The Mg/Ca and Sr/Ca ratios of marine shells have been
widely used in environmental paleoreconstructions to understand past marine
conditions. Temperature calibrations to ostracod Mg/Ca ratios are known to
be species-specific but only available for a few species, despite the large
number of known ostracod species. Here, we develop temperature calibrations
for two shallow marine ostracods, Sinocytheridea impressa and Neomonoceratina delicata, using modern sediment samples. Our
results show that adult specimens of these two species might be useful as a
paleothermometer. We observed significant correlations using the Mg/Ca
ratios of both species to the annual
(Mg/CaS. impressa=3.7 ⋅T-62.7; Mg/CaN. delicata=1.6⋅T-16.8) and April (Mg/CaS. impressa=2.8 ⋅T-39.2;
Mg/CaN. delicata=1.6 ⋅T-15.7) temperatures. The
correlation of temperature to the Mg/Ca ratio of S. impressa is more significant and
therefore should be preferred for paleoreconstructions. Re-analysis from
satellite data allows us to validate our temperature calibration to an
extended area around the Pearl River estuary. Our results show that Mg/Ca of
S. impressa and N. delicata ostracods can be used to reconstruct water temperature at a regional
scale, which provides information on the oceanic circulation in coastal
areas of the South China Sea. Sr/Ca ratios of both species do not correlate
with any of the 24 water parameters recorded by the Environmental Protection
Department of Hong Kong, including temperature (21.7–24.1 ∘C),
salinity (23.8–33.7 PSU), dissolved oxygen (4.3–7.1 mg L-1),
suspended solids (1.9–35.4 mg L-1) and pH (7.7–8.2).
Introduction
Element / calcium ratios (E/Ca) of secreted biogenic calcium carbonate by
marine organisms, such as foraminifera and corals, have been used as proxies
for past environmental marine parameters
(Hendy
et al., 2002; Lea, 2003; Lea and Boyle, 1989; Linsley et al., 2000; Martin
et al., 2002). Mg/Ca in foraminifera and Sr/Ca in corals have been
frequently used to reconstruct water temperatures
(Beck
et al., 1992; Cohen et al., 2001, 2002; Lea, 2003; Rosenthal et al., 2006;
Sinclair et al., 1998; Yu and Elderfield, 2008). In addition, Mg/Ca of
ostracod shells has also provided valuable information about water
temperatures
(Chivas
et al., 1983, 1986a; De Deckker and Forester, 1988; Dwyer et al., 2002). The
thermodependency of the Mg incorporation into calcite has been observed in
natural environments
(Cadot
and Kaesler, 1977; Corrège and De Deckker, 1997; Cronin et al., 2005a;
Dwyer et al., 1995) and culture experiments
(Chivas
et al., 1986b; Kondo et al., 2005). Several studies have focused their
efforts on the development of calibrations for deep water genera, such as
Krithe, which are found in the Pacific, Atlantic and Arctic oceans
(Corrège
and De Deckker, 1997; Cronin et al., 1996; Dwyer et al., 1995, 2002; Elmore
et al., 2012; Farmer et al., 2011, 2012; Rodriguez et al., 2020). Other
studies have investigated species found in shallow marine environments, such
as those from the genus Loxoconcha
(Cronin
et al., 2003, 2005a) and Cyprideis (Holmes and De
Deckker, 2016; Roberts et al., 2020). However, there is uncertainty in
temperature calibrations to Mg/Ca of marine ostracods due to the low number
of calibrations developed in comparison to the number of known species
(Holmes and De Deckker, 2012) and the contrasting calibration
slopes observed in different species
(Yamada et al., 2014). Developing
calibrations for new ostracod species can enhance our understanding of the
processes controlling ostracod Mg/Ca uptake and broaden its use in other
areas of the globe (Holmes and De Deckker, 2012; Lea,
2003). The comparison of Mg/Ca and Sr/Ca with multiple water parameters can
also improve our understanding of the variables controlling the
incorporation of trace elements into the ostracod carapace. Mg/Ca and Sr/Ca
of ostracod shells have also been used as a proxy for salinity in enclosed
water bodies (Chivas et al., 1983) based on two
main assumptions: (1) Sr/Cawater and Mg/Cawater exert a control
on Sr/Cashell and Mg/Cashell (Dettman and Dwyer,
2012) and (2) salinity increases simultaneously with the removal of Ca by
low-Mg calcite precipitation during evaporation, increasing the water
content of Mg relative to Ca (Ito et al., 2003).
However, there are several variables that limit their applicability, such as
groundwater inputs and the non-equilibrium state of calcite precipitation (Ito et al., 2003). A weak control of water
temperature and alkalinity on Sr/Ca ratios has also been documented in
lacustrine species (De Deckker et al., 1999;
Gouramanis and De Deckker, 2010). In spite of this use in lacustrine
systems, Sr/Ca of ostracod shells does not seem to be related to salinity or
temperature in shallow marine environments
(Dettman
and Dwyer, 2012; Gouramanis and De Deckker, 2010; Ingram, 1998; Roberts et
al., 2020). Here, we develop parametric calibrations for Mg/Ca and Sr/Ca of
two geochemically unknown species, Sinocytheridea impressa and Neomonoceratina delicata.
