Rare earth elements (REEs) and yttrium in seawater
originate from atmospheric fallout, continental weathering, and transport
from rivers, as well as hydrothermal activity. Previous studies have reported the
use of REE and Y measurements in biogenic carbonates as a means to
reconstruct these surface processes in ancient times. As coastal seawater
REE and Y concentrations partially reflect those of nearby rivers, it may be
possible to obtain a regional fingerprint of these concentrations from
bivalve shells for seafood traceability and environmental monitoring
studies. Here, we present a dataset of 297 measurements of REE and Y abundances by laser ablation
inductively coupled plasma mass spectrometry (LA-ICP-MS) from two species (Crassostrea gigas and Ostrea edulis). We measured a total of 49
oyster specimens from six locations in France (Atlantic Ocean and
Mediterranean Sea). Our study reports that there is no significant
difference in concentrations from shell parts corresponding to winter and
summer periods for both species. Moreover, interspecific vital effects are
reported from specimens from both species and from the same locality. REE
and Y profiles as well as t-distributed stochastic neighbour embedding processing
(t-SNE; a discriminant statistical method) indicate that REE and Y measurements from C. gigas shells can be discriminated from one locality to another,
but this is not the case for O. edulis, which presents very similar concentrations in
all studied localities. Therefore, provenance studies using bivalve shells
based on REEs and Y have to first be tested for the species. Other methods
have to be investigated to be able to find the provenance of some species,
such as O. edulis.
Introduction
Rare earth elements (REEs) are a group of 15 elements (La to Lu) with a similar
electronic configuration of atoms, similar properties, and similar chemical
behaviour (Elderfield, 1988), with the exceptions of Ce and Eu, which present
multiple oxidation states. The main sources of REEs in seawater are
atmospheric fallout (Elderfield and Greaves, 1982; De Baar et al., 1983)
and riverine input through continental weathering (Goldstein et al., 1984;
Frost et al., 1986), as well as hydrothermal activity (Olivarez and Owen,
1991). In addition to these various sources, the concentrations of REEs in
seawater are impacted by adsorption processes of REEs to mineral surfaces and
complexation with organic ligands, especially near the ocean surface
(Sholkovitz et al., 1994; Schijf et al., 2015).
Reconstruction of the REE compositions of seawater is generally used to provide
information on past continental weathering, tectonic activity, and water
mass circulation (Greaves et al., 1991; Censi et al., 2004; Haley et al.,
2005; Piper and Bau, 2013). Moreover, specific elemental ratios, such as
Y / Ho, have been investigated as potential provenance proxies. Indeed,
although the average Y / Ho value is equivalent to that of chondritic
meteorites and mid-ocean-ridge basalt (MORB; Jochum et al., 1986; Taylor
and McLennan, 1988), it has been shown that Y / Ho fractionates in sediment
particles, not only in seawater with depth, but also probably in waterbodies
from watersheds (rivers and estuaries), whose composition has been modified
depending on the weathered continental rocks (Bau et al., 1995; Nozaki et
al., 1997; Prajith et al., 2015). The Y / Ho ratios in estuaries could
therefore exhibit different values according to the regional inputs related
to the mineralogical variability in continental covers.
It has been demonstrated that the seawater composition in REEs and yttrium is
at least partially recorded in carbonate materials, such as ooids (Li et
al., 2019), brachiopod shells (Zaky et al., 2015, 2016), foraminifera tests
(Osborne et al., 2017), and coral skeletons (Sholkovitz and Shen, 1995). In
addition, the anthropogenic REE contamination of the Rhine (Germany)
has been demonstrated by the shell composition of freshwater mussels
(Merschel and Bau, 2015). The reconstruction of the REE and Y fingerprints
in a coastal environment from mollusc shells could therefore be useful, not
only to monitor potential contaminations from anthropic activities (Le Goff
et al., 2019), but also as a provenance proxy for quality control of
cultured organisms prior to human consumption (Bennion et al., 2019;
Morrison et al., 2019). Indeed, public interest is rising regarding the
origin of food for various reasons including decreased confidence in the
quality and safety of the remote food supply (Kelly et al., 2005; Gopi et al.,
2019). The geographic origin of seashells can also be of interest in
archaeology, since mollusc shells can sometimes be unearthed very far from
the nearest shoreline (Bardot-Cambot, 2014), in order to rebuild historic
trade routes. Seafood traceability is therefore important for both modern
and archaeological contexts. However, “vital effects” (compositional shifts
between inorganic and biogenic carbonate due to metabolic activity; Urey et
al., 1951) have been reported to alter this regional fingerprint of REEs
between species (Akagi et al., 2004); therefore, a feasibility study needs
to be conducted on molluscs before any extended seafood traceability
perspective is considered.
