The B/Ca ratio in calcareous marine species is
informative of past seawater CO32- concentrations, but scarce data
exist on B/Ca in coralline algae. Recent studies suggest influences of
temperature and growth rates on B/Ca, the effect of which could be critical
for the reconstructions of surface ocean pH and atmospheric pCO2. In
this paper, we present the first laser ablation inductively coupled plasma mass
spectrometry (LA-ICP-MS) analyses of Mg, Sr, Li, and B in
the coralline alga Lithothamnion corallioides collected from different geographic settings and depths
across the Mediterranean Sea and in the Atlantic Ocean. We produced the
first data on putative temperature proxies (Mg/Ca, Li/Ca, Sr/Ca, Mg/Li) and
B/Ca in a coralline algal species grown in different basins from across the
photic zone (12, 40, 45, and 66 m depth). We tested the B/Ca
correlation with temperature proxies and growth rates in order to evaluate
their possible effect on B incorporation. Our results suggested a growth
rate influence on B/Ca, which was evident in the sample with the lowest growth rate of
0.10 mm yr-1 (Pontian Isl., Italy; 66 m depth) and in Elba (Italy; 45 m depth), where the algal growth rate was the highest (0.14 mm yr-1). At these
two sites, the measured B/Ca was the lowest at 462.8 ± 49.2 µmol mol-1 and the highest at 757.7 ± 75.5 µmol mol-1, respectively. A positive
correlation between B/Ca and temperature proxies was found only in the
shallowest sample from Morlaix (Atlantic coast of France; 12 m depth), where
the amplitude of temperature variation (ΔT) was the highest (8.9 ∘C). Still, fluctuations in B/Ca did not mirror yearly seasonal
temperature oscillations as for Mg/Ca, Li/Ca, and Sr/Ca. We concluded that
growth rates, triggered by the different ΔT and light availability
across depth, affect the B incorporation in L. corallioides.
Introduction
Warming and acidification are major anthropogenic perturbations of
present-day oceans (Callendar, 1938; Fairhall, 1973; Brewer, 1997; Gattuso,
1999; Caldeira, 2005; Hönisch et al., 2012; Masson-Delmotte et al.,
2021). Ocean acidification reduces the saturation state of calcite and
aragonite, lowering the dissolution threshold of biominerals and threatening
habitat-forming species of critical ecological importance such as coralline
red algae and corals (Morse et al., 2006; Hoegh-Guldberg et al., 2007;
Andersson et al., 2008, 2011; Basso, 2012; Ragazzola et al., 2012; Ries et
al., 2016). Coralline algae, which precipitate high-Mg calcite (>8 mol %–12 mol % MgCO3) (Morse et al., 2006), are particularly suitable as
proxy archives for paleoclimate reconstruction because of their worldwide
distribution and longevity. Importantly, they show indeterminate growth
with no ontogenetic trend (Halfar et al., 2008), which means the growth trend of
coralline algae does not slow down asymptotically with age, as in bivalves,
thus preserving the resolution of the geochemical signals in all stages of
growth (Adey, 1965; Frantz et al., 2005; Halfar et al., 2008). Moreover,
coralline algae thin sections under optical microscopy reveal bands that
reflect the growth pattern (Cabioch, 1966; Basso, 1995a, b; Foster, 2001),
similar to tree rings (Ragazzola et al., 2016) that can be targeted for
high-resolution geochemical analyses. Seasonal growth bands, indeed, consist
of the perithallial alternation of dark and light bands that together
constitute the annual growth patterns (Freiwald and Henrich, 1994; Basso,
1995a, b; Kamenos et al., 2009). Dark bands correspond to slow-growing cells
produced in the cold season, which are shorter, thick-walled, and with lower
Mg contents, while light bands are fast-growing cells produced in the warm
season, which are longer, less calcified, and with higher Mg concentrations
(Kamenos et al., 2009; Ragazzola et al., 2016). The high-Mg calcite of
calcareous red algae records ambient seawater temperature (Halfar et al.,
2000; Kamenos et al., 2008; Nash et al., 2016; Hetzinger er al., 2018),
primary productivity (Chan et al., 2017; Hou et al., 2019), and salinity
(Kamenos, 2012), proving to be a suitable paleoclimate archive. Most of the
data were collected from high-latitude (Kamenos et al., 2008; Anagnostou et
al., 2019) and tropical species (Caragnano et al., 2014; Darrenougue et al.,
2014), whereas less attention has been given to coralline algae from
mid-latitudes.
Trace element variations in marine calcareous species inform the
reconstruction of changes in the environmental parameters which
characterized the seawater during their growth (Hetzinger et al., 2011;
Montagna and Douville, 2017). Boron is incorporated into the mineral lattice
of calcareous marine species during calcite precipitation. In the ocean, B
occurs in two molecular species: boric acid B(OH)3 and borate ion
B(OH)4- (Dickson, 1990), which are related by the following
acid–base equilibrium reaction:
B(OH)3+H2O↔B(OH)4-+H+,
which shows the dependence of the two species concentrations on pH. The first
analyses of the isotopic signal of marine carbonates evidenced a strong
similarity with the isotopic composition of B(OH)4- in solution,
suggesting that borate would preferentially be incorporated into marine
carbonates (Vengosh et al., 1991; Hemming and Hanson, 1992; Zeebe and Wolf-Gladrow, 2001; DeCarlo et al., 2018). The B content and its isotopic
signature (δ11B) in calcareous marine species record
information about the seawater carbonate system. The δ11B is
used to reconstruct past seawater pH (Hönisch and Hemming, 2005; Foster,
2008; Douville et al., 2010; Paris et al., 2010; Rae et al., 2011). The
boron-to-calcium ratio (B/Ca) proved to be informative about past seawater
CO32- concentrations in different empirical studies on benthic
foraminifera (Yu and Elderfield, 2007; Yu et al., 2007; Rae et al., 2011)
and in synthetic aragonite (Holcomb et al., 2016). Most of the literature on
boron studies is focused on its isotopic composition (Hemming and
Hönisch, 2007; Klochko et al., 2009; Henehan et al., 2013; Fietzke et
al., 2015; Cornwall et al., 2017; Ragazzola et al., 2020), whereas less
attention has been given to B/Ca records, especially in coralline algae.
