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

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

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Palaeogeography, Palaeoclimatology, Palaeoecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p a l a e o

Long-term stability of δ13C with respect to biological age in the aragonite shell of mature specimens of the bivalve mollusk Arctica islandica Paul G. Butler a,⁎, Alan D. Wanamaker Jr. b, James D. Scourse a, Christopher A. Richardson a, David J. Reynolds a a b

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

a r t i c l e

i n f o

Article history: Received 5 November 2009 Received in revised form 26 February 2010 Accepted 14 March 2010 Available online 19 March 2010 Keywords: Arctica islandica Stable carbon isotopes Sclerochronology Mollusk Dissolved inorganic carbon North Atlantic

a b s t r a c t The stable carbon isotope ratio in bivalve shells (δ13CS) is an enigmatic geochemical archive whose interpretation is often frustrated by the intrusion of variable and unpredictable vital effects which can influence the mix of metabolic and dissolved inorganic carbon (DIC) in the shell material. The impacts of vital effects and rapid changes in calcification rates on the variability and value of δ13CS have been described in a number 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, by contrast, spend most of their lives in the mature, slow-growing phase, and it might be expected that in these instances the effect of changes in calcification rates on δ13CS would be less marked, or even absent. Analysis of δ13CS in mature (N 40 years old) Arctica islandica, reported here, indicates that this is the case. δ13CS in shell samples with biological ages between 42 and 391 years from four distinct sites in the North Atlantic shelf seas (Gulf of Maine, north Icelandic shelf, Irish Sea and North Sea) shows no age-related trend. This suggests that metabolic vital effects in mature A. islandica may be reasonably stable at the population level. If the drivers 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 in nutrient 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 to have significant potential as a natural archive of the marine environment 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 increments deposited in its shell which encapsulate the growth history of each individual in the variability of the increment widths. Individual increment width patterns have been shown to be synchronized both within and between populations, providing prima facie evidence that increment width variability incorporates a common environmental signal (Witbaard et al., 1997; Marchitto et al., 2000; Schöne et al., 2002; Helama et al., 2006; Butler et al., 2009a,b, 2010). It has recently been shown that by using crossmatching and detrending techniques derived from dendrochronology it is possible to construct multicentennial master chronologies extending back before the lifetime of any living animals and before the introduction of instrumental records of environmental parameters (Butler et al., 2009b, 2010). Such ⁎ Corresponding author. Tel.: + 44 1248 382853; fax: +44 1248 716367. E-mail addresses: [email protected] (P.G. Butler), [email protected] (A.D. Wanamaker), [email protected] (J.D. Scourse), [email protected] (C.A. Richardson), [email protected] (D.J. Reynolds). 0031-0182/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2010.03.038

chronologies make available absolutely dated shell material from which long annually resolved time series of geochemical data can be derived. Where they can be shown to reflect a consistent response function of known parameters, geochemical properties can function as powerful and robust environmental proxies. For example, the response of the stable oxygen isotope ratio (δ18OS) in biogenic aragonite to seawater temperature and seawater δ18O is well known (Grossman and Ku, 1986; Goodwin et al., 2001) and this response has been used together with δ18OS analyses from A. islandica to reconstruct palaeotemperatures (e.g. Schöne et al., 2005a,c; Wanamaker 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 shell material (δ13CS) are less well understood. They include the δ13C of the dissolved inorganic carbon in the ambient seawater (δ13CDIC), the δ13C of the animals' food source (δ13CF) and the proportions of metabolic and 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 and Gillikin, 2008; Owen et al., 2008). The analysis is further complicated by complex exchanges between the organic and inorganic pools of dissolved carbon, with δ13CDIC being increased when photosynthesizing organisms preferentially remove 12C from the inorganic pool and decreased by the subsequent oxidation of organic matter (McKenzie,

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1985; Coffin and Cifuentes, 1999; Gillikin et al., 2006). If carbon isotope fractionation during shell formation occurs in isotopic equilibrium with seawater DIC, or if the non-equilibrium element can be accounted for, then δ13CS in Arctica islandica has the potential to act as a proxy for δ13CDIC in the amphi-Atlantic shelf seas. This is a key goal of research into the connections between the carbon cycle and global climate change, since oceanic δ13CDIC has been identified as a significant parameter in the determination of the role of the ocean 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 equilibrium may occur as a result of vital effects, precluding or complicating the use of δ13CS as a reliable indicator of δ13CDIC. Following McConnaughey (1989a), vital effects can be categorized as metabolic or kinetic, where metabolic effects are due to the introduction of 13C-depleted respired carbon into the internal DIC pool and kinetic effects result from incomplete isotopic partitioning during hydration and hydroxylation of CO2 at the shell calcification site. In marine mollusks, metabolic effects are thought to be the cause of ontogenetically decreasing δ13CS, with increasing proportions of 13C-depleted metabolic carbon being incorporated in the inorganic shell matrix as the animal becomes older and the metabolic rate increases in relation to the growth rate (Keller et al., 2002; Lorrain et al., 2004; Gillikin et al., 2007). By contrast, kinetic effects discriminate against the heavy isotopes of carbon and oxygen when high rates of calcification do not allow isotopic partitioning at the calcification site to proceed to completion (McConnaughey, 1989b). In this case similar processes affect both carbon and oxygen partitioning, so that in the absence of any freshwater influence the presence of kinetic disequilibrium effects can be inferred from a positive correlation between δ13CS and δ18OS. The isotopic fractionation of shell aragonite out of equilibrium with its ambient surroundings constitutes a significant constraint on the use of δ13CS as an environmental proxy. Since the extent of metabolic and kinetic disequilibrium effects can be interpreted as a response to changes in calcification rates (and hence growth rates), the conventional ontogenetic trend in mollusks of rapidly decreasing growth rates during the early years of life may be mirrored in the value of δ13CS, expressing itself as a trend to a lighter isotopic ratio. A number of studies in which such trends have been observed in marine mollusks are cited by McConnaughey and Gillikin (2008). For example Krantz et al. (1987) found δ13CS decreasing by 1–2‰ in modern and fossil 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 old and Gillikin et al. (2007) found decreases of as much as 4‰ in δ13CS in Mercenaria mercenaria shells up to 40 years old. Conversely, Keller et al. (2002) found no trend in δ13CS in Callista chione up to 11 years old. A consistent aspect of these and other studies, however, is that their focus is precisely on those periods of rapidly decreasing growth rates when ontogenetic trends in δ13CS are most likely to be observed. The majority of mollusk species are not especially long-lived; hence the phases of very fast initial growth followed by decreasing growth rates in subsequent years characterize all or nearly all of the available shell material and it is not surprising to find that analyses of δ13CS have tended to reflect strong gradients in calcification rates. No previous analysis of δ13CS has specifically targeted those parts of the shells of long-lived animals that are not characterized by strong ontogenetic growth trends. The extremely long-lived bivalve mollusk Arctica islandica shows little or no trend in growth rate after the first ∼ 40 years of life (Schöne et 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 available for the study of stable carbon isotope ratios which are not (if the argument advanced in this paper is correct) affected by changes in calcification rates. If there are no significant vital effects impacting