To this end, REE and Y measurements have been performed by laser ablation
inductively coupled plasma mass spectrometry (LA-ICP-MS) on modern and
archaeological oyster shells from various French localities. The aim of this
study is to assess interspecific effects using specimens from two edible
species: the flat oyster Ostrea edulis (Linnaeus, 1758), commonly found at antique sites
but still found on modern shores, and the cupped oyster Crassostrea gigas (Thunberg, 1793),
which first appeared on the French coastline during the 20th century.
Multiple measurements were performed on each of the specimens to evaluate
the intraspecific variations, in particular regarding the potential seasonal
fluctuations of rainfall intensity, weathering, and rate of river flows. A
recent statistical method, t-SNE (t-distributed
stochastic neighbour embedding; van der Maaten and Hinton, 2008), is
introduced as an attempt to discriminate the nine oyster groups of the
study in order to highlight significant interspecific and inter-regional
differences between REE incorporations.
Material and methodsModern-day settings and specimensBaie des Veys (Normandy)
The Géfosse area, in Baie des Veys (Normandy, France), is currently used
as a commercial oyster farm location. This open-sea area is characterized by
a semidiurnal tidal range of 8 m from the English Channel and an overall
siltation due to weaker ebb than flow, inducing a poor resuspension of
sediment particles (Le Gall, 1970). The Baie des Veys is recharged with
fresh water by the Isigny Channel, formed by the Vire and Aure rivers, and
the Carentan Channel, constituted by the Douve and the Taute rivers, which
drain a large part of the Bessin plain and the Cotentin. The watershed
comprises limestone as well as basalt, acidic, and alkaline metavolcanic rock
and diorite (Baize et al., 1997). The respective flows of the Isigny and
Carentan channels are 19 and 33 m3 s-1, with these
rates having no significant impact on the salinity of the shoreline
(Sylvand, 1995).
Oyster specimens from this locality were gathered during a previous rearing
experiment conducted between 2005 and 2006 (Lartaud et al., 2010a, b;
Mouchi et al., 2013). Although these specimens have been transplanted in
several localities during their lives (for details, see Lartaud et al.,
2010a), the part of the shells analysed in the present study is restricted
to that corresponding to their Baie des Veys stay. This period is recognized
in the shells owing to in vivo chemical labelling performed during the rearing
experiment (Huyghe et al., 2019). Both Crassostrea gigas (n=5) and Ostrea edulis (n=5) specimens from
this locality having shared the same breeding location were
considered (Fig. 1, Table 1, Fig. S1 in the Supplement). Crassostrea gigas was recently renamed Magallana gigas by Salvi
and Mariottini (2016); however, as this genus change is still debated (Bayne
et al., 2017) and C. gigas is the most commonly found occurrence in the literature,
this paper refers to this species by its original genus name. As
modern specimens, these are referred to as Mod_BDV_Cgig and Mod_BDV_Oedu
groups in this paper for C. gigas and O. edulis, respectively.
Map of the localities of modern (squares) and archaeological
(stars) specimens. The coordinates of the modern sites are indicated in Table 1.
Marennes–Oléron bay (Charente-Maritime)
The Marennes–Oléron bay is located on the Atlantic coast of
France. It is bordered by the Oléron island on the western side and
opens to the Atlantic on its northern and southern borders. Its surface area
is approximately 180 km2. Atlantic seawater runs through the
bay from north to south (Dechambenoy et al., 1977). In the area, the tidal
range is 5 m with a semidiurnal rhythm. The large watershed covers 10 000 km2 of land and comprises Cenozoic river deposits,
limestones, and clays (Bourgueil et al., 1968, 1972; Platel et al., 1977,
1978; Bambier et al., 1982; Hanztpergue et al., 1984; Mourier et al., 1989).
The bay is recharged with fresh water by two rivers, the Charente (north side),
with a 36 m3 s-1 flow, and the Seudre (south side) whose flow is
30 times less significant (Soletchnik et al., 1998).
The bay hosts 30 km2 of aquaculture domains, including
oysters. This site was also used during a rearing experiment (Lartaud et
al., 2010a, b): both the C. gigas (n=3) and O. edulis (n=3) shell parts analysed in the
present study refer to the shell portions corresponding to their stay at
this site, highlighted by in vivo labels. These two groups are referred to as
Mod_MO_Cgig and Mod_MO_Oedu for C. gigas and O. edulis specimens, respectively.
Specimen groups and information on their respective localities.
Temperature and salinity ranges at Marennes–Oléron, Tès, and Baie des
Veys are from Lartaud et al. (2010b), and those at Leucate are from Andrisoa (2019).
