Asami et al. Progress in Earth and Planetary Science
https://doi.org/10.1186/s40645-021-00434-7(2021) 8:38

RESEARCH ARTICLE

Progress in Earth andPlanetary Science

Open Access

Reconstruction of ocean environment timeseries since the late nineteenth century
using sclerosponge geochemistry in thenorthwestern subtropical Pacific
Ryuji Asami1* , Taketo Matsumori2, Ryuichi Shinjo2, Ryu Uemura3, Yuki Miyaoka4, Masaru Mizuyama5, Yuji Ise6 andTakashi Sakamaki7

Abstract
The geochemistry of calcifying marine organisms is an excellent proxy for reconstructing paleoceanographic history,
but studies of hypercalcified demosponges (sclerosponges) are considerably fewer than those of corals, foraminifers,
and bivalves. For this study, we first generated near-annual resolved stable carbon and oxygen isotope (δ13C andδ18O) and element/Ca ratios (Sr/Ca, Ba/Ca, Pb/Ca, U/Ca) time series for 1880–2015 from sclerosponge samples(Acanthochaetetes wellsi) collected at Miyako Island and Okinawa Island in the Ryukyu Islands of southwesternJapan. The δ13C records exhibited a typical variation of anthropogenically derived Suess effects, demonstrating thatthe rates of decrease of –0.0043‰/year before 1960 and – 0.024‰/year after 1960 in the northwestern subtropical
Pacific were respectively similar to and about 1.4 times higher than those of the Caribbean Sea in the tropicalAtlantic. Spectral analysis of the δ18O time series revealed significant periodicity of approximately 2, 3, 6.5, 7–10, and
20–30 year/cycle, indicating that sea surface conditions in the southern Ryukyu Islands had been dominated byinterannual and decadal variations in temperature and seawater δ18O since the late nineteenth century. The Sr/Caand U/Ca ratios for the species A. wellsi (high-Mg calcite) might not be a robust proxy for seawater temperatures,
unlike Astrosclera willeyana and Ceratoporella nicholsoni sclerosponges (aragonite). An evident increasing Pb/Ca
trend after 1950 found in the samples is probably attributable to Pb emissions from industrial activities andatmospheric aerosols in eastern Asian countries. The Ba/Ca variations differ greatly among sampling sites, whichmight be attributable to the respective local environments. This evidence demonstrates that more high-resolution
age determinations and geochemical profilings enable delineation of secular variations in ocean environments onannual and interannual timescales. Results of our study suggest that if sclerosponges living in deeper ocean
environments are collected, spatial and vertical oceanographic variations for the last several centuries will bereconstructed along with coral proxy records.
Keywords: Sclerosponge, Acanthochaetetes wellsi, Oxygen and carbon isotopic composition, Minor and traceelements, Isotope equilibrium, Paleoenvironmental proxy, Ryukyu Islands* Correspondence: ryuji.asami.b5@tohoku.ac.jp1
Institute of Geology and Paleontology, Graduate School of Science, Tohoku
University, 6-3, Aramaki-Aza-Aoba, Sendai 980-8578, Japan
Full list of author information is available at the end of the article© The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License,
which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give
appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate ifchanges were made. The images or other third party material in this article are included in the article's Creative Commonslicence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commonslicence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain
permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Asami et al. Progress in Earth and Planetary Science(2021) 8:38

1 Introduction
Hypercalcified demosponges (“sclerosponges” hereinafter), members of the earliest branching metazoan
taxon (Porifera), persisted as dominant reef-building
marine organisms throughout the Phanerozoic (Vacelet
1985; Reitner and Engeser 1987; Wood 1990; Reitner
1992). The genus Acanthochaetetes Fischer 1970 ispresent in the fossil record from the Early Cretaceous(Reitner 1992). In modern coral reefs, sclerosponges canbe found in cryptic niches of dark environments, unlike
zooxanthellate scleractinian corals (Wörheide 1998).
Sclerosponges, commonly mushroom-shaped, deposit a
calcium carbonate skeleton at a very slow growth rate of
mostly fewer than about 2 mm/year; they can grow for
up to several hundred years (Benavides and Druffel
1986; Böhm et al. 1996; Reitner and Gautret 1996;
Wörheide et al. 1997; Wörheide 1998; Swart et al. 2002;
Fallon et al. 2003; Grottoli et al. 2010).
To elucidate climate change and global warming,
environmental proxies such as trees, sediments, andcorals are strongly needed for demonstrating
temperature variations over the last millennia (PAGES
2k Consortium 2013; Abram et al. 2016). The stable carbon and oxygen isotope records (δ13C and δ18O) ofsclerosponges are a proxy for reconstructing dissolved
inorganic carbon δ13C of seawater (e.g., Böhm et al.
1996; Swart et al. 2010) and seawater temperature andsalinity (e.g., Wörheide 1998; Böhm et al. 2000; Moore
et al. 2000; Rosenheim et al. 2005a) for the past. Earlier
studies have revealed that similarly to corals, the δ13C
and δ18O values of sclerosponges respectively reflect theincrease of fossil fuel CO2 in seawater (Böhm et al. 2002;
Swart et al. 2010) and interannual climate variation(Swart et al. 2002; Grottoli 2006; Grottoli et al. 2010;
Wu and Grottoli 2010). Other minor and trace elements
and isotopes can be a proxy for monitoring ocean environments and chemistry (Lazareth et al. 2000; Fallon
et al. 2005; Rosenheim et al. 2005b; Ohmori et al. 2014).
Particularly, some studies have shown that sclerosponge
strontium/calcium (Sr/Ca) presents some potential for
determining seawater paleotemperatures (e.g., Rosenheim
et al. 2004; Waite et al. 2018). Its fidelity as apaleoenvironmental proxy has been verified by evaluationand calibration studies of sclerosponges (Böhm et al. 2000;
Rosenheim et al. 2005b, 2009; Asami et al. 2020a).
Importantly, sclerosponges can live in environmentswith less sunlight (e.g., reef caves and overhangs) and at
greater water depths of up to several hundred meters in
Indo-Pacific tropical regions (e.g., Hartman 1980) and in
the Atlantic and Caribbean regions (e.g., Druffel andBenavides 1986; Böhm et al. 1996), unlike zooxanthellate
corals and giant clams living in shallow coral reefs. For
that reason, their skeletal chemistry can be useful for
elucidating the vertical variations of physical andPage 2 of 16

