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Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2017) xxx–xxx

PALAEO-08382; No of Pages 21

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Palaeogeography, Palaeoclimatology, Palaeoecology

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Tropical seasonality in the late Campanian (late Cretaceous): Comparisonbetween multiproxy records from three bivalve taxa from Oman

Niels J. de Winter a,⁎, Steven Goderis a,b, Frank Dehairs a, John W.M. Jagt c, René H.B. Fraaije d,Stijn J.M. Van Malderen b, Frank Vanhaecke b, Philippe Claeys a

a Analytical, Environmental and Geochemistry (AMGC) Department, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgiumb Department of Analytical Chemistry (A&MS), Ghent University, Krijgslaan 281, Campus Sterre - S12, 9000 Ghent, Belgiumc Natuurhistorisch MuseumMaastricht (NHMM), Bosquetplein 7, 6211 KJ, Maastricht, The Netherlandsd Oertijdmuseum De Groene Poort, Bosscheweg 80, 5283 WB Boxtel, The Netherlands

⁎ Corresponding author.E-mail address: [email protected] (N.J. de Winte

http://dx.doi.org/10.1016/j.palaeo.2017.07.0310031-0182/© 2017 Elsevier B.V. All rights reserved.

Please cite this article as: de Winter, N.J., etrecords from three bivalve taxa from O..., Pa

a b s t r a c t
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Article history:Received 5 April 2017Received in revised form 24 July 2017Accepted 27 July 2017Available online xxxx

Geochemical proxy records from calcite shells of bivalves constitute an important archive for the reconstructionof palaeoenvironmental conditions on sub-annual timescales. However, the incorporation of these trace elementand stable isotope proxies into the shell is influenced by a multitude of physiological and environmental factorsthat need to be disentangled to enable reliable reconstruction of palaeoclimate and palaeoenvironment. In thisstudy, records of multiple proxies in three bivalve taxa from the same late Campanian locality in Oman areused to study the expression of various geochemical proxies in relation to each other and to thepalaeoenvironment. Micro-X-Ray Fluorescencemapping allows the localization, discussion and evasion of diage-netically altered parts of the fossil shells. X-Ray Fluorescence line scanning calibrated with Laser Ablation Induc-tively Coupled Plasma Mass Spectrometry is used to measure trace element profiles through well-preservedcalcitic parts of the shells. Records of stable carbon and oxygen isotope ratios of shell calcite are combinedwith these high-resolution trace element concentration profiles to study sub-annual variations in shell chemistryand reconstruct changes in the palaeoenvironment of the bivalves on a seasonal scale. Spectral analysis routinesare used to detect cyclicity in stable isotope (δ18O and δ13C) and trace element (Mg/Ca, Sr/Ca, S/Ca and Zn/Ca)records. Differences in seasonal expression between these chemical proxies and between individual shells arediscussed in terms of the relative influence of palaeoenvironment and potential species-specific physiological ef-fects. Stable oxygen isotope ratios between shells suggest a local palaeotemperature seasonality of 8 °C around anannualmean of 28 °C,with the shell of the rudistid Torreites sanchezi milovanovici yielding slightly higher averagetemperatures. The discussion of the application of various Mg/Ca palaeotemperature calibrations on Mg/Ca re-cords in these bivalve species emphasizes the complexity of using trace element proxies in extinct bivalve spe-cies. It shows that long-term changes in Mg/Ca ratios in ocean water need to be taken into account and thatMg/Ca ratios in bivalves might be influenced by vital effects. Sr/Ca and S/Ca ratios in these fossil taxa are likelycontrolled by growth andmetabolic rates of the shell, although an influence of local salinity on strontium-to-cal-cium ratios cannot be excluded. Sub-annual variations in zinc concentrations in shell calcite may reflect seasonalvariations in palaeoproductivity and redox conditions in the water column.

© 2017 Elsevier B.V. All rights reserved.

Keywords:PalaeotemperatureMolluscRudistTrace elementStable isotopeμXRF

1. Introduction

1.1. Late cretaceous climate reconstruction

The Late Cretaceous is a well-studied interval of geological time, inpart due to its hothouse climate punctuated by episodes of rapid climat-ic and environmental change (Jenkyns, 1980; Huber et al., 1995; Li andKeller, 1999; Jenkyns et al., 2004). During the Late Cretaceous,

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al., Tropical seasonality in thelaeogeogr. Palaeoclimatol. Pal

atmospheric pCO2 levels are estimated to have been two to four timeshigher (i.e. ~400 to ~1000 ppmV) compared to the pre-industrial level(280 ppmV; e.g., Berner, 1990; Andrews et al., 1995; Ekart et al., 1999;Quan et al., 2009). The values projected by the IntergovernmentalPanel on Climate Change (IPCC, 2013) indicate that such high valuesmay be reached within the 21st century – the current global meanpCO2 value is already N400 ppmV and rises at a rate of 2–3 ppmV/year(Dlugokencky and Tans, 2017). This makes the Late Cretaceous an im-portant geological time period to study the effects of increased pCO2

on Earth's climate. As such, long-term changes in climate and environ-ment during this time period have received much attention (e.g.,

late Campanian (late Cretaceous): Comparison between multiproxyaeoecol. (2017), http://dx.doi.org/10.1016/j.palaeo.2017.07.031

http://dx.doi.org/10.1016/j.palaeo.2017.07.031

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Eshet and Almogi-Labin, 1996; Clarke and Jenkyns, 1999; Huber et al.,2002; Faul et al., 2003; Friedrich et al., 2012). However, climatic and en-vironmental changes in the Cretaceous greenhouse world should alsobe understood on a much shorter timescale to put long term climatemodels and reconstructions in their proper context. Therefore, there isa need to supplement widely available, long-term palaeoclimate re-cords, such as those obtained through deep-sea drilling expeditionsand continuous sedimentary records (e.g. Li and Keller, 1999; Huber etal., 2002), with more rare data sets that record sub-annual variations.

1.2. Bivalve shells as climate recorders

Fossil bivalve shells arewell-studied records that track these sub-an-nual climate fluctuations. Marine bivalves record changes in their envi-ronment, and thus local climate, as a result of environment-dependentchemical and isotopic fractionation that takes place during the incre-mental growth of their carbonate (aragonitic/calcitic) shell (Epstein etal., 1953; Grossman and Ku, 1986; Jones, 1980, 1983; Klein et al.,1996a; Lazareth et al., 2003). Chemical variations of pristinely preservedshell material can record changes in the animal's environment and localclimate down to daily resolution, much higher than can be retrievedthrough conventional long timescale climate archives. Thick-shelledrudistid (Mollusca: Hippuritida, see Newell, 1965) and ostreid bivalves(Mollusca: Ostreoida, see Bouchet et al., 2010) are suitable taxa forthis type of research because their thick calcitic shells aremore resistantto diagenesis than those of their aragonitic relatives (Al-Aasm andVeizer, 1986a, 1986b; Steuber, 1999; Ullmann and Korte, 2015). Theuse of such shells to reconstruct climate on a sub-seasonal scale hasbeen amply demonstrated by earlier work on both rudistid (Steuber,1996, 1999; Steuber et al., 2005; Immenhauser et al., 2005; Hennhöferet al., 2012) and ostreid shells (Kirby et al., 1998; Brigaud et al., 2008;Ullmann et al., 2010; Fan et al., 2011). However, there are complicationswith the use of shells of extinct bivalve species to reconstruct climatebecause of potential species-specific differences in physiological(“vital”) effects, such as the effects of varying growth and metabolicrate on palaeoclimate proxies (Fastovsky et al., 1993; Steuber, 1999;Lorrain et al., 2005; Gillikin et al., 2005; Immenhauser et al., 2005;Schöne et al., 2011). This requires the construction of species-specifictransfer functions for the relationship between climatic and environ-mental parameters and geochemical proxies in the shell, which requiresculture experiments (e.g. Wanamaker et al., 2007; Freitas et al., 2008).For extinct bivalve species, proxy data sets can be cross calibratedusing related extant species (e.g. Armendáriz et al., 2008). For specieswithout close extant relatives, such as rudistids, the use of modern bi-valve transfer functions can, however, severely reduce the reliability ofreconstructions.

1.3. Multi-species approach

The reliability of proxy interpretation in these bivalves can be im-proved by comparing records frommultiple species and by usingmulti-ple proxies. This approach allows isolation of the effect of differentparameters on the measured proxies when culture experiments cannotbe carried out (Klein et al., 1996b; Carroll et al., 2009). The presentworkdiscusses a multi-proxy analysis of a single ostreid shell and two associ-ated rudistid taxa from the Campanian Samhan Formation from theSaiwan area in the Sultanate of Oman, which is characterized by longhorizontally-continuous successions of reef-like deposits of bivalves,stromatoporoids and corals. This shallow marine Tethys Ocean succes-sion contains exceptionally well-preserved rudistids and other bivalvesin life position, allowing multi-species paleoenvironmental reconstruc-tions to be placed in a wider framework of Late Cretaceous reconstruc-tions in the Tethys Ocean. The use of three different species in a multi-proxy approach enables an assessment of potential species-specific dif-ferences in proxy relationships and offers a unique opportunity to iso-late seasonal fluctuations of climatic parameters recorded in extinct

Please cite this article as: de Winter, N.J., et al., Tropical seasonality in therecords from three bivalve taxa from O..., Palaeogeogr. Palaeoclimatol. Pal

bivalve species. In addition to reconstructing past seasonality, the useof multiple species andmultiple proxies permits a more general discus-sion of the value of trace element and stable isotope records from fossilbivalve shells.