Recent studies suggest that B/Ca is a function of seawater pH, as well as of
other environmental variables such as temperature, the effect of which should be
considered in the attempt to reconstruct surface ocean pH and atmospheric
pCO2 (Wara et al., 2003; Allen et al., 2012; Kaczmarek et al., 2016).
To achieve the best reliability of geochemical proxies for climate
reconstructions, it is important to recognize the influence of multiple
factors on a single proxy (Kaczmarek et al., 2016; Donald et al., 2017). For
instance, more recently the effects of temperature and growth rate on B
incorporation have been investigated through experiments on both synthetic
and biogenic carbonates (Wara et al., 2003; Yu et al., 2007; Gabitov et al.,
2014; Mavromatis et al., 2015; Uchikawa et al., 2015; Kaczmarek et al.,
2016; Donald et al., 2017). In particular, a culture experiment on the
coralline alga Neogoniolithon sp. showed a positive correlation of B/Ca with growth rate
and a negative correlation with Sr/Ca, which was proposed as a proxy for dissolved inorganic carbon (DIC)
(Donald et al., 2017). Moreover, a culture experiment on the high-latitude
species Clathromorphum compactum (Kjellman) Foslie 1898 revealed non-significant temperature
influences on B/Ca and a significant inverse relationship with growth rate
(Anagnostou et al., 2019). The factors which influence the B incorporation
in calcareous red algae are therefore still debated. Recent experiments also
suggest that coralline algae can control the calcifying fluid pH (pHcf)
(Cornwall et al., 2017), as already observed in corals (Comeau et al.,
2017). Both organisms have a species-specific capability to elevate pH at
calcification sites in response to variations of ambient pH, also
influencing precipitation rates (Cornwall et al., 2017). Differences between
carbonate polymorphs were also highlighted (McCulloch et al., 2012; Cornwall
et al., 2018), showing more elevated pHcf in aragonitic corals than
calcites, pointing to the relevance of the mineralogical control on
biological up-regulation. So far, no investigations on pHcf
modifications in natural systems have been performed on calcareous red
algae.
No studies have been conducted so far on the correlation between temperature
proxies (Mg, Sr, Li/Ca) and B/Ca. The Mg/Ca ratio is extensively used as a
temperature proxy in coralline algae (Halfar et al., 2008; Kamenos et al.,
2008; Fietzke et al., 2015; Ragazzola et al., 2020), since the substitution
of Mg2+ with Ca2+ ions in the calcite lattice is an endothermic
reaction. Accordingly, Mg incorporation increases with temperature (Moberly,
1968; Berner, 1975; Ries, 2006; Caragnano et al., 2014, 2017). Sr/Ca and
Li/Ca ratios in calcareous red algae have also been investigated as climate
proxies, showing significant positive correlations with temperature in
different species (Kamenos et al., 2008; Hetzinger et al., 2011;
Caragnano et al., 2014; Darrenougue et al., 2014). The Mg/Li ratio showed a
strong correlation with seawater temperature in cultured C. compactum (Anagnostou et
al., 2019) and in empirical studies on high-Mg calcites, including
coralline algae (Stewart et al., 2020). Conversely, the Mg/Li calibration did
not reveal improvements in the Mg/Ca or Li/Ca proxies in Lithophyllum spp. (Caragnano et
al., 2014, 2017).
Here, we present laser ablation inductively coupled plasma mass
spectrometry (LA-ICP-MS) conducted on a wild-grown coralline alga with a
wide geographic scope. This technique, which allows high-resolution analysis
of a broad range of trace elements in solid-state samples, has been widely
used in biogenic carbonates to extract records of seawater temperature,
salinity, and water chemistry (Schöne et al., 2005; Corrège, 2006;
Hetzinger et al., 2009, 2011; Fietzke et al., 2015; Ragazzola et al., 2020).
Measurements were made on the non-geniculate coralline alga Lithothamnion corallioides (P. Crouan and H. Crouan) P. Crouan and H. Crouan 1867, which is widely distributed in the
Mediterranean Sea and in the north-eastern Atlantic Ocean from Scotland to the
Canary Islands (Irvine and Chamberlain, 1999; Wilson et al., 2004; Carro et
al., 2014), usually constituting maerl beds (Potin et al., 1990; Foster,
2001; Martin et al., 2006; Savini et al., 2012; Basso et al., 2017). It
forms rhodoliths as unattached branches (Basso et al., 2016) with obvious
banding in longitudinal sections (Basso, 1995b). These characteristics
combine to make this species a suitable model for the measurement of
geochemical proxies by comparing different environmental settings.
In this paper, we provide the first LA-ICP-MS data on putative temperature
proxies (Mg/Ca, Sr/Ca, Li/Ca, Mg/Li) and B/Ca measured on L. corallioides collected from
different geographic settings and depths across the Mediterranean Sea and in
the Atlantic Ocean. We test the influence of temperature and growth rate on
the B/Ca ratio, which could be crucial in assessing the reliability of B/Ca
as a proxy for the seawater carbonate system.
Materials and methodsSampling sites and collection of Lithothamnion corallioides
Samples of the coralline alga L. corallioides were collected in the western Mediterranean
Sea and in the Atlantic Ocean (Fig. 1). In the Mediterranean Sea, the
samples collected in the Pontian Islands (Italy) at 66 m depth were gathered by
grab during the cruises of the R/V Minerva Uno in the framework of the
Marine Strategy Campaigns 2016 (Table 1). The last two Mediterranean samples
were collected by one of the authors (DB) by scuba diving during local
surveys at 45 m off the coasts of Pomonte (Elba Island, Italy) (Basso and
Brusoni, 2004) and at 40 m depth in the Aegadian Islands (Marettimo, Italy).