chemical parameters of seawater and for generating theirseveral-centuries-long time series that overlap with andextend beyond instrumental oceanographic data. However, sclerosponge-based climate reconstructions over ahundred years are extremely few relative to those ofcorals. Moreover, they have not yet been extracted fromthe northwestern subtropical Pacific.
We first generated > 100-year-long multiple proxyrecords of δ13C, δ18O, and elements/Ca ratios, Sr/Ca,
barium/Ca (Ba/Ca), lead/Ca (Pb/Ca), and uranium/Ca(U/Ca), in living sclerosponges (Acanthochaetetes wellsi
Hartman and Goreau 1975) collected from the Ryukyu
Islands of southwestern Japan. Based on radiocarbon
and δ13C results, near-annually resolved time series of
the geochemical records were established for the last
one hundred years and more, which are expected to be
useful for paleoclimate archives such as corals. The
study results emphasize that the geochemical time series
show secular decade-scale variations of ocean environments in the subtropical Northwest Pacific.

2 Materials and methods
2.1 Study site and modern environment

The study sites are located off the southern coast of
Miyako Island and at Manza Cape around the western
coast of Okinawa Island in the Ryukyu Islands of southwestern Japan (Fig. 1). The northward-flowing warm
Kuroshio current (the western North Pacific current)
passes along the Ryukyu Islands, which has allowed thedevelopment of coral reefs with high biodiversity in theislands. The Kuroshio current, the strong northwesterncomponent of the subtropical North Pacific gyre, advects
a large amount of heat from the tropics to northern
mid-latitudes. The climate is subtropical, with atmospheric temperatures of 17.6–28.5 °C and 16.5–28.6 °C
and an annual mean of 23.4 °C and 22.8 °C at Miyako
and Okinawa Islands for 1961–2015 (Japan Meteorological Agency; http://www.jma.go.jp/jma/indexe.html).
The mean annual precipitation is greater than 2000
mm/year, with a rainy season (May–June) and typhoonseason (August–September) at the two sites. Sea surface
temperatures (SST) with a 2°–2° grid for 1961–2015,
available at the study sites (NOAA NCDC ERSST ver.
3b, http://iridl.ldeo.columbia.edu/), show variation of
22.9–29.1 °C and 21.8–28.9 °C with annual means of
26.1 °C and 25.4 °C in Miyako (23°–25° N, 125°–127° E)
and Okinawa (25°–27° N, 127°–129° E), respectively.
According to monthly average data available from theJapan Oceanographic Data Center (JODC) for 1906–
2003 (http://www.jodc.go.jp/), the sea surface salinity(SSS) varies 34.3–34.9 and 34.1–35.0, respectively, withannual means of 34.7 and 34.6 at Miyako (24°–25° N,
125°–126° E) and Okinawa (26°–27° N, 127°–128° E).

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Fig. 1 Map of eastern Asian and the northwestern Pacific regions showing the locations of Miyako Island and Okinawa Island (this study) andIshigaki Island (Abe et al. 2009; Hirabayashi et al. 2017) and Kume Island (Ohmori et al. 2014) discussed in the text

2.2 Samples

The sclerosponges (Acanthochaetetes wellsi) examinedin this study were growing on the wall in a dark submarine crevasse (Miyako Island) and cave (Okinawa Island)of outer reef edges. In June 2012, a living sclerosponge
sample (SMJ-2-S1) was collected at 10.2 m water depth
from Miyako Island (24° 42′ 24.2″ N, 125° 19′ 02.6″ E)(Figs. 1 and 2). The sample SMJ-2-S1 is 7 cm in height,
21 cm in length of the major axis, and 18 cm in lengthof the minor axis. In October 2015, a living sclerosponge
sample (MNZ-S1) was collected at 2 m water depth
from Okinawa Island (26° 30′ 14.9″ N, 127° 50′ 52.5″
E) (Figs. 1 and 2). The sample MNZ-S1 is 9 cm inheight, 19 cm in length of the major axis, and 18 cm inlength of the minor axis. The skeletal surfaces (tissue
layer zones) of samples were mostly light brown or orange, which has a thickness of less than 2 mm. The samples were well rinsed ultrasonically with milli-Q water(resistance = 18.2 MΩ·cm; Millipore Corp.). They werethen dried.
The sclerosponge samples were slabbed to 3 mm
thickness parallel to the axis of skeletal growth. Xradiographs were taken under exposure conditions of 30
kV, 3 mA, and a distance of 53 cm between a lamp anda film with exposure time of 15–60 s, using soft X-ray

film shooting equipment (Soft X-Ray Sofron SRO-405A;
Soken Co., Ltd.) and a computed radiographic reader(FCR PRIMA T2; FUJI FILM Corp.) at the University of
the Ryukyus (UR). The X-radiographic images of thesamples showed skeletal banding comprising alternating
high-density (dark) and low-density (light) bands (Fig. 2).
Powder subsamples for geochemical analyses were taken
every 1 mm along the skeletal growth direction manuallyusing a pre-cleaned diamond drill, roughly corresponding to the annual sampling resolution. To determine thetime series of geochemical records, radiocarbon values(Δ14C, ‰) of 13 subsamples along the growth directionof the SMJ-2-S1 sample were analyzed by Paleo-Lab Co.
Ltd., Japan (Supplementary Table S1). The data arereported in terms of deviation from the activity of the
pre-industrial wood standard (Stuiver and Polach 1977),
which is corrected for isotope fractionation to a δ13C
value of −25.0‰. In addition, powder subsamples weretaken from different portions of the skeleton surface toevaluate within-skeleton variations in the geochemistry,following the method described by Asami et al. (2020a).
2.3 Skeletal structures

To check the mineralogy and preservation state of theskeleton, the fragments were examined using X-ray