Sinocytheridea impressa and N. delicata are shallow marine ostracods from the superfamily Cytheroidea
(Brandão and Karanovic, 2020), which are mainly
distributed in Asian waters
(Hong et
al., 2019; Tanaka et al., 2011). Species of S. impressa and N. delicata have been reported in
sediment records from the Miocene and Pleistocene respectively
(Irizuki
et al., 2005, 2009). The abundance of both species has been used as an
indicator of the paleoenvironmental response to sea-level transgressions
(Chunlian et al., 2013). A high abundance of both species
rarely occurs simultaneously as S. impressa is commonly found in hypoxic environments
with low salinity and high turbidity, while N. delicata is common in well-ventilated,
polyhaline bays
(Hong
et al., 2019; Irizuki et al., 2005). Paleoenvironmental investigations have
focused on the study of assemblages of these two species but not on the
elemental composition of their shells as an indicator of environmental marine
variables, such as temperature or salinity. The calibration of E/Ca ratios
of their shells with ocean parameters in an estuary-dominated system may be
used to reconstruct shallow marine environments in Asia and complement
previous studies on the paleoenvironmental response to sea-level
transgressions (Chunlian et al., 2013).
Estuaries are ecosystems with high productivity and biodiversity
(Day et al., 2013). Water temperature and salinity are
important physical properties of these ecosystems. These parameters are
controlled by the combined effects of oceanic currents, upwelling waters,
river discharge, and atmospheric forcings such as winds and precipitation.
The study of water temperature and salinity can help us understand the
evolution of marine currents and global atmospheric patterns, which can
improve our understanding of glaciation cycles and sea-level transgressions.
For example, Mg/Ca of Loxoconcha specimens from Chesapeake Bay has been used as a
temperature proxy to evaluate anthropogenic and North Atlantic Oscillation
(NAO) impacts on past and present climates
(Cronin et al., 2005b). Hong Kong
(HK) and the surrounding waters of the Pearl River estuary (PRE) are
similar. The local waters are affected by multi-annual oceanic and
atmospheric patterns such as El Niño–Southern Oscillation
(Niu,
2013; Zhang et al., 2013). The development of a new water temperature and
salinity proxy will give us a tool to improve our understanding of past
marine conditions as well as better knowledge of oceanic and atmospheric
regional patterns. However, the calibration of marine shells with ocean
parameters in estuarine systems is challenging due to the highly dynamic
chemical and physical variabilities (Snedden et al., 2013)
and the combined presence of ostracod populations from different years.
Here, we investigate the applicability of ostracod Mg/Ca and Sr/Ca ratios as
proxies for temperature in a freshwater-influenced marine system and several
factors that control the robustness of the parametric calibrations
including (1) number of shells per site, (2) seasonal variability in ocean
parameters, (3) ostracod molting time and (4) the life stage of the ostracods.
MethodologyWater parametersMarine stations
The main dataset consists of measurements of water parameters around the PRE
and Hong Kong waters. Water parameters from Hong Kong were obtained from the
Environmental Protection Department of Hong Kong (EPD), which records 24
parameters of water quality, including temperature, salinity, pH and
dissolved oxygen, around HK (Fig. 1). Monthly single
measurements are performed in eight water control zones: Tolo Harbour, Southern
Waters, Port Shelter, Junk Bay, Deep Bay, North Western, Mirs Bay, Western
Buffer, Eastern Buffer and Victoria Harbour (Fig. S1). The records
correspond to one or two daily values per month from 1986 to the present
date (EPD, 2018). The sedimentation rate in Hong Kong
varies from 0.2 to 5 cm yr-1
(Owen and Lee, 2004; Tanner
et al., 2000), which suggests the presence of specimens from different
years. For the calibration, we calculated monthly mean values using the last
20 years of data from the collection time of our sediment samples (i.e., 2012) in order to determine a robust monthly mean value with the maximum
number of available data. Extreme values with a probability of exceedance
higher than 99 % and lower than 1 % were removed from each parameter, in
order to consider the most probable values. This was calculated by
organizing the historical dataset in descending order and estimating the
probability of occurrence of each value regarding the whole dataset.
Seawater Mg, Sr and Ca concentrations are available in the environmental
impact assessment (EIA) study of the desalination plant in Tseung Kwan O
submitted to the EPD in 2013 (Black and Veatch Hong Kong Limited
and Water Supplies Department, 2013).
Sampling sites around the Pearl River estuary (PRE) and the
Yatsushiro bay in Japan. Ostracods were collected from sediment samples
obtained by the Environmental Protection Department of Hong Kong (EPD) and
OCEAN-HK in Hong Kong. Monthly water quality data were obtained from different
sampling locations across Hong Kong (EPD stations). Mean bottom-water
temperature (BWT) for the year 2011 was obtained from the satellite product
of the Copernicus Marine Environment Monitoring Service (CMEMS).
Additionally, seawater surface temperatures at a 0.5 m depth were retrieved
from Tanoura buoy to estimate water temperatures at the site of
ostracod collection in the Yatsushiro Sea. These data are available on the
web page of the Kumamoto Prefectural Fisheries Research Center
(2021).
Copernicus products
Worldwide potential bottom-water temperature (BWT), provided by the
Copernicus Marine Environment Monitoring Service (CMEMS) of the European
Union, is available from 1993 to 2018 at a spatial resolution of
1/12∘ grid. Potential BWT is a product calculated from
re-analysis, which is intended to be as close as possible to real
observations (Drévillon et al., 2018). The product is
obtained after the assimilation of satellite observations through real-time
marine observations and the modeling of atmospheric and oceanic variables,
such as tidal and heat fluxes (CMEMS, 2020). The
product has low biases at regional and global scales (<0.4 and <0.1∘C respectively), but higher
errors are present in coastal regions due to land cover and river inputs. We
calculated the bias and correction factors between the BWTs from the CMEMS
and EPD in areas where the data overlap (Fig. S1). These factors were
applied to correct the potential BWT in areas where we do not have direct
measurements such as in the sampling locations of OCEAN-HK.