The Atlantic sample was collected by grab at 12 m depth in Morlaix Bay
(Brittany, France) (Table 1).
Map showing the distribution of sampling sites where
Lithothamnion corallioides samples were collected: Morlaix Bay (48∘34′42′′ N, 3∘49′36′′ W), Aegadian Islands (37∘97′36′′ N, 12∘14′12′′ E), Elba (42∘44′56.4′′ N, 10∘07′08.4′′ E), and
Pontian Islands (40∘54′ N, 12∘45′ E). Service layer
credits: source Esri, GEBCO, NOAA, National Geographic, Garmin, https://www.geonames.org/ (last access: 21 December 2021),
and other contributors.
(a) Thalli of Lithothamnion corallioides collected in Morlaix (scale bar: 5 mm). (b)
Longitudinal section through the L. corallioides branch sampled in Morlaix showing the
LA-ICP-MS transects targeting each growth band (scale bar: 200 µm).
The identification of the algal samples was achieved by morphological
analyses of epithallial and perithallial cells using a field emission gun
scanning electron microscope (SEM-FEG) Gemini 500 Zeiss. Samples were
prepared for SEM according to Basso (1995a). Morphological identification
was based on Adey and McKibbin (1970) and Irvine and Chamberlain (1994).
Other information about maerl species distribution in Morlaix was provided
by Carro et al. (2014) and Melbourne et al. (2017). L. corallioides was selected as the
target species because of its presence in both Mediterranean and Atlantic
waters. The Atlantic sample (Morlaix) was used as voucher specimen for the
subsequent identification of the Mediterranean samples, since
Phymatolithon spp. and L. corallioides are the only components of the Morlaix maerl (Carro et al., 2014;
Melbourne et al., 2017). Hence, once its inclusion under the genus
Phymatolithon was excluded, the Morlaix sample identified as L. corallioides was used as a reference for
the most reliable identification of the other Mediterranean samples.
Sample preparation
The selected algal branches were embedded in Epo-Fix resin, which was
stirred for 2 min with a hardener (13 % w/w); they were then left to
dry at room temperature for 24 h. Afterwards, the treated branches were
cut by an IsoMet diamond wafering blade 15HC along the direction of growth.
In the laboratory of the Institute of Geosciences and Earth Resources
of the National Research Council (IGG-CNR) in Pavia (Italy), the sections were
polished with a MetaServ grinder–polisher (400 RPM) using a diamond paste
solution, finally cleaned ultrasonically in distilled water for 10 min,
and dried at 30 ∘C for 24 h.
Trace elements analyses and environmental data
LA-ICP-MS analyses were carried out at the IGG-CNR laboratory on one algal branch per sampling site. 43Ca, 7Li,
25Mg, 88Sr, and 11B contents were measured using an Agilent
ICP-QQQ 8900 quadrupole ICP-MS coupled to an Excimer laser ablation system
(193 nm wavelength, MicroLas with GeoLas optics). Element / Ca ratios were
calculated for these isotopes, as was the Mg/Li ratio. Measurements were
performed with laser energy densities of 4 J cm-2 and helium as a carrier
gas.
Correlation plots of Mg/Ca with Li/Ca and Sr/Ca. For each analysis
the Spearman's coefficient r, the p value, and the line equation are given.
The laser transects crossed the algal growth direction with a spot size of
50 µm, attempting to target each growth band change which marked the
transition between the cells usually produced in the warm season and those
usually produced in the cold season, hereinafter referred to as long and
short cells (Figs. 2, S1, S2, S3). NIST 612 was used as an external standard
(e.g. Fietzke et al., 2010; Jochum et al., 2012), whereas Ca was adopted as
an internal standard. Accuracy and precision were better than 4 % for NIST
612 and 8 % for Ca standard. Minimum detection limits (99 % confidence)
of measured elements were Ca = 16.91, Li = 0.07, Mg = 0.11, Sr = 0.004, and B = 2.64 ppm. Each analysis was carried out in
MS/MS mode for 3 min by acquiring 60 s of background before and
after the sampling period by the laser on the polished surface. The first
part of the signal was not used for the integration to avoid surface
contamination. The Glitter software (v. 4.4.4) was used for data reduction.
Box plot of the statistical tests performed to evaluate the
differences of Mg/Ca in L. corallioides collected at different sampling sites. The
horizontal black lines indicate the median values. The black dots
and the numbers inside the plot indicate the mean values.
Box plots of the statistical tests performed to evaluate the
differences of Mg/Ca in the long and short cells of L. corallioides collected at different
sampling sites. The horizontal black lines indicate the median values. The
black dots and the numbers inside the plot indicate the mean
values.
In the absence of in situ environmental data, the seawater temperature has
been extracted by 11 years of monthly reanalysis spanning 1979–2016 from
from the Ocean ReAnalysis System 5 (ORAS5) at 0.25∘ horizontal resolution (Zuo
et al., 2019). The time interval of extraction for each site corresponded to
11 years before sample collection (Bracchi et al., 2021). Minimum, maximum,
and mean values, as reported in Table 1, refer to the temperature at
sampling depth and have been measured over the entire time interval of
extraction.
Correlation plot between Mg/Li and seawater temperature. Data are
shown for cultured C. compactum (Anagnostou et al., 2019) and L. corallioides (this paper). L. corallioides results are
shown separately in long and short cells per sampling site.
For the purpose of this work, we considered temperature data in terms of (a) the amplitude of temperature variation (ΔT) and (b) the temperature
maxima and minima. ΔT represents the temperature fluctuations during
the algal growth and has been measured as the difference between the maximum
and minimum temperature registered at the site over 11 years. We used
ΔT when comparing the sampling sites, given their differences in
depth and geographical regions. The temperature peaks (maximum and minimum)
have rather been used when considering data corresponding to long and short
cells, since they are related to warm and cold periods of growth,
respectively. We used the temperature peaks over the entire time interval of
extraction (11 years) when comparing the mean elemental ratios of long and
short cells per sampling site. The maximum and minimum temperature within
each year have been used instead for the reconstruction of the algal age
model. In the sample from Morlaix Bay, indeed, the good visibility of the
growth bands allowed us to relate the temperature record with the algal
growth at annual resolution. We therefore plotted all the element ratios
against the average seawater temperature values of the coldest and warmest
months of the year to reconstruct the temperature variations during the
algal growth (Moberly, 1970; Corrège, 2006; Williams et al., 2014;
Ragazzola et al., 2020; Caragnano et al., 2014). Missing element ratios,
possibly due to non-targeted consecutive bands, were calculated as the means
of known values.
