This article appeared in a journal published by Elsevier. The attachedcopy is furnished to the author for internal non-commercial researchand education use, including for instruction at the authors institution

and sharing with colleagues.

Other uses, including reproduction and distribution, or selling orlicensing copies, or posting to personal, institutional or third party

websites are prohibited.

In most cases authors are permitted to post their version of thearticle (e.g. in Word or Tex form) to their personal website orinstitutional repository. Authors requiring further information

regarding Elsevier’s archiving and manuscript policies areencouraged to visit:

http://www.elsevier.com/copyright

Author's personal copy

Long-term stability of δ13C with respect to biological age in the aragonite shell ofmature specimens of the bivalve mollusk Arctica islandica

Paul G. Butler a,⁎, Alan D. Wanamaker Jr. b, James D. Scoursea, Christopher A. Richardsona, David J. Reynoldsa

a School of Ocean Sciences, College of Natural Sciences, Bangor University, Menai Bridge, Anglesey, LL59 5AB, Wales, UKbDepartment of Geological and Atmospheric Sciences, Iowa State University, Ames, IA 50011-3212, USA

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

Article history:Received 5 November 2009Received in revised form 26 February 2010Accepted 14 March 2010Available online 19 March 2010

Keywords:Arctica islandicaStable carbon isotopesSclerochronologyMolluskDissolved inorganic carbonNorth Atlantic

The stable carbon isotope ratio in bivalve shells (δ13CS) is an enigmatic geochemical archive whoseinterpretation is often frustrated by the intrusion of variable and unpredictable vital effects which caninfluence the mix of metabolic and dissolved inorganic carbon (DIC) in the shell material. The impacts of vitaleffects and rapid changes in calcification rates on the variability and value of δ13CS have been described in anumber of studies and in many bivalve species with typical lifespans between a few years and a few decades,δ13CS has been observed to change (usually decreasing) with biological age. Very long-lived animals, bycontrast, spend most of their lives in the mature, slow-growing phase, and it might be expected that in theseinstances the effect of changes in calcification rates on δ13CS would be less marked, or even absent. Analysisof δ13CS in mature (N40 years old) Arctica islandica, reported here, indicates that this is the case. δ13CS in shellsamples with biological ages between 42 and 391 years from four distinct sites in the North Atlantic shelfseas (Gulf of Maine, north Icelandic shelf, Irish Sea and North Sea) shows no age-related trend. This suggeststhat metabolic vital effects in mature A. islandica may be reasonably stable at the population level. If thedrivers of isotopic disequilibrium between shell and ambient environment can be identified and quantified,it may be feasible to adjust for them and use δ13CS in mature A. islandica to investigate long-term changes innutrient sources and as a robust proxy for δ13C of environmental DIC.

© 2010 Elsevier B.V. All rights reserved.

1. Introduction

The long-lived bivalve mollusk Arctica islandica is considered tohave significant potential as a natural archive of the marineenvironment in the climatically important North Atlantic region(Thompson and Jones, 1977; Scourse et al., 2006; Schöne and Fiebig,2009). Its potential is based initially on annual growth incrementsdeposited in its shell which encapsulate the growth history of eachindividual in the variability of the increment widths. Individualincrement width patterns have been shown to be synchronized bothwithin and between populations, providing prima facie evidence thatincrement width variability incorporates a common environmentalsignal (Witbaard et al., 1997; Marchitto et al., 2000; Schöne et al.,2002; Helama et al., 2006; Butler et al., 2009a,b, 2010). It has recentlybeen shown that by using crossmatching and detrending techniquesderived from dendrochronology it is possible to construct multi-centennial master chronologies extending back before the lifetime ofany living animals and before the introduction of instrumental recordsof environmental parameters (Butler et al., 2009b, 2010). Such

chronologies make available absolutely dated shell material fromwhich long annually resolved time series of geochemical data can bederived. Where they can be shown to reflect a consistent responsefunction of known parameters, geochemical properties can functionas powerful and robust environmental proxies. For example, theresponse of the stable oxygen isotope ratio (δ18OS) in biogenicaragonite to seawater temperature and seawater δ18O is well known(Grossman and Ku, 1986; Goodwin et al., 2001) and this response hasbeen used together with δ18OS analyses from A. islandica toreconstruct palaeotemperatures (e.g. Schöne et al., 2005a,c; Wana-maker et al., 2008b) and to determine the growing season of A.islandica (Weidman et al., 1994).

The determinants of stable carbon isotope ratios in aragonitic shellmaterial (δ13CS) are less well understood. They include the δ13C of thedissolved inorganic carbon in the ambient seawater (δ13CDIC), the δ13Cof the animals' food source (δ13CF) and the proportions of metabolicand inorganic carbon incorporated in the shell matrix (Keith et al.,1964; Tanaka et al., 1986; McConnaughey et al., 1997; Dettman et al.,1999; Lorrain et al., 2004; Gillikin et al., 2007; McConnaughey andGillikin, 2008; Owen et al., 2008). The analysis is further complicatedby complex exchanges between the organic and inorganic pools ofdissolved carbon, with δ13CDIC being increased when photosynthesiz-ing organisms preferentially remove 12C from the inorganic pool anddecreased by the subsequent oxidation of organic matter (McKenzie,

Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 21–30

⁎ Corresponding author. Tel.: +44 1248 382853; fax: +44 1248 716367.E-mail addresses: p.g.butler@bangor.ac.uk (P.G. Butler), adw@iastate.edu

(A.D. Wanamaker), oss048@bangor.ac.uk (J.D. Scourse), c.a.richardson@bangor.ac.uk(C.A. Richardson), osp607@bangor.ac.uk (D.J. Reynolds).

0031-0182/$ – see front matter © 2010 Elsevier B.V. All rights reserved.doi:10.1016/j.palaeo.2010.03.038

Contents lists available at ScienceDirect

Palaeogeography, Palaeoclimatology, Palaeoecology

j ourna l homepage: www.e lsev ie r.com/ locate /pa laeo

Author's personal copy

1985; Coffin and Cifuentes, 1999; Gillikin et al., 2006). If carbonisotope fractionation during shell formation occurs in isotopicequilibrium with seawater DIC, or if the non-equilibrium elementcan be accounted for, then δ13CS in Arctica islandica has the potentialto act as a proxy for δ13CDIC in the amphi-Atlantic shelf seas. This is akey goal of research into the connections between the carbon cycleand global climate change, since oceanic δ13CDIC has been identifiedas a significant parameter in the determination of the role of theocean as a source or sink for anthropogenic CO2 (Quay et al., 1992;Bacastow et al., 1996; see also Butler et al., 2009b; Schöne et al.,2011-this issue).

Departures from isotopic equilibriummay occur as a result of vitaleffects, precluding or complicating the use of δ13CS as a reliableindicator of δ13CDIC. Following McConnaughey (1989a), vital effectscan be categorized as metabolic or kinetic, wheremetabolic effects aredue to the introduction of 13C-depleted respired carbon into theinternal DIC pool and kinetic effects result from incomplete isotopicpartitioning during hydration and hydroxylation of CO2 at the shellcalcification site. In marine mollusks, metabolic effects are thought tobe the cause of ontogenetically decreasing δ13CS, with increasingproportions of 13C-depleted metabolic carbon being incorporated inthe inorganic shell matrix as the animal becomes older and themetabolic rate increases in relation to the growth rate (Keller et al.,2002; Lorrain et al., 2004; Gillikin et al., 2007). By contrast, kineticeffects discriminate against the heavy isotopes of carbon and oxygenwhen high rates of calcification do not allow isotopic partitioning atthe calcification site to proceed to completion (McConnaughey,1989b). In this case similar processes affect both carbon and oxygenpartitioning, so that in the absence of any freshwater influence thepresence of kinetic disequilibrium effects can be inferred from apositive correlation between δ13CS and δ18OS.

