesicles) in this speciescan be advantageous. Particular attention should also be given toindividual differences regarding the capability to record environ-mental pollution. Once a more robust sclerochronology is con-structed in which multiple specimens are available for each timeslice, a time-series analysis can be conducted to determine possiblelinks between pollutant levels and climate dynamics. A moredetailed analysis of intra-annual variations of the metal contentcan potentially provide information on seasonal changes in thebioavailability of these substances or phytoplankton and emissiondynamics. Furthermore, Pb and Fe isotope data may be useful totrack the possible sources of pollution.

Acknowledgements

Shells used in this study were kindly provided by WolfgangDreyer (Univ. of Kiel, Germany), Ingrid Kröncke (Senckenberg amMeer, Wilhelmshaven, Germany), Ronald Janssen and MichaelTuerkay (Senckenberg Research Institute and Natural HistoryMuseum, Frankfurt/Main, Germany), Heye Rumohr (Geomar/Helmholtz Centre for Ocean Research, Kiel, Germany), and Anne-miek Vink (Bundesanstalt für Geowissenschaften und Rohstoffe,Hannover, Germany). Our special thanks go to Brigitte Stoll andUlrike Weis (Max-Planck-Institute for Chemistry, Mainz) for theirhelp during the LA-ICP-MS measurements. We gratefully acknowl-edge the help of Amy Prendergast for improving the English gram-mar and style. This study has been made possible by a PhDscholarship of the Earth System Research Center Geocycles (toHAH) and a Grant by the German Research Foundation (DFG) (toBRS: SCHO793/10).

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