2. Background

2.1. Palaeoenvironmental proxies in calcite skeletons

A wide range of marine calcifying organisms has been the subjectof studies aiming to reconstruct sub-annual climate. Detailed studiesof stable isotope ratios and trace element concentrations in corals(Goreau, 1977; Swart, 1983; Sinclair et al., 1998), coralline algae(Halfar et al., 2000; Hetzinger et al., 2011), sclerosponges (Lazarethet al., 2000; Swart et al., 2002), molluscs (e.g. Jacob et al., 2008;McConnaughey and Gillikin, 2008; Elliot et al., 2009; Goodwin etal., 2013; Ullmann et al., 2010, 2013, 2015), brachiopods (Veizer etal., 1986; Grossman et al., 1996) and stromatolites (Chafetz et al.,1991; Andrews and Brasier, 2005) have shown that many of theseorganisms and colonies record changes in the chemistry of theircarbonate skeleton in response to seasonal changes in their environ-ment. It is reported that most of these marine organisms precipitatetheir carbonate skeletons in equilibrium with ambient seawater,allowing sub-annual reconstruction of palaeotemperature fromtheir stable isotope ratios. However, several other environmental pa-rameters, such as salinity, nutrient availability and sea water chem-istry, complicate the reconstruction of palaeoseasonality in shallowmarine records (Klein et al., 1996b; Purton and Brasier, 1997; Surgeand Lohmann, 2002). In response to these complications and in anattempt to obtain a more complete picture of sub-annual variationsin the local environment, several trace element proxies for changesin sea water chemistry have been developed for calcifying organ-isms. Magnesium-to-calcium (Mg/Ca) ratios in carbonates havebeen proposed as proxies for palaeotemperature, potentiallyallowing independent control on temperature reconstructions andthe determination of salinity changes in combination with stable ox-ygen isotope ratios (Mitsuguchi et al., 1996; Klein et al., 1996a;Richardson et al., 2004; Wanamaker et al., 2008; Schöne et al.,2011). Additionally, strontium-to-calcium (Sr/Ca) ratios have beenshown to vary with calcification temperature and salinity in some bi-valves and corals (Dodd and Crisp, 1982; de Villiers et al., 1995;Richardson et al., 2004; Freitas et al., 2006). Several trace elementproxies have been suggested to record changes in palaeoproductivityand redox conditions in ambient sea water. Examples include redoxsensitive elements such as manganese (Mn; Freitas et al., 2006), ele-ments that are enriched in the skeletons of primary producers suchas barium (Ba; Gillikin et al., 2008; Marali and Schöne, 2015) andmicronutrients such as zinc (Zn) and cadmium (Cd) which are read-ily taken up into the shells of bivalves (Carriker et al., 1980; Calmanoet al., 1993; Jackson et al., 1993; Wang and Fisher, 1996; Guo et al.,1997). Other studies have demonstrated the reproducibility oftrace element profiles between specimens living in the same envi-ronment, showing that these records are likely to be governed by en-vironmental factors (Gillikin et al., 2008; Marali et al., 2017).

2.2. Vital effects

However, it is now recognized that trace elements are often nottaken up in equilibrium with the environment and that vital effects in-fluence many of these proxies (see Weiner and Dove, 2003 and refer-ences therein). Examples include studies that show relationshipsbetween trace element concentrations and mineral growth in bivalves(Lorrain et al., 2005; Gillikin et al., 2005; Freitas et al., 2006; Carré etal., 2006; Schöne et al., 2011), evidence of the breakdown of proxy rela-tionships during periods of growth stress (Lorens and Bender, 1980;Hendry et al., 2001; Takesue and van Geen, 2004) and the effect of



3N.J. de Winter et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2017) xxx–xxx

changing redox conditions in the sea water (Vander Putten et al., 2000;Hendry et al., 2001; Freitas et al., 2006; Beck et al., 2017). Independentchronologies and proxies for the amount of organic matrix in the shell(e.g. sulphur (S) concentrations) may be used to better constrain vitaleffects in biogenic carbonate records by reconstructing the physiologicalcycle of the organism (de Villiers et al., 1994; Sinclair et al., 1998;Rosenberg et al., 2001; Dauphin et al., 2003; Marali and Schöne,2015). An example of how the integration of proxies for physiologicalchanges enables the discussion of proxy interpretation, is the observa-tion of covarying magnesium (Mg) and sulphur (S) concentrations inbivalve records as evidence for physiological control on the incorpora-tion of trace elements into bivalve shell calcite (Lorens and Bender,1980; Dauphin et al., 2003; England et al., 2007; Perrin et al., 2017). Re-cent studies have therefore focused on the integration of multi-proxyrecords from multiple sub-annual climate records in order to isolatethe effects of environmental parameters (e.g. Black et al., 2009;Wanamaker et al., 2011; Marali et al., 2017).

2.3. Geological setting

The three bivalve specimens described in this study originate fromthe upper Campanian middle member of the Samhan Formation in theSaiwan area of the Huqf Desert in east-central Oman (Schumann,1995). The two rudistid specimens were retrieved in life position froma 200 m wide Vaccinites-dominated rudist biostrome that containsmany large Torreites rudists (Unit V1 in profile 1 in Schumann, 1995;biostrome unit 2 in Philip and Platel, 1995), while the thick-shelled oys-ter (Oscillopha figari) originated from the top of the marly limestoneunit directly below the rudistid horizon (top of Unit 1 in profile 1 inSchumann, 1995). The Samhan Formation records the development ofa shallow marine carbonate platform during a gradual transgression(Platel et al., 1994). Previously established as early Campanian (Platelet al., 1994), the middle and upper Samhan Formation were laterdated as late Campanian using ammonite biostratigraphy by Kennedyet al. (2000). This is in congruence with the dating of the Orbitoidestissoti zone, in which the Samhan Formation is found (Philip andPlatel, 1995), to the early late Campanian (Korbar et al., 2010).Schumann (1995) described the Samhan Formation as a shelf settingfar from the coast, with no evidence of coastal sedimentation. Thepalaeoenvironment was frequently disturbed by strong currents andstorm events and was characterized by high input of weathering prod-ucts from Omani ophiolites. The Vaccinites-dominated biostromes arepresumably formed during periods of relatively lower hydro-energyand were very short-lived (100 s of years; Schumann, 1995). However,it is hypothesized that the low diversity of these biostromes suggests anadaptation of Vaccinites and Torreites to a highly turbulent environment.The O. figari specimen was found 1-2 m below the biostrome and istherefore assumed to have lived before the closely associated rudistidspecies.

2.4. Late Campanian palaeoclimate

The late Campanian period is characterized by a climatic optimumwith mean annual sea surface temperatures in northern Europe risingto 19–20 °C (Thibault et al., 2016). Modelling results indicate thatmean annual temperatures were approximately 10 °C warmer com-pared to today (Deconto, 1996), but meridional temperature gradientswere probably lower, meaning that tropical temperatures were likelyless different from the present day situation, with tropical surface tem-peratures estimated at 30 °C (Huber et al., 1995; Brady et al., 1998;Alsenz et al., 2013). At the same time, a higher eustatic sea level causedcontinental shelves to be submerged and continents were likelysurrounded by extensive shallow seas (Brady et al., 1998). The geo-graphical setting of this study's locality fits this description, with shal-low marine conditions above the storm wave base occurring withoutsigns of deltaic sedimentation. Palaeoceanographic studies in the area


have demonstrated that the Late Cretaceous Tethys Ocean was proneto rapid changes in palaeoproductivity and redox conditions as thebasin became progressively more confined (Dercourt et al., 1986;Almogi-Labin et al., 1993; Steuber and Löser, 2000; Jarvis et al., 2002;Fleurance et al., 2013). Besides these local changes, long-term trendsin global ocean water chemistry also significantly influenced the envi-ronment in which the bivalves in this study precipitated their shells.Marine magnesium-to-calcium (Mg/Ca) and strontium-to-calcium (Sr/Ca) ratios were much lower (1–2 mol/mol and 4–6 mmol/mol, respec-tively, compared to 5 mol/mol and 8–9 mmol/mol in modern oceans;Stanley and Hardie, 1998; Coggon et al., 2010; Rausch et al., 2013),which is likely to have influenced the trace element concentrations re-corded in shell calcite (e.g. Lear et al., 2015).

3. Methods

3.1. Specimen acquisition and preparation

The shells of two rudistid bivalves (Torreites sanchezi milovanoviciDouvillé, 1927; Natuurhistorisch Museum Maastricht collections,NHMM 2014 052, hereafter TS and Vaccinites vesiculosus Woodward,1855; Oertijdmuseum De Groene Poort collections, MAB D.R.81 5/19078, hereafter VV) and a thick-shelled oyster (Oscillopha figariFourtau, 1904, NHMM 2014 050a, hereafter OF; Malchus, 1990;Aqrabawi, 1993) were acquired for the present study. The VV shellwas subject of an earlier publication by de Winter and Claeys (2016).All shells were collected in life position in the upper Campanian SamhanFormation in the Saiwan area of the Huqf Desert in east-central Oman(Unit 1 of Schumann, 1995, 30°39′ N, 57°31′ E, see also Platel et al.,1994; Philip and Platel, 1995; Kennedy et al., 2000 and section above).Shells were cut longitudinally along their central growth axis andhigh-grade polished by increasingly fine-grained silicon carbidepolishing discs (up to P2400) at the Vrije Universiteit Brussel (VUB, Bel-gium). High-resolution (6400 dpi) colour scans were produced of theshell surfaces to track all sample locations in an overview figure (Fig. 1).

3.2. μXRF element mapping

High-resolution elemental abundance maps of the polished surfaceof shells were created using a Tornado M4 micro X-ray fluorescence(μXRF) scanner (Bruker nano GmbH, Berlin, Germany). μXRF mappingwas done along a 2D grid with 50 μm spacing, a spot size of 25 μmand an integration time of 1 ms per pixel. The X-ray source was operat-ed under maximum energy settings (600 μA, 50 kV) and no source fil-ters were applied. Details of the setup of the Tornado M4 scanner forthe mapping of bivalve calcite can be found in de Winter and Claeys(2016). Higher resolution (25 μm spacing) maps were made of smallerareas of the shells. Mapping by μXRF permitted qualitative elementabundance distributions to be visualized (see Fig. 1).