The isotopic fractionation of shell aragonite out of equilibriumwith its ambient surroundings constitutes a significant constraint onthe use of δ13CS as an environmental proxy. Since the extent ofmetabolic and kinetic disequilibrium effects can be interpreted as aresponse to changes in calcification rates (and hence growth rates),the conventional ontogenetic trend in mollusks of rapidly decreasinggrowth rates during the early years of life may be mirrored in thevalue of δ13CS, expressing itself as a trend to a lighter isotopic ratio. Anumber of studies in which such trends have been observed in marinemollusks are cited byMcConnaughey and Gillikin (2008). For exampleKrantz et al. (1987) found δ13CS decreasing by 1–2‰ in modern andfossil Spisula solidissima shells up to 6 years old, Kennedy et al. (2001)found it decreasing by ∼1.5‰ in Pinna nobilis shells up to 10 years oldand Gillikin et al. (2007) found decreases of as much as 4‰ in δ13CS inMercenaria mercenaria shells up to 40 years old. Conversely, Kelleret al. (2002) found no trend in δ13CS in Callista chione up to 11 yearsold. A consistent aspect of these and other studies, however, is thattheir focus is precisely on those periods of rapidly decreasing growthrates when ontogenetic trends in δ13CS are most likely to be observed.The majority of mollusk species are not especially long-lived; hencethe phases of very fast initial growth followed by decreasing growthrates in subsequent years characterize all or nearly all of the availableshell material and it is not surprising to find that analyses of δ13CShave tended to reflect strong gradients in calcification rates. Noprevious analysis of δ13CS has specifically targeted those parts of theshells of long-lived animals that are not characterized by strongontogenetic growth trends.

The extremely long-lived bivalve mollusk Arctica islandica showslittle or no trend in growth rate after the first ∼40 years of life (Schöneet al., 2004; Helama et al., 2006; Scourse et al., 2006; Butler et al.,2009b). Its maximum longevity exceeds 400 years (Wanamaker et al.,2008a), making many decades or centuries of shell material availablefor the study of stable carbon isotope ratios which are not (if theargument advanced in this paper is correct) affected by changes incalcification rates. If there are no significant vital effects impacting

δ13CS during most of the lifetime of the animal, or if such vital effectsas exist are reasonably stable and can be quantified, a significantconstraint on the usefulness of the archive would be removed, andother associated complexities, such as the proportions of metabolicand inorganic carbon that go to make up the shell matrix, might beapproached in a more systematic way. It may then become feasible touse extended δ13CS time series based on multi-centennial cross-matched A. islandica chronologies to investigate long-term changes infood sources or in the role of the shelf seas as a source or sink foratmospheric CO2.

This study reports δ13C analyses of samples with biological agesbetween 42 years and 391 years taken from Arctica islandica shellsfrom sites in US, Icelandic and UK waters. The chronological dates ofthese shells, determined by AMS radiocarbon dating or by scler-ochronology (i.e. increment width counting and pattern matching;Helama et al., 2006; Butler et al., 2009b), are distributed throughoutthe past 1300 years. The material reported here is derived from anumber of different studies which focussed variously onmultiple δ13Canalyses of single shells (Witbaard et al., 1994; Wanamaker et al.,2008b) or single analyses of multiple shells (Butler et al., 2009b), soalthough the number of δ13C determinations reported for individualshells ranges between one and 109, most of the shells were analysedonly once. It is hypothesized here that the within shell variability ofδ13CS in mature A. islandica does not exceed the variability of δ13CS inthe population and is not dependant in any way on the biological ageof the analysed sample. The term ‘mature’ is used here to refer tospecimens whose shell growth is not characterized by the strongdecreasing trend typical of younger animals. Although the cut offpoint between the earlier period of strong growth trend and the laterperiod of little or no trend can be quite variable, both betweenindividuals and between populations, previous research indicates thata figure of 40 years can be regarded as an acceptable approximation(see for example Schöne et al., 2004, fig. 6; Helama et al., 2007, fig. 2;Butler et al., 2009b, fig. 3) as long as the precise date is not critical tothe analysis.

The focus of this paper is on the stability of the δ13CS signal withrespect to biological age in mature specimens of A. islandicacontrasted with the typical strong trends that characterize the shellsof younger animals.

2. Data and methods

The data used in this study are derived from stable carbon isotopeanalyses of single shells or groups of shells from four sites (Fig. 1):

(a) Western Gulf of Maine, US waters (43° 13′N 69° 48′W). Materialwas sampled from the left valves of three articulated fossilspecimens (GOM30, GOM4047 and GOM48) collected in avibracore from a depth of 38 m (see Wanamaker et al., 2008bfor further details of the collection and preparation proce-dures). The data used here are annualised averages of analysesof multiple micromilled samples taken from within eachgrowth increment. For the analysis of δ13CS in older animals,measurements were only available from GOM30 (biologicalages from 41 to 114 years). AMS 14C dating indicates that theanimals were living during the 10th century AD (GOM48) andthe 14th and 15th centuries AD (GOM30 and GOM4047). Stablecarbon isotope ratios were measured at University of Frankfurt(Germany) on a Finnigan MAT-253 continuous-flow massspectrometer, to a precision of 0.05‰, and are reported as δ13Crelative to the VPDB carbonate standard based on NBS-19calibrated values of +2.02‰.

(b) North Icelandic shelf, close to the island of Grimsey (66° 32′N18° 12′W). Material was sampled from thirteen single valves fromfossil shells and one articulated pair from a live-collected

22 P.G. Butler et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 21–30

Author's personal copy

specimen. All shells were trawled from the seabed at a depth of∼75 m using a bespoke dredge (see Wanamaker et al., 2008afor further details of collection and preparation). Thirteen ofthe samples consisted of bulk material removed from theventral margin (i.e. the most recently deposited part of theshell) for AMS 14C rangefinder determinations. In order toavoid the inclusion of material from the nacreous (inner) shelllayer the samples were cut distal to the pallial line. Thesesamples are assumed to integrate up to ∼40 years of shelldeposition. In the case of three of the shells (061297, 061312and 061664), material was drilled from the exposed cross-sectional surface (see Wanamaker et al., 2008a, fig. 3) at anumber of positions between the umbo and the ventral marginwith the intention of analysing shell material produced duringspecified periods within the lifetime of the animal. Twentysamples were obtained in this way (four from 061297, sevenfrom 061312 and nine from 061664). The maximum number ofyears integrated in these samples is 5 years. All samples havebeen precisely dated using sclerochronology (incrementcounting and increment pattern matching) and the dates ofthe midpoints of the samples range between AD 705 and AD1915. Stable carbon isotope ratios were measured at Universityof Aarhus (Denmark) on a GV Instruments Isoprime stableisotope mass spectrometer, to a precision of 0.15‰, and arereported as δ13C relative to the VPDB carbonate standard basedon NBS-19 calibrated values of +1.95‰.For the analysis of δ13CS in younger animals, measurementswere obtained from another shell from Icelandic waters (M07;Schöne et al., 2005a). In this case, the data are annualisedaverages of analyses of multiple micromilled samples takenfrom within each growth increment for biological ages 2 to39 years. The precise provenance of this shell (which wasobtained from a museum collection) is unknown, although it isthought to come from the south Icelandic shelf (Schöne et al.,2005a; Wanamaker et al., 2008a). The samples described herehave been precisely dated using band counting to the years AD1496–1533. For this shell, stable carbon isotope ratios weremeasured at University of Frankfurt (Germany) on a FinniganMAT-253 continuous-flowmass spectrometer, to a precision of0.05‰, and are reported as δ13C relative to the VPDB carbonatestandard based on NBS-19 calibrated values of +2.02‰.