Mg/Li ratio of L. corallioides collected in Morlaix Bay. Note the lack of cyclic
variations in Mg/Li results. In the timeline, the coldest and the warmest
months have been reported. Mg/Li ratios in the missing bands (asterisks) have been
calculated as the means of the values measured in warm and cold periods.
Monthly means of seawater temperature have been extracted by ORAS5
reanalysis.
Carbon system parameters for each site have also been estimated. Even if
they were not available in the same time interval of temperature data, the
seasonal variations occurring in the extracted period allowed the
characterization of the sampling sites. Monthly mean seawater pH has been
derived by the EU Copernicus Marine Service Information (CMEMS) global
biogeochemical hindcast spanning 1999–2017 at 0.25∘ horizontal
resolution (Perruche, 2018). Monthly means of DIC in the time interval 1999–2017 have been
extracted by CMEMS biogeochemical reanalysis for the Mediterranean Sea at
0.042∘ horizontal resolution (Teruzzi et al., 2021). At the Atlantic
site, monthly means of DIC in 1999–2017 were derived from the CMEMS IBI
biogeochemical model at 0.083∘ horizontal resolution (Copernicus Marine Environmental Monitoring Service, 2020). The pH and DIC
data showed consistent variations among sites, despite being derived from
different biogeochemical models. The mean values of DIC and pH, as reported
in Table 1, refer to sampling depth and have been measured over the entire
time interval of extraction. The complete timeline of temperature and carbon
data used in this paper is shown in Supplement Figs. S5, S6, S7, and S8.
Correlation plots of B/Ca with Mg/Ca, Li/Ca, and Sr/Ca in L. corallioides
collected in Morlaix Bay. For each analysis the Spearman's coefficient r,
the p value, and the line equation are given.
Growth rate estimation
Growth rates were estimated under light microscope by measuring the length
of the LA-ICP-MS transect and dividing it by the number of annual growth
bands crossed by the transect (Bracchi et al., 2021). The obtained values
are expressed in linear extension per year (mm yr-1). In the samples
wherein the growth bands were not easily detectable under microscope, i.e. the
Elba sample, we also used the Mg/Ca results in order to check for the
correspondence of Mg peaks with growth bands.
Box plot of the statistical tests performed to evaluate the
differences of B/Ca in L. corallioides collected at different sampling sites. The
horizontal black lines indicate the median values. The black dots
and the numbers inside the plot indicate the mean values.
Statistical analysis
Statistics were calculated for both the dataset with all the spot analyses and
the dataset with the records from long and short cells separately. Short
cells refer to slow-growing cells in dark bands, usually produced in
the cold season; long cells correspond to fast-growing cells in light
bands, usually produced in the warm season (Kamenos et al., 2009; Ragazzola
et al., 2016). For each spot, a distinction between the cells was thus made
by image analyses, except for the Elba sample, given the poor resolution of
the growth bands. The Spearman's correlation was tested to provide the
statistical comparisons between Mg/Ca, Li/Ca, Sr/Ca, and B/Ca records from
the LA-ICP-MS analyses in L. corallioides. The Kruskal–Wallis test, followed by the Dunn's
test for comparisons, and the one-way analysis of variance (ANOVA), followed by the Tukey's test for
post hoc analysis, were used to compare the geochemical signals among
sampling sites and to evidence the differences between group medians and
means. All statistical analyses were run in R 3.6.3 software.
Box plots of the statistical tests performed to evaluate the
differences of B/Ca in the long and short cells of L. corallioides collected at different
sampling sites. The horizontal black lines indicate the median values. The
black dots and the numbers inside the plot indicate the mean
values.
ResultsEnvironmental data
The temperature data obtained by ORAS5 reanalysis revealed a lower amplitude
of the seasonal temperature change in the Mediterranean samples with respect
to the Atlantic site, as shown by the standard deviation and ΔT
values in Table 1. This difference is explained in terms of the different
sampling depths, with the seasonal variations decreasing with increasing
depth.
Temperature variations in Morlaix Bay (Atlantic Ocean) were higher,
registering an overall mean seawater temperature of 12.4 ∘C (Table 1). Among Mediterranean samples, mean seawater temperatures were highest in
the Aegadian Isl., followed by Elba and the Pontian Isl. (Table 1).
Aegadian Isl. also registered the highest temperature variations among the
Mediterranean sites (Table 1). Moderate temperature variations characterized
the site in Elba, which registered the lowest monthly mean temperature among
Mediterranean sites (Table 1). At the Pontian Isl., consistent with the
fact that it is the deepest sampling site at 66 m depth, the lowest seawater
temperature variations were found (Table 1).
The pH estimates at the Mediterranean sites were all similarly high at
∼8.13 and less variable than the Atlantic site (8.05). The
mean pH had slightly higher values in Pontian Isl. and Elba than Aegadian
Isl. (Table 1). Similarly, DIC was higher in the Mediterranean sites and
decreased in Morlaix, as this largely dictates the pH (Table 1).
Correlation plots of growth rates and seawater temperature with
B/Ca in L. corallioides samples analysed in this study. Spearman's coefficient r, the
p value, and the line equation are given. Temperature variations (ΔT)
correspond to the differences between the maximum and minimum temperature
registered over 11 years of monthly reanalysis (ORAS5). The B/Ca means
measured in long and short cells respectively correspond to the maximum and
minimum temperature.