δ13CS during most of the lifetime of the animal, or if such vital effects as exist are reasonably stable and can be quantified, a significant constraint on the usefulness of the archive would be removed, and other associated complexities, such as the proportions of metabolic and inorganic carbon that go to make up the shell matrix, might be approached in a more systematic way. It may then become feasible to use extended δ13CS time series based on multi-centennial crossmatched A. islandica chronologies to investigate long-term changes in food sources or in the role of the shelf seas as a source or sink for atmospheric CO2. This study reports δ13C analyses of samples with biological ages between 42 years and 391 years taken from Arctica islandica shells from sites in US, Icelandic and UK waters. The chronological dates of these shells, determined by AMS radiocarbon dating or by sclerochronology (i.e. increment width counting and pattern matching; Helama et al., 2006; Butler et al., 2009b), are distributed throughout the past 1300 years. The material reported here is derived from a number of different studies which focussed variously on multiple δ13C analyses of single shells (Witbaard et al., 1994; Wanamaker et al., 2008b) or single analyses of multiple shells (Butler et al., 2009b), so although the number of δ13C determinations reported for individual shells ranges between one and 109, most of the shells were analysed only once. It is hypothesized here that the within shell variability of δ13CS in mature A. islandica does not exceed the variability of δ13CS in the population and is not dependant in any way on the biological age of the analysed sample. The term ‘mature’ is used here to refer to specimens whose shell growth is not characterized by the strong decreasing trend typical of younger animals. Although the cut off point between the earlier period of strong growth trend and the later period of little or no trend can be quite variable, both between individuals and between populations, previous research indicates that a 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 to the analysis. The focus of this paper is on the stability of the δ13CS signal with respect to biological age in mature specimens of A. islandica contrasted with the typical strong trends that characterize the shells of younger animals. 2. Data and methods The data used in this study are derived from stable carbon isotope analyses 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). Material was sampled from the left valves of three articulated fossil specimens (GOM30, GOM4047 and GOM48) collected in a vibracore from a depth of 38 m (see Wanamaker et al., 2008b for further details of the collection and preparation procedures). The data used here are annualised averages of analyses of multiple micromilled samples taken from within each growth increment. For the analysis of δ13CS in older animals, measurements were only available from GOM30 (biological ages from 41 to 114 years). AMS 14C dating indicates that the animals were living during the 10th century AD (GOM48) and the 14th and 15th centuries AD (GOM30 and GOM4047). Stable carbon isotope ratios were measured at University of Frankfurt (Germany) on a Finnigan MAT-253 continuous-flow mass spectrometer, to a precision of 0.05‰, and are reported as δ13C relative to the VPDB carbonate standard based on NBS-19 calibrated values of + 2.02‰. (b) North Icelandic shelf, close to the island of Grimsey (66° 32′N 18° 12′ W). Material was sampled from thirteen single valves from fossil shells and one articulated pair from a live-collected