(c) Irish Sea, UKwaters, off thewest coast of the Isle ofMan (54° 10′N4°50′W). Material was sampled from thirty-seven single valvesfrom fossil shells trawled from the seabed at depths between30 m and 70 m using a bespoke dredge (see Butler et al., 2009b

for further details of collection and preparation). All samplesconsisted of bulk material removed from the ventral margindistal to the pallial line for AMS 14C rangefinder determinations,and are assumed to integrate up to ∼40 years of shell deposition.These samples have been precisely dated using sclerochronologyand the dates of themidpoints of the samples range between AD1573 andAD1981. Stable carbon isotope ratiosweremeasured atthe NERC Radiocarbon Laboratory (UK) using a dual-inlet massspectrometer, to a precision of 0.14‰, and are reported as δ13Crelative to the VPDB carbonate standard based on NBS-19calibrated values of +1.95‰.

(d) Oyster Grounds, southern North Sea, off the Netherlands coast (53°41′ N 4° 25′ E). Material was sampled from articulated pairs ofvalves from two live-collected specimens collected at waterdepth ∼30 m (RWL7 and RW4C; see Witbaard et al., 1994 forfurther details of collection and preparation). All samplesconsisted of bulk material removed from the outer shell surfacefor AMS 14C rangefinder determinations and were reported tointegrate 5 years of deposition. Thefive samples from shell RWL7with biological ages greater than 40 years have been dated byincrement counting; their midpoints range between AD 1966and AD 1986. Stable carbon isotope ratios were measured at theUniversity of Utrecht (Netherlands) and are expressed as a permille (‰) deviation from the Pee Dee Belemnite (PDB) standard.The analytical precision was not reported.

The hypothesis that there is no ontogenetic trend in stable carbonisotope ratios in the shells of mature Arctica islandica was tested byregressing the δ13CS values for each of the four sites against thebiological ages of the samples used for analysis. Further, the δ13CSvalues for each site were normalized by subtracting the local meanfrom each individual value and combined into a single dataset whichwas also regressed against the biological ages. The data presented inall the charts in this paper can be found in the accompanyingAppendix.

3. Results and discussion

3.1. Relationship between δ13CS and biological age

Fig. 2 shows for each location the relationship between δ13CS and thebiological age of the samples. The regression parameters and theirsignificance levels are shown in Table 1, and the mean δ13CS values andtheir standard deviations for each of the four groups are in Table 2.

Fig. 1. Collection sites (black circles) of specimens of Arctica islandica used in this study.

23P.G. Butler et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 21–30

Author's personal copy

At three of the four sites considered, no trend is apparent in therelationship between the value of δ13CS and the biological age of theanalysed sample. The set of results for Grimsey, in particular, includessamples with a wide range of biological ages (42 to 391 years) whichnevertheless maintain consistent values of δ13CS and relatively lowvariability (standard deviation=0.27). The variability of the Irish Seameasurements is greater than that of any of the other groups but herealso no trend in δ13CS is apparent for biological ages between 42 and219 years. The North Sea analyses, all of which come from a singleshell, are limited in number and range of ages but within theseconstraints no trend is apparent. Only the Gulf of Maine measure-ments appear to contradict the hypothesis that there is no linkbetween the value of δ13CS and biological age. The seventy-fourannualised averages from a single shell show a significant positivetrend in δ13CS between 41 and 114 years. The range and standarddeviation of the δ13CS values, however, remain below those of the verystable Grimsey group (range=0.77‰, SD=0.17 for Gulf of Maine;range=0.93‰, SD=0.27 for Grimsey) and the range is close to themaximum variability of 0.76‰ reported elsewhere in this issue in astudy of four extended time series of annually resolved δ13CS

measurements in Arctica islandica from Iceland and the Gulf ofMaine (Schöne et al., 2011-this issue), none of which show any long-term trends apart from those associated with the oceanic 13C Suesseffect. The apparent positive trend in δ13CS in the Gulf of Maine shell istherefore consistent with natural variability. This conclusion is furthersupported by the observation that the rising trend is not consistentthrough the series but in fact emerges from a sequence consisting of adecreasing trend from 40 to 70 years, then a short period of relativelylow values and low variability, followed by a rapid increase between80 and 90 years and finally a more gradual return to lower values. The

sharp increase leading to the spike around 90 years appears to bestrong enough to impart a significant trend to the entire series.

The variability observed in this shell may reflect variability in theδ13CDIC of the water in the Gulf of Maine. The composition of Gulf ofMaine waters is most likely influenced by the relative strength on theadjacent slope of waters from the cold south-flowing LabradorCurrent and the warm north-flowing Gulf Stream (e.g. Gatien, 1976;Petrie and Drinkwater, 1993; see Wanamaker et al., 2008b for anoverview of the relevant literature). The difference in δ13CDIC betweenthe two water masses may be of the order of 1‰ (see fig. 8 inKroopnick, 1980) so if we assume a constant enrichment factor forbiogenic aragonite the range of δ13CS in the Gulf of Maine shell isconsistent with changes in the relative influence of the local watermasses. The timescales of such changes can be linked to dominantmodes of climate forcing in the region, specifically the AtlanticMultidecadal Oscillation (AMO) (Sutton and Hodson, 2005) and theNorth Atlantic Oscillation (NAO) (Greene and Pershing, 2003). The40–50 year period in the δ13CS record described here is slightly shorterthan that of the AMO inmodern times (Sutton and Hodson, 2005), buta reconstruction of the AMO based on tree-rings indicates that itsfrequency may have been higher in the middle part of the lastmillennium (see fig. 3(b) in Gray et al., 2004). A second driver ofδ13CDIC variability in the Gulf of Maine may be the input of freshwaterfrom the surrounding catchment, which has been shown to affect theconcentrations and character of seawater DIC close to the collectionsite of the shell described here (Salisbury et al., 2009). That study wasconcerned only with seasonal changes, but a further strong associa-tion has been described between rainfall patterns in the continentalUS (including specifically the northeast) and the AMO mode whichindicates that freshwater input from the continent may also act as a

Fig. 2. Stable carbon isotope ratios (δ13CS) from the shell of Arctica islandica plotted against the biological age of the analysed material. Shells were collected from the Gulf of Maine(crosses), Grimsey (filled markers), the Irish Sea (open circles), and the North Sea (open triangles). Multiple samples from three shells from the Grimsey site are identified with filleddiamonds (shell 061664), filled circles (shell 061312) and filled triangles (shell 061297). Lines show linear regressions for each location (see Table 1 for the regression parameters).The analytical errors for the δ13C analyses are comparable to the size of the symbols. For the Gulf of Maine group, the data points are annualised averages of multiple analyses, all ofthem from a single shell (GOM30). For the North Sea group the analyses integrate ∼5 annual increments and for the Grimsey and Irish Sea groups they integrate up to 40 annualincrements.

Table 1Regression parameters for the trend lines shown in Fig. 2. The significance levels (p)demonstrate that only for the Gulf of Maine shell is there a significant relationshipbetween δ13CS and the biological age of the shell material.

Location Gradient r2 N p

Gulf of Maine 0.0034 0.1562 74 b0.001Grimsey 0.0002 0.0031 33 0.76 nsIrish Sea −0.0003 0.0005 37 0.90 nsNorth Sea 0.0012 0.0021 5 0.93 ns

Table 2Mean and standard deviation of measurements of δ13CS in groups of A. islandica shellsamples with various biological ages from four locations.

Location Mean δ13CS(‰)

SD(‰)

Number ofanalyses

Range of biological ages(years)

Gulf of Maine 2.25 0.17 74 41–114Grimsey 2.12 0.27 33 42–391Irish Sea 1.21 0.56 37 42–219North Sea 1.44 0.22 5 43–64

24 P.G. Butler et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 21–30

Author's personal copy

driver of δ13CDIC variability (and consequently δ13CS variability) onmultidecadal timescales (Enfield et al., 2001).

