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In Situ Geochemical Analysis of Organics in Growth Lines of Antarctic Scallop Shells: Implications for Sclerochronology

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In Situ Geochemical Analysis of Organics in Growth Lines of Antarctic Scallop Shells: Implications for Sclerochronology minerals Article In Situ Geochemical Analysis of Organics in Growth Lines of Antarctic Scallop Shells: Implications for Sclerochronology Alberto Pérez-Huerta 1,* , Sally E. Walker 2 and Chiara Cappelli 1 1 Department of Geological Sciences, The University of Alabama, Tuscaloosa, AL 35487, USA; [email protected] 2 Department of Geology, University of Georgia, Athens, GA 30602, USA; [email protected] * Correspondence: [email protected] Received: 10 May 2020; Accepted: 4 June 2020; Published: 10 June 2020 Abstract: Bivalve shells are extensively used as bioarchives for paleoclimate and paleoenvironmental reconstructions. Proxy calibrations in recent shells are the basis for sclerochronology and the applications of geochemistry data to fossils. Shell geochemical information, however, could be altered with the disappearance of intercrystalline organic matrix components, including those linked to shell growth increments, during early diagenesis. Thus, an evaluation of the chemistry of such organics is needed for the correct use of sclerochronological records in fossil shells. Here, we use atom probe tomography (APT) for in situ geochemical characterization of the insoluble organic matrix in shell growth increments in the Antarctic scallop, Adamussium colbecki. We confirm the presence of carboxylated S-rich proteoglycans, possibly involved in calcite nucleation and growth in these scallops, with significant concentrations of magnesium and calcium. Diagenetic modification of these organic components could impact proxy data based on Mg/Ca ratios, but more importantly the use of the δ15N proxy, since most of the shell nitrogen is likely bound to the amide groups of proteins. Overall, our findings reinforce the idea that shell organics need to be accounted for in the understanding of geochemical proxies. Keywords: atom probe tomography (APT); biomineralization; proteoglycans; carboxylic acid; Adamussium colbecki; Antarctica; proxies; Mg/Ca; δ15N 1. Introduction Chemical proxy data from calcium-carbonate-based biomineral structures are extensively used for paleoclimate and paleoenvironmental reconstruction [1,2]. This proxy information is especially significant for high-resolution climate records and environmental monitoring in the context of sclerochronology [3]. Proxy calibrations using sclerochronology of bivalve shells are significant for the understanding of past environmental events, in particular for archeological and Holocene records [3,4]. However, these calibrations could be compromised if the geochemistry of the organics associated with shell growth is not considered [5] in the development and applications of proxies. Thus, the precise chemical characterization of organics in growth lines is important in the development and application of proxies in the context of sclerochronology. However, the in situ geochemical characterization of such organics is challenging because non-destructive techniques, with the exception of nano-SIMS (Secondary Ion Mass Spectrometry), can rarely target shell elements with dimensions below 5 µm, which is the case for bivalve shell growth lines. In this study, we use the atom probe tomography (APT) technique for the geochemical analysis of organics within growth lines of the Antarctic scallop, Adamussium colbecki. This species was chosen Minerals 2020, 10, 529; doi:10.3390/min10060529 www.mdpi.com/journal/minerals Minerals 2020, 10, 529 2 of 14 Minerals 2020, 10, x FOR PEER REVIEW 2 of 16 because of its importance within the benthic communities of Antarctica [6] and its potential as resolutiona high-resolution bioarchive bioarchive to understand to understand glacial ice glacial dynamics ice dynamicsin Antarctica in Antarctica[7,8]. Furthermore, [7,8]. Furthermore, we discuss wethe discussimplications the implications of the geochemical of the geochemical make-up of make-upgrowth lines of growth for shell lines biomineralization. for shell biomineralization. Finally, we evaluateFinally, we the evaluate potential the impact potential of diagenesis impact of diagenesisin proxy applications in proxy applications for this species for this and species other and bivalves other usedbivalves in sclerochronological used in sclerochronological studies. studies. 