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

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

specimen. All shells were trawled from the seabed at a depth of ∼75 m using a bespoke dredge (see Wanamaker et al., 2008a for further details of collection and preparation). Thirteen of the samples consisted of bulk material removed from the ventral margin (i.e. the most recently deposited part of the shell) for AMS 14C rangefinder determinations. In order to avoid the inclusion of material from the nacreous (inner) shell layer the samples were cut distal to the pallial line. These samples are assumed to integrate up to ∼ 40 years of shell deposition. In the case of three of the shells (061297, 061312 and 061664), material was drilled from the exposed crosssectional surface (see Wanamaker et al., 2008a, fig. 3) at a number of positions between the umbo and the ventral margin with the intention of analysing shell material produced during specified periods within the lifetime of the animal. Twenty samples were obtained in this way (four from 061297, seven from 061312 and nine from 061664). The maximum number of years integrated in these samples is 5 years. All samples have been precisely dated using sclerochronology (increment counting and increment pattern matching) and the dates of the midpoints of the samples range between AD 705 and AD 1915. Stable carbon isotope ratios were measured at University of Aarhus (Denmark) on a GV Instruments Isoprime stable isotope mass spectrometer, to a precision of 0.15‰, and are reported as δ13C relative to the VPDB carbonate standard based on NBS-19 calibrated values of + 1.95‰. For the analysis of δ13CS in younger animals, measurements were obtained from another shell from Icelandic waters (M07; Schöne et al., 2005a). In this case, the data are annualised averages of analyses of multiple micromilled samples taken from within each growth increment for biological ages 2 to 39 years. The precise provenance of this shell (which was obtained from a museum collection) is unknown, although it is thought to come from the south Icelandic shelf (Schöne et al., 2005a; Wanamaker et al., 2008a). The samples described here have been precisely dated using band counting to the years AD 1496–1533. For this shell, stable carbon isotope ratios were measured at University of Frankfurt (Germany) on a Finnigan MAT-253 continuous-flow mass spectrometer, to a precision of 0.05‰, and are reported as δ13C relative to the VPDB carbonate standard based on NBS-19 calibrated values of +2.02‰. (c) Irish Sea, UK waters, off the west coast of the Isle of Man (54° 10′N 4° 50′W). Material was sampled from thirty-seven single valves from fossil shells trawled from the seabed at depths between 30 m and 70 m using a bespoke dredge (see Butler et al., 2009b

for further details of collection and preparation). All samples consisted of bulk material removed from the ventral margin distal 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 sclerochronology and the dates of the midpoints of the samples range between AD 1573 and AD 1981. Stable carbon isotope ratios were measured at the NERC Radiocarbon Laboratory (UK) using a dual-inlet mass spectrometer, to a precision of 0.14‰, and are reported as δ13C relative to the VPDB carbonate standard based on NBS-19 calibrated 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 of valves from two live-collected specimens collected at water depth ∼30 m (RWL7 and RW4C; see Witbaard et al., 1994 for further details of collection and preparation). All samples consisted of bulk material removed from the outer shell surface for AMS 14C rangefinder determinations and were reported to integrate 5 years of deposition. The five samples from shell RWL7 with biological ages greater than 40 years have been dated by increment counting; their midpoints range between AD 1966 and AD 1986. Stable carbon isotope ratios were measured at the University of Utrecht (Netherlands) and are expressed as a per mille (‰) deviation from the Pee Dee Belemnite (PDB) standard. The analytical precision was not reported. The hypothesis that there is no ontogenetic trend in stable carbon isotope ratios in the shells of mature Arctica islandica was tested by regressing the δ13CS values for each of the four sites against the biological ages of the samples used for analysis. Further, the δ13CS values for each site were normalized by subtracting the local mean from each individual value and combined into a single dataset which was also regressed against the biological ages. The data presented in all the charts in this paper can be found in the accompanying Appendix.

3. Results and discussion 3.1. Relationship between δ13CS and biological age Fig. 2 shows for each location the relationship between δ13CS and the biological age of the samples. The regression parameters and their significance levels are shown in Table 1, and the mean δ13CS values and their standard deviations for each of the four groups are in Table 2.

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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 filled diamonds (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 of them 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 annual increments.

At three of the four sites considered, no trend is apparent in the relationship between the value of δ13CS and the biological age of the analysed sample. The set of results for Grimsey, in particular, includes samples with a wide range of biological ages (42 to 391 years) which nevertheless maintain consistent values of δ13CS and relatively low variability (standard deviation = 0.27). The variability of the Irish Sea measurements is greater than that of any of the other groups but here also no trend in δ13CS is apparent for biological ages between 42 and 219 years. The North Sea analyses, all of which come from a single shell, are limited in number and range of ages but within these constraints no trend is apparent. Only the Gulf of Maine measurements appear to contradict the hypothesis that there is no link between the value of δ13CS and biological age. The seventy-four annualised averages from a single shell show a significant positive trend in δ13CS between 41 and 114 years. The range and standard deviation of the δ13CS values, however, remain below those of the very stable 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 the maximum variability of 0.76‰ reported elsewhere in this issue in a study of four extended time series of annually resolved δ13CS measurements in Arctica islandica from Iceland and the Gulf of Maine (Schöne et al., 2011-this issue), none of which show any longterm trends apart from those associated with the oceanic 13C Suess effect. The apparent positive trend in δ13CS in the Gulf of Maine shell is therefore consistent with natural variability. This conclusion is further supported by the observation that the rising trend is not consistent through the series but in fact emerges from a sequence consisting of a decreasing trend from 40 to 70 years, then a short period of relatively low values and low variability, followed by a rapid increase between 80 and 90 years and finally a more gradual return to lower values. The