Grimsey shell 061312, for which eight determinations areavailable (filled circles in Fig. 2), shows an initial trend (throughbiological ages 67 to 212 years) of increasing δ13CS before reverting tothe mean value for the site. In the other three cases where there aremultiple determinations for individual shells (Grimsey shell 061297(filled triangles), Grimsey shell 061664 (filled diamonds) and NorthSea shell RWL7 (open triangles)) no trend is apparent. Althoughshorter term trends in δ13CS similar to those observed in the Gulf ofMaine specimen may also be present in these shells, it is not possibleto discriminate them because of the low resolution of the time series(but see Schöne et al., 2011-this issue for examples of interannualvariability in shells from Gulf of Maine and Icelandic waters).

It is apparent from Fig. 2 that the shells from UK waters (Irish Seaand North Sea) are slightly depleted (by ∼0.8‰) in 13C whencompared with the shells from Grimsey and the Gulf of Maine.Assuming that the proportion of metabolic carbon incorporated in theshell does not vary between populations, this difference can beascribed to a corresponding depletion in 13C in the seawater DIC. Theprinciple drivers of seawater δ13CDIC are (a) the net removal ofisotopically light carbon in surface waters during photosynthesis andthe net reintroduction of isotopically light carbon to deep watersduring remineralisation (McKenzie, 1985; Broecker, 1992) (b)isotopic equilibration with atmospheric CO2 which produces atemperature driven 13C enrichment gradient with colder watersmore enriched than warmer waters (Broecker, 1992) and (c)intrusion of 13C depleted freshwater from regional catchments(Mook and Tan, 1991). All four sites considered here are shelf sealocations with high and broadly comparable levels of biologicalproductivity, so it is unlikely that the differences in δ13CS betweensites result purely from differences in biological drawdown of 12C. Therelative enrichment of the shells from Grimsey compared with thosefrom UK waters may be related to one or both of the other drivers ofseawater δ13CDIC, since both seawater temperatures and freshwaterinfluence are significantly lower on the North Icelandic Shelf. Thesame factors, however, should result in δ13CS values for the Gulf ofMaine being closer to those found in UK waters. This discrepancycannot be explained further with the available data, but it is useful tobear in mind that the Gulf of Maine measurements are derived from asingle shell and are probably subject to life and environmental effectsthat are constrained in space and time, whereas the Grimsey and Irish

Sea values, being distributed in time and derived frommultiple shells,likely present a more synoptic overview.

When the four groups are combined bymerging residuals from thelocal means into a single dataset (Fig. 3), the trend line is flat. It shouldhowever be noted that the data as shown in Fig. 3 combine annualisedaverages from the Gulf of Maine shell with integrated measurementsfrom the other sites. They are presented in this way to aidvisualization, but need to be homogenized for statistical validity byassigning the δ13C value for each integrated sample to each yearwithin the integration before calculating the mean and residuals. Forthe homogenization: (1) for the samples from Grimsey and Irish Seashells that were removed from the ventral margin it was assumed that19, 29 and 39 years were integrated where the biological age at thesample point was respectively b100, 101–200 and N200 years; (2) forthe samples from Grimsey shells that were drilled from the exposedcross-sectional surface it was assumed that 5 years were integrated ineach sample; and (3) for the samples from North Sea shells it wasassumed that 5 years were integrated in each sample. Afterhomogenization, all the data points represent annual values andthere is no significant trend (r2=0.0017, N=1702, p=0.09 for all thedata; r2=0.002, N=1628, p=0.07 if the Gulf of Maine measure-ments are excluded). The regression line shown in Fig. 3 is derivedfrom the homogenized data including the annualised Gulf of Mainemeasurements.

3.2. Comparison with trends in δ13CS during the first 40 years of life

The apparent lack of trend in δ13CS in mature Arctica islandica canusefully be contrasted with its variability in juvenile specimens (Fig. 4and Table 3). Typically, juvenile A. islandica exhibits the decreasing13C/12C ratios often observed in other young and fast growingmollusks (see references in the Introduction to this paper). Forexample, in all three shells from the Gulf of Maine (GOM30, GOM4047 and GOM48 in Fig. 4) δ13CS decreased during the first 40 years ofgrowth, the magnitude of the decrease between ∼0.4‰ and ∼1‰(Fig. 4). In two shells from the North Sea reported by Witbaard et al.(1994), δ13CS decreased by ∼0.5‰ during the first 25 and 40 years(RW4C and RWL7 in Fig. 4; while the negative trend is evident in thefigure, the number of data points is too small to reach statisticalsignificance), and in three shells from Scottish inshore waters (notshown here) reported by Foster (2007; see also Foster et al., 2009)δ13CS also decreased by between 1.2‰ and 2.5‰ over periods of

Fig. 3. Linear regression of δ13CS on biological age for the combined dataset of measurements from Gulf of Maine, Grimsey, Irish Sea and North Sea. All values of δ13CS have beennormalized by subtracting the local mean from the individual measurements. In order to ensure statistical equivalence for the regression, the data were homogenized by assigningannual δ13CS values to all years included in the bulk samples from Grimsey, the Irish Sea and the North Sea, as described in Section 3.1. The regression line shown here is based on thehomogenized data, but for ease of visualization only the central point is shown for each bulk sample.

25P.G. Butler et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 21–30

Author's personal copy

between 18 and 32 years. Only in the case of the very long-livedspecimen from Icelandic waters (M07) reported by Schöne et al.(2005a) does there appear to be no trend in δ13CS during the first40 years of life (filled circles in Fig. 4). In another shell from the NorthSea, also reported by Witbaard et al. (1994), the initial 6 years ofgrowth were sampled at high resolution. In this case, δ13CS actuallyincreased by ∼1‰. Since the first few years of growth in A. islandica arecharacterized by a rapidly increasing growth rate, this may be anindication that δ13CS is sensitive to growth rate in the mannerdescribed by Lorrain et al. (2004). They argue that the ratio betweenthe availability of metabolic carbon and the amount of carbonateprecipitated determines the proportion of metabolic carbon incorpo-rated into the shell and hence the value of δ13CS.When growth is slow,this ratio is high and a greater proportion of isotopically lightmetabolic carbon is utilized, so that δ13CS decreases as the growthrate decreases.

The very early years of growth were not always analysed in thestudies described here, but where they are reported the results seemto confirm the rising trend seen by Witbaard et al. (1994). Detailedsubannual δ13CS measurements are available for the first 40 years ofgrowth for four of the shells used in this study (three from the Gulf ofMaine and one Icelandic specimen (M07; Schöne et al., 2005a)). Fig. 5shows a composite dataset consisting of residuals of the annualiseddata for these four shells. Three distinct phases in the relationshipbetween δ13CS and biological age are apparent; an initial period (ages1 to 8) of strong positive correlation (pb0.0001), an intermediateperiod (ages 9 to 15) of no trend, and a final phase (ages 16 to 40) ofstrong negative correlation (pb0.0001). The period of stable δ13CSbetween ages 9 and 15 is apparent in each individual specimen anddoes not appear to be an artefact of the variability of timing of

maximum δ13CS. This age range is of particular interest. As well asbeing a period of rapidly changing growth rate, it also marks the onsetof sexual maturity in Arctica islandica (Thompson et al., 1980). It ispossible that an additional burden is placed on the pool of metaboliccarbon during this period, reducing the availability of metaboliccarbon for shell deposition and leaving the shell enriched in 13C evenwhile growth rates are decreasing.