3.3. μXRF line scanning

To determine the best approach for μXRF scanning, trace elementprofiles were measured on the outer calcite layer along the length ofthe VV shell using three methods: 1) conventional μXRF line scanningaccording to de Winter and Claeys (2016), 2) a μXRF point-by-pointline scanning method with longer integration time (60 s) after deWinter et al. (2017), and 3) two different transects quantified by LaserAblation-Inductively Coupled Plasma-Mass Spectrometry (LA-ICP-MS).To optimize the results, XRF maps were used to guide sampling ofwell-preserved parts of the shells in all transient line scanningmethods.The method for conventional XRF line scanning on bivalve calcite is de-tailed in deWinter and Claeys (2016). For point-by-point line scanning,the X-ray beam is allowed to dwell on each point for 60 s at maximizedenergy settings (50 kV, 600 μA, no source filter) with a sampling resolu-tion of 100 μm for a total of 978 and 1051 points respectively for VV and



Fig. 1. Overview of colour scans and XRF maps of Vaccinites vesiculosus (VV, 1A), Torreites sanchezi milovanovici (TS, 1B) and Oscillopha figari (OF, 1C) sections. Images on the left showcolour scans of the polished surface of the bivalves with locations of the lines of measurement in yellow. Central images show XRF maps of relative intensities of Fe (red), Si (green)and Ca (blue). Images on the right-hand side show XRF heatmaps of the relative intensity of Fe and Mn, with red colours indicating higher concentrations and blue colours indicatinglower concentrations (see scale bar in 1A). Fig. 1B and C contain close-ups showing growth microstructure of the calcite in the outer shell layer and the hinge of the TS and OF shells,respectively. Background of the VV maps (1A) shows glass beads used to stabilize the shell during measurement. This was not necessary for the measurement of the heavier TS and OFshells (1B and 1C). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)


TS and a total of 431 points for the OF shell. This allows more time foreach XRF spectrum to be accumulated and results in more reproducibleresults (de Winter et al., 2017). All XRF line scans were quantified ac-cording to the Fundamental Parameters method of the Esprit softwarecalibrated to BAS CRM393 limestone trace element reference material(Bureau of Analyzed Samples Ltd., UK). XRF point-by-point scans werecarried out on the outer calcite layer in the growth direction of therudistid shells (VV and TS) and through a polished section of thehinge of the OF shell perpendicular to the growth layers (see Fig. 1).

3.4. LA-ICP-MS line scanning

LA-ICP-MS measurements were carried out at the Atomic and MassSpectrometry research unit of Ghent University (Ghent, Belgium). A


detailed account of LA-ICP-MSmethodology is found in Supplementarydata 1. XRF line scanswere calibrated by using the bulk concentration ofone of the LA-ICP-MS transects as an additional standard and establish-ing a calibration curve. The results of the application of these methodsand a schematic overview of the calibration of XRF results with LA-ICP-MS results are shown in Fig. 2. A detailed explanation of the cal-ibration calculations is given in Supplementary data 1. After this cor-rection, the average offset of strontium (Sr) concentrations betweencorrected XRF measurements and results of the second LA-ICP-MSline scan (not used in the correction) was 9.1% for point-by-pointanalysis and 12% for conventional line scan analysis. All trace ele-ment profiles discussed further in this study are measured bypoint-by-point XRF line scanning and calibrated using the LA-ICP-MS calibration. Reproducibility standard deviations and instrument



A B

C

Fig. 2. A) Plots of Sr concentrations measured along the growth axis of Vaccinites vesiculosus (VV) using LA-ICP-MS (blue and green) and two μXRF methods; conventional line scanning(linescan) in red and point-by-point (pt-by-pt) scanning in purple. XRF data in 2A are corrected using conventional single-standard correctionwith CRM393. Dashed linesmarked “A”, “B”and “C” correspond tomarks on the sampling lines in Fig. 1A. B) Schematic representation of the correction of XRF data from single-standard calibration (solid grey line) to two-standardcalibration (solid black line). This re-correction allows any single-standard calibrated value [M]old to be corrected to a two-standard calibrated value ([M]new; see formula and explanationin supplementary data). C) Linear regression plots of Sr concentrations of thefirst LA-ICP-MS line (blue line in 2A) against strontium concentrationsmeasured in the other three line scans,both before (left) and after the calibrationwith the second LA-ICP-MS linescan. (For interpretation of the references to colour in thisfigure legend, the reader is referred to theweb versionof this article.)


errors are reported in Table 1 and were calculated according to deWinter et al. (2017). Data of all calibrated trace element and stableisotope measurements used in this study are provided in Supple-mentary data 2–5.

3.5. Stable isotopic analysis

Pristine calcite in cross sections of all three bivalve shells was sam-pled for stable isotope analysis using a microscope guided drill(Merchantek/Electro Scientific Industries Inc. (ESI), Portland (OR),USA, coupled to Leica GZ6, Leica Microsystems GmbH,Wetzlar, Germa-ny) equippedwith a 300 μmwide tungsten carbide drill bit. Samples forstable isotope analysis were taken at a resolution of 500 μm for TS (243measurements) and 250 μm for VV and OF (328 and 92 measurementsrespectively). The spatial sampling resolution was decided upon basedon the presence of annual growth bands and recognized annual cyclesin trace element ratios measured by μXRF, and was chosen such thateach interpreted year contained at least four samples. Samples for stableisotope analysiswere taken along the same transects as XRF and LA-ICP-MSmeasurements (see Fig. 1). In the OF shell, all samples for stable iso-tope analysis were taken in the dense foliated calcite layers which areconcentrated in the hinge of the left valve of the shell (Fig. 1). Samplealiquotswith a typicalweight of 30–50 μgwere reactedwith phosphoricacid (H3PO4·H2O) at 70 °C in a Nu Carb carbon preparation device


coupled via dual inlet to a Nu Perspective isotope ratio mass spectrom-eter (Nu Instruments, UK) and the resulting CO2was analyzed for stablecarbon and oxygen isotope ratios. Analytical uncertainty was deter-mined by repeated measurement (N = 194) of the in-house referencematerial MAR2 (Marbella marble, δ13C: 3.41 ± 0.10‰VPDB; δ18O: 0.13± 0.20‰ VPDB; 1 standard deviation, SD) and found to be 0.05‰ and0.09‰ for δ13C and δ18O values (1 SD), respectively. This MAR2 refer-ence material was previously calibrated using the international NBS-19 stable isotope standard (Friedman et al., 1982). All stable isotopevalues are reported in permille relative to the Vienna Pee Dee Belemnitestandard (‰VPDB).

3.6. Statistical analyses

Statistical analyses were performed to assess the possible presenceof seasonal cyclicity in the records. To test for periodic behaviour inproxy records, periodograms were generated by R 3.1.2 software pack-age (R Development Core Team, 2008) using three methods of spectralanalysis in a frequency range of 10−5 and 10−3 μm−1: 1) A Lomb-Scargle Periodogram (LSP, see Lomb, 1976; Scargle, 1982) was calculat-ed from untreated datasets using the R “lomb” package by Ruf (1999)with an oversampling factor of 100 and a confidence level of 90%. 2) AMulti Taper Method Spectral Analysis (MTM, see Thomson, 1982) wascarried out on uniformly resampled and linearly detrended datasets



Table 1Overview of measured average concentrations, measurement reproducibility (1 standard deviation, SD) and instrumental uncertainty (1 SD) based on XRF deconvolution for major andtrace element measurements on the Vaccinites vesiculosus (VV) shell using the two XRFmethods (conventional line scanning and point-by-point analysis) and LA-ICP-MS. For LA-ICP-MS,the coefficient of determination (R2) of the calibration curve based on standard measurements is given.

Mean value(ug/g)

Reproducibilitystandarddeviation

(ug/g)

Instrumen terror(ug/g)

Mean value(ug/g)


(ug/g)

Instrumen terror(ug/g)

Isotopemeasured

Mean value(ug/g)


(ug/g)

R2calibration line

Na 5,530 n.d. 218 317 391 13 23 992 14 1.000

Mg 4,744 2240 130 3,143 422 86 25 2,799 101 0.993

Al 1,132 109 68 259 31 16 27 19 0 0.998

Si 4,041 403 13 7,383 148 23 29 130 1 0.984

P 273 10 5 114 4 2 31 33 2 0.998

S 13 148 1 1,267 121 118 34 190 32 1.000

Cl 11,721 n.d. 5 650 n.d. 0 37 93 54 0.628

K 844 n.d. n.d. 149 n.d. n.d. 39 122 3 0.997

Ca 383,224 477 103 385,361 395 104 43 385,000 n.d. 1.000

Ti 179 54 3 601 26 9 47 20 1 0.997

Cr 55 11 0 20 2 0 53 1 0 0.982

Mn 303 11 2 362 4 3 55 207 2 0.997

Fe 2,187 15 2 2,094 6 2 57 295 10 0.989

Ni 58 183 0 9 35 0 60 1 0 0.997

Cu 27 41 1 17 11 1 63 2 0 0.995

Zn 167 163 0 65 11 0 66 147 4 0.991

Br n.d. n.d. n.d. 18 4 n.d. n.d. n.d. n.d.

Rb n.d. n.d. n.d. n.d. n.d. n.d. 85 0 0 1.000

Sr 416 7.71 4 650 3 7 88 852 14 0.996

Ba n.d. n.d. n.d. 25 44 n.d. 137 2 0 0.989

Pb 44 31 0 18 3 0 208 1 0 0.992

Conventional XRF line scan Point-by-point XRF line scan LA-ICP-MS


using the R “astrochron” package by Meyers (2014). 3) A simpleperiodogram (SP, see Bloomfield, 2004) was calculated from uniformlyresampled and linearly detrended datasets using R core functions. Con-fidence levels for detected frequencies were calculated via “red noise”estimation and harmonic F-test calculation (Thomson, 1982) usingfunctions in the R “astrochron” package by Meyers (2012) and signifi-cant periodicities were extracted from the records by bandpass filtering(Hays et al., 1976) using the “bandpass” function in the R “astrochron”package (Meyers, 2012) on untreated datasets using a Cosine-taperedwindow and a zero-padding factor of 5. The script used for these spec-tral analysis routines including the parameters that were used and theresultant data of filters, powerspectra and confidence levels is given inSupplementary data 6–9. In addition to spectral analysis, p-values andPearson's correlation coefficients were calculated for correlations be-tween all palaeoenvironmental records from the bivalve shells to pro-vide a statistical basis for the visually observed correlations betweenrecords.