2. Materials Materials and Methods 2.1. Materials Materials Living shells of the Antarctic scallop, Adamussium colbecki, were collected in November 2008 from Explorers Cove (77(77°34.259’◦34.2590 S, 163°30.699’ 163◦30.6990 E),E), located located in in western western McMurdo McMurdo Sound, Antarctica [6] [6] (Figure1 1).). Figure 1. AntarcticAntarctic scallop scallop ( (AdamussiumAdamussium colbecki ) shell. shell. ( (AA)) Top Top view view of of a a right right valve valve used used in in this this study. study. Note: the the red red line line marks marks the the section taken taken along along th thee shell length from the umbo region (U) to the posterior region (P). (B) Image of the shellshell interiorinterior ofof thethe samesame valve.valve. (C) Shell regions polished and prepared for SEM (Scanning Electron Microscopy) and APT analyses. Note: The red rectangle marks the location of the shell analyzed. ( (D)) SEM SEM image image of of the the shell shell surface surface sh showingowing the the locations locations of surficial surficial striae (S) and substrial growth lines (white arrows). (E) Detailed view of some substrial growth lines (dashed lines) from the markedmarked areaarea (red(red squaresquare inin ((CC)).)). 2.2. Methods 2.2.1. General Sample Preparation and Selection of Regions of Interest From a group of disarticulated, tissue-free valves, one right valve was selected and embedded in resin. After embedding, the valve was sectioned along the length (from the umbo region to the posterior region; Figure 1) and the resulting sections were ultrapolished with a suspension of alumina Minerals 2020, 10, 529 3 of 14 2.2. Methods 2.2.1. General Sample Preparation and Selection of Regions of Interest From a group of disarticulated, tissue-free valves, one right valve was selected and embedded Minerals 2020, 10, x FOR PEER REVIEW 3 of 16 in resin. After embedding, the valve was sectioned along the length (from the umbo region to the (Micropolishposterior region; II Buehler, Figure1 )USA; and the1.0 resultingmicron for sections 5 min were and ultrapolished0.3 micron for with 10 min) a suspension on polishing of alumina cloths. After(Micropolish polishing, II Buehler,sections were USA; ultrasonicated 1.0 micron for with 5 min dionized and 0.3 water micron for for 3 min. 10 min) One onsection polishing was used cloths. to Afterstudy polishing,the microstructure sections through were ultrasonicated SEM imaging, with whereas dionized the waterother section for 3 min. was One used section for APT was sample used preparation.to study the microstructure through SEM imaging, whereas the other section was used for APT sampleThe preparation. SEM imaging was conducted in the posterior shell region (Figure 1C) to analyze the different typesThe of SEMgrowth imaging lines wasand conductedtheir locations in the in posterior relation shellto the region surficial (Figure striae1C) to(Figure analyze 1D,E). the di Severalfferent substrialtypes of growth growth lines lines and measuring their locations ~1.5 µm in relationin thickness to the were surficial found striae in the (Figure same1D,E). location Several as the substrial striae ongrowth the shell lines surface measuring (Figure ~1.5 1E).µm In in thicknessthe polished were sect foundion, the in the growth same lines location were as also the striaevisible, on and the shellthus wesurface could (Figure easily1 E).identify In the the polished location section, of areas the for growth sample lines preparation. were also visible, Each stria and thushas a we bundle could of easily two substrialidentify thelines location that correspond of areas for to sample the same preparation. growth increment Each stria (Figure has a bundleS1). Multiple of two attempts substrial were lines madethat correspond to capture tothe the growth same lines growth (Figure increment S1) and (Figure we finally S1). Multiplemanaged attempts to target wereeach madepair of to substriae capture underpinningthe growth lines a certain (Figure stria S1) andin order we finallyto make managed APT samples, to target with each one pair wedge of substriae in each underpinningof them (Figure a 2).certain stria in order to make APT samples, with one wedge in each of them (Figure2). Figure 2.2. TargetedTargeted areas areas for for APT APT analyses. analyses. (A) Shell(A) Shell region region image image showing showing the location the location of the platinum of the platinum(Pt) deposits (Pt) fordeposits focused for ion focused beam ion (FIB) beam milling (FIB) of milling two wedges of two (wedge wedges 7 (wedge (W7) and 7 (W7) wedge and 8 (W8))wedge on 8 (W8))the coupled on the growthcoupled lines growth corresponding lines corresponding to one stria. to one (B) Detailedstria. (B) imageDetailed of image W7 on of top W7 of on the top substrial of the substrialline (red dashedline (red lines). dashed (C) lines). Detailed (C) image Detailed of W8 image on top of ofW8 the on substrial top of the line substrial (red dashed line lines).(red dashed lines). 2.2.2. Scanning Electron Microscopy (SEM) Imaging The valve section, in contrast to the one used for APT preparation, was etched with 2% HCl for 30 s and sputter coated with gold for 120 s. Imaging was conducted using a JEOL 7000 FEG-SEM (JEOL, Tokyo, Japan; 30 kV, medium (10) spot size, and 11 mm working distance)
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