GroupSpeciesLocality of originCoordinatesAgeAnnualAnnualNumberNumbertemperaturesalinityofofrangerangespe-measure-(PSU)cimensmentsMod_BDV_CgigC. gigasGéfosse, Baie des Veys (Normandy)49∘23.11 N, 1∘06.05 WModern5–20 ∘C30–34530Mod_BDV_OeduO. edulisGéfosse, Baie des Veys (Normandy)49∘23.11 N, 1∘06.05 WModern5–20 ∘C30–34541Mod_MO_CgigC. gigasMarennes–Oléron, Charente-Maritime (Atlantic Ocean)45∘52.23 N, 1∘10.60 WModern5–26 ∘C24–38324Mod_MO_OeduO. edulisMarennes–Oléron, Charente-Maritime (Atlantic Ocean)45∘52.23 N, 1∘10.60 WModern5–26 ∘C24–38313Mod_TES_CgigC. gigasTès, Arcachon (Atlantic Ocean)44∘40.01 N, 1∘08.18 WModern5–26 ∘C25–35858Mod_LEU_CgigC. gigasLeucate, Aude (Mediterranean pond)42∘52.48 N, 3∘01.50 WModern2–32 ∘C26–42514Anc_CYB1_OeduO. edulisUnknownUnknown20–30 CEUnknownUnknown644Anc_CYB2_OeduO. edulisUnknownUnknown20–30 CEUnknownUnknown730Anc_MAL_OeduO. edulisUnknownUnknown6th c. CEUnknownUnknown643Tès (Arcachon basin)
The Arcachon basin is a lagoon of 156 km2 on the French Atlantic
coastline. The area is subdivided into a subtidal zone and an intertidal
zone with a semidiurnal tidal range of 3 m, where the studied oysters grew.
Fresh water is provided from a watershed of 4138 km2 by three main
channels, the Eyre, the Porge, and the Landes, as well as 26 other
streams and local groundwater, for a total supply of 1×34×106 m3
of fresh water per year (Lamour and Balades, 1979; Auby et al., 1994). The
largest part of this watershed consists of Cenozoic river deposits with, to
a lesser extent, limestone, clay (Dubreuilh and Bouchet, 1992), and some
iron oxide deposits historically used as building material (Gourdon-Platel
and Maurin, 2004).
Crassostrea gigas specimens (n=8; Fig. 1, Table 1) from this locality originate from the
same rearing experiment as those that were placed at Baie des Veys, and
measurements were restricted to the parts of the shells corresponding to the
period spent at this locality (Lartaud et al., 2010a). These specimens are
referred to as Mod_TES_Cgig.
Leucate (Aude)
The Salses–Leucate lagoon is located on the southwestern French
Mediterranean coast. It corresponds to a shallow coastal basin 14 km long
and 5 km wide, separated from the Mediterranean Sea by a sandy barrier
interrupted by three narrow marine inlets. The average water depth is 1.7 m, and the hydrology is a balance between the entrance of marine waters from the
Mediterranean Sea, a supply of groundwater discharge from two main karstic
springs with flows of 3×105 and 2×105 m3 d-1, respectively (Fleury et al., 2007), and rainfall of approximately
500 mm yr-1 restricted to the fall and spring periods. The superficial
watershed covers 162 km2, but the total area including the karstic
waters is not yet known accurately, but it is likely extended to 60 km inland far from
the shore (Salvayre, 1989; Ladagnous and Le Bec, 1997), with karstic waters
penetrating Jurassic and Cretaceaous limestone and dolomite. While the tidal
range is restricted, the seawater level changes in the lagoon are controlled by
strong northwesterly winds regularly exceeding 10 m s-1 (Rodellas et
al., 2018).
Crassostrea gigas oysters (n=5; Fig. 1, Table 1) originate from a wild brood stock in the
vicinity of the local oyster farming area. We were not able to collect
reliable O. edulis specimens from the Mediterranean Sea shoreline for comparison, as
only aquaculture specimens of C. gigas are now available here. Specimens from this
group are referred to as Mod_LEU_Cgig.
Archaeological sites and specimensLyon, Auvergne–Rhône–Alpes
In the area of the Fourvière hill in Lyon, where the remains of a
building were tentatively identified as a sanctuary of the goddess Cybèle, a
pit was filled with food waste, which included around 200 valves of the flat
oyster O. edulis (Bardot-Cambot, 2013). Absolute dating of this pit is currently
being re-evaluated and is approximated to the beginning of the current era
or during the 1st century CE. The provenance of these oysters is
debated (Bardot-Cambot, 2013). Two groups of animals, one originating from
the Mediterranean Sea coastline and the other from the Atlantic
coastline, were identified based on morphometric measurements and associated
mollusc shells (Bardot-Cambot, 2013). Six O. edulis specimens were selected from the
first group (later referred to as the Anc_CYB1_Oedu group) and seven more from the second group (Anc_CYB2_Oedu group) for the preservation quality of their umbo
(Fig. 1, Table 1).
La Malène, Occitanie
This medieval site (circa the 6th century CE) is located on top of a
cliff and is comprised of the remains of a fortified construction (Schneider
and Clément, 2012). This castrum corresponds to one of the last antique sites
where oysters were consumed by the elite, with supposedly
spatially restricted commercial travel (Bardot-Cambot and Forest, 2014).