Asami et al. Progress in Earth and Planetary Science(2021) 8:38

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Fig. 2 Photos and X-radiographic positive images of the two modern sclerosponges show skeletal growth bandings comprising alternating highdensity (dark) and low-density (light) bands. Slab samples were extracted by cutting along the blue lines. Geochemical analyses were conductedalong sampling transects for generating the time series (red lines) and at selected portions of the coeval skeleton for evaluating within-skeleton
variation (yellow squares). Radiocarbon measurements were taken at selected skeletal portions (pink squares)

diffraction (XRD) analysis and scanning electron microscopy (SEM), following the methods reported by Asami
et al. (2015, 2020a). At UR, XRD analysis was conductedusing a multipurpose XRD device (RINT Ultima/PC;
Rigaku Corp.) to test for mineralogy. After powderedsamples were mounted on well-cleaned glass slides with
HCl, ethanol, and milli-Q water, they were analyzed
using Cu Kα radiation (40 kV, 30 mA) by scanning from
20° to 37° at a 2θ angle at 0.02° steps. A microscope(TM3030; Hitachi High-Tech. Corp.) was used for SEM
imaging of the skeleton. Also, XRD analysis revealed that
the A. wellsi samples consisted of high-Mg calcite with
20.1 mol% Mg for SMJ-2-S1 and 17.3 mol% Mg for

MNZ-S1, consistent with data reported from earlier
studies (Reitner and Engeser 1987; Reitner and Gautret
1996; Grottoli et al. 2010). The SEM observations revealed that skeletal aspects of our sclerosponge samples(Fig. 3) closely resemble those found in earlier studies(Reitner and Engeser 1987; Reitner et al. 1997; Giliset al. 2013), clearly showing a typical macrostructureorganization with vertical calicles subdivided by horizontal tabulae and a microstructure of high-Mg calcite skeleton. Additionally, results confirmed that the samples
had a well-preserved skeleton without physical evidenceof diagenetic alteration, such as overgrowth of inorganically precipitated secondary cement, traces of dissolution,

Asami et al. Progress in Earth and Planetary Science(2021) 8:38

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Fig. 3 Scanning electron micrograph images of sclerosponges. A well-preserved pristine calcite skeleton is visible. A and B Macrostructuralorganization of high-Mg calcite skeleton with vertical calicles subdivided by horizontal tabulae. C and D Lamellar microstructure of high-Mg
calcite skeleton, the secondary structure of the tabulae and coatings of the tubes, randomly oriented single crystals. E and F Spicular skeletonand spiraster microscleresor bioerosion. Consequently, these results indicate that
A. wellsi samples used for this study can retain pristine
calcite skeleton with original values of isotope composition and elemental concentrations.
2.4 Stable isotope analyses

Stable carbon (δ13C) and oxygen (δ18O) isotope analysesof calcium carbonate (0.14–0.16 mg) were conductedusing a continuous-flow isotope ratio mass spectrometerattached to a Gasbench II and a GC-PAL auto-sampler(Delta V Advantage; ThermoFisher Scientific Inc.) at
UR, following the method presented by Asami et al.
(2015, 2020a). Isotopic ratios were reported in conventional δ notation relative to Vienna Pee Dee Belemnite(VPDB). External precision (1σ, N = 190) throughout theentire analysis was ± 0.04‰ and ± 0.06‰ for δ13C andδ18O. Accuracy of the measurements of sclerosponge
samples was evaluated based on replicates of IAEA CO1 calcite standard, yielding average δ13C and δ18O valuesof 2.46 ± 0.05‰ and −2.41 ± 0.06‰ (N = 27), which respectively show excellent agreement with recommended
values.
2.5 Elements/Ca analyses

Elements/Ca ratios (Sr/Ca, Ba/Ca, Pb/Ca, U/Ca) wereanalyzed using an inductively coupled plasma-mass
spectrometer (XSeries II; ThermoFisher Scientific Inc.)at UR, fundamentally following the method reported by
Asami et al. (2009, 2020a). Each sclerosponge powder
sample (approx. 0.15 mg) was dissolved in 4.5 mL of 0.5
mol/L high-purity HNO3 diluted with ultrapure Milli-Q
water. Each seawater sample of 125 μL was diluted 80

Asami et al. Progress in Earth and Planetary Science(2021) 8:38

times with high-purity HNO3 and ultrapure Milli-Q
water. Internal standard elements (Sc, Y, and Yb) wereadded to all the solutions to produce equal concentrations to control matrix effects and to correct for
instrumental noise. Solutions were analyzed for 43Ca,
44
Ca, 45Sc, 87Sr, 88Sr, 89Y, 137Ba, 138Ba, 172Yb, 208Pb, and238
U. Measurements were conducted in triplicate.
Calibrations of the five gravimetric standard solutions
yielded high correlation coefficients of r > 0.99998 for
Ca and Sr and of r > 0.99995 for Ba, Pb, and U. A reference solution, matched gravimetrically to the Ca concentration of the average sclerosponge sample solutions,was measured at intervals of three samples to correct instrumental drift. Based on replicate measurements of thesolution of carbonate reference material JCp-1 (Okaiet al. 2002), external precisions for Sr/Ca, Ba/Ca, Pb/Ca,and U/Ca determinations were better than 0.30%, 1.7%,
4.1%, and 0.77% relative standard deviations (N = 166).
The measurement values of samples were calibratedusing the widely accepted values of Hathorne et al.
(2013).

3 Results and discussion
3.1 Within-skeleton variations and comparison withequilibrium calcite

The within-skeleton variations of geochemical components in an A. wellsi specimen were estimated at thecoevally precipitated skeleton (Fig. 4A). The standard
deviations (1σ) of geochemical analyses of SMJ-2-S1 and
MNZ-S1 samples were, respectively, ± 0.049‰ and ±0.039‰ for δ13C, ± 0.056‰ and ± 0.093‰ for δ18O, ±0.061 and ± 0.045 mmol/mol for Sr/Ca (RSD, 3.9% and3.6%), ± 0.54 and ± 0.17 μmol/mol for Ba/Ca (RSD, 7.7%
and 9.9%), ± 172 and ± 253 nmol/mol for Pb/Ca (RSD,
8.1% and 7.8%), and ± 0.021 and ± 0.012 μmol/mol forPage 6 of 16