3.3. Influence of growth rate on δ13CS in juvenile and mature Arcticaislandica

Although it has been shown above that the kind of strongontogenetic trends in δ13CS characteristic of the shells of biologicallyyoung animals are not detectable in increments deposited after theage of 40 years, it is still possible to argue that an association betweenδ13CS and growth rate persists after the initial phase of rapidlychanging increment widths. Such an association, if it existed, mightnot propagate into the analyses described above in Section 3.1because the part of the variability of δ13CS linked to the growth ratewould likely decrease in proportion to the decrease in the variabilityof the growth rate itself. The impact of other (external) drivers ofvariability in δ13CS would not be affected by any change in growth rateand would therefore exert a greater proportionate influence on δ13CS,tending to mask the growth rate signal. In addition the analysisdescribed here relies to a considerable extent on bulk analyses fromdistinct shells which integrate multiple growth increments so thatvariability in δ13CS between different shells or between differentpopulations may be sufficient to mask any growth rate signal.

The only data that can be used to investigate this association isderived from the most long-lived shell from the Gulf of Maine(GOM30), this being the only shell for which annually resolvedgrowth increment widths and δ13CS analyses are available forbiological ages in excess of 40 years. The relationship betweenincrement width and δ13CS is shown in Fig. 6 and demonstratesthat, for this shell at least, there is no correlation between δ13CS andincrement width after the age of 40 years (r2=0.02,N=74, p=0.23).The cyclical low frequency variability shown in the δ13CS time seriesfrom this shell (Fig. 2) does not propagate to any link with incrementwidth. This is a further indication that the δ13CS signal in matureArctica islandica may constitute a coherent and identifiable responseto external drivers.

For younger specimens, a curious bimodal pattern emerges fromthe association between δ13CS and growth rate. The pattern of thelinks between δ13CS and biological age described earlier (Section 3.2

Fig. 4. Trends of δ13CS with biological age in six juvenile (ages up to 40 years) A. islandica. Data from Gulf of Maine (solid grey or red lines and open symbols) and Iceland (thick blackor blue line and filled circles) are annually averagedmeasurements from single shells; data from the North Sea (thin black or green lines and filled triangles) are from two shells, eachmeasurement integrated over ∼5 annual increments (see Witbaard et al., 1994, Table 2).

Table 3Regression parameters for the trend lines shown in Fig. 4. Strongly significantrelationships between δ13CS and biological age are apparent for GOM30 and GOM48.The relationship for GOM4047 is not quite significant at the p=0.05 level. Trends in thetwo North Sea specimens are not significant, probably because of the small number ofdata points.

Location and shell Gradient r2 N p

Gulf of Maine GOM30 −0.0183 0.5188 35 b0.0001Gulf of Maine GOM4047 −0.0089 0.0963 34 0.07 nsGulf of Maine GOM48 −0.0284 0.5721 37 b0.0001Iceland M07 −0.0026 0.0209 38 0.40 nsNorth Sea RWL7 −0.0202 0.3072 7 0.20 nsNorth Sea RW4C −0.0715 0.4324 6 0.16 ns

26 P.G. Butler et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 21–30

Author's personal copy

and Fig. 5) suggests that the association with growth rate should bepositive. Although there is a positive correlation for the whole dataset(r2=0.04, N=144, pb0.05), it is significant only at the 95% level, andthe stronger pattern evident from Fig. 7 is a positive association forincrement widths ≤2 mm (r2=0.24, N=118, pb0.0001) and anegative association for widths N2 mm (r2=0.32, N=26, pb0.01).This may indicate kinetic isotopic disequilibrium at high growth rates(see Section 3.5 below). Around the threshold growth rate (which, asindicated in Fig. 7 may correspond to increment widths between2 mm and 4 mm) δ13CS is at a maximum. Above this threshold 13Cdepletion may be driven by kinetic disequilibrium (which increaseswith faster growth rates). Below the threshold 13C depletion mayresult from a relative increase in the proportion of metabolic carbonavailable for shell construction (Lorrain et al., 2004).

3.4. δ13CS in Arctica islandica as a proxy for δ13CDIC

If δ13CS in Arctica islandica is indeed driven by the ratio ofmetabolic to precipitated carbon as argued by Lorrain et al. (2004),the contrast between the clear trends in the association between δ13CSand biological age during the juvenile years (Figs. 4 and 5) and thelack of trend during the mature years (Figs. 2 and 3) is instructive. Itsuggests that the ratio of metabolic to precipitated carbonate in theshell is effectively constant through the major part of the life of long-

lived specimens of A. islandica. This conclusion is further supported bythe lack of any significant correlation between δ13CS and growth ratein the single shell for which this association could be tested (Fig. 6).Uncertainty about the level and variability of the ratio of metabolic toprecipitated carbonate has hitherto been a significant constraint onattempts to use stable carbon isotope ratios in the study of long-termchanges in oceanic δ13CDIC on the one hand and in the compositionand source of nutrients on the other (Gillikin et al., 2007).

In principle δ13CDIC in local waters can be derived using an isotopicmixing equation proposed by McConnaughey et al. (1997):

R δ13CF

� �+ 1−Rð Þδ13CDIC = δ13CS–� ð1Þ

where � is an enrichment factor for 13C fractionation betweenaragonite and bicarbonate, R is the fraction of metabolic carbonatein the shell and δ13CF is the isotopic ratio of the food source. Anexpression for δ13CDIC can be derived from Eq. (1):

δ13CDIC = δ13CS–�–R δ13CF

� �h i= 1−Rð Þ ð2Þ

� can be taken to be the equilibrium 13C fractionation for aragonite,estimated as 2.7‰ (Romanek et al., 1992) and δ13CF can beapproximated using organic material from the shell (O'Donnell

Fig. 5. Linear regressions of δ13CS on biological age for ages 1–8, 9–15 and 16–40 for a combined dataset incorporating data from three Gulf of Maine shells and one from the southIcelandic shelf. The regressions show a highly significant positive correlation for ages 1–8 (r2=0.63, N=22, pb0.0001) and a highly significant negative correlation for ages 16–40(r2=0.41,N=94, pb0.0001) with an intermediate range (ages 9–15) where no correlation is apparent (r2=0.0016,N=28, p=0.84). The data used here are the same data from theGulf of Maine and Iceland shells as were shown in Fig. 4, normalized by subtracting the local mean δ13CS from the individual measurements (annualised values were not available forthe North Sea shells).

Fig. 6. Regression of δ13CS on increment width for Gulf of Maine shell GOM30, including only increments deposited after biological age 40 years. No significant trend is apparent inthis regression (r2=0.02, N=74, p=0.23), demonstrating that — for this shell at least — δ13CS is not correlated with the growth rate.

27P.G. Butler et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 21–30

Author's personal copy

et al., 2003; Gillikin et al., 2007) or by using the global estimate of−22±5‰ reported for particulate organic carbon by Goericke andFry (1994). If disequilibrium between δ13CS and δ13CDIC results onlyfrom metabolic vital effects, and if the proportion of metaboliccarbonate in the shell can be quantified — possibly using the modelsuggested by Lorrain et al. (2004) — and turns out to be effectivelyconstant at the population level, there would appear to be potential touse long Arctica islandica chronologies to reconstruct δ13CDIC overmulti-centennial timescales.