Still, the shells found in a dump, along with other evidence of the high
social status of the occupants (such as golden currency and silver nails;
Schneider and Clément, 2012), had been transported over 120 km from
the Mediterranean Sea. This origin is certified because some valves are
fixed on valves of Flexopecten glaber, which is endemic to the Mediterranean Sea. Six O. edulis
specimens were selected for the preservation quality of their umbo (Fig. 1, Table 1). As ancient specimens, those are referred to as
Anc_MAL_Oedu.
Sample preparation
All specimens were mechanically cleaned of any epibiont and were selected
according to the preservation state of their umbo region. The umbo was cut
from the rest of the shell and embedded in Huntsman Araldite 2020 epoxy
resin. Longitudinal thick sections (approx. 750 µm thick) were
manufactured to expose the preserved internal structures (Fig. 2) in
order to perform geochemical analyses on this protected region away from
shell surface organic or chemical contaminants. An extensive chemical
cleaning of the section surfaces, as advised by Zaky et al. (2015), was not
performed as the analytical surface was preserved from any external
contaminants over the history of the shell. However, the influence of
organic matter occluded in the crystal lattice cannot be discarded, as in
any LA-ICP-MS work on biominerals.
Typical archaeological Ostrea edulis(a) and modern Crassostrea gigas(b) specimens. The umbo
region (c) is cut following the dashed white line; laser ablation craters
(200 µm in diameter) are indicated by circles. Multiple
measurements have been performed on each shell for both winter and summer
parts. Red and blue circles represent measurements corresponding to summer
and winter periods, respectively, based on cathodoluminescence.
All sections were observed under cathodoluminescence using a cathodyne OPEA
cold cathode at ISTeP, Sorbonne Université (Paris, France). Observation
settings were 15–20 kV and 200–400 µA mm-2 at a pressure of
0.05 Torr. Areas potentially affected by diagenesis or damaged were
identified in order to avoid any analysis of these regions by LA-ICP-MS. In
addition, cathodoluminescence (CL) observations were used to define the seasonal
calibration of the umbo, according to Langlet et al. (2006) and Lartaud et
al. (2010a). Only Leucate specimens did not have seasonal calibration as the
CL signal was uniform and nearly absent for these specimens. A second
seasonal calibration method from Kirby et al. (1998), based on a
sclerochronological record on the ligamental area in the form of external
convex and concave bands, was attempted. Unfortunately, umbos from Leucate
specimens did not exhibit the necessary curved surface to conduct such a
study. Consequently, measurement data from Leucate specimens were removed
from the dataset used for the study of seasonal contrasts in the REE and Y fingerprints.
Geochemical analyses
Chemical analyses were carried out by LA-ICP-MS at ISTE (University of
Lausanne, Switzerland). Measurements were performed using an Element XR
(Thermo Scientific) ICP-MS coupled with a RESOlution 193 nm ArF excimer
ablation system equipped with an S155 two-volume ablation cell (Australian
Scientific Instruments). A pulse repetition rate of 20 Hz and an on-sample
energy density of 4 J cm-2 were used. Pre-ablation of spots was first
conducted in order to clean the surface of potential contaminants that could
possibly be introduced during the sanding and polishing of the samples. The
analytical spots were 200 µm in diameter. Ablation was performed on
the areas of each sample section corresponding to winter and summer periods
(according to the cathodoluminescence seasonal calibration). This protocol
allows the REE and Y incorporation to be compared for different seasons
throughout the life of the oysters (Fig. 2c), with the exception of
Leucate specimens, which did not exhibit seasonal cathodoluminescence
signals. Sections from Leucate specimens were analysed at random positions
over the umbo region instead. Multiple measurements were performed on each
section to avoid bias from potential internal variability. Repeated
measurements of NIST SRM 612, prior to and after each 15-sample
analytical series, were used for external standardization. Accuracy was
checked against measurements of the BCR-2 basalt reference material from the
USGS according to the GeoReM preferred values (Jochum et al., 2005).
The relative standard deviation from 22 measurements of BCR-2 was always better
than 2.8 % for all REEs and Y. Measured and expected values are indicated
in Table S1. Measured elements were La, Ce, Pr, Nd, Sm, Eu, Gd, Tb, Dy,
Ho, Er, Tm, Yb, Lu, Hf, Y, and Ca as the internal standard. Data reduction
was performed using the LAMTRACE software (Jackson, 2008). A total of 297
measurements were made.