U/Ca (RSD, 8.5% and 4.3%). The variations of sclerosponge geochemical records are small among all skeletal
portions, with no marked trend, except for Ba/Ca and
Pb/Ca, which accord well with those of Astrosclera willeyana sclerosponge reported by Asami et al. (2020a).
These results reflect that within-skeleton variations inδ13C, δ18O, Sr/Ca, and U/Ca are slight for the A. wellsi
species.
To evaluate the fidelity of A. wellsi as apaleoenvironmental proxy, we compared our data withthe δ13C and δ18O values of calcite that is precipitatedinorganically in isotopic equilibrium with seawater at thesclerosponge growth site: so-called equilibrium calcite.
The δ13C values of the equilibrium calcites were estimated using DIC δ13C of seawater, the carbon-isotope
fractionation factors among CO2 species (Zhang et al.
1995), and the calcite–HCO3− enrichment factor (1.0 ±0.2‰; Romanek et al. 1992). Because of the lack of dataon DIC δ13C of seawater around the study sites, the annual mean DIC δ13C value is assumed to fall within arange of 0.58‰ in November to 0.78‰ in August, estimated respectively using two significant relations fromwest of Okinawa Island (Takayanagi et al. 2012) andsoutheast of Okinawa Island (Suzuki et al. 2009). Consequently, the δ13C values of the equilibrium calcites are
expected to be roughly 1.6–2.2‰ (Fig. 4B). The δ18O
values were calculated using an equation derived fromlaboratory synthesis experiments of calcite (Kim andO’Neil 1997), with correction for MgCO3 in calcite(Tarutani et al. 1969). The annual mean seawater temperatures of 26.3 °C for 2010–2012 in Miyako Island and25.2 °C for 2013–2015 in Okinawa Island were usedfrom the ERSST v3b gridded dataset. The seawater δ18O
values of 0.35–0.52‰ and 0.26–0.56‰ were estimatedrespectively for Miyako Island and Okinawa Island from

Fig. 4 A Within-skeleton variations in the geochemistry of the SMJ-2-S1 (open circles) and MNZ-S1 (dotted circles) samples. The Ba/Ca and Pb/Ca
data at the respective sampling point of X = 8 and X = 1 for the MNZ-S1 sample were evaluated as outliers based on the Smirnov-Grubbs test (p< 0.025). B Scatter plot of δ13C and δ18O averages with 1σ standard deviations of coeval skeletal portions in individual samples. Red and green
areas are shown respectively as estimated ranges of isotopically equilibrium calcite precipitated at the study sites of Miyako and Okinawa Islands.
For comparison, aragonite sclerosponge (Astrosclera willeyana) data and an equilibrium aragonite estimate are also shown (Asami et al. 2020a)

Asami et al. Progress in Earth and Planetary Science(2021) 8:38

JODC salinity data using a relation for coral reef environment in Ishigaki Island in the southern Ryukyus (Abeet al. 2009). Results show that the δ18O values of equilibrium high-Mg calcites precipitated at the study sites are
expected to fall within a range of −0.85‰ to −0.67‰ in
Miyako Island and from −0.88 to −0.58‰ in Okinawa
Island (Fig. 4B). Consequently, the δ13C and δ18O valuesof coeval skeletal portions of our A. wellsi samples are
consistent with those of equilibrium calcites, as same as
the findings for A. wellsi (Böhm et al. 1996; Grottoli
et al. 2010) and A. willeyana (Asami et al. 2020a). Theselines of evidence document that our A. wellsi samples
can be suitable for the paleoenvironmental reconstruction study because they probably have a little vital or
biological effect on skeletal geochemistry.
3.2 Time series determination

To convert sclerosponge geochemical records from thedepth domain to the time domain, an age model wasestablished using our Δ14C results of 13 subsamples
along the growth direction of the SMJ-2-S1 sample(Table S1 and Fig. 2) and earlier reported highresolution data of accurately dated coral skeleton collected at a 5 m water depth from Ishigaki Island(Hirabayashi et al. 2017) in the Ryukyu region (Fig. 1). It
is assumed for this study that a difference in local 14C
reservoir effects between Miyako Island and Ishigaki Island can be ignored because the two sites are separated
by only a short distance (approx. 120 km). Moreover,they are located at almost equal water depth in the same
oceanographic setting in the Ryukyu Islands. Figure 5
depicts a comparison showing good consistency between
the two Δ14C profiles for 1947–1997, which yields anage model with a pretty high correlation (r = 0.999)

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under the condition that the skeletal growth rate ofsclerosponge is constant at 1.02 mm/year. Our growthrate estimate accords with earlier studies for the same
species: A. wellsi (1.355 mm/year, Grottoli et al. 2010;
0.80–0.85 mm/year, Ohmori et al. 2014). Applying theage model to the data before 1940, a 130-year-long(1880–2012 AD) time series of the geochemistry was
generated from the SMJ-2-S1 sample. For age determination of MNZ-S1 sample, the δ13C profiles were used forthis study, the method of which is based on evidence
that the δ13C records of our two samples clearly exhibited a typical decreasing trend associated with the anthropogenically derived Suess effects as well as thoseshown in corals and other sclerosponges (see details
presented in the next section). The decreasing trend of
the depth domain MNZ-S1 δ13C record under the condition that the skeletal growth rate is constant at 1.42mm/year corresponded well with that of the SMJ-2-S1
δ13C time series since 1960, yielding a high correlation
coefficient of 0.99 (Supplementary Figure S1). Based on
those results, it can be estimated that the sclerosponge
MNZ-S1 has grown for about 55 years. We identified
65 ± 5 pairs of skeletal density bandings in selected
three transects near the geochemical profile of the Xradiographic image of MNZ-S1 using software (ImageJ64), possibly implying that the growth bandings might
have been formed annually (Fig. 2). However, theoverestimation of 10 ± 5 pairs of density bandings may
indicate that the MNZ-S1 sclerosponge occasionallyhas seasonally formed growth bandings. Therefore, theskeletal bandings of sclerosponges cannot be used forage determination in this study, like corals, because
further validation studies using ultra-high resolution
laser ablation analyses are needed.