sharp increase leading to the spike around 90 years appears to be strong enough to impart a significant trend to the entire series. The variability observed in this shell may reflect variability in the δ13CDIC of the water in the Gulf of Maine. The composition of Gulf of Maine waters is most likely influenced by the relative strength on the adjacent slope of waters from the cold south-flowing Labrador Current and the warm north-flowing Gulf Stream (e.g. Gatien, 1976; Petrie and Drinkwater, 1993; see Wanamaker et al., 2008b for an overview of the relevant literature). The difference in δ13CDIC between the two water masses may be of the order of 1‰ (see fig. 8 in Kroopnick, 1980) so if we assume a constant enrichment factor for biogenic aragonite the range of δ13CS in the Gulf of Maine shell is consistent with changes in the relative influence of the local water masses. The timescales of such changes can be linked to dominant modes of climate forcing in the region, specifically the Atlantic Multidecadal Oscillation (AMO) (Sutton and Hodson, 2005) and the North Atlantic Oscillation (NAO) (Greene and Pershing, 2003). The 40–50 year period in the δ13CS record described here is slightly shorter than that of the AMO in modern times (Sutton and Hodson, 2005), but a reconstruction of the AMO based on tree-rings indicates that its frequency may have been higher in the middle part of the last millennium (see fig. 3(b) in Gray et al., 2004). A second driver of δ13CDIC variability in the Gulf of Maine may be the input of freshwater from the surrounding catchment, which has been shown to affect the concentrations and character of seawater DIC close to the collection site of the shell described here (Salisbury et al., 2009). That study was concerned only with seasonal changes, but a further strong association has been described between rainfall patterns in the continental US (including specifically the northeast) and the AMO mode which indicates that freshwater input from the continent may also act as a

Table 1 Regression 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 relationship between δ13CS and the biological age of the shell material.

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

Location

Gradient

r2

N

p

Gulf of Maine Grimsey Irish Sea North Sea

0.0034 0.0002 −0.0003 0.0012

0.1562 0.0031 0.0005 0.0021

74 33 37 5

b0.001 0.76 ns 0.90 ns 0.93 ns

Location

Mean δ13CS (‰)

SD (‰)

Number of analyses

Range of biological ages (years)

Gulf of Maine Grimsey Irish Sea North Sea

2.25 2.12 1.21 1.44

0.17 0.27 0.56 0.22

74 33 37 5

41–114 42–391 42–219 43–64

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driver of δ13CDIC variability (and consequently δ13CS variability) on multidecadal timescales (Enfield et al., 2001). Grimsey shell 061312, for which eight determinations are available (filled circles in Fig. 2), shows an initial trend (through biological ages 67 to 212 years) of increasing δ13CS before reverting to the mean value for the site. In the other three cases where there are multiple determinations for individual shells (Grimsey shell 061297 (filled triangles), Grimsey shell 061664 (filled diamonds) and North Sea shell RWL7 (open triangles)) no trend is apparent. Although shorter term trends in δ13CS similar to those observed in the Gulf of Maine specimen may also be present in these shells, it is not possible to discriminate them because of the low resolution of the time series (but see Schöne et al., 2011-this issue for examples of interannual variability in shells from Gulf of Maine and Icelandic waters). It is apparent from Fig. 2 that the shells from UK waters (Irish Sea and North Sea) are slightly depleted (by ∼0.8‰) in 13C when compared with the shells from Grimsey and the Gulf of Maine. Assuming that the proportion of metabolic carbon incorporated in the shell does not vary between populations, this difference can be ascribed to a corresponding depletion in 13C in the seawater DIC. The principle drivers of seawater δ13CDIC are (a) the net removal of isotopically light carbon in surface waters during photosynthesis and the net reintroduction of isotopically light carbon to deep waters during remineralisation (McKenzie, 1985; Broecker, 1992) (b) isotopic equilibration with atmospheric CO2 which produces a temperature driven 13C enrichment gradient with colder waters more 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 sea locations with high and broadly comparable levels of biological productivity, so it is unlikely that the differences in δ13CS between sites result purely from differences in biological drawdown of 12C. The relative enrichment of the shells from Grimsey compared with those from UK waters may be related to one or both of the other drivers of seawater δ13CDIC, since both seawater temperatures and freshwater influence are significantly lower on the North Icelandic Shelf. The same factors, however, should result in δ13CS values for the Gulf of Maine being closer to those found in UK waters. This discrepancy cannot be explained further with the available data, but it is useful to bear in mind that the Gulf of Maine measurements are derived from a single shell and are probably subject to life and environmental effects that are constrained in space and time, whereas the Grimsey and Irish

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Sea values, being distributed in time and derived from multiple shells, likely present a more synoptic overview. When the four groups are combined by merging residuals from the local means into a single dataset (Fig. 3), the trend line is flat. It should however be noted that the data as shown in Fig. 3 combine annualised averages from the Gulf of Maine shell with integrated measurements from the other sites. They are presented in this way to aid visualization, but need to be homogenized for statistical validity by assigning the δ13C value for each integrated sample to each year within the integration before calculating the mean and residuals. For the homogenization: (1) for the samples from Grimsey and Irish Sea shells that were removed from the ventral margin it was assumed that 19, 29 and 39 years were integrated where the biological age at the sample point was respectively b100, 101–200 and N200 years; (2) for the samples from Grimsey shells that were drilled from the exposed cross-sectional surface it was assumed that 5 years were integrated in each sample; and (3) for the samples from North Sea shells it was assumed that 5 years were integrated in each sample. After homogenization, all the data points represent annual values and there is no significant trend (r2 = 0.0017, N = 1702, p = 0.09 for all the data; r2 = 0.002, N = 1628, p = 0.07 if the Gulf of Maine measurements are excluded). The regression line shown in Fig. 3 is derived from the homogenized data including the annualised Gulf of Maine measurements. 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 can usefully be contrasted with its variability in juvenile specimens (Fig. 4 and Table 3). Typically, juvenile A. islandica exhibits the decreasing 13 12 C/ C ratios often observed in other young and fast growing mollusks (see references in the Introduction to this paper). For example, in all three shells from the Gulf of Maine (GOM30, GOM 4047 and GOM48 in Fig. 4) δ13CS decreased during the first 40 years of growth, 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 the figure, the number of data points is too small to reach statistical significance), and in three shells from Scottish inshore waters (not shown 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 been normalized by subtracting the local mean from the individual measurements. In order to ensure statistical equivalence for the regression, the data were homogenized by assigning annual 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 the homogenized data, but for ease of visualization only the central point is shown for each bulk sample.