Ostracod samples
We investigated adult specimens of S. impressa (Brady,
1869; Whatley and Zhao, 1988) and N. delicata (Ishizaki and Kato, 1976) from
the uppermost 1 cm sediment layer collected in HK by the EPD in January and
July 2012
(Hong
et al., 2019; Rodriguez, 2021). The temperature calibration was developed
using only samples from HK waters. We also used samples collected around the
PRE by OCEAN-HK in July 2017 to validate the calibrations. Ostracods were
collected from sediment samples sieved in a 150 µm mesh. Most of the
specimens collected from HK and PRE consist of single valves without animal
appendages (Fig. 1). For S. impressa, we distinguished adult
ostracods as those larger than 600 µm
(Irizuki et al., 2005) and with
a well-developed inner lamella (Fig. S2). For N. delicata, we distinguished adult
specimens by size (>450µm) based on Wang et al.
(2018) and Fig. S2. We additionally included S. impressa specimens from
the Yatsushiro Sea collected on 7 June and 7 November 2020
from the intertidal zone (32.624∘ N, 130.640∘ E; 0.5 m
depth; Fig. 1) in order to test the calibration
developed. These specimens present the animal appendages and intact right
and left valves. The size of these ostracods ranged between 550
and 650 µm, and they each had a well-developed inner lamella.
Trace-element analyses
Ostracod shells were sonicated in a methanol bath, rinsed twice with
Milli-Q water, bleached with 5 % sodium hypochlorite for 12–24 h, and
rinsed twice again with Milli-Q water to limit potential contamination
affecting the carbonate Mg/Ca and Sr/Ca
(Rodriguez, 2021). Then,
elemental concentrations on individual shells were measured by inductively coupled plasma mass spectrometry (ICP-MS) Agilent 7900 in the School of Biological Sciences at the University of Hong
Kong. We measured 48Ca, 43Ca, 24Mg, 25Mg, 86Sr and
88Sr. In addition, we measured 27Al and 56Fe to control for
potential contamination in our samples. The data were corrected by a blank
(2 % HNO3) measured every third sample and a multi-element standard
measured every sixth sample, which was prepared from individual pure
elemental solutions (MES1; Mg = 28.1 ppb; Sr = 29.6 ppb; Al = 28.1 ppb;
Fe = 29.4 ppb; Ca = 1830 ppb). A multi-element standard prepared from a pure
multi-element solution (MES2; Mg = 28.6 ppb; Sr = 28.6 ppb; Al = 28.6 ppb;
Fe = 28.6 ppb; Ca = 1861 ppb) and a carbonate standard JCp-1
(Hathorne
et al., 2013; Inoue et al., 2004; Okai et al., 2002) were used to check the
quality of the analysis. Our precision and accuracy improved using 48Ca
and 24Mg. The accuracy and precision (RSD) of the analysis for JCp-1
and MES2 standards are shown in Table 1 (n= 90).
The detection limit of the concentrations was initially estimated using the
blank as 3σ, resulting in a value lower than 0.3 ppb for Mg, Sr, Al
and Fe. Then, the detection limit of the ratios was calculated as 3σ
of a solution with a concentration of 0.1 ppb for Mg, Sr, Al and Fe and 990 ppb of Ca (Yu et al., 2005). The precision and accuracy for
Al and Fe could not be determined for JCp-1 because of the low ratios within
the standard and contamination associated with our analytical procedure.
Detection limit (DL), accuracy (acc.) and precision (RSD) of the
standards used to assess the analytical quality of the measurements.
* The poor accuracy and precision for Al/Ca ratios in JCp-1 are the result of
the low ratios of the standard and external contamination in the analytical
procedure.
ResultsMarine waters
Considering Hong Kong sampling sites, annual mean BWT ranges between
21.8 and 23.9 ∘C (Fig. 1).
The maximum monthly temperature has been recorded close to the PRE
(28.6 ∘C) in August, while the minimum monthly temperature has
been recorded eastward of Hong Kong Island (16.2 ∘C) in February.
Mean annual salinity ranges from 24.7 to 33.7 PSU. The maximum monthly
salinity was measured eastward of Hong Kong Island in August (34.3 PSU), while
the minimum salinity was recorded close to the Pearl River in July (15.6 PSU). A negative linear correlation is observed between the annual
temperature and salinity considering all EPD stations in Hong Kong waters
(R2=-0.67, Fig. S4). BWT and salinities from the EPD grouped by water
control zones are shown in Table 2. A summary of
annual mean values of other parameters such as dissolved oxygen and
suspended solids can be found in Table S1.
Mean and standard deviation (1 SD) of Mg/Ca and Sr/Ca ratios of
adult S. impressa and N. delicata. The number of shells for Mg/Ca and Sr/Ca are the same. Last two
columns show mean and standard deviation (1 SD) of annual bottom-water
salinity and temperature by water control zone of HK.
Average surface water temperatures at the Tanoura buoy recorded in the
months of ostracod collection were 23 and 20.7 ∘C for
June and November respectively. Satellite images reveal a temperature
difference lower than 1 ∘C between the surface temperature in the
Tanoura buoy and the sampling site in the Yatsushiro Sea. Therefore, we
considered surface water temperatures from Tanoura buoy (0.5 m depth) as
representative of the water temperature collected in the sampling site in
the Yatsushiro Sea.
Ostracod ratios
Mg/Ca mean values of adult S. impressa and N. delicata ostracods from EPD samples are 21.1 ± 4.2 mmol mol-1 (n= 170; min = 13.6 mmol mol-1; max = 34.8 mmol mol-1) and 18.7 ± 3.5 mmol mol-1 (n= 80; min = 10.3 mmol mol-1; max = 28.1 mmol mol-1) respectively. Mg/Ca mean values of
adult S. impressa and N. delicata ostracods from OCEAN-HK are 20.1 ± 3.7 mmol mol-1 (n= 51; min = 14.4 mmol mol-1; max = 35.9 mmol mol-1) and 19 mmol mol-1 (n= 30, 14.1 to 24.7 ± 2.8 mmol mol-1) respectively. Mg/Ca mean values in each EPD water control zone
are in Table 2. Mg/Ca mean values of S. impressa specimens from
the Yatsushiro Sea were 21.6 ± 3.8 mmol mol-1 (n= 14;
min = 15.3 mmol mol-1; max = 28 mmol mol-1) and 18.3 ± 5 mmol mol-1 (n= 9; min = 12.1 mmol mol-1; max = 26.1 mmol mol-1)
for June and November respectively.