Fig. 5 A Comparison of the depth domain profile of radiocarbon (Δ14C) data of the SMJ-2-S1 sclerosponge with a coral-derived time series from
Ishigaki Island in the southern part of Ryukyu Islands (Hirabayashi et al. 2017). B Established age model in this study at the assumption thatsclerosponge skeletal rate has been constantAsami et al. Progress in Earth and Planetary Science(2021) 8:38

3.3 Anthropogenic signatures: carbon isotope

The δ C values of SMJ-2-S1 and MNZ-S1 samples were
2.06‰ to 3.49‰ for 1880–2012 and were 1.54‰ to
3.01‰ for 1960–2015 (Fig. 6). The near-annual resolved
δ13C time series of the SMJ-2-S1 sample showeddecreasing trends at low (−0.0043‰/year) and high(−0.023‰/year) rates, respectively before and after 1960
(Table 1; Fig. 6). The latter rate is identical to that of the
MNZ-S1 sample (−0.024‰/year). Such a typical decreasing trend found in this study probably reflects the Suesseffect, which is widely accepted as a result of the burningof 12C-enriched fossil fuels (Keeling et al. 1979; Quay
et al. 1992). The effect has decreased δ13C of dissolved
inorganic carbon (DIC) in seawater since the midtwentieth century because of the accelerated increase ofanthropogenically derived CO2 with isotopically low
δ13C values into the ocean from the atmosphere, resultsof which are recorded in corals and sclerosponges in the
Pacific and Atlantic Oceans (e.g., Böhm et al. 2002;
Asami et al. 2005; Swart et al. 2010). The post-1960 rates
of decrease of our sclerosponge δ13C records are close
to that of the northwestern tropical Pacific coral for
1960–2000 (Asami et al. 2005) (Fig. 6) and of atmospheric
CO2 at Hawaii for 2000–2016 (derived from the Scripps
CO2 Program initiated in 1956 by Keeling CD). It is fascinating that the rate of decrease of our δ13C records(−0.0043‰/year) for 1880–1960 was similar to those(−0.0033 to −0.0060‰/year) of the tropical Atlantic sclerosponges (Lazareth et al. 2000; Böhm et al. 2002; Swartet al. 2002), but our results (−0.019 and −0.020‰/year)
were slightly higher than those (−0.006 to −0.017‰/year)
for 1960–1992 (Table 1; Fig. 6). These results indicate thatthe accelerated increase in anthropogenic CO2 with low
13

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δ13C values has been about 1.4 times greater in the surface
ocean around Miyako and Okinawa Islands of the subtropical Northwest Pacific than in the Caribbean Sea ofthe tropical Atlantic since the mid-twentieth century. The
difference in the decreasing rates of sclerosponge δ13C records between the two regions is consistent with that inannual mean sea-air CO2 flux (Takahashi et al. 2009),
showing that CO2 sink is significantly higher in the northwestern Pacific region, especially during winter than in the
Caribbean Sea.
3.4 Seawater temperature variations: oxygen isotope, Sr/
Ca, and U/CaThe respective δ18O, Sr/Ca, and U/Ca values of the
SMJ-2-S1 sample for 1880–2012 were −1.11‰ to−0.72‰, 1.32 to 1.70 mmol/mol, and 0.22 to 0.27 μmol/
mol and averaged −0.90‰, 1.52 mmol/mol, and 0.24
nmol/mol (Fig. 7). The respective values of the MNZ-S1
sample for 1960–2015 were −1.19‰ to −0.48‰, 1.32 to
1.51 mmol/mol, and 0.26 to 0.34 μmol/mol and averaged−0.75‰, 1.39 mmol/mol, and 0.29 μmol/mol. The δ18O,
Sr/Ca, and U/Ca time series accord well with long-term
variations and trends of the seawater temperatures on
decadal and multi-decadal timescales. Some inconsistency exists between the SSTs and sclerosponge geochemical records on annual-to-interannual timescales,
the reason of which is explainable by the errors (probably less than ± 2 years) of age determination on the assumption that the skeletal growth rate is constant.
Therefore, to discuss seasonal, annual, and interannual
resolved climate signals, specifying annually formed
growth layers in sclerosponge skeleton in combination
with high-resolution 14C measurements will be useful.

Fig. 6 Time series of sclerosponge δ13C from Miyako and Okinawa Islands in the northwestern subtropical Pacific compared to earlier publisheddata from sclerosponges in the tropical Atlantic (Lazareth et al. 2000; Böhm et al. 2002; Swart et al. 2002) and a Porites sp. coral in the western
tropical Pacific (Asami et al. 2005)

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Table 1 Decreasing trends estimated from sclerosponge δ13C records since 1800
Locality

Water
depth
(m)

Before 1960
PeriodAfter 1960
δ13C slope for 1880-1960(‰/year)(‰/year)

Periodδ13C slope for 1960-1992(‰/year)(‰/year)

Pacific Ocean (this study)
MNZ-S1

Okinawa Is.

2

1960-2015−0.024−0.019SMJ-2-S1

Miyako Is.

101880-1960−0.0043−0.0043

1960-2012−0.023−0.020Jamaica Bay

30

1800-1960−0.0037−0.0049

1960-1983−0.010Böhm et al. (2002)(Ce96-1)Montego Bay

20

1800-1960−0.0031−0.0033

1960-1995−0.015−0.015

Böhm et al. (2002)(Ce95-2-1)

Montego Bay

20

1800-1960−0.0030−0.0048

1960-1994−0.016−0.016

Böhm et al. (2002)(Ce95-2-2)Montego Bay

20

1889-1960−0.0040

1960-1993−0.017−0.017

Böhm et al. (2002)

Rio Bueno, Jamaica

20

1827-1960−0.0040−0.0060

1960-1986−0.013

Böhm et al. (2002)

Pedro Bank

125

1800-1960−0.0026−0.0038

Swart et al. (2002)

Tongue of the Ocean

146

1886-1960−0.0079

Atlantic Ocean (Carribean Sea)
Lazareth et al. (2000)

Since 1960, SSTs have increased in the Miyako andOkinawa Islands with respective rates of +0.0162 °C/year
and +0.0124 °C/year (Table 2). Applying a linear regression, the decreasing trends of sclerosponge δ18O, Sr/Ca,
and U/Ca from Miyako and Okinawa Islands are

1960-1992−0.017−0.017

1960-1992−0.006−0.006

estimated respectively as −3.62 × 10−3 and −3.81 × 10−3‰/year, −1.55 × 10−3 and −1.18 × 10−3 mmol/mol/°C/
year, and −0.271 × 10−3 and −0.727 × 10−3 μmol/mol/°C/year (Table 2). The δ18O values of biogenic carbonates are well known to reflect the temperature and δ18O

Fig. 7 Comparison of time series of sclerosponge δ18O (A and B), Sr/Ca (C and D), and U/Ca (E and F) from Miyako Island (left panels) andOkinawa Island (right panels) with instrumental SST for 1880–2016 (ERSST v3b, http://iridl.ldeo.columbia.edu/)

Asami et al. Progress in Earth and Planetary Science(2021) 8:38

Page 10 of 16

Table 2 Post-1960 trends estimated from SST and sclerosponge δ18O, Sr/Ca, U/Ca records
ID

Locality

SST (°C/year)δ18O slope(‰/year)Dependence(‰/°C)

Sr/Ca slope(mmol/mol/year)

Dependence(mmol/mol/°C)

U/Ca slope(μmol/mol/year)

Dependence(μmol/mol/°C)

MNZ-S1

Okinawa Is.