Data processing
Data processing was conducted using the MATLAB software (MathWorks;
https://www.mathworks.com, last access: 17 April 2020; v. R2017a). None of the measured elements exhibit a
normal distribution (Kolmogorov–Smirnov test): the distribution is
right-skewed at larger element abundances. To facilitate further
statistical treatment of such data, they need to be transformed to
normality, for which several mathematical transforms can be used. Here, we
use the cubic root transform (Chen and Deo, 2004). Seasonal differences
(from the seasonal age models from cathodoluminescence) were estimated by
hierarchical cluster analyses of 30 measurements from C. gigas specimens (n=5) and
41 measurements from O. edulis specimens (n=5) from Baie des Veys, as well as 24
measurements from C. gigas specimens (n=3) and 13 measurements from O. edulis specimens
(n=3) from Marennes–Oléron (Fig. S2). For both species, two methods
for calculating cluster distances were tested: (i) unweighted average
distance and (ii) the Ward inner squared distance. A cophenetic correlation
coefficient was calculated, as it is the linear correlation coefficient
between the distances obtained from the cluster tree and the original
distances (in the multivariate space). This coefficient is an indicator of
the accuracy of the distances (estimated on the tree) to faithfully
represent the dissimilarities among the observations. Multivariate analysis
of variance (MANOVA) was used to compare the REE and Y fingerprints obtained
from measurements of C. gigas and O. edulis from Baie des Veys against the null hypothesis
that both datasets belong to the same population. Kruskal–Wallis tests were
performed to compare the Y / Ho ratios of multiple groups against the null
hypothesis that all groups belong to the same population. A recent
statistical method, t-SNE (t-distributed stochastic neighbour embedding;
van der Maaten and Hinton, 2008), was used to compare and classify the
multivariate dataset (exact Euclidean method). The idea of the t-SNE method
is to embed high-dimensional data points in low dimensions in a way that
respects similarities between points. Nearby data points in the
high-dimensional space correspond to nearby embedded low-dimensional points,
and distant points in high-dimensional space correspond to distant embedded
low-dimensional points (MathWorks; http://www.mathworks.com, last access: 17 April 2020; v. R2017a).
ResultsComparisons of the interspecific and intraspecific seasonal record
Firstly, heavy REEs (Tm, Yb, Lu) and Hf were usually not detected (below
0.1 ng g-1) in all the specimen groups and were therefore removed from the
dataset. Secondly, measurements from the Baie des Veys and
Marennes–Oléron specimens allow for interspecific and intraspecific
comparisons, as they were performed on specimens from both C. gigas and O. edulis species.
Data collected from the different seasons for each species did not show any
significant difference in the incorporation of REEs and Y between winter and
summer. For Mod_BDV_Oedu, records from both
winter (n=25) and summer (n=16) in O. edulis shell samples are mixed together
without clustering samples with respect to seasons (Fig. S2); in
addition, the cophenetic correlation coefficients are 0.92 and 0.76 for the
average and Ward methods, respectively, which emphasizes the quality of the
classification. Results are similar for Mod_BDV_Cgig shells (n=19 and n=11 for winter and summer,
respectively; Fig. S2), with cophenetic correlation coefficients
of 0.76 and 0.69 for the average and Ward methods, respectively. Equivalent
results are found for Mod_MO_Cgig (cophenetic
correlation coefficients of 0.75 and 0.74 for the average and Ward methods,
respectively) and Mod_MO_Oedu (cophenetic
correlation coefficients of 0.94 and 0.87 for the average and Ward methods,
respectively; Fig. S2). However, a comparison between C. gigas and O. edulis
(interspecific comparison) clearly exhibits significant differences for
both the winter (MANOVA; p value =1×10-8) and summer (MANOVA; p value =2×10-5) periods between the two species. Therefore, C. gigas and O. edulis seem to
differently record their respective seasonal signals.
The Y / Ho ratio as a provenance proxy
The Y / Ho ratio is commonly used as a provenance proxy (Bau et al., 1995;
Prajith et al., 2015). The Y / Ho ratios in the present study (Fig. 3) do
not display significant differences between the four localities for modern
C. gigas specimens (Kruskal–Wallis; p values =0.70 between groups
Mod_TES_Cgig and Mod_LEU_Cgig, 0.95 between groups Mod_TES_Cgig and Mod_BDV_Cgig, 0.98
between groups Mod_TES_Cgig and
Mod_MO_Cgig, 1.00 between groups
Mod_LEU_Cgig and Mod_BDV_Cgig, 0.31 between groups Mod_LEU_Cgig and Mod_MO_Cgig, and
0.57 between groups Mod_BDV_Cgig and
Mod_MO_Cgig). Also, all O. edulis modern and
archaeological specimens from the other localities, except
Anc_CYB2_Oedu, are similar to each other
(Kruskal–Wallis; p values =0.98 between groups Anc_CYB1_Oedu and Anc_MAL_Oedu,
0.99 between groups Anc_CYB1_Oedu and
Mod_BDV_Oedu, 1.00 between groups
Anc_CYB1_Oedu and Mod_MO_Oedu, 1.00 between groups Anc_MAL_Oedu and Mod_BDV_Oedu, 0.97
between groups Anc_MAL_Oedu and
Mod_MO_Oedu, and 0.97 between groups
Mod_BDV_Oedu and Mod_MO_Oedu) but are different from C. gigas shells (Table S2).