Sr/Ca mean values of adult S. impressa and N. delicata ostracods from EPD samples are 3.5 ± 0.2 mmol mol-1 (n= 170; min = 2.9 mmol mol-1; max = 4.3 mmol mol-1) and 3.5 ± 0.4 mmol mol-1 (n= 80; min = 2.3 mmol mol-1; max = 4.7 mmol mol-1) respectively, while for OCEAN-HK
samples are 3.6 ± 0.2 mmol mol-1 (n= 51; min = 2.9 mmol mol-1; max = 4 mmol mol-1) and 3.5 ± 0.4 mmol mol-1
(n= 30; min = 2.6 mmol mol-1; max = 4.4 mmol mol-1) respectively.
Sr/Ca mean values in each EPD water control area are in
Table 2. Sr/Ca mean values of S. impressa specimens from the
Yatsushiro Sea were 3.9 ± 0.6 mmol mol-1 (n= 14; min = 2.8 mmol mol-1; max = 4.5 mmol mol-1) and 3.3 ± 0.5 mmol mol-1 (n= 9; min = 2.7 mmol mol-1; max = 4.4 mmol mol-1) for June and
November respectively.
Al/Ca mean values of adult S. impressa and N. delicata from EPD samples are 1 ± 1.3 mmol mol-1 (n= 160; min = 0 mmol mol-1; max = 11.7 mmol mol-1)
and 1.8 ± 1.2 mmol mol-1 (n= 76; min = 0 mmol mol-1;
max = 5.5 mmol mol-1) respectively. Al/Ca mean values of adult S. impressa and N. delicata
from OCEAN-HK samples are 1.2 ± 0.7 mmol mol-1 (n= 51; min = 0 mmol mol-1; max = 3.4 mmol mol-1) and 1.5 ± 1.7 (n= 28;
min = 0 mmol mol-1; max = 7 mmol mol-1) respectively. Mg/Ca and
Al/Ca ratios of S. impressa and N. delicata specimens do not correlate (Fig. S3). The low Al/Ca
ratios indicate the absence of clays in the ostracods. Al/Ca mean values of
S. impressa specimens from the Yatsushiro Sea were 2.3 ± 0.8 mmol mol-1 (n= 14; min = 1 mmol mol-1; max = 3.6 mmol mol-1) and
3.3 ± 1.4 mmol mol-1 (n= 9; min = 1.5 mmol mol-1; max = 6 mmol mol-1) for June and November respectively.
Fe/Ca mean values of adult S. impressa and N. delicata from EPD samples are 1.1 ± 1.8 mmol mol-1 (n= 160; min = 0 mmol mol-1; max = 11.9 mmol mol-1)
and 1.5 ± 1.4 mmol mol-1 (n= 67; min = 0 mmol mol-1;
max = 6.1 mmol mol-1) respectively. Fe/Ca mean values of adult S. impressa and N. delicata
from OCEAN-HK samples are 0.6 ± 0.4 mmol mol-1 (n= 47; min = 0 mmol mol-1; max = 2.1 mmol mol-1) and 1.3 ± 1.4 mmol mol-1 (n= 26; min = 0 mmol mol-1; max = 6.5 mmol mol-1)
respectively. The low Fe/Ca values indicate the absence of Mn–Fe oxides in the
ostracods. Fe/Ca mean values of S. impressa specimens from the Yatsushiro Sea were
0.2 ± 0.2 mmol mol-1 (n= 14; min = 0 mmol mol-1;
max = 0.8 mmol mol-1) and 1 ± 0.6 mmol mol-1 (n= 9;
min = 0.4 mmol mol-1; max = 2.1 mmol mol-1) for June and November
respectively.
E/Ca calibrations to water parameters
Mg/Ca ratios of S. impressa significantly correlate to annual water temperatures in HK
waters (RS. impressa2=0.32; pS. impressa=0.007), but
the Mg/Ca ratios of N. delicata ostracods do not correlate if the full dataset is used
(Table 3). However, the removal of sampling sites
with only one shell allows us to produce significant temperature calibrations
for both species (Table 3). The highest R2 at
95 % significance for the temperature calibration to Mg/Ca ratios for S. impressa and
N. delicata was obtained considering a minimum number (η) of 11 and 3 shells per
sampling site respectively (Table 3). The highest
R2 at 99.9 % significance for S. impressa was obtained considering a minimum
number of 7 shells per sampling site, while temperature calibrations for N. delicata
did not reach this level of significance. Juvenile ostracods from both
species do not correlate with temperature. Juvenile ostracods of S. impressa obtained
from samples from the eastern side of HK have similar Mg/Ca ratios to
adults, but juveniles close to the PRE have lower Mg/Ca ratios than adults
(Fig. 2).
Correlation fit and significance of temperature calibrations using
different number of shells per sampling site to calculate the mean value of
ostracod Mg/Ca ratios for S. impressa and N. delicata.
Relationships of Mg/Ca and Sr/Ca with annual temperature for adult
(filled circles) and A-1 juvenile (open circles) ostracod samples of S. impressa
(η= 7) and N. delicata (η= 3). Single-shell samples are shown as small dots. Solid
lines show the linear regressions for adult specimens.