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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 black or blue line and filled circles) are annually averaged measurements from single shells; data from the North Sea (thin black or green lines and filled triangles) are from two shells, each measurement integrated over ∼5 annual increments (see Witbaard et al., 1994, Table 2).

between 18 and 32 years. Only in the case of the very long-lived specimen from Icelandic waters (M07) reported by Schöne et al. (2005a) does there appear to be no trend in δ13CS during the first 40 years of life (filled circles in Fig. 4). In another shell from the North Sea, also reported by Witbaard et al. (1994), the initial 6 years of growth were sampled at high resolution. In this case, δ13CS actually increased by ∼1‰. Since the first few years of growth in A. islandica are characterized by a rapidly increasing growth rate, this may be an indication that δ13CS is sensitive to growth rate in the manner described by Lorrain et al. (2004). They argue that the ratio between the availability of metabolic carbon and the amount of carbonate precipitated determines the proportion of metabolic carbon incorporated into the shell and hence the value of δ13CS. When growth is slow, this ratio is high and a greater proportion of isotopically light metabolic carbon is utilized, so that δ13CS decreases as the growth rate decreases. The very early years of growth were not always analysed in the studies described here, but where they are reported the results seem to confirm the rising trend seen by Witbaard et al. (1994). Detailed subannual δ13CS measurements are available for the first 40 years of growth for four of the shells used in this study (three from the Gulf of Maine and one Icelandic specimen (M07; Schöne et al., 2005a)). Fig. 5 shows a composite dataset consisting of residuals of the annualised data for these four shells. Three distinct phases in the relationship between δ13CS and biological age are apparent; an initial period (ages 1 to 8) of strong positive correlation (p b 0.0001), an intermediate period (ages 9 to 15) of no trend, and a final phase (ages 16 to 40) of strong negative correlation (p b 0.0001). The period of stable δ13CS between ages 9 and 15 is apparent in each individual specimen and does not appear to be an artefact of the variability of timing of

Table 3 Regression parameters for the trend lines shown in Fig. 4. Strongly significant relationships 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 the two North Sea specimens are not significant, probably because of the small number of data points. Location and shell

Gradient

r2

N

p

Gulf of Maine GOM30 Gulf of Maine GOM4047 Gulf of Maine GOM48 Iceland M07 North Sea RWL7 North Sea RW4C

−0.0183 −0.0089 −0.0284 −0.0026 −0.0202 −0.0715

0.5188 0.0963 0.5721 0.0209 0.3072 0.4324

35 34 37 38 7 6

b0.0001 0.07 ns b0.0001 0.40 ns 0.20 ns 0.16 ns

maximum δ13CS. This age range is of particular interest. As well as being a period of rapidly changing growth rate, it also marks the onset of sexual maturity in Arctica islandica (Thompson et al., 1980). It is possible that an additional burden is placed on the pool of metabolic carbon during this period, reducing the availability of metabolic carbon for shell deposition and leaving the shell enriched in 13C even while growth rates are decreasing. 3.3. Influence of growth rate on δ13CS in juvenile and mature Arctica islandica Although it has been shown above that the kind of strong ontogenetic trends in δ13CS characteristic of the shells of biologically young animals are not detectable in increments deposited after the age of 40 years, it is still possible to argue that an association between δ13CS and growth rate persists after the initial phase of rapidly changing increment widths. Such an association, if it existed, might not propagate into the analyses described above in Section 3.1 because the part of the variability of δ13CS linked to the growth rate would likely decrease in proportion to the decrease in the variability of the growth rate itself. The impact of other (external) drivers of variability in δ13CS would not be affected by any change in growth rate and would therefore exert a greater proportionate influence on δ13CS, tending to mask the growth rate signal. In addition the analysis described here relies to a considerable extent on bulk analyses from distinct shells which integrate multiple growth increments so that variability in δ13CS between different shells or between different populations may be sufficient to mask any growth rate signal. The only data that can be used to investigate this association is derived from the most long-lived shell from the Gulf of Maine (GOM30), this being the only shell for which annually resolved growth increment widths and δ13CS analyses are available for biological ages in excess of 40 years. The relationship between increment width and δ13CS is shown in Fig. 6 and demonstrates that, for this shell at least, there is no correlation between δ13CS and increment 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 series from this shell (Fig. 2) does not propagate to any link with increment width. This is a further indication that the δ13CS signal in mature Arctica islandica may constitute a coherent and identifiable response to external drivers. For younger specimens, a curious bimodal pattern emerges from the association between δ13CS and growth rate. The pattern of the links between δ13CS and biological age described earlier (Section 3.2

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27

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 south Icelandic shelf. The regressions show a highly significant positive correlation for ages 1–8 (r2 = 0.63, N = 22, p b 0.0001) and a highly significant negative correlation for ages 16–40 (r2 = 0.41, N = 94, p b 0.0001) 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 the Gulf 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 for the North Sea shells).