Elemental ratios in L. corallioides collected in Morlaix Bay (scale bar: 200 µm). Mg, Li, and Sr/Ca show cyclic variations mirroring the local
seawater temperature. In the timeline, the coldest and the warmest months
have been reported, which correspond to dark and light bands of growth.
Element / Ca ratios in the missing bands (asterisks) have been calculated as the
means of the values measured in warm or cold periods. Monthly means of
temperature have been extracted by ORAS5 reanalysis.
Environmental data from each sampling site. The minimum and maximum
monthly means of temperature are indicated, as are the highest
temperature variation (ΔT), the mean, and the standard deviation of
the time series. Data from monthly means were extracted by 11 years of ORAS5
reanalysis. The pH and DIC for each sampling site are also indicated. The
minimum, maximum, mean, and standard deviation values have been measured over
the time interval 1999–2017. Carbonate system parameters have been extracted
from monthly mean biogeochemical data provided by CMEMS.
Both Li/Ca and Sr/Ca records had positive correlations with Mg/Ca in our
samples of L. corallioides (Figs. 3 and S4). The overall mean Mg/Ca was
225.3 ± 30.4 mmol mol-1, registering the minimum value in the sample
from Aegadian Isl. (171.7 mmol mol-1) and the maximum value in Morlaix (311.2 mmol mol-1) (Fig. 4; Table 2). The Kruskal–Wallis test did not show
significant differences in Mg/Ca among samples (Table A1 in the Appendix; Fig. 4). Among
Mediterranean sites, the algal sample from Aegadian Isl. had the highest
Mg/Ca mean value, followed by Elba and Pontian Isl., which had the lowest
Mg/Ca mean value of all sampling sites (Fig. 4). The highest mean Mg/Ca was
registered in the sample from Morlaix Bay, which also showed a large
dispersion of data above the median Mg/Ca value (Fig. 4).
Long cells had high Mg/Ca values; conversely, short cells corresponded to
areas with a low Mg/Ca ratio.
The ANOVA test followed by the Tukey's test for multiple comparisons
evidenced a significant variability of algal Mg/Ca among three sites in long
cells (Table A2; Fig. 5). In the long cells of L. corallioides collected from Aegadian Isl.
and Pontian Isl., the Mg/Ca data showed a quite similar distribution (Table A2; Fig. 5). The Mg/Ca of the alga from Pontian Isl. was the lowest (Fig. 5). In Morlaix a higher Mg/Ca mean value was registered, which is significantly
different compared to Aegadian and Pontian Isl. (Table A2; Fig. 5). In short
cells, the differences in Mg/Ca among samples were not statistically
significant (Table A1). The magnesium incorporation was slightly higher in
Morlaix and very similar between Aegadian and Pontian Isl. samples (Fig. 5).
Mg/Li values in long and short cells fell in the range found by Anagnostou
et al. (2019) for cultured Clathromorphum compactum (Fig. 6). When plotted against the extracted
seawater temperature in Morlaix (Fig. 7), Mg/Li results did not reflect the
seasonal oscillations in temperature.
B/Ca
The B/Ca ratio in the sample collected from Morlaix showed a moderate
positive correlation with all the examined temperature proxies (Mg/Ca,
Li/Ca, Sr/Ca), with a more defined trend when plotted against Li/Ca
(r=0.68) and slightly less defined against Mg/Ca (r=0.58) and Sr/Ca
(r=0.57) (Fig. 8). On the contrary, the Spearman's analyses did not
evidence significant correlations between B/Ca and the temperature signals
in the algae collected elsewhere (p>0.05).
Overall, the B/Ca ratio in L. corallioides was 661.9 ± 138.9 µmol mol-1,
registering the minimum value in the long cells of the sample from Pontian
Isl. (356.0 µmol mol-1) and the maximum value in Elba (954.1 µmol mol-1) (Fig. 9; Table 2).
The Kruskal–Wallis coefficient showed a highly significant difference in the
B/Ca value among sites, particularly in the L. corallioides from the Pontian Isl., which
had the lowest boron incorporation (Table A3; Fig. 9). The algae collected
in Aegadian Isl. still had significantly lower B/Ca compared to those
collected in Elba and Morlaix (Table A3; Fig. 9). The highest B/Ca mean
value was registered in Elba, with medians comparable to Morlaix (Table A3;
Fig. 9).
The ANOVA test followed by the Tukey's test for multiple comparisons by
site, for long (Table A4) and short cells (Table A5) separately, showed
lower values at the Mediterranean sites and higher values at the Atlantic
site (Fig. 10).
The sample from Pontian Isl. had the lowest mean B/Ca in both seasons,
being significantly different from the samples from both Morlaix and
Aegadian Isl. (Tables A4, A5; Fig. 10). Morlaix had the highest mean B/Ca in
both long and short cells (Tables A4, A5; Fig. 10). L. corallioides from Aegadian Isl. had
an intermediate B/Ca mean value in long cells, differing significantly from
both the Morlaix and Pontian Isl. samples (Table A4; Fig. 10). In short
cells, the sample from Aegadian Isl. slightly differed from the one in
Morlaix (Table A5; Fig. 10).
Interestingly, the long cells of all samples had higher median B/Ca values
compared to short cells (Fig. 10), although only in Morlaix, the differences
between B/Ca measured in long and short cells were statistically significant
(χ2=8.4899, p<0.01).
Growth rates
In the sample from Aegadian Isl., the LA-ICP-MS transect was 1.31 mm long,
and 10 years of growth was detected by coupling microscopical imaging
and Mg/Ca peaks, resulting in a growth rate of 0.13 mm yr-1. In the Elba sample
the laser transect was 1.15 mm long, crossing 8 years of growth, with a
resulting growth rate of 0.14 mm yr-1. The Pontian Isl. sample had 1.08 mm of
transect including 11 years of growth and hence a growth rate of 0.10 mm yr-1.
Finally, the transect from the Morlaix sample was 1.38 mm long, counting 11 years and resulting in a growth rate of 0.13 mm yr-1.