The Mg/Ca ratio of S. impressa and N. delicata also correlates with other water parameters (from Figs. S5–S12) such as volatile suspended solids (RS. impressa2=0.60; pS. impressa<0.001; RN. delicata2=0.49; pN. delicata=0.037), turbidity (RS. impressa2=0.58; pS. impressa<0.001; RN. delicata2=0.5; pN. delicata=0.033), suspended solids
(RS. impressa2=0.56; pS. impressa=0.001;
RN. delicata2=0.50; pN. delicata=0.034), silica
(RS. impressa2=0.48; pS. impressa=0.002;
RN. delicata2=0.47; pN. delicata=0.041), salinity
(RS. impressa2=0.64; pS. impressa<0.001;
RN. delicata2=0.49; pN. delicata=0.037), nitrite
(RS. impressa2=0.60; pS. impressa<0.001;
RN. delicata2=0.51; pN. delicata=0.031) and nitrate
(RS. impressa2=0.62; pS. impressa<0.001;
RN. delicata2=0.56; pN. delicata=0.02).
The temperature calibration to Mg/Ca is more significant in spring–summer
months for both species (Fig. 3) when the ocean
temperature increases. The highest correlation occurred in April for S. impressa and
N. delicata (ηS. impressa=7; RS. impressa2=0.83; pS. impressa<0.001; ηN. delicata=3; RN. delicata2=0.55; pN. delicata=0.015).
(a) Monthly temperature calibrations to Mg/Ca of S. impressa (η= 7) and N. delicata
(η= 3) for adult ostracod. (b) The calibrations for S. impressa and N. delicata for April are
Mg/CaS. impressa=2.8⋅T-39.2 and Mg/CaN. delicata=1.6⋅T-15.7.
A one-way ANOVA determined that Sr/Ca ratios do not show significant
differences between sampling sites for N. delicata (p= 0.16, Type II). Sr/Ca ratios
were significantly different for S. impressa (p= 0.02). However, this was only the
result of samples collected from Victoria Harbour (n= 18). After removal of
these samples, Sr/Ca ratios of S. impressa were no longer significantly different
between sampling sites (p= 0.96). Sr/Ca ratios of both species do not
correlate with any of the 24 water parameters measured by the EPD.
DiscussionControl on Mg/Ca and Sr/Ca ratios of S. impressa and N. delicata
The strongest linear correlation between the 24 parameters (Table S1)
measured by the EPD and Mg/Ca ratio was for the annual mean temperature,
which suggests that water temperature is the main control of Mg/Ca uptake in
adult ostracods of S. impressa and N. delicata (Fig. 2). Correlations with
other parameters are also significant but are likely caused by
multicollinearity of temperature with other water parameters, such as
turbidity, suspended solids, salinity, pH and nitrite (Fig. S4). The
temperature control on the Mg/Ca ratio of biogenic material is well-known and
has been usually described linearly for ostracods, even though inorganic
calcite follows an exponential relationship (Lea, 2003). We
observed a linear correlation between water temperature and Mg/Ca ratios of
S. impressa and N. delicata ostracods (Fig. 2), but the significance of
the linear calibration is higher for the former species, making this species more
suitable for temperature reconstructions.
We evaluated the sensitivity of the calibration using the natural
variability in ostracod Mg/Ca ratios and seawater temperatures in Hong Kong
sampling sites. The error (range) of Mg/Ca mean values in each station used
for the calibration can be established at a certain confidence level
(Holmes, 2008). For S. impressa, the error in Mg/Ca mean values in each
station ranged from 1.5 to 4.1 mmol mol-1 at a 95 %
confidence level. For annual and spring calibrations, the temperature mean
errors are 0.7 ∘C (0.4 to 1 ∘C) and
0.9 ∘C (0.5 to 1.5 ∘C) respectively. These
values are lower than the temperature difference between the stations
(1.6 ∘C), which indicates that differences higher than
1 ∘C can be estimated using S. impressa calibration curves. For N. delicata, the error
in Mg/Ca mean values ranged from 1.1 to 5.7 mmol mol-1.
Annual and spring calibrations have the same slope, which produce
temperature mean errors of 1.9 ∘C (0.7 to
3.6 ∘C). This error is similar to the difference in temperatures
between the stations. Therefore, more shells of ostracods living at
different temperatures would be needed to estimate differences at
1 ∘C for this species. We also investigated the potential impact
of daily temperature fluctuations on the calibrations. We estimated daily
BWT variability by using the Copernicus satellite products. Using the daily
data from 1993 to 2018, we calculated the standard deviation for each month.
We then determined the average variation for each month across all the
years. We performed this calculation on three Hong Kong sampling stations
located (a) at the lower section of the PRE, (b) outside the PRE and south of
Hong Kong Island, and (c) on the eastern side of Hong Kong Island. We found
the variations were 1 ± 0.4, 0.8 ± 0.5
and 0.7 ± 0.5 ∘C respectively. Therefore, daily bottom-water
fluctuations in Hong Kong waters are unlikely impacting the calibrations
obtained.
The Mg/Ca of A-1 juvenile ostracods of S. impressa does not correlate to April
temperature (Fig. 2). A significant weak correlation
is only observed using June temperature (RS. impressa2=0.33;
pS. impressa=0.031; η= 2). Juvenile ostracods usually show higher
Mg/Ca ratios than adults
(Chivas
et al., 1986b; Dwyer et al., 2002). However, juvenile specimens of S. impressa from
sampling sites with salinity lower than 32 PSU have lower Mg/Ca ratios than
adults (Fig. 4). We hypothesize that environmental
factors may increase the bias between ostracod life stages. For example,
strong currents can produce preferential post-mortem transport of lighter
shells (Boomer et al., 2003), which may foster the mixing of
ostracod shells calcified at different temperatures. Our results suggest
that juvenile and adult ostracods of S. impressa cannot be used indistinctly to
reconstruct April temperature, supporting previous findings about the
incompatible use of Mg/Ca ratios of different ostracod stages
(Dwyer et al., 2002).