3.5. Metabolic and kinetic disequilibrium in Arctica islandica

Kinetic vital effects result from fractionation in favour of 12C duringhydration and hydroxylation processes when CO2 reacts in thecalcification region to form HCO3

− (McConnaughey, 1989b). Isotopicequilibrium with the local DIC pool is eventually re-established if thereaction has time to proceed to completion, but during periods of rapidgrowth the shell can precipitate out of equilibrium (McConnaugheyet al., 1997). A similar fractionation process affects the stable oxygenisotope ratio, and the presence of kinetic vital effects can be inferred if18O (which is not subject to metabolic fractionation) is precipitated outof equilibrium with surrounding waters or if there is a positivecorrelation between δ18OS and δ13CS in the absence of significantsalinity variations in the surroundingwater. Kinetic disequilibria are nottypically observed in mollusks, which are thought to use the enzymecarbonic anhydrase to accelerate hydroxylation of CO2 in conditions ofrelatively mild alkalinity (Weiner and Dove, 2003; McConnaughey andGillikin, 2008) and which are usually found to precipitate their shellsclose to 18O equilibrium with their environment (Epstein et al., 1953;Wefer and Berger, 1991; Hickson et al., 1999; Wanamaker et al., 2006,2007). Measurements of ambient δ18O, particularly in bottom waters,are sparse, and in studies which use shell δ18OS in Arctica islandica as aproxy for seawater temperature, ambient δ18O is usually determinedindirectly using a model based on salinity (Weidman et al., 1994;Witbaard et al., 1994; Schöne et al., 2004, 2005b; Foster et al., 2009).However, the fact that these studies generally find good correlationsbetween δ18OS and seawater temperatures is an indication that theassumption that shell oxygen is precipitated in isotopic equilibriumwith its surroundings is correct, and consequently that kineticdisequilibrium effects are absent. Further, comparison between theannualised analyses of δ18OS and δ13CS from the Gulf of Maine discussedin this study shows that there is no correlation between them,confirming that carbon isotope disequilibrium in mature A. islandicaresults only from metabolic vital effects. Where growth is very rapid injuvenile A. islandica (growth increments N2 mm; see Section 3.3 above

and Fig. 7) a negative correlation between δ13CS and increment widthindicates that, for these very wide increments alone, kinetic disequilib-rium behaviour may be driving the 13C deficiency in the shell.

3.6. Possible influence of the 13C Suess effect

The 13C Suess effect is the term given to the trend to isotopicallylighter values of environmental carbon that has occurred duringrecent decades as a result of the anthropogenic emission of fossil fuelcarbon (Suess, 1953; Keeling, 1979). This effect has been demon-strated in Arctica islandica as a decrease of ∼1‰ in δ13CS over the past∼150 years in shells from Irish Sea waters close to the Isle of Man(Butler et al., 2009b; see also Schöne et al., 2011-this issue). It isconceivable that bias in the chronological distribution of shells ofdifferent biological ages may result in the 13C Suess effect masking along-term ontogenetic trend in δ13CS of shells from mature animals.The masked trend would be positive if a significant proportion of thesamples from biologically younger shells came from materialdeposited during themost recent ∼150 years. Conversely, the maskedtrend would be negative if a significant proportion of the samplesfrom biologically older shells consisted of recently depositedmaterial.If the recent samples show an even distribution through time, it canreasonably be assumed that the influence of the 13C Suess effect hasnot masked any significant trends in the regressions shown in Figs. 2and 3, although it may have the effect of reducing slightly the value ofδ13CS in groups which include a significant proportion of recentsamples. Fig. 8 shows the distribution of biological ages of sampleswith respect to time in the period since AD 1850 for the two groupswith both recent (dated later than AD 1850) and earlier samples (theGrimsey group has four recent samples and 19 earlier samples; theIrish Sea group has 18 recent and 19 earlier). There is no trend in thisassociation (r2=0.014, N=22, p=0.95), and we can thereforeconclude that the lack of trend shown in Figs. 1 and 2 is not anartefact of any variation of environmental δ13C with time.

4. Conclusion

δ13C in the shell of Arctica islandica does not appear to be affectedby any age-related trends after the animal has reached a biological ageof around 40 years. The variability of δ13CS with growth rate is acommon characteristic of molluscan shell geochemistry and in mostspecies it constitutes a significant constraint on the use of δ13CS as aproxy for δ13CDIC in the environment. A. islandica is unique amongmollusks, however, in that the bulk of its lifespan (a period which cancover several centuries) is spent in a mature phase not characterized

Fig. 7. Regressions of δ13CS on increment width for increments deposited up to biological age 40 years. These show a highly significant positive correlation for increment widths≤2 mm (r2=0.24, N=118, pb0.0001) and a significant negative correlation for increment widths N2 mm (r2=0.32, N=26, pb0.01). All values of δ13CS have been normalized bysubtracting the local mean from the individual measurements. The data shown here are derived from the same shells from the Gulf of Maine and south Icelandic shelf as are shown inFig. 5.

28 P.G. Butler et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 21–30

Author's personal copy

by any long-term growth trends. Consequently it may be possible toobtain long time series of quite stable δ13CS data which can be linkedto δ13CDIC with relatively small amounts of adjustment. Because of theincorporation of 13C depleted metabolic carbon in the shell, it isunlikely that δ13CS in A. islandica is precipitated in isotopic equilibriumwith the ambient environment, but if the proportion of metaboliccarbon can be determined and if it can be shown to remain stableduring the mature lifetime of the animal, then the extent ofdisequilibrium can be accounted for and a systematic associationcan potentially be established between δ13CS and δ13CDIC.

The results presented here show only that the use as a proxy ofδ13CS from mature specimens of long-lived Arctica islandica may notbe subject to some of the constraints that have been found in otherspecies. Further detailed research will be required to establish theratio of metabolic to inorganic carbon in the shell of A. islandica and itsvariability through time, between individuals and between popula-tions from different regions. It remains necessary to approach thecalibration and interpretation of δ13CS with considerable caution. Thevery slow growth of mature A. islandica presents significantchallenges to the study of carbon fractionation during shell precip-itation, requiring the development and application of experimentalmethods which can obtain meaningful results from very smallamounts of material. A. islandica is nevertheless a unique naturalarchive for the marine environment with relevance to research intoregional ecology, the global carbon cycle and global climate. Theapparent stability of the δ13C signal in its shell is an encouragingindication that this often recalcitrant and unpredictable archive mayyet have something significant to tell us.

Acknowledgements

Research into the material from the Gulf of Maine was fundedthrough the National Science Foundation (NSF ATM-0222553).Collection and study of the shells from Grimsey was funded by theEuropean Union FP6 project 017008 MILLENNIUM. Work on the IrishSea shells was principally funded as part of PGB's PhD research by theCemlyn Jones Trust with additional support from the School of OceanSciences, Bangor University. JDS acknowledges a Royal Society-Leverhulme Trust Senior Research Fellowship. δ13C measurementsfrom a long-lived Icelandic shell (M07) were provided by BerndSchöne. Comments by David Gillikin and one anonymous reviewerenabled us to make significant improvements to the originalmanuscript. We would like to thank the guest editors for inviting usto contribute to this special issue and for their work in preparing it.

Appendix A. Supplementary data

Supplementary data associated with this article can be found, inthe online version, at doi:10.1016/j.palaeo.2010.03.038.

References

Bacastow, R.B., Keeling, C.D., Lueker, T.J., Wahlen, M., Mook, W.G., 1996. The 13C Suesseffect in the world surface oceans and its implications for oceanic uptake of CO2:analysis of observations at Bermuda. Global Biogeochemical Cycles 10, 335–346.

Broecker, W.S., 1992. The influence of air and sea exchange on the carbon isotopedistribution in the sea. Global Biogeochemical Cycles 6, 315–320.

Butler, P.G., Richardson, C.A., Scourse, J.D., Shammon, T.M.,Wanamaker Jr., A.D., Bennell,J.D., 2010. Marine climate in the Irish Sea: analysis of a 489-year marine masterchronology derived from growth increments in the shell of the clam Arcticaislandica. Quaternary Science Reviews. doi:10.1016/j.quascirev.2009.07.010.

Butler, P.G., Richardson, C.A., Scourse, J.D., Witbaard, R., Schöne, B.R., Fraser, N.M.,Wanamaker Jr, A.D., Bryant, C.L., Harris, I., Robertson, I., 2009a. Accurate incrementidentification and the spatial extent of the common signal in five Arctica islandicachronologies from the Fladen Ground, northern North Sea. Paleoceanography 24,PA2210.