Moreover, a significant difference between modern C. gigas and O. edulis shells from the same
localities (Baie des Veys and Marennes–Oléron) is also reported (Table S2). However, the Anc_CYB2_Oedu group
does not share the homogeneity of other modern and ancient O. edulis populations. On
the contrary, the ratios measured in O. edulis specimens from this group are not
significantly different from the ones obtained in modern C. gigas specimens
(Kruskal–Wallis; p values =0.97, 0.26, 0.48, and 1.00 when compared with
specimens from Mod_TES_Cgig,
Mod_LEU_Cgig, Mod_BDV_Cgig, and Mod_MO_Cgig,
respectively).
Box plots of Y / Ho ratios for all groups. The letters on top of the
boxes (a and b) identify the significant differences between groups from
Kruskal–Wallis tests. Note that for the same locality at Baie des Veys (BDV)
and Marennes–Oléron (MO), the Y / Ho ratios are significantly different
depending on the species considered (C. gigas and O. edulis groups). Grey bars represent
median values; the lower and higher large black bars represent the 25th
and 75th percentiles, respectively, and the lower and higher small
black bars represent the minimum and maximum values not considered
outliers, respectively. Outliers are represented by grey crosses.
REE incorporation in shells
For all the specimens, a gradual decrease in REE dispersion (i.e. amplitude of
values relative to Y) is generally observed with increasing atomic
number (Fig. 4). Indeed, several groups can be identified with light REEs
(e.g. Pr and Sm), such as the C. gigas groups. In contrast, middle REE (e.g. Dy and
Er) distributions appear similar for all groups, with the exception of the
Mod_LEU_Cgig group, whose measurements are
isolated from those of the other groups. The REE median profiles (normalized
to Post-Archean Australian Shale; McLennan, 1989) also present similar
trends of middle REEs (from Gd to Er) for most groups (Fig. 5), except for
the Mod_LEU_Cgig group, which exhibits lower
abundances than the other groups for all REEs. However, light REEs are
generally substantially depleted in C. gigas specimens compared to modern and
ancient O. edulis groups (approx. 1 order of magnitude difference). The only
exceptions are La and Ce in C. gigas shells from Baie des Veys (Mod_BDV_Cgig), which present values in the range of those from
modern and ancient O. edulis specimens. This pattern of enriched Ce (and to a lesser
extent, La) is not shared by O. edulis specimens from this same locality
(Mod_BDV_Oedu). Although these two elements
have similar abundances for both species in this locality, all the other REE
abundances are different.
Gradual decrease in REE abundances in oyster shells according to
the REE atomic number, presented against Y. Values are expressed in the cubic
root of abundances (µg g-1) to approach normality.
Measurements from C. gigas and O. edulis are indicated by crosses and filled circles,
respectively.
REE median profiles for all groups of oyster specimens.
Crassostrea gigas groups are symbolized by dashed lines, and continuous lines are for O. edulis groups.
Seawater profiles of the Atlantic Ocean (van der Flierdt et al., 2012) and
the Mediterranean Sea (Censi et al., 2004) are indicated for comparison.
Values are normalized to Post-Archean Australian Shale (PAAS) according to
McLennan (1989).
Results from the entire dataset (i.e. 297 measurements and 12 elements per
measurement) are compared in Fig. 6 using t-SNE. Some groups are well
identified by this method, such as the Mod_LEU_Cgig and Mod_BDV_Cgig groups (Mediterranean
Sea and British Channel coastlines). Both Mod_MO_Cgig and Mod_TES_Cgig
groups, originating from the Atlantic Ocean coastline, appear as one unique
group by t-SNE, with a restricted dispersion. The modern and ancient O. edulis groups
are, however, not discriminated by t-SNE and present a substantially larger
dispersion than the Atlantic Ocean C. gigas groups. In this sample set,
the Anc_CYB1_Oedu, Mod_MO_Oedu, and Mod_BDV_Oedu groups
are relatively similar in terms of the range of distribution, and
Anc_CYB2_Oedu and Anc_MAL_Oedu specimens share similarities, but the five groups
remain poorly differentiated.
Visualization of shell group partitioning using t-SNE applied to
all REE and Y measurements as variables. Crosses and large dots refer to C. gigas
and O. edulis, respectively.