Mg/Ca and Sr/Ca correlation to salinity for S. impressa (η= 7) and N. delicata (η= 3)
for salinity recorded in April considering mean values.
None of the 24 parameters measured by the EPD, including temperature and
salinity, exert control on the Sr/Ca ratios in adult specimens of either
species. The low Sr/Ca variabilities in S. impressa and N. delicata suggest that the potential
control variables of this ratio, such as water Sr/Ca or vital effects, do
not change considerably across different locations within the PRE. A
positive correlation in Sr/Ca with chlorophyll a and dissolved oxygen is
observed for S. impressa specimens, but this relationship is mainly produced by
specimens with low Sr/Ca from one sampling site in Victoria Harbour.
Dissolved oxygen in this sampling site was particularly low, probably as a
result of discharge from the nearby Stonecutters Island sewage treatment
plant.
Mg/Ca ratios of both species are negatively correlated to salinity (Fig. 4). A potential control of seawater Mg/Ca on
ostracod Mg/Ca would be possible if seawater Mg/Ca decreases with salinity.
Marine waters have higher Mg and Ca concentrations in comparison to
freshwater (Open University, 1992; Bruland and Lohan,
2006). Previous studies have shown mostly conservative behavior of Mg and
Ca in estuaries and surrounding areas
(Millero, 2006; Patra et al., 2012),
where these concentrations increase linearly with salinity. Therefore, a
higher Ca concentration over Mg concentration or a lower Mg concentration
over Ca concentration toward more saline waters is unlikely in Hong Kong
waters. Moreover, ostracod Sr/Ca is similar at different salinities (Fig. 4), supporting the idea that changes in seawater Ca concentrations are not
the main control on Mg/Ca and Sr/Ca ostracod ratios. Measurements during
2013 and 2017 at the desalination plant in Tseung Kwan O (Figs. 1 and S13)
show water Mg/Ca and Sr/Ca ranging between 4 and 6 mol mol-1, and
between 8 and 9 mol mol-1 respectively during the year. These values are
mostly stable even when monthly salinity decreases to 25 PSU in some Hong
Kong stations during summer, suggesting that the seawater chemistry may not
be a primary control on ostracod Mg/Ca and Sr/Ca ratios of Hong Kong waters.
Our dataset does not allow us to explore in more detail the potential
relationship between these two variables as more data of the seawater
chemical composition are needed.
Factors controlling the robustness of the temperature calibration to Mg/CaNumber of shells per sampling site
The robustness of the annual temperature calibration to Mg/Ca with respect
to R2 and p values depends on the number of individual shells available
to calculate the mean value of each sampling site
(Table 3). The removal of sampling sites with a low
number of shells increases the R2 of temperature calibrations in both
species, suggesting that a low number of samples does not allow us to
capture all the natural variability exerted by the temperature on ostracod
Mg/Ca ratios. The most significant calibrations were obtained using at least
two to four shells for S. impressa and at least two to three shells per sampling site
for N. delicata respectively (Table 3). The margin of error
(z⋅ SE, where z is critical value and SE is standard error) of confident
intervals can be used to provide an estimation of the number of shells
needed to obtain a desired level of error. Using temperature calibrations
for Bythocypris and Krithe specimens, Corrège and De Deckker (1997) showed that the use of four
shells provides an error in the temperature prediction lower than 1.4 ∘C at a 95 % confidence level. In stratigraphic studies the use of
three to five shells is a common practice (Holmes and De
Deckker, 2012). Holmes (2008) studied the critical sample
size of ostracod specimens to keep a desired error at a 0.99 significance
level in Mg/Ca and Sr/Ca from a stratigraphic sequence. The author
concluded that in modern specimens of Cyprideis torosa from shallow brackish environments
the optimal sample size may vary from 3 to 16 shells. We can use this
approach to estimate the number of shells needed per sampling site to keep
the error at an acceptable level to produce a significant correlation. The
use of one, two, three, four, five, six and seven shells produces margin of errors of 3.4, 2.4,
2.0, 1.7, 1.5, 1.4 and 1.3 ∘C at 95 % significance
respectively, considering the highest standard deviation observed in our
sampling sites (σ=4.7 mmol mol-1; n= 15) and normally
distributed samples (Rodriguez,
2021). Our results suggest that in shallow marine waters the calculation of
mean Mg/Ca ratios with at least four individual shells in more than 10
sampling sites would likely produce a significant temperature calibration at a
99 % significance level (p<0.01), accounting for short-term
temperature variations. In the following analyses, we restricted the minimum
number of shells per sampling site to η= 7 for S. impressa and η= 3 for N. delicata as we obtained
the highest R2 at a significance of 99.9 % and 95 % respectively.
Temporal variability
Most temperature calibrations to Mg/Ca are produced with the annual mean
temperature as they are intended to reflect long-term changes in
paleoceanographic studies. However, ostracods molt their shells in a short
period of time (usually days or weeks). Thus, it may be possible to record
ocean parameters at a shorter timescale if the correct molting time is
known. Our monthly analysis of linear regressions shows that the best
temperature calibrations to Mg/Ca in terms of high R2 and significant
p values were found with the water temperature measured in April for S. impressa and N. delicata (Fig. 3). This suggests that adult ostracods of both
species may inhabit HK waters mainly during spring or early summer, as has
been documented for other shallow marine species
(Cronin et al., 2005a; Kamiya,
1988). July temperature also correlates with Mg/Ca ratios in both species,
showing a second peak (Fig. 3). Two periods of
calcification have recently been shown for C. torosa (Roberts
et al., 2020), which may also occur in S. impressa and N. delicata. The high correlation between
April water temperature and Mg/Ca ratios indicates the possibility of
reconstructing water temperature at a finer temporal scale, which can help to
unravel coastal ocean circulation patterns. For example, the interaction of
the Pearl River and Hainan, Taiwan and Kuroshio currents
(Morton and Wu, 1975) determines the temperature
and salinity of Hong Kong waters. The Hainan current is dominant during
summer, while the Taiwan and Kuroshio currents affect Hong Kong waters
during winter. Sinocytheridea impressa and N. delicata may become important tools to determine the currents'
interaction by providing information on water temperature during the
transition between these currents and freshwater from the Pearl River.