4. Results

4.1. XRF mapping

An overview of all XRFmaps is given in Fig. 1. The element distribu-tionmaps render a qualitative overview of the presence of elements in asample and may therefore be used to detect heterogeneity within thesample. Comparison of the manganese (Mn) and iron (Fe) heatmapwith the colour scan of VV indicates that brown spots visible on thepolished surface of the shell are associated with increased concentra-tions of Fe, Mn and Si. The Fe-Si-Ca map of the VV shell (Fig. 1A) illus-trates how various comparatively Fe- and Mn-rich spots are foundwithin the more Ca-rich outer shell surface. It also shows that the


innermost area of the shell as well as the left valve are characterizedby higher concentrations of Fe andMn. XRFmaps of the second rudistidshell (TS) indicate that a larger part of this shell shows enrichment in el-ements other than Ca compared to VV. The Fe-Si-Ca distribution map(Fig. 1B) indicates that the nature of these enrichments is different inthe sense that a major section of area is enriched in silicon (Si) ratherthan Fe. A large area of the inside of the outer shell layer of TS haslower concentrations of Si, Fe and Mn. Enrichments in Fe, Mn and Sionly occur in the outer ±10 mm of the shell and a corona of severalmillimetres around themore porous inner parts of the shell. The centralpart of the outer calcite layer is characterized by the presence of finegrowth layers, which are shown in the close-up of Fig. 1B. The oystershell (OF; fractured during sample preparation) contains the lowestconcentrations of Fe, Mn and Si (Fig. 1C). Thin coronas of carbonateenriched in Si, Fe and Mn surround the OF shell, while the interiorshows no signs of enrichment in these elements. A close-up of a crosssection through the hinge of the oyster (Fig. 1C) indicates a thin rim ofFe- andMn-rich carbonate, while the inside of the shell is characterizedby low concentrations of these elements and well-preserved darkgrowth layers.

4.2. Trace element concentrations

Fig. 3 provides an overview of the range in concentrations of majorand trace elementsmeasured in all three shells by LA-ICP-MS-calibratedXRF point-by-point line scans. Obtained concentrations of all measuredelements fall within the same order of magnitude between differentshells, with the exception of Fe. Even though an effort was made toavoid inclusions of Mn and Fe based on their location in Fig. 1 (seeabove), the VV record contains higher values for Fe, Mn and Si. Concen-tration ranges of other elements are mostly similar between shells



Fig. 3. Average concentrations of all trace elements measured in the VV (purple), TS (blue) and OF (orange) shells using LA-ICP-MS calibrated point-by-point XRF measurements. Barsindicate ranges of concentrations measured in the shell calcite and black dots indicate the averages of these ranges. Values below 1 ppm are dashed because these are below thedetection limit of the method (de Winter and Claeys, 2016). Elements of interest for this study are highlighted. (For interpretation of the references to colour in this figure legend, thereader is referred to the web version of this article.)


except for Mg, which is significantly lower in the OF record. Concentra-tions of Mg, Sr, S and Zn (±1100, ±900, ±200 and±100 μg/g, respec-tively) are similar to concentrations of these elements found in otherstudies of well-preserved fossil and modern bivalve calcite (Carriker etal., 1980; Al-Aasm and Veizer, 1986a, 1986b; Steuber, 1999; VanderPutten et al., 2000; Holmden and Hudson, 2003).

Figs. 4, 5 and 6 present an overview of a selection of trace elementand stable isotope records of the three characterized shells. Running av-erages of 11 points of the trace element records illustratemm-scale var-iations in the records and are favoured over individual pointmeasurements, which may be influenced by the irregularities on thesample surface (see de Winter and Claeys, 2016; de Winter et al.,2017). A comparison of Fig. 4with Figs. 5 and 6 confirms that concentra-tions of Mn, Fe, and Si in VV are overall higher than in the TS and OFshells. Further inspection of the records of these elements shows thatthe measurements that yield high Mn, Fe, and Si abundances are highlylocalized and are often associated with lower than average Ca concen-trations. As evident from the XRF maps (Fig. 1A), the lower 22 mm ofthe VV shell is characterized by areas with high concentrations of Mn,Fe and Si. In contrast, concentrations of Mn, Fe and Si in TS and OF arean order of magnitude lower (Mn b 150 μg/g, Fe b 40 μg/g, Si b 200μg/g) and Ca concentrations in these shells do not fall below 38 wt%(wt%). Concentrations of other trace elements occur in the same orderof magnitude in all shells, with the exception of Mg, which shows con-sistently lower concentrations in OF than in the rudistid shells (seealso Fig. 3). Records of Mg/Ca, Sr/Ca, Zn/Ca and S/Ca show regular fluc-tuations with an amplitude of 50 to 75% of the average value in allthree shells. Regular fluctuations occur on a scale of 10 mm in VV (Fig.4), 15–20 mm in TS (Fig. 5) and 2–3 mm in the oyster record (OF; Fig.6). The expression of these fluctuations in trace element records, espe-cially those of Zn and S, is in general not sinusoidal but rather shows apunctuated character with rapid shifts in concentration and longer epi-sodes of relative stability. Trace element records often co-vary (most


notably Mg/Ca and Zn/Ca) or show anti-correlations (e.g. Zn/Ca and S/Ca). The Sr/Ca record of OF is characterized by a pronounced ontogenet-ic increase and shows a large drop at the end of the record. Fluctuationsin the Sr record of OF are smaller than in the rudistid shells. Another on-togenetic trend in OF is observed in the S/Ca record, which showsmuchless variation in the initial ±6mmof the record followed by an increasein fluctuation for the remainder of the record. A similar, though less pro-nounced, intensification of the trace element fluctuations is observed inthe records of Mg/Ca and Zn/Ca.

4.3. Stable isotope ratios

Figs. 4–6 show that stable carbon and oxygen isotope ratios (δ13Cand δ18O) fluctuate periodically around a stable background in all bi-valve shells. An exception to this is the last part of the δ13C record inOF (Fig. 6) where a decreasing trend is observed. While δ13C valuesare similar between shells (±0.5‰ to 2.5‰ with a mean value of±1.5‰ in VV and TS and ±2‰ in OF), large inter-shell differences areobserved in δ18O values. Oxygen isotope ratios are highest in OF (rough-ly between−4‰ and−3‰with ameanvalue around−3.5‰) and sig-nificantly lower in TS (−6‰ to −5‰, mean value around −5‰) withintermediate values for VV (between −5‰ and −3‰ with a meanvalue of−4‰). Fluctuations in stable isotope values also vary betweenshells. Measured δ13C values fluctuate with an amplitude of approxi-mately 1‰ in VV and OF, while fluctuations in TS are about 1.5‰. Oxy-gen isotope values fluctuate from 1 to 1.5‰ in TS and OF, but are closerto 2‰ in VV. Stable isotopefluctuations seem to follow the same period-icity as the trace element records (10–20mm in rudistid shells, 2–3mmin OF) and relationships between these records are described in para-graph 4.5. Fluctuations in the stable isotope records are more regularand have a more constant amplitude compared to trace elementrecords.



Fig. 4. Vaccinites vesiculosus (VV) shell. Overview of stable isotope (‰VPDB), elemental abundance (wt% and μg/g) and relative abundance records (mmol/mol, 11 point running average).Shaded vertical red bars indicate intervals with high concentrations of Si, Fe and Mn. Dashed lines marked “I”, “II” and “III” correspond to marks on the sampling lines in Fig. 1A. (Forinterpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)


4.4. Seasonal cyclicity

Relatively scaled powerspectra of threemethods of spectral analysis(MTM, Lomb-Scargle and simple periodogram) are plotted in Figs. 7, 8and 9. Confidence levels for detected frequencies show that frequencieswith high spectral power according to all spectral analysis methods(black rectangle in Figs. 7–9) are generally associated with high(N80%) estimated confidence levels. These are the frequency rangesthat are filtered from the records using bandpass filtering. Resultingbandpass filters in the frequency domain of seasonality pick up fluctua-tions in the records that were identified in Figs. 4–6. Figs. 7–9 show thatthe period best describing the data is±8mm long in VV,±20mm in TSand ±3 mm in OF. Results of spectral analysis show that all recordsshow periodicity in the seasonal range, but cyclicity is, in general, bestrepresented in Sr/Ca, Mg/Ca and stable isotope records, where bandpassfiltersmost successfully pick up the cyclicity in the records. Results fromthe three different methods of spectral analysis are not similar in allcases but agree, in general, in the frequency domainwhere the seasonal


cycle is found. Bandpass filters of the proxy records reflect the periodicvariation in stable isotope records, but fail to explain themajority of thevariation in trace element records, which have a less sinusoidal charac-ter. Furthermore, interpretation of growth seasons in Figs. 7–9 showthat the amount of calcite deposition in the shells is not equal betweenseasons, resulting in larger parts of the TS shell being deposited underhigh-δ18O conditions and slightly larger parts of the VV shell depositedunder low-δ18O conditions. There is no observable difference in thelength of seasons in the OF shell. Interpretation of seasonal cyclicity inthe three shells yields an age of 9 years for OF, 6 years for TS and 8–9 years for VV. Age of VV is uncertain due to the poorly preservedlower ±20 mm which precluded isotope analysis, forcing the growthperiod to be estimated to 2–3 years for this part of the shell (see Fig. 7).

4.5. Phase relationships

As indicated in Figs. 4–9, periodic fluctuations of stable isotope andtrace element records can be traced between different proxy records.



Fig. 5. Torreites sanchezi milovanovici (TS) shell. Overview of stable isotope (‰VPDB), elemental abundance (wt% and μg/g) and relative abundance records (mmol/mol, 11 point runningaverage). Dashed lines marked “I”, “II” and “III” correspond to marks on the sampling lines in Fig. 1B.


An overview of visually observed and statistically significant correla-tions between proxy records of the bivalves is given in Table 2. Figs.7–9 show that many proxies only show clear phase relationships inparts of the record and correlations between total shell records are gen-erally low (see Table 2), as proxies shift in and out of phase. One exam-ple of this is found in the VV shell, where periodicity in Zn/Ca, δ13C and


Sr/Ca is most pronounced in the central part of the record (30–70 mm;Fig. 7). Another case is in the OF record where the last 2 mm are influ-enced by a strong trend in δ13C and Sr/Ca, whereas the part of the recordthat immediately precedes this drop (i.e., 14–22mm) shows clear peri-odic variation. A close inspection of the phase relationships betweenproxies (Figs 7–9) demonstrates that periodicities in δ18O records are



Fig. 6. Oscillopha figari (OF) shell. Overview of stable isotope (‰VPDB) and elemental abundance records (wt% and μg/g) and relative abundance records (mmol/mol, 11 point runningaverage). Dashed lines marked “I”, “II” and “III” correspond to marks on the sampling lines in Fig. 1C.