+0.0124−0.00381−0.307−0.00118−0.095−0.000727−0.059R = 0.605

R = −0.444

SMJ-2-S1

Miyako Is.

+0.0162−0.00362−0.223−0.00155−0.096−0.000271

R = 0.672

R = −0.622

R = −0.551

R = −0.683

R = −0.360−0.017R = −0.380

The R value for the linear regression between age and variable (SST, δ18O, Sr/Ca, and U/Ca) is statistically significant at the 95% confidence limitsof seawater, the evidence of which was also confirmed
for the species A. wellsi sclerosponge (Grottoli et al.
2010). The SST dependence of SMJ-2-S1 δ18O is almost
identical to those of the same species from Saipan (ca.
−0.24‰/°C) (Grottoli et al. 2010) and of inorganic calcite(ca. −0.22‰/°C) (Kim and O’Neil 1997). The value(−0.307‰/°C) of MNZ-S1 δ18O is much higher than expected; implying that seawater δ18O at the sclerosponge
living site in Okinawa has decreased by approximately
0.1‰ since 1960. Although the SST dependencies of Sr/
Ca for the long-term trend are almost identical between
the two sclerosponge samples, several abrupt excursions
in the Sr/Ca signals did not track SST variations (Fig. 7).
For A. wellsi, such inconsistency between Sr/Ca and SST
is explainable by an ICP-MS interference with accurate
Sr/Ca measurement of high-Mg materials and by theinterference of Mg with Sr incorporation into the highMg calcite (Morse and Bender 1990; Grottoli et al.
2010). For U/Ca, the mechanisms of uranyl complexes
incorporation into carbonates are very complicated(Langmuir 1978; DeCarlo et al. 2015). The post-1960 decreasing trend and SST dependency for U/Ca are largely
different between the two samples (Table 2). Furthermore, the U/Ca and Sr/Ca values correlated withmoderately positive r values of 0.66 for SMJ-2-S1 and
0.67 for MNZ-S1, but no significant correlations were

found with δ18O values (Table 3). Considering results ofearlier reports (Grottoli 2006; Grottoli et al. 2010; Wu
and Grottoli 2010), one can infer that the high-Mg calcite Sr/Ca and U/Ca values of A. wellsi sclerosponges
might not be a useful indicator for temperature, unlike
those of aragonite sclerosponges (Astrosclera willeyana
and Ceratoporella nicholsoni) (Rosenheim et al. 2004;
Fallon et al. 2005; Haase-Schramm et al. 2005; Waite
et al. 2018; Asami et al. 2020a).
Unlike the Sr/Ca and U/Ca records, the δ18O timeseries of the SMJ-2-S1 sample clearly showed decadescale variation for 1880–2012 (Fig. 7). Spectral analysesof the 5-year moving average time series using a multitaper method (see the methodology and climatic applications in earlier studies (Mann and Lees 1996; Ghil et al.
2002; Asami et al. 2020b)) revealed a marked concentration of its variance in periodicity of approximately 2, 3,
6.5, 7–10, and 20–30 years/cycle for 1880–2012, which
exceed the 90% confidence level (Fig. 8A). The similar
periodicity roughly corresponds to the significant spectraof instrumental SST in Miyako Island for 1880–2012(Fig. 8B). These results indicate that the sea surface condition around Miyako Island had been highly dominatedby interannual and decadal variations in temperatureand seawater δ18O since the late nineteenth century. It
is conceivable that the interannual variations with

Table 3 Correlations between sclerosponge geochemical recordsa
δ18O

Sr/Ca

Ba/Ca

Pb/Ca

U/Ca

0.51

0.55

0.06

−0.78

0.69

−0.08

−0.19

−0.32

0.09

0.48

−0.59

0.67

MNZ-S1 (Okinawa) 1960-2015
δ13C
δ O
18

Sr/Ca

−0.27

Ba/Ca

0.18
−0.58

Pb/Ca
SMJ-2-S1 (Miyako) 1960-2012
δ13C
δ O
18

Sr/Ca

0.63

0.31

−0.41

0.19

−0.08

−0.24

0.26

0.24

−0.30

0.66

0.37

0.15

Ba/Ca
Pb/Ca
a

Coefficent values in italics and bold fall outside (p > 0.01) and inside (p < 0.01) the 99% confidence intervals, respectively

−0.64

0.36

−0.25

Asami et al. Progress in Earth and Planetary Science(2021) 8:38

Page 11 of 16

Fig. 8 Results of multi-taper method spectral analyses of the SMJ-2-S1 sclerosponge δ18O (A) and instrumental SST (ERSST v3b) (B) for 1880–
2012. The 90%, 95%, and 99% confidence levels are shown as red lines. Numbers denote interannual to decadal periodicity with significant peaks
at the confidence level

relatively shorter and longer periodicity of about 2 years
and 3–8 years are linked respectively to the East Asian
Monsoon and El Niño/Southern Oscillation, which isconsistent with climatic signatures in coral δ18O records
from the Ryukyu Islands (Mishima et al. 2010; Asami
et al. 2020b). The Pacific Decadal Oscillation (PDO), a
dominant climate mode in the Pacific Ocean, was foundto be significant based on modern long-coral δ18O records kept for the northwestern tropical-to-temperate
Pacific region for the last two centuries (Asami et al.
2005; Watanabe et al. 2014). Therefore, it is likely thatthe decadal-scale variations with the periodicity of 20–

30 years detected in the sclerosponge δ18O record might
be associated with the PDO variations.
3.5 Other environmental signals: Ba/Ca and Pb/Ca