Butler, P.G., Scourse, J.D., Richardson, C.A., Wanamaker Jr, A.D., Bryant, C., Bennell, J.D.,2009b. Continuous marine radiocarbon reservoir calibration and the 13C Suesseffect in the Irish Sea: results from the first absolutely dated multi-centennial shell-based marine master chronology. Earth and Planetary Science Letters 279,230–241.

Coffin, R.B., Cifuentes, L.A., 1999. Stable isotope analysis of carbon cycling in the PerdidoEstuary, Florida. Estuaries 22, 917–926.

Dettman, D.L., Reische, A.K., Lohmann, K.C., 1999. Controls on the stable isotopecomposition of seasonal growth bands in aragonitic fresh-water bivalves (union-idae). Geochimica et Cosmochimica Acta 63, 1049–1057.

Enfield, D.B., Mestas-Nunez, A.M., Trimble, P.J., 2001. The Atlantic multidecadaloscillation and its relation to rainfall and river flows in the continental US.Geophysical Research Letters 28, 2077–2080.

Epstein, S., Buchsbaum, R., Lowenstam, H., Urey, H.C., 1953. Revised carbonate-waterisotopic temperature scale. Geological Society of America Bulletin 64, 1315–1326.

Foster, L., 2007. The potential of high resolution palaeoclimate reconstruction fromArctica islandica. PhD. Thesis, University of St. Andrews, St Andrews, UK., 372 pp.

Foster, L.C., Allison, N., Finch, A.A., Andersson, C., Ninnemann, U.S., 2009. Controls ondelta δ18O and δ13C profiles within the aragonite bivalve Arctica islandica.Holocene 19, 549–558.

Gatien, M.G., 1976. Study in Slope Water Region South of Halifax. Journal of theFisheries Research Board of Canada 33, 2213–2217.

Gillikin, D.P., Lorrain, A., Bouillon, S., Willenz, P., Dehairs, F., 2006. Stable carbon isotopiccomposition of Mytilus edulis shells: relation to metabolism, salinity, delta C-13(DIC) and phytoplankton. Organic Geochemistry 37, 1371–1382.

Gillikin, D.P., Lorrain, A., Meng, L., Dehairs, F., 2007. A large metabolic carboncontribution to the delta C-13 record in marine aragonitic bivalve shells.Geochimica et Cosmochimica Acta 71, 2936–2946.

Goericke, R., Fry, B., 1994. Variations of marine plankton δ13C with latitude, temperature,and dissolved CO2 in the world ocean. Global Biogeochemical Cycles 8, 85–90.

Goodwin, D.H., Flessa, K.W., Schöne, B.R., Dettman, D.L., 2001. Cross-calibration of dailygrowth increments, stable isotope variation, and temperature in the Gulf ofCalifornia bivalve mollusk Chione cortezi: implications for paleoenvironmentalanalysis. Palaios 16, 387–398.

Fig. 8. Biological ages of δ13CS samples from Grimsey and the Irish Sea which used shell material deposited since 1850. No bias is apparent (r2=0.0002, N=22, p=0.95), showingthat the 13C Suess effect does not affect the trends shown in Figs. 2 and 3.

29P.G. Butler et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 21–30

Author's personal copy

Gray, S.T., Graumlich, L.J., Betancourt, J.L., Pederson, G.T., 2004. A tree-ring basedreconstruction of the Atlantic Multidecadal Oscillation since 1567 AD. GeophysicalResearch Letters 31.

Greene, C.H., Pershing, A.J., 2003. The flip-side of the North Atlantic Oscillation and modalshifts in slope-water circulation patterns. Limnology and Oceanography 48, 319–322.

Grossman, E.L., Ku, T.L., 1986. Oxygen and carbon isotope fractionation in biogenicaragonite — temperature effects. Chemical Geology 59, 59–74.

Helama, S., Schöne, B.R., Black, B.A., Dunca, E., 2006. Constructing long-term proxyseries for aquatic environments with absolute dating control using a sclerochro-nological approach: introduction and advanced applications. Marine and Fresh-water Research 57, 591–599.

Helama, S., Schöne, B.R., Kirchhefer, A.J., Nielsen, J.K., Rodland, D.L., Janssen, R., 2007.Compound response of marine and terrestrial ecosystems to varying climate: pre-anthropogenic perspective from bivalve shell growth increments and tree-rings.Marine Environmental Research 63, 185–199.

Hickson, J.A., Johnson, A.L.A., Heaton, T.H.E., Balson, P.S., 1999. The shell of the QueenScallop Aequipecten opercularisis (L.) as a promising tool for palaeoenvironmentalreconstruction: evidence and reasons for equilibrium stable-isotope incorporation.Palaeogeography, Palaeoclimatology, Palaeoecology 154, 325–337.

Keeling, C.D., 1979. The Suess effect: 13Carbon–14Carbon interrelations. EnvironmentInternational 2, 229–300.

Keith, M.L., Anderson, G.M., Eichler, R., 1964. Carbon and oxygen isotopic compositionof mollusk shells from marine and freshwater environments. Geochimica etCosmochimica Acta 28, 1757–1786.

Keller, N., Del Piero, D., Longinelli, A., 2002. Isotopic composition, growth rates andbiological behaviour of Chamelea gallina and Callista chione from the Gulf of Trieste(Italy). Marine Biology 140, 9–15.

Kennedy, H., Richardson, C.A., Duarte, C.M., Kennedy, D.P., 2001. Oxygen and carbonstable isotopic profiles of the fan mussel, Pinna nobilis, and reconstruction of seasurface temperatures in the Mediterranean. Marine Biology 139, 1115–1124.

Krantz, D.E., Williams, D.F., Jones, D.S., 1987. Ecological and paleoenvironmentalinformation using stable isotope profiles from living and fossil molluscs.Palaeogeography, Palaeoclimatology, Palaeoecology 58, 249–266.

Kroopnick, P., 1980. The distribution of 13C in the Atlantic Ocean. Earth and PlanetaryScience Letters 49, 469–484.

Lorrain, A., Paulet, Y.M., Chauvaud, L., Dunbar, R., Mucciarone, D., Fontugne, M., 2004.δ13C variation in scallop shells: increasing metabolic carbon contribution withbody size? Geochimica et Cosmochimica Acta 68, 3509–3519.

Marchitto, T.M., Jones, G.A., Goodfriend, G.A., Weidman, C.R., 2000. Precise temporalcorrelation of Holocene mollusk shells using sclerochronology. QuaternaryResearch 53, 236–246.

McConnaughey, T., 1989a. C-13 and O-18 isotopic disequilibrium in biologicalcarbonates. 1. Patterns. Geochimica et Cosmochimica Acta 53, 151–162.

McConnaughey, T., 1989b. C-13 and O-18 isotopic disequilibrium in biologicalcarbonates. 2. Invitro simulation of kinetic isotope effects. Geochimica etCosmochimica Acta 53, 163–171.

McConnaughey, T.A., Gillikin, D.P., 2008. Carbon isotopes in mollusk shell carbonates.Geo-Marine Letters 28, 287–299.

McConnaughey, T.A., Burdett, J., Whelan, J.F., Paull, C.K., 1997. Carbon isotopes inbiological carbonates: respiration and photosynthesis. Geochimica et Cosmochi-mica Acta 61, 611–622.

McKenzie, J.A., 1985. Carbon isotopes and productivity in the lacustrine and marineenvironment. In: Stumm, W. (Ed.), Chemical Processes in Lakes. Wiley, New York,pp. 99–118.