Please cite this article as: de Winter, N.J., et al., Tropical seasonality in the late Campanian (late Cretaceous): Comparison between multiproxyrecords from three bivalve taxa from O..., Palaeogeogr. Palaeoclimatol. Palaeoecol. (2017), http://dx.doi.org/10.1016/j.palaeo.2017.07.031


Fig. 7. Records of stable isotopes and four element-to-calcium ratios from Vaccinites vesiculosus (VV) are plotted together with cyclical components filtered from the data using bandpassfiltering. Spectrograms show powerspectra from the threemethods of spectral analysis (coloured lines) as well as confidence levels calculated using red noise estimation and harmonic F-tests (grey shaded areas) of every record. The black rectangle on the powerspectra indicates the range of frequencieswith significant periodicity used as thewindow for bandpassfiltering.Yellow andwhite bars represent interpreted seasons in the δ18O record. Dashed linesmarked “I”, “II” and “III” correspond tomarks on the sampling lines in Fig. 1A. (For interpretation of thereferences to colour in this figure legend, the reader is referred to the web version of this article.)


generally in phasewithMg/Ca. However, this relationship is only statis-tically significant in OF (Table 2). On the other hand, the positive rela-tionships between Mg/Ca and S/Ca that are visually observed in allshells do have a statistical basis. Positive correlation of Sr/Ca with S/Cais both visually observed and statistically significant in the rudistidshells, but not in the oyster shell. Another difference between therudistids and the oyster is a negative correlation of δ13C with S/Ca andSr/Ca in the rudistid shells, which in the OF shell is positive. The latteris presumably caused in large by the sharp drop in Sr/Ca and δ13C nearthe end of the record. Sr/Ca ratios seem to be in antiphase with Mg/Caratios in most shell records, but this correlation is only weakly signifi-cant in TS and OF. In the TS shell, contrary to the other two shells,both stable isotope records are strongly correlated. The relationship ofZn/Ca with other records is complicated, as not many correlationshave statistically significant p-values (p b 0.05). Pearson's coefficients(r) indicate that Zn/Ca ratios often exhibit weak positive correlationswith Mg/Ca and negative correlations with Sr/Ca. However, these rela-tionships are not always supported by visual inspection,mostly becausethe phase relationship of these records tends to change across the re-cord (see Figs. 4–9). Interestingly, visual inspection suggests a negativerelationship between Zn/Ca and S/Ca, especially in the parts of VV andOF that show well-expressed periodicity. However, this relationship isonly significant in the bulk statistics of the TS record. This again indi-cates that phase relationships between these proxies are complex,change throughout the records and cannot easily by summarized by astatistical value.


5. Discussion

5.1. Shell preservation

5.1.1. Spatial distributionIn the case of fossil bivalve taxa, amap of Fe, Si and calcium (Ca) con-

centrations highlights zones in the sample, where the calcite underwentdiagenetic overprinting. As such, Fig. 1 provides an initial survey of thestate of preservation of the bivalve shells. In addition, a heatmap ofthe combined intensities of Fe and Mn (elements both associated withdiagenesis, see Al-Aasm andVeizer, 1986a, 1986b; Steuber, 1999), high-lights those spots where diagenetic carbonates, (re-)crystallized post-mortem, are most common. XRF maps indicate that the best-preservedcalcite is found in the outer shell layers of rudistid shells. As discussed bydeWinter and Claeys (2016), this layer is punctuated by zones of diage-netic material that should be avoided during sampling. In the VV shell,the left part of the shell cross-section contains a higher amount ofthese spots affected by diagenesis than the right part and spots are pres-ent in greater concentration in the lower part of the shell (as oriented inFig. 1). The concentrations of Ca, Si, Fe and Mn in the sampled parts ofshells (Figs. 3–6) indicate that the preservation state of the calcite sam-pled in TS and OF is better than that of VV. Trace element records to-gether with the XRF maps in Fig. 1 indicate that diagenesis, althoughpresent to some extent in all shells, is more localized and therefore eas-ier to avoid during sampling of TS and OF. This explains why the VV re-cord containsmore intervals with increased concentrations of Si, Fe and



Fig. 8. Records of stable isotopes and four element-to-calcium ratios from Torreites sanchezi milovanovici (TS) are plotted together with cyclical components filtered from the data usingbandpass filtering. Spectrograms show powerspectra from the three methods of spectral analysis (coloured lines) as well as confidence levels calculated using red noise estimation andharmonic F-tests (grey shaded areas) of every record. The black rectangle on the powerspectra indicates the range of frequencies with significant periodicity used as the window forbandpass filtering. Yellow and white bars represent interpreted seasons in the δ18O record. Dashed lines marked “I”, “II” and “III” correspond to marks on the sampling lines in Fig. 1B.(For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)


Mn (see also Fig. 3). Another difference between the VV shell and TSand OF is the relative concentrations of Si, Fe and Mn in altered partsof the shell (Compare Fig. 4 with Figs 5 and 6). This differencemay beexplained by two different types of diagenesis that affected thefossils.

5.1.2. BoringThe first is represented by the highly Fe and Mn enriched spots in

VV, which can be explained by boring into the shell by predators(most likely sponges; Sanders and Baron-Szabo, 1997). Bore holesare later filled in by detrital material rich in Fe, Mn and Si (see deWinter and Claeys, 2016). These bore holes explain the drops (byseveral weight percent) in concentration of Ca observed in Fig. 4,where calcite is replaced by (Fe-, Mn- and Si-rich) inclusions of detri-tal material that filled up the bore holes. This boring into the bivalveshells most likely took place during the life time of the bivalve orearly post-mortem and has most strongly affected the VV shell. Therelatively thin outer shell layers of VV probably made it more suscep-tible to boring predation than the significantly more thick-shelled TSand OF (Sanders and Baron-Szabo, 1997), explaining more frequentbore holes in the VV shell and higher local Fe and Mn concentrations(see also Fig. 3).


5.1.3. SilicificationThe second type of diagenesis is silicification, which is evident from

the corona of Si-rich material that is present on the outside and in thecavity of the TS shell and to a lesser extent on the OF shell (Fig. 1).This silicification took place after burial of the fossils, is strongly con-trolled by the local concentration of Si in the pore fluid (Maliva andSiever, 1988) and has left large (mm- to cm-scale) euhedral quartz crys-tals in the porous cavity of the TS shell (Fig. 1). The fact that VV was rel-atively unaffected by silicification seems counter-intuitive, as VV and TSshells are stratigraphicallymore closely associatedwith each other thanwith OF, which was found slightly lower in the stratigraphy. However,since the V1-member of the Samhan Formation, from which VV andTS originate, is laterally continuous for 200m (Schumann, 1995), it can-not be excluded that local differences in Si content of the pore fluid inthis member were large enough to cause the observed difference inthe extent of silicification between the shells. While traces of silicifica-tion are also visible in OF, it is hypothesized that the calcite shell ofthis bivalve was likely more resistant to replacement by quartz thanthe partly aragonitic TS shell (see Schubert et al., 1997), preventingthe extensive (cm-deep) invasion of Si-rich pore fluid observed in theTS shell from affecting OF. The last 2 mm of the Sr/Ca record in the OFshell (Fig. 6)were probably affected bydiagenesis as drops in Sr concen-tration are much more severe than those observed in pristine modern



Fig. 9. Records of stable isotopes and four element-to-calcium ratios from Oscillopha figari (OF) are plotted together with cyclical components filtered from the data using bandpassfiltering. Spectrograms show powerspectra from the three methods of spectral analysis (coloured lines) as well as confidence levels calculated using red noise estimation andharmonic F-tests (grey shaded areas) of every record. The black rectangle on the powerspectra indicates the range of frequencies with significant periodicity used as the window forbandpass filtering. Yellow and white bars represent interpreted seasons in the δ18O record. Dashed lines marked “I”, “II” and “III” correspond to marks on the sampling lines in Fig. 1C.(For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)


bivalves. The sharp decrease in Sr/Ca is matched by a decrease in δ13C,potentially indicating incorporation of 12C–enriched carbonate duringdiagenesis. The statistically significant positive correlation between Sr/Ca and δ13C (Table 2) is strongly controlled by this diagenetic drop atthe end of the record.

5.1.4. Data filteringIn Fig. 4 (VV), parts of the trace element record that show peaks in

the concentrations of these elements were removed from records ofMg/Ca, Zn/Ca, Sr/Ca and S/Ca to avoid interpretation of parts of the re-cord that were affected by diagenesis. This was not necessary in the re-cords of TS and OF as theMn and Fe concentration in these shellsmostlyremained well below 200 μg/g, which has been proposed as a thresholdfor pristine shell material (Brand and Veizer, 1980; Al-Aasm and Veizer,1986a, 1986b; Steuber, 1999). However, as is evidenced by the presenceof silicification in these shells, thresholds of Mn, Fe and Sr concentra-tions as indicators for pristine carbonate preservation are highly sim-plistic and can only be used to trace calcite recrystallization fromreducingporefluids (Aller, 1980; Brand andVeizer, 1980). Furthermore,fossilization of the bivalves has probably limited the preservation of or-ganic matter in the shells, as indicated by the lower S concentrationsfound in the present study (100–200 μg/g) compared to higher (~500μg/g) S concentrations found in modern bivalve studies (Lorens andBender, 1980; Dalbeck et al., 2006). Microscope-guided drilling for sta-ble isotope samples guided by XRF mapping allowed bore holes and


silicified shell parts to be avoided, and the resulting filtered trace ele-ment and stable isotope records (Fig. 4–6) are indicative for well-pre-served bivalve calcite.