The Ba/Ca values of the SMJ-2-S1 and MNZ-S1 samples
were 0.19–10.3 μmol/mol for 1880–2012 and 0.00–2.80μmol/mol for 1960–2015 (Fig. 9). Considering thewithin-skeleton Ba/Ca variations of ± 0.54 μmol/mol(RSD, 7.7%) for SMJ-2-S1 and ± 0.17 μmol/mol for
MNZ-S1 (RSD, 9.9%) (Fig. 4), the Ba/Ca values and temporal variations differ greatly between the two samples
and also from a different species C. nicholsoni from theFig. 9 Secular Ba/Ca variations in sclerosponges and corals from the Pacific and Atlantic OceansAsami et al. Progress in Earth and Planetary Science(2021) 8:38

Atlantic (Rosenheim et al. 2005b). These can be partiallyattributable to wide interspecific, intraspecific, andwithin-skeleton variations in Ba/Ca, as reported from anearlier study (Asami et al. 2020a) and as portrayed inFig. 4. Another reason for the different Ba/Ca variations
might be related to local environmental effects. Earlier
studies of annually banded corals in the Pacific Ocean
demonstrated that increasing short-term signals in coral
Ba/Ca time series generally corresponded to river discharge and terrestrial runoff associated with heavy rainfall and land-use practices (McCulloch et al. 2003; Sahaet al. 2018) and to ocean currents (Alibert and Kinsley
2008a, 2008b) (Fig. 9). It is noteworthy that the SMJ-2S1 Ba/Ca values have increased markedly since 2000: its
signature is not found in the MNZ-S1 values. That large
difference cannot be explained by regional differences inprecipitation and ocean currents because the two sites
are located in almost identical climate settings (Fig. 1).
One possibility for the abrupt Ba/Ca increase in the
SMJ-2-S1 record would be related to a land-use change:
large-scale roads had been constructed from the late
1990s to the early 2010s, and resort facilities with hot
spring, golf course, and hotel had developed from the
1990s to the 2010s around the study site in the southernpart of Miyako Island (Geospatial Information Authorityof Japan, https://mapps.gsi.go.jp/) (Supplementary FigureS2). Some earlier studies demonstrated that skeletal Ba/
Ca ratios of coral aragonite can be a proxy for theamount of land-based sediment input to the reef environment because Ba is sourced from the fine-grained
components of terrestrial soils (McCulloch et al. 2003;
Fleitmann et al. 2007; Prouty et al. 2010). It is, therefore,
likely that the temporal Ba/Ca variations in our sclerosponge SMJ-2-S1 sample might have recorded the historyof terrigenous sediment flux associated with land development since 1880. Nevertheless, we cannot clarify the

Page 12 of 16

reason from the present study results because thephysiological process and the mode of barium incorporation into the sclerosponge skeleton remain unknown(Rosenheim et al. 2005b; Allison et al. 2012; Asami et al.
2020a).
The Pb/Ca values of the SMJ-2-S1 and MNZ-S1 samples were 228–3349 nmol/mol for 1880–2012 and
1699–4146 nmol/mol for 1960–2015 (Fig. 10). These Pb
concentrations are much higher than those of corals: afact which agrees with results described in earlier reports(Benavides and Druffel 1986; Shen and Boyle 1987). The
relatively high Pb/Ca records are attributable to a biological characteristic by which sclerosponges concentrate
Pb in their skeleton by containing nutrition via filter
feeding particulates with absorbed heavy-metal species(Hartman and Goreau 1966; Willenz and Hartman
1989). The temporal Pb/Ca variations of our sclerosponges showed a similar increasing trend during the latetwentieth century, but the values were significantly
different (Fig. 10), considering the within-skeleton variations of ± 172 nmol/mol (RSD, 8.1%) for SMJ-2-S1 and± 253 nmol/mol (RSD, 7.8%) for MNZ-S1 (Fig. 4).
Moreover, our Pb/Ca ratios of A. wellsi samples (highMg calcite) are higher than that found from Kume Island (Ohmori et al. 2014), despite being close to ourstudy site (Fig. 1), and are higher than those of C. nicholsoni (aragonite) (Lazareth et al. 2000; Rosenheim et al.
2005b). That difference indicates that the mechanisms of
Pb incorporation might have large interspecific, intraspecific, and within-skeleton variations. Those indications
can be partially supported by the results of an evaluation
study of sclerosponge (Rosenheim et al. 2005b; Asami
et al. 2020a) and our results portrayed in Fig. 4. An increasing trend was identifiable in our sclerosponge Pb/
Ca records since 1950 (Fig. 10). The Pb/Ca increase primarily accords with those of corals and sclerosponges

Fig. 10 Secular Pb/Ca and Pb concentration variations in sclerosponges and corals from the Pacific and Atlantic OceansAsami et al. Progress in Earth and Planetary Science(2021) 8:38

from the Pacific and Atlantic oceans, which is attributed
to Pb emission from industrial activities. The increases
in the Atlantic coral and sclerosponge records were
followed by a drop occurring in approximately the1970s, caused by decreased use of lead alkyl additives ingasoline, mainly in the USA (Boutron et al. 1991; Rosman et al. 1993), but those in the Pacific records havebeen maintained since the 1950s (Inoue et al. 2006; thisstudy). The anthropogenic Pb/Ca signature found in oursclerosponge records is probably associated with industrial activities in eastern Asian countries and Chinese atmospheric aerosols (Zheng et al. 2004; Hao et al. 2008).
The predominant source of Pb was identified by leadisotope ratios of the western Pacific corals (Inoue andTanimizu 2008). The increasing Pb/Ca trends of oursclerosponges from Miyako and Okinawa Islands accord
well with the time series of Pb contents in an Ogasawara
coral (Fig. 4), indicating that the continued increase of
Pb/Ca ratios after the 1980s can be caused by a mixtureof Pb emitted from Asian countries with heavy
industrialization. However, the sclerosponge Pb/Ca record from Kume Island (Ohmori et al. 2014) has maintained low until the 1980s and decreased since the late
1990s, the variation of which is not consistent with thoseof the Ogasawara coral and our sclerosponge records.
One possible explanation of the difference is that thesclerosponges lived at different water depths of 2–10 m(this study) and 23 m (Ohmori et al. 2014). That is, it islikely that our sclerosponges and the Ogasawara coral,
living in very shallow waters, may record the temporalvariations in Pb concentration sensitively because aerosols with anthropogenically generated lead are transported to the sea surface through the atmosphere (Inoueand Tanimizu 2008). Further investigations of Pb isotope
ratios (206Pb/207Pb and 208Pb/207Pb) must be conductedof our samples to clarify the potential source of Pb in
the Miyako and Okinawa Islands.