Validation of temperature calibration
April BWTs obtained from the Copernicus product are on average -1.5± 1.8 ∘C (2σ) below the measurements from the EPD (Fig. S1).
BWT differences between EPD stations and the Copernicus product range from 0 to
3 ∘C, being the largest in stations close to the Pearl River (Fig. S1). We corrected the BWTs obtained from the Copernicus product in all
OCEAN-HK sampling locations by -1.5∘C.
The BWTs estimated from ostracod Mg/Ca ratios in OCEAN-HK sampling locations
are in good agreement with BWTs obtained from the Copernicus product for
April (Fig. 5 and Table S2). The difference between
the estimated temperature by the linear regressions and the potential BWT
from the Copernicus product is lower than 0.7 ∘C in seven out of the eight
sites for S. impressa. Only one sampling site shows an error of 1.8 ∘C (Table S2). For N. delicata, the error was lower than 2.3 ∘C in the three stations
considered. This suggests that S. impressa and N. delicata specimens around the PRE follow the
regression line developed with ostracods collected from HK waters. Our
findings also suggest that calibrations may be done without direct
measurements of BWT but using the potential BWT from satellite products. We
highlight that the improvement in the quality of BWT products derived from
satellite images may facilitate the calibration of multiple species across
the world as scientists have global coverage of BWT with a high resolution
(1/12∘,∼9 km).
Mg/Ca ratios of ostracods from the PRE (OCEAN-HK) and Yatsushiro
bay over the calibration for S. impressa (Mg/CaS. impressa=2.8⋅T-39.2) and N. delicata (Mg/CaN. delicata=1.6⋅T-15.7) performed
with samples from Hong Kong (EPD). The BWT from the Copernicus product was
used for OCEAN-HK samples. Surface water temperature from the Tanoura buoy in
the last 15 d in June (21.8 ∘C) and November (21.9 ∘C) were considered for the Yatsushiro Sea samples.
The Mg/Ca ratios of S. impressa ostracods from the Yatsushiro Sea are within the range
of Mg/Ca ratios found in Hong Kong ostracods (June 21.6 ± 3.8 mmol mol-1 and November 18.3 ± 5 mmol mol-1,
Fig. 5). Using the Hong Kong calibration developed
for April, temperatures in the Yatsushiro Sea were estimated to be
21.5 ∘C in June and 20.4 ∘C in November. We compared
these temperatures with seawater temperatures recorded (a) during the day of
sampling (June 21.6 ∘C and November 15 ∘C, in situ) and as the
mean of (b) 10 d (June 22.0 ∘C and November 21.6 ∘C, buoy),
(c) 20 d (June 21.5 ∘C and November 22.1 ∘C, buoy), (d) 30 d (June 20.7 ∘C and November 22.6 ∘C, buoy) and (e) 60 d (June 18.8 ∘C and November 23.9 ∘C, buoy) before the
specimen collection. The estimation of water temperatures using ostracod
Mg/Ca ratios in November is not similar to the temperatures recorded on the
same day as sampling. This is likely due to the exposure of the site to
freshwater inputs, which may have affected local water temperatures. In
addition, the ostracod calcification may have occurred several days before
its collection. The consideration of the mean temperature across the 10 d
before the ostracod collection produced the greatest agreement with
Mg/Ca-estimated temperatures. Thus, our results suggest that ostracods from
the Yatsushiro Sea may have calcified the shells during the last few days
before their collection.
Calibrations at a superfamily level
Sinocytheridea impressa and N. delicata are related at a superfamily level (Cytheroidea). A few studies have
developed calibrations for ostracod species from the same superfamily. A
unique calibration for ostracods from the same superfamily cannot be
performed according to our results. Temperature calibrations to Mg/Ca ratios
have been developed for specimens of the same superfamily, including the
genus Krithe (Cadot and Kaesler, 1977; Corrège and De Deckker, 1997; Cronin et
al., 1996; Dwyer et al., 1995, 2002; Elmore et al., 2012; Farmer et al.,
2012), Loxoconcha (Cronin et al.,
2003), Cytheropteron (Yamada et al., 2014) and
Xestoleberis (Kondo et al., 2005).