5.2. Multi-proxy records

5.2.1. Comparison with modern shellsElement-to-Ca ratios of Mg, Zn and Sr of fossil shells in this study are

in agreement with ratios found in modern bivalves (e.g. Carriker et al.,1980; Al-Aasm and Veizer, 1986a, 1986b; Steuber, 1999; VanderPutten et al., 2000; Holmden and Hudson, 2003). Mg/Ca and Sr/Ca inOF are similar to those found in modern oyster species (Carriker et al.,1980; Ullmann et al., 2013; Mouchi et al., 2013), though with lowerMg/Ca than found in the estuarine oyster Crassostrea virginica (Surgeand Lohmann, 2008). Concentrations of Zn, Mn and Fe are also inclose agreement with those found in modern oyster shells (Carriker etal., 1980; Ullmann et al., 2013), and S concentrations are similar tothose found in foliated calcite structures of Crassostrea gigas byDauphin et al. (2013), though slightly lower than those found in othermarine bivalves such as Mytilus edulis (Lorens and Bender, 1980;Dalbeck et al., 2006). Trace element concentrations are generally higherin VV and TS, and are in closer agreement with those in calcite shells ofmodernmarine bivalves (Vander Putten et al., 2000; Gillikin et al., 2005;Freitas et al., 2009), with the exception of S, which is lower than foundin calcite of marine bivalves (Lorens and Bender, 1980; Dalbeck et al.,



Table 2Overviewmatrix of correlations between proxy records in the three bivalves. Uppermatrices show correlationsmade on the basis of on visual inspection. Red fills indicate antiphase correlationswhile green fills signify in-phase correlations. Matricesin the second row show p-values of correlations between these records. Green fills indicate statistically significant relationships (p b 0.05), while red fills indicate no significant relationship. The bottom row ofmatrices show Pearson's coefficients (r)of correlations between records. Green fills indicate positive correlations between records (r N 0) and red and orange fills indicate negative correlations (r b 0). White fills indicate that there is no significant correlation between the records.

S/Ca Zn/Ca Sr/Ca Mg/Ca d13C d18O S/Ca Zn/Ca Sr/Ca Mg/Ca d13C d18O S/Ca Zn/Ca Sr/Ca Mg/Ca d13C d18O

S/Ca S/Ca S/Ca

Zn/Ca Zn/Ca Zn/Ca

Sr/Ca Sr/Ca Sr/Ca

Mg/Ca Mg/Ca Mg/Ca

d13C d13C d13C

d18O d18O d18O


S/Ca 0.323 0.000 0.000 0.001 0.105 S/Ca 0.000 0.000 0.000 0.796 0.062 S/Ca 0.040 0.519 0.000 0.063 0.013

Zn/Ca 0.323 0.078 0.000 0.402 0.001 Zn/Ca 0.000 0.257 0.813 0.151 0.138 Zn/Ca 0.040 0.311 0.193 0.861 0.112

Sr/Ca 0.000 0.078 0.000 0.010 0.508 Sr/Ca 0.000 0.257 0.025 0.011 0.187 Sr/Ca 0.519 0.311 0.001 0.000 0.072

Mg/Ca 0.000 0.000 0.000 0.721 0.000 Mg/Ca 0.000 0.813 0.025 0.204 0.215 Mg/Ca 0.000 0.193 0.001 0.067 0.001

d13C 0.001 0.402 0.010 0.721 0.063 d13C 0.796 0.151 0.011 0.204 0.000 d13C 0.063 0.861 0.000 0.067 0.000

d18O 0.105 0.001 0.508 0.000 0.063 d18O 0.062 0.138 0.187 0.215 0.000 d18O 0.013 0.112 0.072 0.001 0.000


S/Ca 0.312 0.286 -0.185 S/Ca -0.225 0.328 0.206 0.017 S/Ca 0.099 0.425 0.261

Zn/Ca 0.357 -0.176 Zn/Ca -0.225 Zn/Ca 0.099

Sr/Ca 0.312 0.138 -0.138 Sr/Ca 0.328 -0.070 0.163 Sr/Ca -0.153 0.607

Mg/Ca 0.286 0.357 0.138 -0.199 Mg/Ca 0.206 -0.070 Mg/Ca 0.425 -0.153 0.343

d13C -0.185 -0.138 d13C 0.017 0.163 0.618 d13C 0.607 -0.476

d18O -0.176 -0.199 d18O 0.618 d18O 0.261 0.343 -0.476

Vacciniteas vesiculosus (VV) Torreites sanchezi milovanovici (TS) Oscillopha figari (OF)

r-values

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2006) and low-Mg calcite shells of brachiopods (England et al., 2007),but in closer agreement with concentrations in the aragonitic tridacnidbivalve Hippopus hippopus (Yoshimura et al., 2013). Higher concentra-tions of trace elements in rudistid bivalves compared to the hinge ofthe oyster are in agreement with similar offsets between prismaticand foliated calcite structures in modern oysters (Carriker et al.,1980). The fact that Mg/Ca ratios are low compared to modern shellsis likely a result of the lower Mg/Ca ratios in Late Cretaceous oceanwater, in which the bivalves grew (Stanley and Hardie, 1998). The factthat Mg/Ca ratios in these bivalves approach modern values if the (3.3times) lower Mg/Ca ratios of seawater in which they grew wheretaken into account indicates that these bivalves lived in full marine con-ditions and that they incorporated Mg into their shell proportional toambient Mg/Ca ratios similar to modern bivalves (Surge andLohmann, 2008).

5.2.2. Phase relationshipsThe complexity of phase relationships in this multi-proxy study is il-

lustrated by the lack of significant, strong (p b 0.05; r N 0.60) correla-tions between proxy records (Table 2). This lack of linear relationshipsis caused by different parameters acting on the proxies at differenttimes and because the expression of seasonality in the shells is not al-ways equally strong (Figs. 7–9). A close examination of Figs. 7–9shows that this is indeed the case, as filtered sinusoidal trends only ex-plain a part of the variation. The amplitude of seasonality observed inproxy records is also highly variable along the length of the shell re-cords, and on many occasions this seasonality (especially in trace ele-ment records) is overprinted by short-lived variations, obscuringphase relationships between proxies. Finally, the amount of shell mate-rial deposited in a year is variable, generally becoming shorterwith shellage, an observation that is in agreement with observations in modernbivalves (e.g. Richardson et al., 2004; Schöne et al., 2005, 2011).

5.3. Bivalve physiology

5.3.1. Ontogenetic trendsDespite the fact that bivalves in this study were relatively short-

lived, someontogenetic trends are observed in the record. The graduallydecreasing trend in Sr/Ca in the OF shell is similar to ontogenetic trendsin Sr/Ca found in modern oysters (Ullmann et al., 2013), suggesting aneffect of growth rate on the incorporation of Sr into OF. Discarding thefinal drop in δ13C, no significant ontogenetic trend in δ13C values is ob-served in OF. On a seasonal scale, lows in Sr/Ca coincide with highδ13C (Figs. 7 and 9), indicating that differences in metabolic rate mayhave controlled Sr/Ca ratios, as observed in culture studies on modernbivalves (Lorrain et al., 2005; Freitas et al., 2006). Since Sr/Ca seasonalityin OF is weak, its correlation is controlled by the stronger ontogenetictrend. This illustrates that it remains important to visually inspect andcompare seasonal records to complement bulk statistical analysis ofthe proxy records. Interpretation of seasonal cycles in these figures fur-ther indicates that shell growth varies seasonally. The length of theinterpretedwarm/low-salinity season (lower δ18O) and cold/higher-sa-linity season (higher δ18O) are not equal, showing differential growthrates between the seasons or even complete growth halts during ex-treme conditions (Wanamaker et al., 2011). The difference in theamount of shellmaterial deposited duringdifferent seasons indicates ei-ther that the records of TS was more strongly affected by extreme con-ditions in thewarm/low-salinity season than the other shells, or that itsgrowth conditions were more extreme in terms of high temperaturesand/or low salinities than those of VV and OF. The former hypothesismight indicate that TS was more resistant to extreme conditions, butthe latter hypothesis cannot be excluded because the length of theseshort-lived bivalve records means that the probability of these organ-isms living at the samemoment in time is small. Thickness of annual de-posits in the shells decreases with age, suggesting ontogeneticallydecreasing growth rates, in agreement with other studies of rudistids


(Steuber, 1995, 1996) and oysters (Ullmann et al., 2010). Periodic fluc-tuations in the stable isotope records of the OF shell are paced to thegrowth increments observed in Fig. 1, showing that these growth incre-ments are likely annual inOscillopha figari, contrary to those observed inmodern Crassostrea gigas (Ullmann et al., 2013).

5.3.2. Physiological control on trace element incorporationThe correlation between Mg/Ca and S/Ca found by Lorens and

Bender (1980) is also observed in the bivalve records in the presentstudy (Table 2), and is especially clearly visible in the OF record. S ispresent in the organicmatrices of bivalve calcite in the formof ester sul-phates and comprises approximately 10% of the organic matter in theshell, meaning that S/Ca ratios of up to 10 mmol/mol can be explainedby the occurrence of S in organic matter in the shell (Crenshaw, 1972;Lorens and Bender, 1980). However, more recent studies have conclud-ed that a large fraction of S in bivalve shells is present in inorganic form(Yoshimura et al., 2014). Annual fluctuations in S contents in extant ara-gonitic and calcitic bivalves have been linked to growth rate and con-centrations in the calcifying fluid, with lower S concentrations duringmore rapid growth (Yoshimura et al., 2013, 2014). These fluctuationsbecome progressivelymore pronouncedwith age in the OF shell, show-ing that perhaps these short episodes of rapid growth become morecommon with age in the oyster shell. This increase in fluctuation ofthe S/Ca record is mirrored in the Mg/Ca record. The covariations of S/Ca with Mg/Ca can be explained by local increases in the amount of or-ganic matrix in the carbonate structure of the shell. It has been shownthat bivalves secrete additional sulphate-bearing organic matter underthe influence of crystal growth-inhibiting concentrations of Mg inorder to seed calcite growth by locally increasing Ca concentrations,causing local enrichments of Mg and S in the shell (Lorens andBender, 1980). This physiological control on Mg-incorporation wouldmean that Mg concentrations, whenever correlated to S concentrations,are associated with the organic matrix of the shell rather than the cal-cite, implying that caution must be exercised when interpreting Mg/Ca ratios in terms of palaeotemperature (Rosenberg and Hughes,1991; England et al., 2007). Alternatively, if part of the Mg in the shellsis bound to the organicmatrix rather than the calcite lattice, increases inS/Ca and Mg/Ca ratios may indicate calcite deposited during times ofstress, when more organic matter is secreted (Lorens and Bender,1980; Rosenberg et al., 1989, 2001). Such periods of increased stressmay also be controlled by growth rate or environmental stress, as epi-sodes of rapid growth or outside stress may rupture the periostracalrim resulting in increased organic matrix production and allowing sul-phate-rich sea water to enter the extra-pallial fluid (Carriker et al.,1980; Skelton et al., 1990; Rosenberg et al., 2001). This hypothesis isconsistent with the occurrence of storm events in the turbulent envi-ronmental setting of the bivalves, which could have caused disruptionof the bivalve's life environment on a regular basis.