Growth rates did not show any linear relationship with Mg, Li, and Sr/Ca, but
they were positively correlated with the sample mean B/Ca values (Fig. 11).
Discussion
Temperature variations affect many physiological processes
involved in biomineralization, and the rate of calcification, along with
the preservation state of mineral structures, influences the content of
trace elements in carbonates (Lorens, 1981; Rimstidt et al., 1998; Gussone
et al., 2005; Noireaux et al., 2015; Kaczmarek et al., 2016). Trace element
concentrations recorded from the four L. corallioides branches analysed in this study were
consistent with previously published values for other calcareous red algae
(Chave, 1954; Hemming and Hanson, 1992; Hetzinger et al., 2011; Darrenougue
et al., 2014). Particularly, the Mg/Ca ratios recorded in this study ranged
from 172 to 311 mmol mol-1, which is comparable to previous studies on rhodoliths of
Lithothamnion glaciale Kjellman 1883 grown at 6–15 ∘C (148–326 mmol mol-1) (Kamenos et
al., 2008). The B/Ca ratios in L. corallioides from our results range from 356 to 954 µmol mol-1, which is wider than the range measured by solution ICP-MS on bulk samples
of Neogoniolithon sp. (352–670 µmol mol-1) (Donald et al., 2017) and C. compactum (320–430 µmol mol-1) (Anagnostou et al., 2019), both cultured with controlled
pCO2 and a pH ranging from 7.2 to 8.2. The high resolution given by
laser ablation should be more effective in measuring the heterogeneity of
B/Ca across the thallus, thus explaining the wider range of our data.
The Mg/Ca results evidenced a strong relationship with the seawater
temperatures extracted from ORAS5 (Table 1; Fig. 12), as expected. L. corallioides from
Aegadian Isl. had slightly higher Mg/Ca values, followed by Elba and Pontian
Isl. (Fig. 4). This was consistent with local temperature values in the
Mediterranean (Table 1), since Pontian Isl. registered the lowest mean value
and the lowest ΔT, while Aegadian Isl. showed the highest mean
temperature and ΔT. On the contrary, the sample from Morlaix,
collected at 12 m depth, showed high Mg/Ca values in both long and short
cells (Table A2; Fig. 5). The monthly mean temperatures had the highest
variations during the year (ΔT in Table 1) due to the shallower
depth (12 m) and the geographical location. Temperature correlates with
seasons, influencing primary production, respiration, and calcification in
L. corallioides (Payri, 2000; Martin et al., 2006) as well as other calcareous red algae
(Roberts et al., 2002). The high seasonality that characterized the sample
from Morlaix, represented by the high ΔT (Table 1), was probably
responsible for the highest variation of Mg/Ca values and undoubtedly
accounted for most of the differences with Mediterranean samples. For the
first time, we confirmed the reliability of the temperature proxies
Li/Ca and Sr/Ca on a wild-grown coralline alga collected at different depths
and locations. Li/Ca and Sr/Ca records were positively correlated with Mg/Ca
in L. corallioides (Fig. 3), which, in turn, showed a strong relationship with seawater
temperature. Moreover, both Li and Sr/Ca showed periodical oscillations in
correspondence to long and short cells, related to seasonal temperature
variations (Fig. 12). Therefore, Li/Ca and Sr/Ca could be regarded as
temperature proxies in L. corallioides, as could Mg/Ca. The coupling of the Mg/Ca ratio with
Li/Ca and Sr/Ca can be considered a useful technique to gather information about
past temperature for paleoclimate reconstructions (Halfar et al., 2011;
Caragnano et al., 2014; Williams et al., 2014; Fowell et al., 2016;
Cuny-Guirriec et al., 2019).
Element / Ca ratio measurements in L. corallioides.
The B/Ca ratio in coralline algae has rarely been measured, and it is not
clear how the environmental factors control its incorporation. The carbonate
system primarily drives the changes in B incorporation (Hemming and Hanson,
1992; Yu and Elderfield, 2007). In benthic foraminifera, B/Ca increases with
[CO32-] (Yu and Elderfield, 2007), whereas there is no consensus
on the effect of [CO32-] on Mg/Ca and Sr/Ca (Rosenthal et al.,
2006; Dueñas-Bohórquez et al., 2011). Experiments with inorganic
calcite showed a positive correlation between B/Ca and [DIC] (Uchikawa et
al., 2015). Nevertheless, in culture experiments of the coralline algae
Neogoniolithon sp. (Donald et al., 2017) and corals (Gagnon et al., 2021), [DIC] had a
negative effect on B/Ca. DIC and B/Ca values showed a negative relationship
in the samples from Morlaix, Aegadian Isl., and Pontian Isl., which was not observed in
Elba (Fig. 9; Table 1). Significant differences among B/Ca values in the
Mediterranean samples were not expected, since DIC concentrations were
similar (Table 1). This evidence suggests influences other than DIC on the
B signal.
The mean estimated growth rate of L. corallioides was 0.13 ± 0.02 mm yr-1, and it was
supposed to decrease with increasing depth as a direct consequence of lower
light availability (Halfar et al., 2011); indeed, the growth rate of the
sample from Pontian Isl. was the lowest (0.10 mm yr-1). As already suggested
by previous studies on both synthetic and biogenic calcite, B incorporation
is likely affected by growth rate (Gabitov et al., 2014; Mavromatis et al.,
2015; Noireaux et al., 2015; Uchikawa et al., 2015; Kaczmarek et al., 2016).
Indeed, in the cultured calcareous red alga Neogoniolithon sp. B/Ca increases with
increasing growth rate (Donald et al., 2017). The slowest growth rate found
in Pontian Isl. possibly contributed to the lowest B/Ca value; similarly,
the highest growth rate (0.14 mm yr-1) in the sample from Elba could be
responsible for the highest B/Ca (Figs. 9, 11). The mean annual growth rate
of the shallowest sample (Morlaix) was intermediate (0.13 mm yr-1) and likely
not constant during the year. In Morlaix, the alga probably significantly
slowed down the growth in cold months, when the monthly mean seawater
temperature was the lowest of all sampling sites (Table 1). Nevertheless,
its growth rate likely sped up in the warm season due to the abundant
light availability at shallow depth and the warming of seawater (Table 1),
contributing to the significantly higher B/Ca values in long cells (Fig. 10). According to this interpretation, the effect of the growth rate on B/Ca
might be significant across depth and geographical regions (Fig. 11).