Discussion
In both studied species, the decrease in the range of variation of REE
abundances with increasing atomic number (except for Tm, Yb, Lu, and Hf,
which were not quantified in the shells) can be explained by the increased
affinity of heavy REEs for complexation in seawater, as has been
demonstrated in previous studies (Cantrell and Byrne, 1987; Byrne and Kim,
1990; De Baar et al., 1991). As these elements are trapped in complexed
forms or ligands, their bioavailability in seawater is strongly reduced,
limiting their insertion in the oyster ionic pumps leading to the
mineralization locus. These bioavailability restrictions of REEs have already
been demonstrated in the freshwater mussel Corbicula fluminea for Gd (Merschel and Bau, 2015)
and heavy REEs in Mytilus edulis (Ponnurangam et al., 2016). Another explanation can be
advanced regarding the technique used. An LA-ICP-MS device analyses both the
mineral and organic phases ablated from the biomineral without the
possibility to assess their relative proportions. Although the mean
proportion of organic compounds in oyster shells is limited (<0.5 % for C. gigas; Mouchi et al., 2016), it is known that organic REE abundances
are depleted in heavy REEs (Freslon et al., 2014). The decreasing abundance
with increasing atomic number may then be caused by protein and
polysaccharide contents. Only extensive cleaning for solution-based ICP-MS
analyses would be able to entirely remove the organic molecules before
measurements, but this would not fit the fast REE assessment of a large
number of specimens we aimed to conduct in this study.
In this study, the Y / Ho ratios, which are usually proposed as a provenance
proxy (Bau et al., 1995; Prajith et al., 2015), are affected by strong vital
effects for both oyster species, potentially due to the decrease in REE
abundance with increasing atomic number. In addition, significant
differences between species from the same locality are also reported. Hence,
the Y / Ho ratio generally does not depend on the original location (Fig. 3). Consequently, Y / Ho should not be used directly as a provenance proxy (at
least from LA-ICP-MS data collected on biogenic carbonates), or it should be used with extreme
caution after having discarded any potential vital effect. As the decreased
REE abundance with increasing atomic number discussed above prevents a
locality-specific variation of Ho, other Y / REE ratios have been tested as
alternative provenance proxies using lighter REEs (Fig. 4). Y / La, Y / Ce,
Y / Pr, and Y / Nd were all unsuccessful in providing the identification of locality
groups and also present similar values for all modern and ancient O. edulis. For Y / La
and Y / Ce ratios, C. gigas specimens from Baie des Veys were identical to all modern
and ancient O. edulis specimens, while for Y / Pr and Y / Nd ratios, C. gigas specimens from Baie
des Veys were identical to all C. gigas specimens from the other localities.
Overall, Y / REE ratios appear unsuccessful for provenance discrimination.
Measurements performed on Baie des Veys and Marennes–Oléron specimens
(Mod_BDV_Cgig and Mod_BDV_Oedu, as well as Mod_MO_Cgig and Mod_MO_Oedu) have been used to study
the incorporation of REEs inside a single species in order to evaluate its
intraspecific variation. Contrary to the model experiments performed for different
temperatures on the mussel Mytilus edulis (Ponnurangam et al., 2016), the seasonal
conditions do not have any impact on the REE incorporation for O. edulis or
C. gigas shells (in the range of 5–20 ∘C; Table 1). Parameters other than
temperature and pH, used by Ponnurangam et al. (2016), are probably in
effect, which lowers the impact of temperature on REE incorporation. This
observation implies that any part of a shell can be sampled without
necessarily having to define a temporal calibration of the umbo. However,
REE abundances fluctuate widely within a single specimen, and the “local
fingerprint” of these elements needs to be clarified and based on multiple
measurements performed on each of several specimens. These intra-individual
fluctuations cannot be due to seasonally controlled environmental factors,
such as temperature, precipitation, or plankton blooms. However, a potential
source of REEs for oysters can be pore water or resuspended sediment
(Haley et al., 2004; Crocket et al., 2018), and therefore the relative
abundances may fluctuate without precise temporal cyclicity.
The reasons for these intraspecific and interspecific vital effects remain
unknown. Indeed, as far as we know, no study has ever shown evidence or
suspicion of the use of REEs in metabolic processes that could induce an
effective filter of these elements between seawater and the extrapallial
cavity where shell mineralization occurs. Nevertheless, it has been reported
that REEs, or other unsuspectedly useful elements, are indeed used by
organisms in specific environmental settings; an example is provided by
diatoms in Zn-depleted conditions, under which Zn is used as a co-factor of
carbonic anhydrase (Lee et al., 1995). Another example is given by
methanotrophic archaea, which use Cd, a toxic element, as a co-factor of
methanol dehydrogenase (Pol et al., 2014).