5.4. Sea water chemistry

5.4.1. Zn/Ca ratios and palaeoproductivityParts of all shell records show periodic spikes in Zn/Ca, indicating

that there were seasonal changes in productivity in the environment.The punctuated character of the Zn/Ca record, with sharp increasesrather than more sinusoidal fluctuation, can be explained by episodesof release of Zn into the environment after productivity blooms. Thefact that Zn concentrations are lower during the remainder of the recordis ascribed to its role as a micronutrient. It is continuously taken up byprimary producers and bound to organic ligands without beingreplenished fast enough unless during timeswhen respiration increasesdramatically, i.e. after productivity blooms (Bruland, 1989; Calvert andPedersen, 1993; Vance et al., 2017). If Zn concentrations in the shell in-crease after episodes of increased productivity, as shown inmodern en-vironment studies (Calvert and Pedersen, 1993; Jackson et al., 1993;Guo et al., 2002), Zn/Ca fluctuations record blooms of




palaeoproductivity in the shallow marine environment of the shells.This also explains why often multiple peaks in Zn/Ca ratios per yearare observed, especially in the OF and TS shell records, which displaydouble peaks in Zn/Ca paced to seasonal variation in δ18O records.These increases in palaeoproductivity likely strongly affected the localsurface ocean chemistry, especially in the progressively more confinedLate Cretaceous Tethys Ocean (Dercourt et al., 1986; Almogi-Labin etal., 1993; Steuber and Löser, 2000; Jarvis et al., 2002; Fleurance et al.,2013). Indeed, Zn/Ca peaks in VV and OF seem to be paced to intervalswith higher δ13C values, which may reflect increased δ13C values inthe water indicative of increased productivity (Grossman, 1984; Jarviset al., 2002; Takesue and van Geen, 2004) or decreasedmetabolic activ-ity (Klein et al., 1996b; Owen et al., 2002; Gillikin et al., 2006). The lattermay be explained by changes in the redox state of the shallowocean as aconsequence of the reduction of organic matter after a productivitybloom. It has been proposed that this relationship between metabolicrate and δ13C values is especially strong during periods of relativelylow respiration and low ambient CO2/O2 ratios, as is the case inwell-ox-ygenated waters (McConnaughey et al., 1997; Gillikin et al., 2006). Theobserved anti-phase relationship between Zn/Ca and Sr/Ca in VV andOFsupports this hypothesis of reduced metabolic rate in the shells duringperiods corresponding to peaks in Zn/Ca ratios. Such seasonal changesin redox conditions in the surface ocean are common in present-daylow-latitude settings (Morrison et al., 1998). Under more oxygen-poorconditions, the mobility and bioavailability of redox sensitive elementsin the water column increases significantly (Zwolsman et al., 1997;Gerringa et al., 2001). Seasonal cycles in Zn/Ca and S/Ca are especiallyevident in the OF shell, showing that changes in Zn availability are read-ily recorded in oyster shells, as shown by Carriker et al. (1980) and Guoet al. (2002). Large S/Ca shifts show that seasonal changes in the organicmatter fraction incorporated in the shell of OF are more pronouncedthan in the rudistid shells.

5.4.2. S/Ca ratios and sea water chemistryIn parts of VV andOFwhere Zn/Ca showswell-expressed periodicity,

the record is in antiphase with S/Ca ratios, which might be interpretedas evidence for an environmental control mechanism on S concentra-tions in the shells (Figs. 4, 6, 7, 9). One hypothesis might be that morereducing conditions allow S to be precipitated in sulphides while moreoxidizing conditions can remobilize S from the sediment, increasing Sconcentrations (Ku et al., 1999; Kah et al., 2004). However, since the sul-phate concentration in ocean water is several orders of magnitudehigher than the concentrations of S found in the present study, it is un-likely that changes in redox conditions in this shallow, open-marine sys-tem could have brought about conditions where this source would belimited (Chester, 2009). Evidence of a highly turbulent environment inwhich these bivalves lived renders severe redox stratification unlikely(Schumann, 1995). Furthermore, a redox shift that allows the precipita-tion of sulphideswould also reduce the bioavailability of Zn bymeans ofprecipitation of Zn sulphides, and this is not consistent with the ob-served antiphase relationship between Zn/Ca and S/Ca (Calvert andPedersen, 1993; Guo et al., 1997). Furthermore, the precipitation ofZnS requires more reducing conditions than may be expected in theshallow marine, turbulent environment of the bivalves in this study(Guo et al., 1997; Schumann, 1995). Instead, it is more likely that achange in growth and metabolic rate caused by increases in productiv-ity, when Zn concentrations are highest, resulted in an increase in S/Caratios.

5.5. Palaeotemperature seasonality

5.5.1. Stable oxygen isotope ratiosIn several studies, relationships have been found between chemical

proxies (Mg/Ca, Sr/Ca and δ18O) in biogenic carbonates and the calcifi-cation temperature of these carbonates (e.g. Epstein et al., 1953; Craig,1965; O'Neil et al., 1969; Tarutani et al., 1969; Hays and Grossman,


1991; Takesue and van Geen, 2004; Wanamaker et al., 2008). Sinceother factors (e.g., salinity, growth rate and water chemistry) also ap-pear to control these proxies in molluscan shells, different proxiesneed to be compared to isolate the effect of temperature. Temperaturetransfer functions were either obtained through controlled inorganiccalcium carbonate precipitation (e.g., Epstein et al., 1953; O'Neil et al.,1969; Kim and O'Neil, 1997) or from culture experiments and compar-ison of proxy data with historical temperature records in bivalves aswell as in other calcifying organisms (e.g., de Villiers et al., 1995;Freitas et al., 2005; Takesue and van Geen, 2004; Surge and Lohmann,2008; Wanamaker et al., 2008). For palaeotemperature reconstructionsbased on δ18O values, a value of −1‰ is assumed for Late Cretaceousseawater (Savin and Yeh, 1981; Steuber, 1995). Temperature estimatesofminima andmaxima of the seasonal cycle based on stable oxygen iso-tope ratios from shell OF and VV yield temperatures of 25 °C and 32 °Crespectively within a 1–2 °C range depending on the calibration used(e.g. Epstein et al., 1953; Craig, 1965; O'Neil et al., 1969; Tarutani et al.,1969; Hays and Grossman, 1991). Minimum seasonal temperaturesbased on δ18O values in the OF and VV shells are in agreement, whilemaximum seasonal temperatures recorded in VV (~34 °C) exceedthose determined for OF (~30 °C). Temperatures for the TS shell usingthe same parameters turn out higher, ranging between 34 °C and 43°C. Temperatures determined based on OF and VV are in agreementwith temperatures found for Vaccinites cornuvaccinum, Vaccinitesultimus, Vaccinites oppeli, all of which are in the same family as VV, aswell as to temperatures derived from other rudistid taxa from theUpper Cretaceous (Steuber, 1995, 1996, 1999). Temperatures found inthe seasonal cycle of TS overlap with those documented for otherrudistids, but are still exceptionally high (Steuber et al., 2005), suggest-ing that δ18O values in this rudistid may have been controlled by otherfactors besides temperature. Seasonal changes in salinity could accountfor a change in stable oxygen isotope ratios (Klein et al., 1996a). The dis-tal, open marine environmental setting of these shells, however, pre-cludes a strong riverine component to explain large changes insalinity. Because of the relatively high δ18O values of rainfall in tropicalclimates, changes in salinity in the order of 10 g/kg would be requiredto account for a 1‰ difference in δ18O in the TS shell (Ravelo andHillaire-Marcel, 2007). However, it cannot be excluded that seasonal sa-linity changes did influence the stable isotope records of the shells dif-ferently, primarily because it is not certain exactly how much timeexisted between the lifetimes of the bivalves. Furthermore, as speculat-ed above, it is likely that extremeparts of the seasonal cyclewere not re-corded in one species while they were recorded in another. Thepreferential exclusion of part of the seasonal cycle from the TS shell(in this case the 18O–depleted warm/low-salinity part of the cycle)would explain the difference in seasonality between the δ18O recordof this shell and that of the closely associated VV, but does not explainthe 1‰ difference in mean value between the records. Differences inseasonality between the rudistid shells and the OF are probably ex-plained by actual changes in climate between their lifetimes, as a signif-icant amount of time may separate their formation. The fact that δ18Orecords inmodern oysters seem to faithfully recordwater temperatures(if δ18O of seawater is well-constrained; see Surge and Lohmann, 2008;Ullmann et al., 2010) puts slightly more confidence in the temperaturesreconstructed from the VV shell. Although isotope ratios from Torreitesshells from the same region have been interpreted to fractionate in dis-equilibriumwith respect to ambient seawater (Steuber, 1999), the datain this study cannot confirm or disprove this statement. However, sincedisequilibrium fractionation of isotopes in marine calcitic bivalve shellsis rare, it cannot be excluded that TS precipitated its calcite under signif-icantly lower-salinity (−10 g/kg) or higher temperature (+8 °C) withrespect to the other two bivalves. Furthermore, it must be stated thatthe use of one specimen for each species in this study precludes the dis-cussion of specimen-specific effects and therefore adds a certain uncer-tainty to the reconstructions. This uncertainty is somewhat alleviated bythe agreement of the temperature reconstructions in this study with




other bivalve-based (Steuber, 1995, 1996, 1999) and other reconstruc-tions (e.g. Huber et al., 1995; Brady et al., 1998; Alsenz et al., 2013).