Mook, W.G., Tan, F.C., 1991. Stable carbon isotopes in rivers and estuaries. In: Degens,E.T., Kempe, S., Richey, J.E. (Eds.), Biogeochemistry of Major World Rivers. JohnWiley and Sons Ltd, London, pp. 245–264.

O'Donnell, T.H., Macko, S.A., Chou, J., Davis-Hartten, K.L., Wehmiller, J.F., 2003. Analysisof delta C-13, delta N-15, and delta S-34 in organic matter from the biominerals ofmodern and fossil Mercenaria spp. Organic Geochemistry 34, 165–183.

Owen, E.F., Wanamaker, A.D., Feindel, S.C., Schone, B.R., Rawson, P.D., 2008. Stablecarbon and oxygen isotope fractionation in bivalve (Placopecten magellanicus)larval aragonite. Geochimica et Cosmochimica Acta 72, 4687–4698.

Petrie, B., Drinkwater, K., 1993. Temperature and salinity variability on the Scotian Shelfand in the Gulf of Maine 1945–1990. Journal of Geophysical Research—Oceans 98,20,079–20,089.

Quay, P.D., Tilbrook, B., Wong, C.S., 1992. Oceanic uptake of fossil-fuel CO2–13C

evidence. Science 256, 74–79.Romanek, C.S., Grossman, E.L., Morse, J.W., 1992. Carbon isotopic fractionation in

synthetic aragonite and calcite — effects of temperature and precipitation rate.Geochimica et Cosmochimica Acta 56, 419–430.

Salisbury, J., Vandemark, D., Hunt, C., Campbell, J., Jonsson, B., Mahadevan, A., McGillis,W., Xue, H.J., 2009. Episodic riverine influence on surface DIC in the coastal Gulf ofMaine. Estuarine, Coastal and Shelf Science 82, 108–118.

Schöne, B.R., Fiebig, J., 2009. Seasonality in the North Sea during the Allerod and LateMedieval Climate Optimum using bivalve sclerochronology. International Journalof Earth Sciences 98, 83–98.

Schöne, B.R., Kröncke, I., Houk, S.D., Castro, A.D.F., 2002. The cornucopia of chillywinters: ocean quahog (Arctica islandica L., Mollusca) master chronology revealsbottom water nutrient enrichment during colder winters (North Sea). Senck-enbergiana Maritima 32, 1–13.

Schöne, B.R., Castro, A.D.F., Fiebig, J., Houk, S.D., Oschmann, W., Kröncke, I., 2004. Seasurface water temperatures over the period 1884–1983 reconstructed from oxygenisotope ratios of a bivalve mollusk shell (Arctica islandica, southern North Sea).Palaeogeography, Palaeoclimatology, Palaeoecology 212, 215–232.

Schöne, B.R., Fiebig, J., Pfeiffer, M., Gless, R., Hickson, J., Johnson, A.L.A., Dreyer, W.,Oschmann, W., 2005a. Climate records from a bivalved Methuselah (Arcticaislandica, Mollusca; Iceland). Palaeogeography, Palaeoclimatology, Palaeoecology228, 130–148.

Schöne, B.R., Houk, S.D., Castro, A.D.F., Fiebig, J., Oschmann, W., Kröncke, I., Dreyer, W.,Gosselck, F., 2005b. Daily growth rates in shells of Arctica islandica: assessing sub-seasonal environmental controls on a long-lived bivalvemollusk. Palaios 20, 78–92.

Schöne, B.R., Pfeiffer, M., Pohlmann, T., Siegismund, F., 2005c. A seasonally resolvedbottom-water temperature record for the period AD 1866–2002 based on shells ofArctica islandica (Mollusca; North Sea). International Journal of Climatology 25,947–962.

Schöne, B.R., Wanamaker Jr, A.D., Fiebig, J., Thébault, J., Kreutz, K.J., 2011. Annuallyresolved δ13C shell chronologies of long-lived bivalve mollusks (Arctica islandica)reveal oceanic carbon dynamics in the temperate North Atlantic during recentcenturies. Palaeogeography Palaeoclimatology Palaeoecology 302, 31–42(this issue).

Scourse, J.D., Richardson, C.A., Forsythe, G., Harris, I., Heinemeier, J., Fraser, N.M., Briffa,K.R., Jones, P.D., 2006. First cross-matched floating chronology from the marinefossil record: data from growth lines of the long-lived bivalve mollusc Arcticaislandica. Holocene 16, 967–974.

Suess, H.E., 1953. Natural radiocarbon and the rate of exchange of carbon dioxidebetween the atmosphere and the sea. In: Aldrich, W. (Ed.), Nuclear Processes inGeologic Settings. University of Chicago Press, Chicago, pp. 52–56.

Sutton, R.T., Hodson, D.L.R., 2005. Atlantic Ocean forcing of North American andEuropean summer climate. Science 309, 115–118.

Tanaka, N., Monaghan, M.C., Rye, D.M., 1986. Contribution of metabolic carbon tomollusk and barnacle shell carbonate. Nature 320, 520–523.

Thompson, I., Jones, D.S., 1977. The ocean quahog, Arctica islandica, “tree” of the northAtlantic shelf. Annual Meeting of the Geological Society of America Abstracts, 9,p. 1199.

Thompson, I., Jones, D.S., Ropes, J.W., 1980. Advanced age for sexual maturity in theocean quahog Arctica islandica (Mollusca: Bivalvia). Marine Biology 57, 35–39.

Wanamaker, A.D., Kreutz, K.J., Borns, H.W., Introne, D.S., Feindel, S., Barber, B.J., 2006. Anaquaculture-based method for calibrated bivalve isotope paleothermometry.Geochemistry, Geophysics, Geosystems 7.

Wanamaker, A.D., Kreutz, K.J., Borns, H.W., Introne, D.S., Feindel, S., Funder, S., Rawson,P.D., Barber, B.J., 2007. Experimental determination of salinity, temperature,growth, and metabolic effects on shell isotope chemistry of Mytilus edulis collectedfrom Maine and Greenland. Paleoceanography 22.

Wanamaker, A.D., Heinemeier, J., Scourse, J.D., Richardson, C.A., Butler, P.G., Eiriksson, J.,Knudsen, K.L., 2008a. Very long-lived mollusks confirm 17th century AD tephra-based radiocarbon reservoir ages for north Icelandic shelf waters. Radiocarbon 50,399–412.

Wanamaker, A.D., Kreutz, K.J., Schöne, B.R., Pettigrew, N., Borns, H.W., Introne, D.S.,Belknap, D., Maasch, K.A., Feindel, S., 2008b. Coupled North Atlantic slope waterforcing on Gulf of Maine temperatures over the past millennium. Climate Dynamics31, 183–194.

Wefer, G., Berger, W.H., 1991. Isotope paleontology — growth and composition ofextant calcareous species. Marine Geology 100, 207–248.

Weidman, C.R., Jones, G.A., Lohmann, K.C., 1994. The long-lived mollusc Arcticaislandica: a new paleoceanographic tool for the reconstruction of bottomtemperatures for the continental shelves of the northern north Atlantic ocean.Journal of Geophysical Research 99, 18,305–18,314.

Weiner, S., Dove, P.M., 2003. An overview of biomineralization processes and theproblem of the vital effect. Reviews in Mineralogy and Geochemistry 54, 1–29.

Witbaard, R., Jenness, M.I., Vanderborg, K., Ganssen, G., 1994. Verification of annualgrowth increments in Arctica islandica L from the North Sea by means of oxygenand carbon isotopes. Netherlands Journal of Sea Research 33, 91–101.

Witbaard, R., Duineveld, G.C.A., DeWilde, P.A.W.J., 1997. A long-term growth recordderived from Arctica islandica (Mollusca, Bivalvia) from the Fladen Ground(northern North Sea). Journal of the Marine Biological Association (UnitedKingdom) 77, 801–816.

30 P.G. Butler et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 21–30