The incorporation of REEs differs between the two studied species. C. gigas shells not only
present different REE profiles between groups (unlike those of O. edulis), but
the positive Gd anomaly, a characteristic of modern coasts under pressure from
anthropic activities (Bau and Dulski, 1996; Nozaki et al., 2000; Le Goff et
al., 2019), is also observed solely for “modern” C. gigas specimens from
the Mod_BDV_Cgig, Mod_MO_Cgig, and Mod_TES_Cgig groups
(Fig. 5), which correspond to the only watersheds with major cities. The
Gd anomaly is visible neither in modern C. gigas from Mod_LEU_Cgig nor in modern O. edulis. The systematically low abundances
of REEs in the Leucate shells can also be explained by the regional geology
(Ladagnous and Le Bec, 1997), as watersheds in the other localities of C. gigas
specimens present substratum types with higher REE contents than karsts
(e.g. basalts; Baize et al., 1997). The dispersion of measurements
using t-SNE seems to be ineffective in discriminating between
the Mod_MO_Cgig and Mod_TES_Cgig groups. Both these groups are located on the
Atlantic coastline of France, and both respective watersheds comprise
the same rock types (i.e. mainly limestones and some clays and river deposits).
One could therefore expect a similar riverine water REE content. Overall,
these species-specific characteristics indicate that C. gigas can be used as a
sentinel species regarding REE pollution of coastal waters. However,
we cannot confirm that O. edulis is a proper candidate for such studies.
Several reasons for these interspecific differences can be advanced. It is
known that oysters can be selective in their diet, composed mainly of
diatoms (Yonge, 1928; Paulmier, 1971) of a specific size range, and
preferentially digest specific species of diatoms over others (Shumway et
al., 1985; Cognie et al., 2001). If food is a source of REEs, it may be
possible that each oyster species does not feed on the same prey, which can
present different abundances of these elements. Aquarium experiments have
reported different ingestion rates in the 5–15 µm algal size range
between these oyster species (Nielsen et al., 2017), but there is no
indication of the REE content of the food. Alternatively, O. edulis, which exhibits
generally higher abundances of REEs (nearly 1 order of magnitude higher for
light REEs, except for La and Ce for Mod_BDV_Cgig specimens; Fig. 5), could present a higher bioaccumulation of these
elements in its soft tissues (and eventually shell) compared to C. gigas. Ong et al. (2013) presented trace element measurements from the soft tissues of both
species from the Baie de Quiberon (Brittany, France), indicating that the soft
tissues of O. edulis contain generally less Cu and Zn but more Cd and Pb than those
of C. gigas. Such species-specific bioaccumulation and incorporation differences
could also be in effect for REEs. Finally, it is possible to explain the
higher abundance of light REEs in O. edulis shells compared to C. gigas by suggesting that O. edulis ingests more clay particles. As heavy REEs are trapped in complexed form in
seawater, mainly light REEs must be available for adsorption on clay
particles and are eventually integrated into the forming carbonate shell.
In any case, this study shows that t-SNE can be used on REE and Y measurements from C. gigas shells to identify the regions of origin of specimens from
this species. However, it appears that intraspecific vital effects prevent
its efficiency in O. edulis, whose specimens exhibit the same fingerprint for several
localities of origin. For this reason, we cannot confirm or refute a
different origin of the two populations of Cybèle archaeological
specimens (Anc_CYB1_Oedu and
Anc_CYB2_Oedu) with these elements.
Conclusions
Multiple types of vital effects and other factors regarding REE incorporation in
C. gigas and O. edulis oyster shells have been highlighted in this study. Intraspecific
variations in REE abundances are significant but not related to seasonal
fluctuations. A gradual decrease in REE incorporations with increasing
atomic numbers has been observed, and it appears that heavy REEs are less
discriminant than light REEs in identifying the various studied groups. The
Y / Ho ratio, previously reported as a proxy for provenance studies, is
ineffective in oyster shells. Finally, interspecific variations underline
the ability of the t-SNE procedure to correctly separate C. gigas specimens of various
regions of origin but not O. edulis specimens, which also implies that only C. gigas can be
used as a monitor species of light REE pollution. Reconstruction of the
provenance of oyster specimens will therefore have to be performed
separately for each studied species, as the regional geochemical fingerprints of
the shells appear to be species-dependant. In order to be able to identify
the regions of origin of species affected by strong vital effects (such as
O. edulis), it is necessary to investigate other chemical elements as potential
provenance proxies. Moreover, increased efficiency in identifying the
locality (and not only the region) of origin of C. gigas specimens could be achieved
by also measuring elements other than REEs.
Data availability
The data used in this paper have been deposited in the Zenodo data
repository (10.5281/zenodo.3529419, Mouchi et al., 2019; 10.5281/zenodo.3731254, Mouchi et al., 2020).
The supplement related to this article is available online at: https://doi.org/10.5194/bg-17-2205-2020-supplement.
Author contributions
VM conceived the study. VM, CG, and AU performed the data analysis. VF and FL
provided specimens. VM and EPV performed statistics and data processing. VM,
CG, MdR, LE, EPV, and FL interpreted the results. VM wrote the paper with
contributions from all authors.
Competing interests
The authors declare that they have no conflict of interest.
Acknowledgements
The authors would like to thank Frédéric Delbès for the work he
performed on the preparation of the thin sections.
Review statement
This paper was edited by Aninda Mazumdar and reviewed by Anne Osborne and one anonymous referee.
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