Sinocytheridea impressa and N. delicata show lower Mg/Ca ratios at the same temperature in comparison to other
species (Fig. 6). Similar Mg/Ca ratios to those of S. impressa and N. delicata have
been observed in Krithe specimens at seawater temperatures ranging between
10 and 20 ∘C. The residual standard errors (RSEs) for
the calibration of S. impressa and N. delicata are 1.1 mmol mol-1 for both species, showing
one of the best regression fits of all calibrations for the superfamily
Cytheroidea (Fig. 6). The calibration of N. delicata has a
similar slope in comparison to Xestoleberis specimens (Fig. 6),
but S. impressa has the highest slope of all species from the superfamily, which shows
that different species from the same superfamily do not share the same
calibration slope and intercept. In addition, ostracods from the same
superfamily under similar conditions of temperature and salinity may show
significant differences in their calibration parameters, such as S. impressa and N. delicata
specimens in HK waters or Xestoleberis specimens
(Kondo et al., 2005). Factors such
as the development of temperature calibrations from multiple species, the
number of shells considered per site and variability induced after the burial
of ostracods might impoverish the calibration fit. Our
study suggests that when species-specific calibrations are performed, the
residual standard error in the temperature calibration to Mg/Ca may be
around 1 mmol mol-1. This happens in shells which have not been buried,
are oxide-free, and were treated with non-corrosive cleaning reagents such
as 5 % sodium hypochlorite and methanol
(Rodriguez, 2021). The Mg/Ca of
ostracods is temperature-sensitive at a very small temperature range and
may be useful to understand variation in a localized region. Sinocytheridea impressa and N. delicata ostracods
from other locations can improve the calibration shown in this study by
expanding the temperature range.
Temperature versus Mg/Ca ratios for specimens of the superfamily
Cytheroidea. Krithe samples were retrieved from Farmer et al.
(2012) and the study of Elmore et
al. (2012) which
contains the collection of Mg/Ca and BWT from different studies including
Cadot and Kaesler (1977), Corrège and De Deckker
(1997), Dwyer et al.
(1995), Cronin et al. (1996), and Dwyer
et al. (2002).
The lower Mg/Ca in S. impressa and N. delicata ostracods in comparison to other species from the
same superfamily such as Krithe or Loxoconcha may be the result of other variables such as
pH, dissolved inorganic carbon (DIC), CO3 concentration or the calcite saturation index (Ω).
These variables have been suggested to partially control the incorporation
of ostracod Mg/Ca ratios
(Elmore
et al., 2012; Farmer et al., 2012; Holmes and De Deckker, 2012).
Loxoconcha from Chesapeake Bay
(Cronin
et al., 2003, 2005a) most likely dwells in the environment most similar to that of
Sinocytheridea and Neomonoceratina due to its presence in a large estuary in a polyhaline system at
similar depths. Measurements of pH and DIC in
HK and Chesapeake Bay waters allow us to compare the saturation index in
both basins. A bottom-water pH ranging from 7.8 to 8.2
(EPD, 2018) and DIC over 1850 µM
(Guo
et al., 2008; Yuan et al., 2011) indicate that the seawater is oversaturated
with calcite (Ω∼3) in our sampling sites for most of
the year. On the other hand, pH and DIC in the bottom waters of the
Chesapeake lower bay in 2006 ranged from 7.92 to 7.96 and 1717.4 to
1865.4 µM respectively, with a calcite saturation index over 2.8
(Brodeur et al., 2019),
suggesting that the lower ostracod Mg/Ca ratios in S. impressa and N. delicata ostracods are not a
direct result of different conditions of pH, DIC or the calcite saturation
index. Species-specific biomineralization types (i.e., ostracod
calcification) may also play an important role in the temperature response
to ostracod Mg/Ca ratios of different species, but our measurements do not
allow us to explore this factor.
Conclusions
The Mg/Ca ratios of S. impressa and N. delicata ostracods can be used as proxies for water
temperature in shallow marine environments. The temperature dependence of
S. impressa is higher, and therefore it is more suitable for temperature
reconstructions. This study shows that (1) the number of shells per sampling
site has an important impact on the calibration robustness due to the strong
seasonal variability in temperature in estuaries and coastal areas, and
therefore we recommend the use of four or more shells per sampling site; (2) ostracods can give information on monthly water temperatures; (3) the
temperature reconstruction based on Mg/Ca ratios of S. impressa and N. delicata specimens has the
potential to give insight into past ocean circulation in coastal areas of the
South China Sea; and (4) ostracods from the same superfamily show different
calibration curves, which do not seem to be controlled by the Mg/Ca ratios
of marine waters, temperature or the carbonate system. Better understanding
of ostracod molting time will likely improve calibrations and the
identification of the calcification temperature for S. impressa and N. delicata ostracods.
Data availability
Data used for this study are available from EarthChem
(10.26022/IEDA/111891; Rodriguez and Not, 2021).
The supplement related to this article is available online at: https://doi.org/10.5194/bg-18-1987-2021-supplement.
Author contributions
CN and MR designed the project and wrote the manuscript. MR carried out the experiments, calculations and interpretation of the results under the supervision of CN.
Competing interests
The authors declare that they have no conflict of interest.
Acknowledgements
We are thankful to the Theme-based
Research Scheme project of OCEAN-HK (T21-602/16R) for providing access to sediment
samples and CTD data. This study has been conducted using EU Copernicus
Marine Service information. We wish to thank Moriaki Yasuhara and
Yuanyuan Hong for their contribution in the provision of sediment samples
and the identification of ostracod species and stages. We greatly thank
Gengo Tanaka for providing us with ostracod specimens from the Yatsushiro
Sea in Japan as well. Finally, we would like to thank Kayi Chan for
proofreading a version of this paper.
Financial support
This research has been supported by the seed funding program for basic research of the University of Hong Kong (project code no. 104003882) and the start-up fund for new staff from the Science Faculty of the University
of Hong Kong, awarded to Christelle Not. Maximiliano Rodriguez was supported by the HKU SPACE Research Fund (no. 200004912) granted to Christelle Not. The sample collection
in Hong Kong waters was also partially supported by the Environment and Conservation Fund of Hong Kong (project code 19/2012), the General Research Fund of the Research Grants Council of Hong Kong (project codes HKU 17302518 and HKU 17303115), and
the seed funding program for Basic Research of the University of Hong Kong (project codes 201111159140 and 201611159053) awarded to Moriaki Yasuhara.
Review statement
This paper was edited by Hiroshi Kitazato and reviewed by Thomas M. Cronin and one anonymous referee.
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