In Morlaix, B/Ca showed a weak positive correlation with temperature proxies
(Mg/Ca, Li/Ca, and Sr/Ca; Fig. 8). A positive correlation between B/Ca and
Mg/Ca was already observed in planktonic foraminifera (Wara et al., 2003; Yu
et al., 2007). Therefore, we reconstructed the elemental variations during
algal growth in the Morlaix sample at annual resolution in order to
highlight the influence of temperature (Fig. 12). Contrary to Mg, Li, and
Sr/Ca, the B/Ca did not mirror the seasonal temperature variations as
accurately as the other proxies.
In the sample from the Pontian Isl., the seasonal ΔT, Mg/Ca, and B/Ca
values were the lowest among sites. In particular, B/Ca was significantly
low (Fig. 9), differing more from the other samples than the results for
Mg/Ca (Fig. 4). This suggests that in this sample the B incorporation should
be influenced by factors other than those affecting Mg. In general, the poor
correlation with seawater temperature (Fig. 11), and most of all the lack of
distinct seasonal oscillations in B/Ca across the algal thallus (Fig. 12),
excludes the suitability of B/Ca as a temperature proxy and suggests a
closer relationship with growth rate than temperature.
Knowing the biogeochemistry and the variation of the environmental variables
of seawater is crucial for a more comprehensive picture of the reliability
of geochemical proxies like the ones investigated here (Mg, Li, Sr/Ca, and
B/Ca). Boron incorporation in marine carbonates is still debated, raising
questions about the boron isotopic fractionation, the seawater isotopic
composition, and the so-called “vital effects” (i.e. the metabolic
activities that can bias the proxy record). Vital effects include
species-specific biologically controlled up-regulations of pH in the
calcifying fluid in both corals and coralline algae in response to pH
manipulations mimicking the ongoing ocean acidification (Cornwall et al.,
2017, 2018). Natural marine pH undergoes pH fluctuations with characteristic
ranges of about 0.3 pH units in very shallow coastal water, in areas with
restricted circulation, or in shallow nearshore communities supporting high
rates of benthic metabolism, such as seagrass beds (Cornwall et al., 2013;
Duarte et al., 2013; Hofmann et al., 2011). However, this study analysed the
trace element record in a single high-Mg-calcite species grown in a natural
wide bathymetric interval (from 10 to 66 m depth) characterized by normal
marine pH (range 8.05–8.13, Table 1). Therefore, we considered
up-regulation, if present, to be constant among our conspecific specimens and
thus irrelevant for the measured B/Ca variations. Moreover, no significant
yearly pH fluctuations are expected at each site. Thus, within a single
specimen, the observed differences in B/Ca between short and long cells
(i.e. cold and warm periods of growth) (Fig. 10) are unlikely to be related
to changes in pHcf.
The paucity of B/Ca measurements from coralline algae and, most of all, the
complete absence of these data on specimens grown in nature make it
difficult to compare our B/Ca data with the literature. This observation
takes stock of the significance of our results and emphasizes the importance
of collecting more representative B/Ca data in coralline algae. Further
studies on L. corallioides and other calcareous red algae should be carried out to clarify
the environmental factors influencing the B/Ca in these organisms and to
ensure the reliability of this proxy for paleoclimate reconstructions.
Conclusions
This paper presents the first measures of trace elements (Mg, Sr, Li, and B)
from the coralline alga L. corallioides collected across the Mediterranean Sea and in the
Atlantic Ocean at different oceanographic settings and depths (12, 40,
45, and 66 m depth), providing the first geochemical data on a wild-grown
coralline algal species sampled at different depths and geographical
locations. LA-ICP-MS records of Mg/Ca, Sr/Ca, and Li/Ca have shown a similar
trend, primarily controlled by seawater temperatures in the algal habitat.
On the contrary, Mg/Li did not provide a valuable temperature proxy in this
species. In order to evaluate the control exerted by temperature over B
incorporation, we also tested the correlation of B/Ca with Mg/Ca, Li/Ca.
and Sr/Ca. This led us to provide the first B/Ca data on wild-grown
coralline algae from across the photic zone in different basins. The
correlation between B/Ca and Mg/Ca in L. corallioides was statistically significant only in
the shallow Atlantic waters of Morlaix, where seasonality, and hence the
seasonal temperature variations, during the algal growth was the strongest
among sites. Accordingly, B incorporation differences between long and short
cells of L. corallioides strongly depend on seasonality, being statistically significant
just in Morlaix. Nevertheless, in contrast to Mg, Li, and Sr/Ca, B/Ca
oscillations across the algal growth showed a poor relationship with
seasonal variations in seawater temperature. We found high B/Ca values in
the Atlantic sample, wherein pH and DIC were the lowest. Carbon data did not
explain the low B concentration in the Pontian Isl. sample (66 m depth),
though, wherein pH and DIC were similar to the other Mediterranean sites. The
estimation of growth rate, which was low in the Pontian Isl. sample (0.10 mm yr-1) and got higher in the other Mediterranean samples and in Morlaix
(∼0.13 mm yr-1), led us to conclude that B/Ca relates to growth
rate rather than seawater temperature. B incorporation is therefore subject
to the specific algal growth patterns and rates, knowledge of which is
essential in order to assess the reliability of B/Ca in tracing seawater
carbon variations.
(a) Statistically non-significant results of tests performed to
evaluate (a) the differences of Mg/Ca in L. corallioides and (b) the differences of Mg/Ca
in the short cells of L. corallioides collected at different sampling sites. Test
significance at α=0.05.