5.5.2. Mg/Ca ratiosEven thoughMg/Ca ratios have been proposed as a proxy for calcifi-

cation temperature in a range of calcifying organisms (e.g. Klein et al.,1996a; Vander Putten et al., 2000; Elderfield and Ganssen, 2000;Takesue and van Geen, 2004; Freitas et al., 2005; Wanamaker et al.,2008; Surge and Lohmann, 2008; Cléroux et al., 2008; Mouchi et al.,2013), empirically determined dependencies of Mg concentrations onsea water temperature as well as mean concentrations of Mg in thesebiogenic calcites differ strongly, causing widely different transferfunctions between these studies, as illustrated in Fig. 10. The fact thatMg/Ca ratios in the OF shell are systematically lower than those fromthe rudistid shells shows that applying the same transfer function forthese shells would lead to different palaeotemperature reconstructions.Using oyster-based calibrations to calculate temperatures from Mg/Caratios in the OF shells yields unrealistically cold mean annual tempera-ture estimates of 2.9 °C (Surge and Lohmann, 2008) and 8.8 °C (Mouchiet al., 2013) with a seasonal temperature variability of ±2.5 °C and ±6°C, respectively. A probable reason for these underestimations of tem-perature with respect to the temperature reconstructions based onδ18O is that the Mg/Ca ratio of ocean water in the Late Cretaceous (1–2 mol/mol; Stanley and Hardie, 1998; Coggon et al., 2010) was lowerthan it is today (5mol/mol; Stanley and Hardie, 1998).While the incor-poration of trace elements into bivalve calcite is not yet fully under-stood, it seems likely that concentrations in ambient sea water exert adominant control on the concentrations in the shell. Taking this estimat-ed decrease in sea water Mg/Ca ratios by a factor of 3.3 with respect topresent-day values into account and recalculating temperatures basedon Mg/Ca ratios in the OF shell yields mean annual palaeotemperatureestimates of 9 °C with a temperature seasonality of 10 °C using theSurge and Lohmann (2008) calibration and 25 °C with a temperature

Fig. 10. Crossplot showing the Mg/Ca ratios in biogenic calcite and its relationship tocalcification temperature. Dashed lines indicate palaeothermometer calibrations offoraminifera (blue), oysters (green) and other bivalves (purple). Shaded boxes indicatethe ranges of Mg/Ca ratios and δ18O-inferred palaeotemperatures in this study. Thearrow points towards Mg/Ca values that were corrected for Mg/Ca values of that seawater, estimated to be ±3.3 times lower than today. Horizontal and vertical barsindicate the seasonal amplitude of the records. (For interpretation of the references tocolour in this figure legend, the reader is referred to the web version of this article.)


seasonality of 14 °C for the Mouchi et al. (2013) calibration. Thesemean annual temperature estimates, especially those based on Surgeand Lohmann (2008), are still much lower than those based on δ18Ovalues, and temperature seasonalities of 10 °C or more seem unrealisticfor tropical ocean water. When this correction for different sea waterMg/Ca ratios is applied on theMg/Ca records of VV and TS, reconstruct-ed seasonalities based on bivalve calibrations (Klein et al., 1996a;Vander Putten et al., 2000; Takesue and van Geen, 2004; Wanamakeret al., 2008) are unrealistically high aswell (N10 °C), whilemean annualtemperatures varywidely depending on the calibration that is used (seeFig. 10). It is possible that the temperature dependence of the incorpo-ration of Mg into bivalve calcite was different in low-Mg/Ca oceans orin the much hotter climate of the Late Cretaceous, or that a part of theMg in bivalve shells is associated with the organic matrix in the shelland controlled by physiological processes rather than ambient temper-ature (Freitas et al., 2009; see Discussion in Section 5.3). In any case, thepresent exercise shows that palaeotemperature reconstructions basedon the Mg/Ca proxy need to be treated with care until the mechanismscontrolling the incorporation of Mg into the shell is better understood.

5.5.3. Sr/Ca ratiosPalaeotemperature estimates based on Sr/Ca ratios in bivalve calcite

also need to be treated with care, since previous studies have shownthat changes in Sr/Ca ratios correlate with changes in growth and met-abolic rate (Klein et al., 1996b; Lorrain et al., 2005; Freitas et al., 2006)and salinity (Klein et al., 1996b; Wanamaker et al., 2008). Nevertheless,some authors have proposed relationships between Sr/Ca ratios and seawater temperature (Takesue and van Geen, 2004; Wanamaker et al.,2008). Calibrations from both these studies show a positive correlationof Sr/Ca with temperature, while a negative relationship would be ex-pected based on experimental data and thermodynamic considerations(Rimstidt et al., 1998). Applying these calibrations on this study's Sr/Carecords leads to severely inconsistent estimates and consistent underes-timation of sea water temperatures with respect to temperatures basedon δ18O values (−13 °C to 30 °C mean annual temperatures accordingto the calibration of Wanamaker et al., 2008 assuming 32 g/kg salinityand 5 °C to 8 °C mean annual temperatures according to the Takesueand van Geen, 2004 intertidal aragonite shell calibration). Furthermore,theWanamaker et al. (2008) calibrations yield unrealistically large sea-sonal temperature ranges. Correction for lower Sr/Ca ratios in Late Cre-taceous ocean water or use of a low salinity model fromWanamaker etal. (2008) yields impossibly high temperature estimates (N100 °C).Using the calibration from Takesue and van Geen (2004) with seawater-corrected Sr/Ca values yields temperatures closer to tempera-tures based on δ18O, though much lower (mean annual temperaturesrange from 12 °C for OF to 14 °C for TS with temperature seasonalitiesof 1.5 °C for OF and 10 °C for the rudistids). Nevertheless, reconstruc-tions based on Sr/Ca ratios vary significantly between specimens andaremuch lower thanwould be expected of this locality. These results il-lustrate the complexity of Sr/Ca ratios in bivalves and shows that theyare not necessarily temperature dependent (e.g. Lorens and Bender,1980; Klein et al., 1996b; Steuber, 1999). It is possible that the Sr/Ca isin part controlled by temperature, while much of the larger variationin Sr/Ca is caused by other processes such as the above-mentionedgrowth rate and salinity effects.

6. Conclusions

The study of three co-occurring extinct bivalve taxa sheds light ondifferences in the response of these bivalves to seasonally changing en-vironmental conditions. μXRF line scanning on polished shell surfacesprovides a method for simultaneous acquisition of multiple trace ele-ment records, including S, along the growth axis of the shells with astrong control on possible effects by diagenesis. A combination ofthese trace element records with stable carbon and oxygen isotopemeasurements illustrates the complex interplay of environmental and




physiological processes that control the incorporation of trace elementsand stable isotopes into bivalve shells in this low-latitude setting in thelate Campanian south eastern Tethys Ocean on the seasonal scale. Ourresults indicate that δ18O-based temperature reconstructions yield aseasonal temperature cycle of ±8 °C around a mean annual sea surfacetemperature of ±28 °C, which is comparable to the present-day situa-tion in the oceans near Oman and in agreement with other reconstruc-tions. Temperature reconstructions based on Mg/Ca or Sr/Ca ratiosremain problematic in fossil bivalves, because of the vast differencesin the transfer functions found for modern bivalves and the uncertaintyin long-term fluctuations of trace element concentrations in the oceans.Correction of Mg/Ca ratios for reconstructed differences in sea waterMg/Ca ratios between the present and the Late Campanian yields tem-peratures that are close to those reconstructed via stable oxygen iso-topes, but such reconstructions exhibit much larger seasonaldifferences, indicating that Mg/Ca ratios in these bivalves are controlledbymore than just seawater temperature. The existence of physiologicaleffects onMg incorporation into these bivalve shells is evidenced by co-varying Mg/Ca and S/Ca ratios. Palaeotemperature reconstructionsusing Sr/Ca ratios are different from those based on stable oxygen iso-tope ratios, leading to the conclusion that temperature dependence ofthis proxy isweak at best and that other factors such as growth rate,me-tabolism and salinity probably have strong effects on the Sr/Ca ratios. Znrecords show that these Late Campanian shallow seas were character-ized by productivity blooms, which control Zn concentrations in thewater column analogous to present-day shallow-marine systems.After these blooms, enhanced respiration remobilized Zn in the surfaceocean and decreased growth rates of the bivalves, leading to the de-creased incorporation of S in their shells. The oyster species Oscillophafigari appears to have been especially sensitive to these changing condi-tions and a clear periodic record of Zn and S is recorded in its shell. Sincesome of the studied proxies are likely to have been controlled by theanimal's growth rate and metabolism, further research into the quanti-fication of growth rates as recorded in extinct bivalve shells could reflecta valuable tool in the interpretation of these multi-proxy records.

Supplementary data to this article can be found online at http://dx.doi.org/10.1016/j.palaeo.2017.07.031.

Acknowledgments

The authors thank Prof. Dr. AlanWanamaker and one anonymous re-viewer for their thorough and insightful review comments that helped toimprove this manuscript.We also thank Prof. Dr. Thomas Algeo for guid-ing the review process. This work is made possible by the loan of fossilbivalve shells from the Oertijdmuseum De Groene Poort in Boxtel, theNetherlands and the Natuurhistorisch Museum Maastricht. NJW is fi-nanced by a personal PhD fellowship from IWT Flanders (IWT700). SGis a Postdoctoral Fellow of the Research Foundation Flanders (FWO,OZR1994BOF). PC thanks the Hercules foundation Flanders for an up-grade of the stable isotope laboratory (grant HERC9) and the acquisitionof XRF instrumentation (grant HERC1309). The authors acknowledge fi-nancial and logistic support from the Flemish Research Foundation(FWO, research project G017217N) and Teledyne CETAC Technologies(Omaha, NE, USA) as well as support from VUB Strategic Research(BAS48). SVM is a Ph.D. Fellow of the FWO. We thank Lieven Bekaertand Quintin Dierckens for their help with the sample preparation.

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