4 Conclusions
From Acanthochaetetes wellsi sclerosponge samples for
1880–2012 and 1960–2015, collected respectively at
Miyako Island and Okinawa Island in the Ryukyu Islandsof southwestern Japan, we first generated near-annual
resolved time series of skeletal δ13C, δ18O, and element/
Ca ratios (Sr/Ca, Ba/Ca, Pb/Ca, U/Ca). The δ13C values
have decreased at an increasing rate since the midtwentieth century, indicating the anthropogenically derived Suess effect. Our estimations demonstrated thatthe δ13C decrease rate in the northwestern subtropical
Pacific was similar to the Caribbean Sea before 1960 but
about 1.4 times higher after 1960. The δ18O records
were mostly accorded with long-term variations in seawater temperatures. Using spectral analysis, we detectedsignificant periodicity of 2, 3, 6.5, 7–10, and 20–30 year/

Page 13 of 16

cycle in the δ18O time series, which indicates that sea
surface conditions around the southern Ryukyu Islands
had been dominated by interannual and decadal variations in temperature and seawater δ18O since the latenineteenth century.
In contrast to aragonite sclerosponges (A. willeyana
and C. nicholsoni), the validity of Sr/Ca and U/Ca
records of A. wellsi with high-Mg calcite skeleton for arobust proxy of seawater temperature cannot be determined from data used for this study. Compared to previously published data, the increasing Pb/Ca trends after
1950 found in our sclerosponge records are probably
caused by Pb emissions from industrial activities in eastern Asian countries and Chinese atmospheric aerosols.
A great difference in the Ba/Ca variations is apparent between our two sclerosponges, which might be related to
local environments. However, large intraspecific andwithin-skeleton variations in Ba/Ca and Pb/Ca preventthe interpretation of environmental signals recorded in
the sclerosponge samples. This study suggests that, withmore high-resolution age determinations, sclerospongebased reconstruction studies can elucidate secular variations in ocean environments on seasonal, annual, andinterannual time scales.
The Kuroshio Current allows the development ofwidely distributed reefs with a highly diversified biota of
the Ryukyu Islands during the late Quaternary (Iryu
et al. 2006). In combination with the geochemistry of
calcified marine organisms such as corals and giant
clams, if long-lived sclerosponges are collected fromdeeper ocean environments, we can generate long timeseries reflecting spatial and vertical changes in coral reef
environments of the Ryukyu Islands that have takenplace over the past few hundred years, extending far
beyond the limits of meteorological observation data,and over the last deglaciation.
Abbreviations
JODC: Japan Oceanographic Data Center; VPDB: Vienna Standard Pee Dee
Belemnite

5 Supplementary Information
The online version contains supplementary material available at https://doi.
org/10.1186/s40645-021-00434-7.
Additional file 1: Table S1. Radiocarbon data reported as Δ14C of thesample series extracted from the sclerosponge SMJ-2-S1 with the estimated date of skeletal formation. Figure S1. Comparison of the depth
domain δ13C profile of the sclerosponge MNZ-S1 with the δ13C timeseries of SMJ-2-S1 determined by radiocarbon data. The decreasing trendof MNZ-S1 δ13C record under the condition that the skeletal growth rate
is 1.42 mm/year shows good agreement with that of SMJ-2-S1 for 1960–
2012, yielding a high correlation between the two regression lines (r =0.99). Figure S2. Aerial photos of the southern part of Miyako Island in
1995 and 2019 (modified from Geospatial Information Authority of Japan,
https://mapps.gsi.go.jp/), showing the locations of the sclerosponge sampling site and large-scale road and resort constructions.

(2021) 8:38

Page 14 of 16

Acknowledgements
We are grateful to an editor (Dr. Y. Okazaki) and two anonymous reviewers
for their helpful and valuable suggestions on the manuscript. We also thankS. Ishikawa, M. Chinen, and Y. Akamine (University of the Ryukyus) for help
with experiments.

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Asami et al. Progress in Earth and Planetary Science

Authors’ contributions
RA designed the study, analyzed the samples and data, and wrote themanuscript. YM, MM, and TS carried out the fieldwork and sampling. TM, RS,
RU, and YI collaborated with RA in the experimental study. The authors readand approved the final manuscript.
Funding
This research was supported by the Japan Society for the Promotion of
Science KAKENHI (Grant-in-Aid for Scientific Research) Grant numbers
26550012, 26707028, and 18K18522 to RA and 15H01729 to RU, and theNEXT Program Grant Number GR083 to TS.
Availability of data and materials
Sclerosponge data generated in this study will be available at NOAA NCDCWorld Data Center for Paleoclimatology (https://www.ncdc.noaa.gov/dataaccess/paleoclimatology-data). Please contact the corresponding author fordata requests.

Declarations
Competing interests
The authors declare that they have no competing interests.
Author details
1
Institute of Geology and Paleontology, Graduate School of Science, Tohoku
University, 6-3, Aramaki-Aza-Aoba, Sendai 980-8578, Japan. 2Department of
Physics and Earth Sciences, Faculty of Science, University of the Ryukyus, 1
Senbaru, Nishihara, Okinawa 903-0213, Japan. 3Department of Earth andEnvironmental Sciences, Graduate School of Environmental Studies, Nagoya
University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan. 4Trans-disciplinary
Research Organization for Subtropical Island Studies, University of the
Ryukyus, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan. 5Graduate School ofEngineering and Science, University of the Ryukyus, 1 Senbaru, Nishihara,
Okinawa 903-0213, Japan. 6Tropical Biosphere Research Center, Sesoko
Station, University of the Ryukyus, 3422 Sesoko, Motobu, Okinawa 905-0227,
Japan. 7Department of Civil and Environmental Engineering, Graduate Schoolof Engineering, Tohoku University, 6-6-06 Aramaki-Aza-Aoba, Sendai
980-8579, Japan.
Received: 10 November 2020 Accepted: 8 June 2021

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