and Fig. 5) suggests that the association with growth rate should be positive. Although there is a positive correlation for the whole dataset (r2 = 0.04, N = 144, p b 0.05), it is significant only at the 95% level, and the stronger pattern evident from Fig. 7 is a positive association for increment widths ≤2 mm (r2 = 0.24, N = 118, p b 0.0001) and a negative association for widths N2 mm (r2 = 0.32, N = 26, p b 0.01). This may indicate kinetic isotopic disequilibrium at high growth rates (see Section 3.5 below). Around the threshold growth rate (which, as indicated in Fig. 7 may correspond to increment widths between 2 mm and 4 mm) δ13CS is at a maximum. Above this threshold 13C depletion may be driven by kinetic disequilibrium (which increases with faster growth rates). Below the threshold 13C depletion may result from a relative increase in the proportion of metabolic carbon available 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 of metabolic to precipitated carbon as argued by Lorrain et al. (2004), the contrast between the clear trends in the association between δ13CS and biological age during the juvenile years (Figs. 4 and 5) and the lack of trend during the mature years (Figs. 2 and 3) is instructive. It suggests that the ratio of metabolic to precipitated carbonate in the shell is effectively constant through the major part of the life of long-

lived specimens of A. islandica. This conclusion is further supported by the lack of any significant correlation between δ13CS and growth rate in the single shell for which this association could be tested (Fig. 6). Uncertainty about the level and variability of the ratio of metabolic to precipitated carbonate has hitherto been a significant constraint on attempts to use stable carbon isotope ratios in the study of long-term changes in oceanic δ13CDIC on the one hand and in the composition and source of nutrients on the other (Gillikin et al., 2007). In principle δ13CDIC in local waters can be derived using an isotopic mixing equation proposed by McConnaughey et al. (1997):
 13 13 13 R δ C F + ð1−RÞδ C DIC = δ C S –


ð1Þ

where
is an enrichment factor for 13C fractionation between aragonite and bicarbonate, R is the fraction of metabolic carbonate in the shell and δ13CF is the isotopic ratio of the food source. An expression for δ13CDIC can be derived from Eq. (1): h
i 13 13 13 δ C DIC = δ C S –
–R δ C F = ð1−RÞ

ð2Þ


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

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 in this regression (r2 = 0.02, N = 74, p = 0.23), demonstrating that — for this shell at least — δ13CS is not correlated with the growth rate.

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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, p b 0.0001) and a significant negative correlation for increment widths N 2 mm (r2 = 0.32, N = 26, p b 0.01). All values of δ13CS have been normalized by subtracting 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 in Fig. 5.

et al., 2003; Gillikin et al., 2007) or by using the global estimate of −22 ± 5‰ reported for particulate organic carbon by Goericke and Fry (1994). If disequilibrium between δ13CS and δ13CDIC results only from metabolic vital effects, and if the proportion of metabolic carbonate in the shell can be quantified — possibly using the model suggested by Lorrain et al. (2004) — and turns out to be effectively constant at the population level, there would appear to be potential to use long Arctica islandica chronologies to reconstruct δ13CDIC over multi-centennial timescales. 3.5. Metabolic and kinetic disequilibrium in Arctica islandica Kinetic vital effects result from fractionation in favour of 12C during hydration and hydroxylation processes when CO2 reacts in the calcification region to form HCO− 3 (McConnaughey, 1989b). Isotopic equilibrium with the local DIC pool is eventually re-established if the reaction has time to proceed to completion, but during periods of rapid growth the shell can precipitate out of equilibrium (McConnaughey et al., 1997). A similar fractionation process affects the stable oxygen isotope ratio, and the presence of kinetic vital effects can be inferred if 18 O (which is not subject to metabolic fractionation) is precipitated out of equilibrium with surrounding waters or if there is a positive correlation between δ18OS and δ13CS in the absence of significant salinity variations in the surrounding water. Kinetic disequilibria are not typically observed in mollusks, which are thought to use the enzyme carbonic anhydrase to accelerate hydroxylation of CO2 in conditions of relatively mild alkalinity (Weiner and Dove, 2003; McConnaughey and Gillikin, 2008) and which are usually found to precipitate their shells close 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 a proxy for seawater temperature, ambient δ18O is usually determined indirectly 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 correlations between δ18OS and seawater temperatures is an indication that the assumption that shell oxygen is precipitated in isotopic equilibrium with its surroundings is correct, and consequently that kinetic disequilibrium effects are absent. Further, comparison between the annualised analyses of δ18OS and δ13CS from the Gulf of Maine discussed in this study shows that there is no correlation between them, confirming that carbon isotope disequilibrium in mature A. islandica results only from metabolic vital effects. Where growth is very rapid in juvenile A. islandica (growth increments N2 mm; see Section 3.3 above

and Fig. 7) a negative correlation between δ13CS and increment width indicates that, for these very wide increments alone, kinetic disequilibrium behaviour may be driving the 13C deficiency in the shell. 3.6. Possible influence of the