(a) Kruskal–Wallis test (Mg/Ca) Dfχ2PSite33.7990.284(b) One-way ANOVA test (Mg/Ca) Short cells DfSum sq.Mean sq.F valuePr (>F)Site2788.1394.01.46470.2496Residuals266994.5269.0Shapiro–Wilk normality test P=0.6442Bartlett's Ksquared P=0.5856
Results of statistical tests performed to evaluate the differences
of Mg/Ca in the long cells of L. corallioides collected at different sampling sites.
Statistically significant p values are given in bold. ANOVA test
significance at α=0.05; Tukey's test significant at p≤α.
One-way ANOVA test (Mg/Ca) Long cells DfSum sq.Mean sq.F valuePr (>F)Site210 897.75448.916.4130.0001Residuals206639.8332.0Shapiro–Wilk normality test P=0.1440Bartlett's K squared P=0.5826Tukey's test Multiple comparisons of means SiteMean difference95 % confidence interval P. adjusted Sitelower boundupper boundMorlaix–Aegadian Isl.38.3291815.0981661.560190.00130Pontian Isl.–Aegadian Isl.-10.84361-35.4838213.796610.51716 Pontian Isl.–Morlaix-49.17278-72.40380-25.941770.00009
Results of statistical tests performed to evaluate the differences
of B/Ca in L. corallioides collected at different sampling sites. Statistically significant
p values are given in bold. Kruskal–Wallis test significance at α=0.05; Dunn's test significant at p≤α/2.
Kruskal–Wallis test (B/Ca) Dfχ2PSite379.816<2.2×10-16Dunn's test Comparisons by site (Bonferroni) ZAegadian Isl.ElbaMorlaixP. adjustedElba-4.645800.00000Morlaix-3.077551.172490.006300.72300Pontian Isl.2.805648.386736.156630.015100.000000.00000
Results of statistical tests performed to evaluate the differences
of B/Ca in the long cells of L. corallioides collected at different sampling sites.
Statistically significant p values are given in bold. ANOVA test
significance at α=0.05; Tukey's test significant at p≤α.
One-way ANOVA test (B/Ca) Long cells DfSum sq.Mean sq.F valuePr (>F)Site2428 364214 18233.0660.0000Residuals20129 5466477Shapiro–Wilk normality test P=0.5527Bartlett's K squared P=0.5470Tukey's test Multiple comparisons of means SiteMean difference95% confidence interval P. adjusted Sitelower boundupper boundMorlaix–Aegadian Isl.190.1173087.50374292.730940.00040Pontian Isl.–Aegadian Isl.-135.42490-244.26303-26.586720.01342Pontian Isl.–Morlaix-325.54220-428.15581-222.928620.00000
Results of statistical tests performed to evaluate the differences
of B/Ca in the short cells of L. corallioides collected at different sampling sites.
Statistically significant p values are given in bold. ANOVA test
significance at α=0.05; Tukey's test significant at p≤α.
One-way ANOVA test (B/Ca) Short cells DfSum sq.Mean sq.F valuePr (>F)Site2216 232108 11635.3600.0000Residuals26794973058Shapiro–Wilk normality test P=0.1699Bartlett's K squared P=0.0576Tukey's test Multiple comparisons of means SiteMean difference95 % confidence interval P. adjusted Sitelower boundupper boundMorlaix–Aegadian Isl.43.09640-19.61932105.812120.22146 Pontian Isl.–Aegadian Isl.-156.90170-223.66771-90.135740.00001Pontian Isl.–Morlaix-199.99810-260.58727-139.408980.00000Data availability
Data resulting from this study are available at
https://doi.org/10.1594/PANGAEA.932201 (last access: 28 January 2022, Piazza et al., 2021).
Environmental data were provided by EU Copernicus Marine Service
Information.
DIC data in the Mediterranean:
https://doi.org/10.25423/CMCC/MEDSEA_MULTIYEAR_BGC_006_008_MEDBFM3 (last access: 28 January 2022, Teruzzi et al., 2021).
DIC data in the Atlantic Ocean:
https://resources.marine.copernicus.eu/?option=com_cswview=detailsproduct_id=IBI_MULTIYEAR_BGC_005_003 (last access: 28 January 2022, Copernicus Marine Environmental Monitoring Service, 2020.)
The pH data: https://resources.marine.copernicus.eu/?option=com_cswview=detailsproduct_id=GLOBAL_REANALYSIS_BIO_001_029 (last access: 13 October 2021, Perruche, 2018)
Temperature data:
https://icdc.cen.uni-hamburg.de/daten/reanalysis-ocean/easy-init-ocean/ecmwf-oras5.html (last access: 28 January 2022, Zuo et al., 2019).
The supplement related to this article is available online at: https://doi.org/10.5194/bg-19-1047-2022-supplement.
Author contributions
DB, VAB, and GP conceptualized the research question and study design. AL,
DB, and VAB conducted the experimental work. ANM and GP performed the environmental data
extraction. GP performed the data analysis and prepared the draft of the
paper. All authors contributed to the editing and reviewing of the paper.
Competing interests
The contact author has declared that neither they nor their co-authors have any competing interests.
Disclaimer
Publisher's note: Copernicus Publications remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Acknowledgements
We are grateful to the anonymous referees whose comments
enabled us to significantly improve the paper. This paper is a contribution to the project MIUR-Dipartimenti di Eccellenza
2018–2022 DISAT-UNIMIB.
The Pontian Isl. sample has been collected in the framework of “Convenzione
MATTM-CNR per i Programmi di Monitoraggio per la Direttiva sulla Strategia
Marina (MSFD, Art. 11, Dir. 2008/56/CE)”. The captain, crew, and scientific staff
of the RV Minerva Uno cruise Strategia Marina Ligure–Tirreno are acknowledged
for their efficient and skilful cooperation at sea.
Financial support for GP was provided by the University of Milano–Bicocca as
a PhD fellowship.
Financial support
This research has been supported by the national project FISR (grant no. 2019_04543 CRESCIBLUREEF).
Review statement
This paper was edited by Aninda Mazumdar and reviewed by five anonymous referees.
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