13

C Suess effect

The 13C Suess effect is the term given to the trend to isotopically lighter values of environmental carbon that has occurred during recent decades as a result of the anthropogenic emission of fossil fuel carbon (Suess, 1953; Keeling, 1979). This effect has been demonstrated 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 is conceivable that bias in the chronological distribution of shells of different biological ages may result in the 13C Suess effect masking a long-term ontogenetic trend in δ13CS of shells from mature animals. The masked trend would be positive if a significant proportion of the samples from biologically younger shells came from material deposited during the most recent ∼150 years. Conversely, the masked trend would be negative if a significant proportion of the samples from biologically older shells consisted of recently deposited material. If the recent samples show an even distribution through time, it can reasonably be assumed that the influence of the 13C Suess effect has not masked any significant trends in the regressions shown in Figs. 2 and 3, although it may have the effect of reducing slightly the value of δ13CS in groups which include a significant proportion of recent samples. Fig. 8 shows the distribution of biological ages of samples with respect to time in the period since AD 1850 for the two groups with both recent (dated later than AD 1850) and earlier samples (the Grimsey group has four recent samples and 19 earlier samples; the Irish Sea group has 18 recent and 19 earlier). There is no trend in this association (r2 = 0.014, N = 22, p = 0.95), and we can therefore conclude that the lack of trend shown in Figs. 1 and 2 is not an artefact of any variation of environmental δ13C with time. 4. Conclusion δ13C in the shell of Arctica islandica does not appear to be affected by any age-related trends after the animal has reached a biological age of around 40 years. The variability of δ13CS with growth rate is a common characteristic of molluscan shell geochemistry and in most species it constitutes a significant constraint on the use of δ13CS as a proxy for δ13CDIC in the environment. A. islandica is unique among mollusks, however, in that the bulk of its lifespan (a period which can cover several centuries) is spent in a mature phase not characterized

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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), showing that the 13C Suess effect does not affect the trends shown in Figs. 2 and 3.

by any long-term growth trends. Consequently it may be possible to obtain long time series of quite stable δ13CS data which can be linked to δ13CDIC with relatively small amounts of adjustment. Because of the incorporation of 13C depleted metabolic carbon in the shell, it is unlikely that δ13CS in A. islandica is precipitated in isotopic equilibrium with the ambient environment, but if the proportion of metabolic carbon can be determined and if it can be shown to remain stable during the mature lifetime of the animal, then the extent of disequilibrium can be accounted for and a systematic association can potentially be established between δ13CS and δ13CDIC. The results presented here show only that the use as a proxy of δ13CS from mature specimens of long-lived Arctica islandica may not be subject to some of the constraints that have been found in other species. Further detailed research will be required to establish the ratio of metabolic to inorganic carbon in the shell of A. islandica and its variability through time, between individuals and between populations from different regions. It remains necessary to approach the calibration and interpretation of δ13CS with considerable caution. The very slow growth of mature A. islandica presents significant challenges to the study of carbon fractionation during shell precipitation, requiring the development and application of experimental methods which can obtain meaningful results from very small amounts of material. A. islandica is nevertheless a unique natural archive for the marine environment with relevance to research into regional ecology, the global carbon cycle and global climate. The apparent stability of the δ13C signal in its shell is an encouraging indication that this often recalcitrant and unpredictable archive may yet have something significant to tell us.

Acknowledgements Research into the material from the Gulf of Maine was funded through the National Science Foundation (NSF ATM-0222553). Collection and study of the shells from Grimsey was funded by the European Union FP6 project 017008 MILLENNIUM. Work on the Irish Sea shells was principally funded as part of PGB's PhD research by the Cemlyn Jones Trust with additional support from the School of Ocean Sciences, Bangor University. JDS acknowledges a Royal SocietyLeverhulme Trust Senior Research Fellowship. δ13C measurements from a long-lived Icelandic shell (M07) were provided by Bernd Schöne. Comments by David Gillikin and one anonymous reviewer enabled us to make significant improvements to the original manuscript. We would like to thank the guest editors for inviting us to 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, in the 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 Suess effect 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 isotope distribution 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 master chronology derived from growth increments in the shell of the clam Arctica islandica. 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 increment identification and the spatial extent of the common signal in five Arctica islandica chronologies 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 Suess effect in the Irish Sea: results from the first absolutely dated multi-centennial shellbased 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 Perdido Estuary, Florida. Estuaries 22, 917–926. Dettman, D.L., Reische, A.K., Lohmann, K.C., 1999. Controls on the stable isotope composition of seasonal growth bands in aragonitic fresh-water bivalves (unionidae). Geochimica et Cosmochimica Acta 63, 1049–1057. Enfield, D.B., Mestas-Nunez, A.M., Trimble, P.J., 2001. The Atlantic multidecadal oscillation 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-water isotopic temperature scale. Geological Society of America Bulletin 64, 1315–1326. Foster, L., 2007. The potential of high resolution palaeoclimate reconstruction from Arctica 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 on delta 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 the Fisheries Research Board of Canada 33, 2213–2217. Gillikin, D.P., Lorrain, A., Bouillon, S., Willenz, P., Dehairs, F., 2006. Stable carbon isotopic composition 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 carbon contribution 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 daily growth increments, stable isotope variation, and temperature in the Gulf of California bivalve mollusk Chione cortezi: implications for paleoenvironmental analysis. Palaios 16, 387–398.

30

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

Gray, S.T., Graumlich, L.J., Betancourt, J.L., Pederson, G.T., 2004. A tree-ring based reconstruction of the Atlantic Multidecadal Oscillation since 1567 AD. Geophysical Research Letters 31. Greene, C.H., Pershing, A.J., 2003. The flip-side of the North Atlantic Oscillation and modal shifts in slope-water circulation patterns. Limnology and Oceanography 48, 319–322. Grossman, E.L., Ku, T.L., 1986. Oxygen and carbon isotope fractionation in biogenic aragonite — temperature effects. Chemical Geology 59, 59–74. Helama, S., Schöne, B.R., Black, B.A., Dunca, E., 2006. Constructing long-term proxy series for aquatic environments with absolute dating control using a sclerochronological approach: introduction and advanced applications. Marine and Freshwater 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: preanthropogenic 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 Queen Scallop Aequipecten opercularisis (L.) as a promising tool for palaeoenvironmental reconstruction: evidence and reasons for equilibrium stable-isotope incorporation. Palaeogeography, Palaeoclimatology, Palaeoecology 154, 325–337. Keeling, C.D., 1979. The Suess effect: 13Carbon–14Carbon interrelations. Environment International 2, 229–300. Keith, M.L., Anderson, G.M., Eichler, R., 1964. Carbon and oxygen isotopic composition of mollusk shells from marine and freshwater environments. Geochimica et Cosmochimica Acta 28, 1757–1786. Keller, N., Del Piero, D., Longinelli, A., 2002. Isotopic composition, growth rates and biological 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 carbon stable isotopic profiles of the fan mussel, Pinna nobilis, and reconstruction of sea surface temperatures in the Mediterranean. Marine Biology 139, 1115–1124. Krantz, D.E., Williams, D.F., Jones, D.S., 1987. Ecological and paleoenvironmental information 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 Planetary Science 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 with body size? Geochimica et Cosmochimica Acta 68, 3509–3519. Marchitto, T.M., Jones, G.A., Goodfriend, G.A., Weidman, C.R., 2000. Precise temporal correlation of Holocene mollusk shells using sclerochronology. Quaternary Research 53, 236–246. McConnaughey, T., 1989a. C-13 and O-18 isotopic disequilibrium in biological carbonates. 1. Patterns. Geochimica et Cosmochimica Acta 53, 151–162. McConnaughey, T., 1989b. C-13 and O-18 isotopic disequilibrium in biological carbonates. 2. Invitro simulation of kinetic isotope effects. Geochimica et Cosmochimica 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 in biological carbonates: respiration and photosynthesis. Geochimica et Cosmochimica Acta 61, 611–622. McKenzie, J.A., 1985. Carbon isotopes and productivity in the lacustrine and marine environment. 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. John Wiley and Sons Ltd, London, pp. 245–264. O'Donnell, T.H., Macko, S.A., Chou, J., Davis-Hartten, K.L., Wehmiller, J.F., 2003. Analysis of delta C-13, delta N-15, and delta S-34 in organic matter from the biominerals of modern 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. Stable carbon 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 Shelf and 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 of Maine. Estuarine, Coastal and Shelf Science 82, 108–118.

Schöne, B.R., Fiebig, J., 2009. Seasonality in the North Sea during the Allerod and Late Medieval Climate Optimum using bivalve sclerochronology. International Journal of Earth Sciences 98, 83–98. Schöne, B.R., Kröncke, I., Houk, S.D., Castro, A.D.F., 2002. The cornucopia of chilly winters: ocean quahog (Arctica islandica L., Mollusca) master chronology reveals bottom water nutrient enrichment during colder winters (North Sea). Senckenbergiana Maritima 32, 1–13. Schöne, B.R., Castro, A.D.F., Fiebig, J., Houk, S.D., Oschmann, W., Kröncke, I., 2004. Sea surface water temperatures over the period 1884–1983 reconstructed from oxygen isotope 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 (Arctica islandica, Mollusca; Iceland). Palaeogeography, Palaeoclimatology, Palaeoecology 228, 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 subseasonal environmental controls on a long-lived bivalve mollusk. Palaios 20, 78–92. Schöne, B.R., Pfeiffer, M., Pohlmann, T., Siegismund, F., 2005c. A seasonally resolved bottom-water temperature record for the period AD 1866–2002 based on shells of Arctica 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. Annually resolved δ13C shell chronologies of long-lived bivalve mollusks (Arctica islandica) reveal oceanic carbon dynamics in the temperate North Atlantic during recent centuries. 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 marine fossil record: data from growth lines of the long-lived bivalve mollusc Arctica islandica. Holocene 16, 967–974. Suess, H.E., 1953. Natural radiocarbon and the rate of exchange of carbon dioxide between the atmosphere and the sea. In: Aldrich, W. (Ed.), Nuclear Processes in Geologic Settings. University of Chicago Press, Chicago, pp. 52–56. Sutton, R.T., Hodson, D.L.R., 2005. Atlantic Ocean forcing of North American and European summer climate. Science 309, 115–118. Tanaka, N., Monaghan, M.C., Rye, D.M., 1986. Contribution of metabolic carbon to mollusk and barnacle shell carbonate. Nature 320, 520–523. Thompson, I., Jones, D.S., 1977. The ocean quahog, Arctica islandica, “tree” of the north Atlantic 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 the ocean 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. An aquaculture-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 collected from 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 tephrabased 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 water forcing on Gulf of Maine temperatures over the past millennium. Climate Dynamics 31, 183–194. Wefer, G., Berger, W.H., 1991. Isotope paleontology — growth and composition of extant calcareous species. Marine Geology 100, 207–248. Weidman, C.R., Jones, G.A., Lohmann, K.C., 1994. The long-lived mollusc Arctica islandica: a new paleoceanographic tool for the reconstruction of bottom temperatures 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 the problem of the vital effect. Reviews in Mineralogy and Geochemistry 54, 1–29. Witbaard, R., Jenness, M.I., Vanderborg, K., Ganssen, G., 1994. Verification of annual growth increments in Arctica islandica L from the North Sea by means of oxygen and 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 record derived from Arctica islandica (Mollusca, Bivalvia) from the Fladen Ground (northern North Sea). Journal of the Marine Biological Association (United Kingdom) 77, 801–816.